Publications by year
In Press
Regan CE, Pilkington JG, Berenos C, Pemberton JM, Smiseth PT, Wilson AJ (In Press). Accounting for female space sharing in St. Kilda Soay sheep (Ovis aries) results in little change in heritability estimates. Journal of Evolutionary Biology
Lane S, Wilson A, Briffa M (In Press). Analysis of direct and indirect genetic effects in fighting sea anemones. Behavioral Ecology
Houslay TM, Wilson A (In Press). Avoiding the misuse of BLUP in behavioral ecology. Behavioral Ecology
Stothart MR, Greuel R, Gavriliuc S, Henry A, Wilson A, McLoughlin PD, Poissant J (In Press). Bacterial dispersal and drift drive microbiome diversity patterns within a population of feral hindgut fermenters. Molecular Ecology
Santostafano F, Wilson AJ, Niemala PT, Dingemanse NJ (In Press). Behavioural mediators of genetic life-history trade-offs: a test of the pace-of-life syndrome hypothesis in field crickets. Proceedings of the Royal Society B: Biological Sciences
McCain S, Kopelic S, Houslay T, Wilson A, Lu H, Earley R (In Press). Choice consequences: Salinity preferences and hatchling survival in the mangrove rivulus fish (Kryptolebias marmoratus). The Journal of Experimental Biology
Styga JM, Houslay T, Wilson A, Earley RL (In Press). Development of G: a test in an amphibious fish. Heredity
Sharman P, Young A, Wilson A (In Press). Evidence of maternal and paternal age effects on speed in thoroughbred racehorses. Royal Society Open Science
Bonneaud C, Tardy L, Giraudeau M, Hill G, McGraw K, Wilson A (In Press). Evolution of host resistance and damage-limiting mechanisms to an emerging bacterial pathogen.
Abstract:
Evolution of host resistance and damage-limiting mechanisms to an emerging bacterial pathogen
Understanding how hosts minimise the cost of emerging infections has fundamental implications for epidemiological dynamics and the evolution of pathogen virulence. Despite this, few experimental studies conducted in natural populations have explicitly tested whether hosts evolve resistance, which prevents infections or reduces pathogen load through immune activation, or tolerance, which limits somatic damages without decreasing pathogen load. In addition, none have done so controlling for the virulence of the pathogen isolate used, despite critical effects on host responses to infection. Here, we conducted an experimental inoculation study to test whether eastern North American house finches (Haemorrhous mexicanus) have evolved resistance or tolerance to their emerging bacterial pathogen, Mycoplasma gallisepticum, using 55 distinct isolates of varying virulence. First, we show that peak pathogen loads, which occurred around 8 days post-inoculation, did not differ between experimentally inoculated finches from disease-exposed (eastern) versus unexposed (western) population. However, pathogen loads subsequently decreased faster and to a greater extent in finches from exposed populations, indicating that they were able to clear the infection through adaptive immune processes. Second, we found no between-population difference in the regression of clinical symptom severity on pathogen load; if tolerance had evolved then the slope of this regression is predicted to be shallower (less negative) in the exposed population. However, finches from exposed populations displayed lower symptom severity for a given pathogen load, suggesting that damage-limitation mechanisms have accompanied the evolution of immune clearance. These observations show that resistance and damage-limitation mechanisms - including, but not limited to the standard conceptualisation of tolerance - should not be seen as mutually exclusive. Nevertheless, we propose that host resistance is especially likely to evolve in response to pathogens such as M. gallisepticum that require virulence for successful infection and transmission.
Abstract.
White S, Wilson A (In Press). Evolutionary genetics of personality in the Trinidadian guppy I: Maternal and additive genetic effects across ontogeny. Heredity
White S, Houslay T, Wilson A (In Press). Evolutionary genetics of personality in the Trinidadian guppy II: Sexual dimorphism and genotype-by-sex interactions. Heredity
Regan C, Tuke L, McLoughlin P, Colpitts J, Wilson A, Poissant J (In Press). Evolutionary quantitative genetics of juvenile body size in a population of feral horses reveals sexually antagonistic selection. Evolutionary Ecology
Houslay TM, Earley RL, White SJ, Lammers W, Grimmer AJ, Travers LM, Johnson EL, Young AJ, Wilson AJ (In Press). Genetic integration of behavioural and endocrine components of the stress response.
Abstract:
Genetic integration of behavioural and endocrine components of the stress response
AbstractThe vertebrate stress response comprises a suite of behavioural and physiological traits that must be functionally integrated to ensure organisms cope adaptively with acute stressors. Natural selection should favour functional integration, leading to a prediction of genetic integration of these traits. Despite the implications of such genetic integration for our understanding of human and animal health, as well as evolutionary responses to natural and anthropogenic stressors, formal quantitative genetic tests of this prediction are lacking. Here we demonstrate that acute stress response components in Trinidadian guppies are both heritable and integrated on the major axis of genetic covariation. This integration could either facilitate or constrain evolutionary responses to selection, depending upon the alignment of selection with this axis. Such integration also suggests artificial selection on the genetically correlated behavioural responses to stress could offer a viable non-invasive route to the improvement of health and welfare in captive animal populations.
Abstract.
Houslay T, Earley RL, White SJ, Lammers W, Grimmer AJ, Travers LM, Johnson EL, Young AJ, Wilson AJ (In Press). Genetic integration of behavioural and endocrine components of the stress response.
eLifeAbstract:
Genetic integration of behavioural and endocrine components of the stress response
The vertebrate stress response comprises a suite of behavioural and physiological traits that must be functionally integrated to ensure organisms cope adaptively with acute stressors. Natural selection should favour functional integration, leading to a prediction of genetic integration of these traits. Despite the implications of such genetic integration for our understanding of human and animal health, as well as evolutionary responses to natural and anthropogenic stressors, formal quantitative genetic tests of this prediction are lacking. Here we demonstrate that acute stress response components in Trinidadian guppies are both heritable and integrated on the major axis of genetic covariation. This integration could either facilitate or constrain evolutionary responses to selection, depending upon the alignment of selection with this axis. Such integration also suggests artificial selection on the genetically correlated behavioural responses to stress could offer a viable non-invasive route to the improvement of health and welfare in captive animal populations.
Abstract.
Prentice P, Houslay T, Martin J, Wilson A (In Press). Genetic variance for behavioural ‘predictability’ of the stress response. Journal of Evolutionary Biology
Marjamäki P, Dugdale H, Delahay R, McDonald R, Wilson A (In Press). Genetic, social and maternal contributions to Mycobacterium bovis infection status in European badgers (Meles meles). Journal of Evolutionary Biology
Houslay T, Earley R, Young A, Wilson A (In Press). Habituation and individual variation in the endocrine stress
response in the Trinidadian guppy (Poecilia reticulata). General and Comparative Endocrinology
Houslay TM, Earley RL, Young AJ, Wilson AJ (In Press). Habituation and individual variation in the endocrine stress response in the Trinidadian guppy (<i>Poecilia reticulata</i>).
Abstract:
Habituation and individual variation in the endocrine stress response in the Trinidadian guppy (Poecilia reticulata)
AbstractThe vertebrate stress response enables individuals to react to and cope with environmental challenges. A crucial aspect of the stress response is the elevation of circulating glucocorticoids. However, continued activation of the stress response under repeated (or chronic) stress can be damaging to fitness. Under certain circumstances it may therefore be adaptive to habituate to repeated exposures to a particular stressor by reducing the magnitude of any associated release of glucocorticoids. Here, we investigate whether Trinidadian guppies (Poecilia reticulata) habituate to repeated exposure to a mild stressor, using a waterborne hormone sampling approach that has previously been shown to elicit a stress response in small fish. We also test for individual variation in the extent of habituation to this stressor. Concentrating on freely circulating cortisol, we found that the first exposure to the assay induced high cortisol release rates but that guppies tended to habituate quickly to subsequent exposures. There were consistent differences among individuals in their average cortisol release rate (after accounting for effects of variables such as body size) over repeated exposures. Our analyses did not find evidence of individual differences in habituation rate, although limitations in statistical power could account for this finding. We also present data on free 11-ketotestosterone, in addition to conjugated forms of both hormones. We discuss consistent individual differences around the general pattern of habituation in the flexible stress response, and highlight the potential for individual variation in habituation to facilitate selection against the deleterious effects of chronic stress.Summary statementTrinidadian guppies habituate quickly to repeated stress exposure, and exhibit consistent differences in their endocrine stress response. We provide a framework for analysing individual variation in habituation rate.
Abstract.
Boulton K, Sinderman B, Pearce MR, Earley RL, Wilson AJ (In Press). He who dares only sometimes wins: physiological stress and contest behaviour in Xiphophorus helleri. Behaviour, 149, 977-1002.
Sorato E, Zidar L, Garnham L, Wilson A, Løvlie H (In Press). Heritabilities and co-variation among cognitive traits in red junglefowl. Philosophical Transactions B: Biological Sciences
Wilson A (In Press). How should we interpret estimates of individual repeatability?. Evolution Letters
Santostefano F, Wilson A, Niemala P, Dingemanse N (In Press). Indirect genetic effects: a key component of the genetic architecture of behaviour. Scientific Reports
Prentice PM, Mnatzaganian C, Houslay TM, Thornton A, Wilson AJ (In Press). Individual differences in spatial learning are correlated across cognitive tasks but not associated with stress response behaviour in the Trinidadian guppy.
Abstract:
Individual differences in spatial learning are correlated across cognitive tasks but not associated with stress response behaviour in the Trinidadian guppy
AbstractCognition is vital for carrying out behaviours required for survival and reproduction. In animals, we now know that cognitive performance varies not just among species, but also among individuals within populations. While this variation is a prerequisite for contemporary natural selection, it is also true that selection does not act on traits in isolation. The extent to which cognitive traits covary with other aspects of phenotype (e.g. personality traits) is therefore expected to be an important factor in shaping evolutionary dynamics. Here we adopt a multivariate approach to test for spatial learning ability in a captive population of male Trinidadian guppies (Poecilia reticulata), and ask whether differences in cognitive performance are associated with (repeatable) differences in stress response behaviour. We focus on stress response for two reasons. First, functional links between cognitive traits and ‘stress coping style’ have been hypothesised. Second, individual-level studies of cognitive performance typically rely on multiple testing paradigms that may themselves be a stressor. Thus, there is a risk that variation in stress responsiveness is itself a cause of apparent, but artefactual variance in cognitive ability. Using a set of fish exposed repeatedly to two distinct spatial learning tasks (maze layouts), and an acute stress response test (open field trial), we find differences among-individuals in task performance that are repeatable within- and across maze layouts. On average performance improves with experience in the first maze, consistent with spatial learning, but not in the second. In both mazes, there is among-individual variation in the trajectory of mean performance with trial number suggesting individuals differ in ‘learning rate’. Acute stress response behaviour is repeatable but predicts neither average time to solve the maze nor learning rate. We thus find no support for among-individual correlation between acute stress response and cognitive performance. However, we highlight the possibility that cumulative, chronic stress effects may nonetheless cause observed declines in performance across repeats for some individuals (leading to lack of improvement in mean time to solve the second maze). If so, this may represent a pervasive but difficult challenge for our ability to robustly estimate learning rates in studies of animal cognition.
Abstract.
Prentice P, mnatzaganian C, Houslay T, Thornton A, Wilson A (In Press). Individual differences in spatial learning are correlated across tasks but not with stress response behaviour in guppies. Animal Behaviour
Marjamäki P, Dugdale H, Dawson D, McDonald R, Delahay R, Burke T, Wilson A (In Press). Individual variation and the source-sink group dynamics of extra-group paternity in a social mammal. Behavioral Ecology
Santostefano F, Wilson A, Araya-Ajoy YG, Dingemanse NJ (In Press). Interacting with the enemy: indirect effects of personality on conspecific aggression in crickets.
Behavioral EcologyAbstract:
Interacting with the enemy: indirect effects of personality on conspecific aggression in crickets
In animal contests, individuals respond plastically to the phenotypes of the opponents that they confront. These ‘opponent’ – or ‘indirect’ – effects are often repeatable, e.g. certain opponents consistently elicit more or less aggressiveness in others. ‘Personality’ (repeatable among-individual variance in behavior) has been proposed as an important source of indirect effects. Here, we repeatedly assayed aggressiveness of wild-caught adult male field crickets Gryllus campestris in staged dyadic fights, measuring aggressiveness of both contestants. Measurements of their personality in non-social contexts (activity and exploration behavior) enabled us to ask whether personality caused indirect effects on aggressiveness. Activity, exploration, and aggressiveness were positively associated into a behavioral syndrome eliciting aggressiveness in conspecifics, providing direct evidence for the role of personality in causing indirect effects. Our findings imply that a multivariate view of phenotypes that includes indirect effects greatly improves our ability to understand the ecology and evolution of behavior.
Abstract.
Regan C, Pemberton J, Pilkington J, Smiseth P, Wilson A (In Press). Linking genetic merit to behavioral data: behavior and genetic effects on
lamb growth in Soay sheep?. Behavioral Ecology
Rapkin J, Archer CR, Grant CE, Jensen K, House CM, Wilson AJ, hunt J (In Press). Little evidence for intralocus sexual conflict over the optimal intake of nutrients for lifespan and reproduction in the black field cricket Teleogryllus commodus. Evolution
White SJ, Kells TJ, Wilson AJ (In Press). Metabolism, personality and pace of life in the Trinidadian guppy, Poecilia reticulata. Behaviour
Narayan VP, Wasana N, Wilson AJ, Chenoweth SF (In Press). Misaligned plastic and evolutionary responses of lifespan to novel carbohydrate diets.
Abstract:
Misaligned plastic and evolutionary responses of lifespan to novel carbohydrate diets
AbstractDiet elicits varied effects on longevity across a wide range of animal species. For example, diets low in protein and high in carbohydrate typically extend lifespan while diets high in protein tend to reduce it. Although studies have also shown that diet-induced lifespan changes can persist through transgenerational plasticity, whether such changes lead to evolutionary shifts in lifespan remains unclear. In this study we combine experimental evolution and phenotypic plasticity assays to address this gap. UsingDrosophila serrata, we investigated the evolutionary potential of lifespan in response to four novel diets spanning a carbohydrate-protein gradient. We also examined developmental plasticity effects using a set of control populations that were raised on the four novel environments. Our results show that although lifespan evolved in response to changes in dietary carbohydrate concentration, the plastic responses for lifespan differed from the evolved responses. The direction of the evolved response (increased lifespan) observed on low carbohydrate diets was in the opposite direction to the plastic response (decreased lifespan). Our results imply that plastic responses to low carbohydrates can be maladaptive for lifespan and misaligned with the evolved responses, laying the groundwork for future investigations of carbohydrate contributions to evolved and plastic effects on lifespan.
Abstract.
Capilla-Lasheras P, Wilson AJ, Young AJ (In Press). Mothers front-load their investment to the egg stage when helped in a wild cooperative bird.
Abstract:
Mothers front-load their investment to the egg stage when helped in a wild cooperative bird
AbstractIn many cooperative societies, including our own, helpers assist with the post-natal care of breeders’ young, and may thereby benefit thepost-nataldevelopment of offspring. Here we present evidence of a novel mechanism by which such post-natal helping could also have hitherto unexplored beneficial effects onpre-nataldevelopment: by lightening post-natal maternal workloads, helpers may allow mothers to increase their pre-natal investment per offspring. We present the findings of a decade-long study of cooperatively breeding white-browed sparrow weaver,Plocepasser mahali, societies. Within each social group, reproduction is monopolized by a dominant breeding pair, and non-breeding helpers assist with nestling feeding. Using a within-mother reaction norm approach to formally identify maternal plasticity, we demonstrate that when mothers have more female helpers they decrease their ownpost-natalinvestment per offspring (feed their nestlings at lower rates) but increase theirpre-natalinvestment per offspring (lay larger eggs, which yield heavier hatchlings). That these plastic maternal responses are predicted by female helper number, and not male helper number, implicates the availability of post-natal helpingper seas the likely driver (rather than correlated effects of group size), because female helpers feed nestlings at substantially higher rates than males. We term this novel maternal strategy “maternal front-loading” and hypothesize that the expected availability ofpost-natalhelp allows helped mothers to focus maternal investment on thepre-natalphase, to which helpers cannot contribute directly. Such cryptic maternally mediated helper effects on pre-natal development may markedly complicate attempts to identify and quantify the fitness consequences of helping.
Abstract.
Styga J, Houslay T, Wilson A, Earley R (In Press). Ontogeny of the morphology-performance axis in an amphibious fish (Kryptolebias marmoratus). Journal of Experimental Zoology Part A: Comparative Experimental Biology
Boulton K, Walling CA, Grimmer AJ, Rosenthal GG, Wilson A (In Press). Phenotypic and genetic integration of personality and growth under competition in the sheepshead swordtail, Xiphophorus birchmanni. Evolution
Roff DA, Wilson A (In Press). Quantifying genetic by environmental interactions in laboratory systems. In (Ed) Genotype-by-environment interactions and sexual selection.
Videlier M, Careau V, Wilson A, Rundle HD (In Press). Quantifying selection on standard metabolic rate and body mass in Drosophila melanogaster. Evolution
Gold S, Regan CE, McLoughlin PD, Gilleard JS, Wilson A, Poissant J (In Press). Quantitative genetics of gastrointestinal strongyle burden and associated body condition in feral horses. International Journal of Parasitology: Parasites and Wildlife
Sharman P, Wilson A (In Press). Racehorses are getting faster.
Biology LettersAbstract:
Racehorses are getting faster
Previous studies have concluded that thoroughbred racehorse speed is improving very slowly, if at all, despite heritable variation for performance and putatively intensive selective breeding. This has led to the suggestion that racehorses have reached a selection limit. However, previous studies have been limited, focussing only on the winning times of a few elite races run over middle and long distances, and failing to account for potentially confounding factors. Using a much larger dataset covering the full range of race distances and accounting for variation in factors such as ground softness, we show that improvement is in fact on-going for the population as a whole, but driven largely by increasing speed in sprint races. In contrast, speed over middle and long distances, at least at the elite level, appears to be reaching an asymptote. Whether this reflects a selection limit to speed over middle and long distances or a shift in breeding practices to target sprint performances remains to be determined.
Abstract.
Yong L, Croft DP, Troscianko J, Ramnarine I, Wilson A (In Press). Sensory-based quantification of male colour patterns in Trinidadian guppies reveals nonparallel phenotypic evolution across an ecological transition in multivariate trait space.
Abstract:
Sensory-based quantification of male colour patterns in Trinidadian guppies reveals nonparallel phenotypic evolution across an ecological transition in multivariate trait space
ABSTRACTParallel evolution, in which independent populations evolve along similar phenotypic trajectories, offers insights into the repeatability of adaptive evolution. Here, we revisit a classic example of parallelism, that of repeated evolution of brighter males in the Trinidadian guppy. In guppies, colonisation of low predation habitats is associated with emergence of ‘more colourful’ phenotypes since predator-induced viability selection for crypsis weakens while sexual selection by female preference for conspicuity remains strong. Our study differs from previous investigations in three respects. First, we adopt a multivariate phenotyping approach to characterise parallelism in multi-trait space. Second, we use ecologically-relevant colour traits defined by the visual systems of the two selective agents (i.e. guppy, predatory cichlid). Third, we estimate population genetic structure to test for adaptive (parallel) evolution against a model of neutral phenotypyc divergence. We find strong phenotypic differentiation that is inconsistent with a neutral model, but only limited support for the predicted pattern of greater conspicuity at low predation. Effects of predation regime on each trait were in the expected direction, but weak, largely non-significant, and explained little among-population variation. In multi-trait space, phenotypic trajectories of lineages colonising low from high predation regimes were not parallel. Our results are consistent with reduced predation risk facilitating adaptive differentiation by female choice, but suggest that this proceeds in (effectively) independent directions of multi-trait space across lineages. Pool-sequencing data also revealed SNPs showing greater differentiation than expected under neutrality and/or associations with known colour genes in other species, presenting opportunities for future genetic study.
Abstract.
Wilson A, Boulton K, Grimmer AJ, Walling CA, Rosenthal GG (In Press). Sex-specific plasticity and genotype x sex interactions for age and size of maturity in the sheepshead swordtail, Xiphophorus birchmanni.
Wilson A, Pascoal S, Hunt J, Mendrok M, Bailey NW (In Press). Sexual Selection and Population Divergence II. Divergence in Different Sexual Traits and Signal Modalities in Field Crickets (Teleogryllus oceanicus). Evolution
Fisher D, Wilson A, Boutin S, Dantzer B, Lane J, Coltman D, Gorrell J, McAdam A (In Press). Social effects of territorial neighbours on the timing of spring breeding in North American red squirrels. Journal of Evolutionary Biology
Boonekamp J, Rodríguez-Muñoz R, Hopwood P, Zuidersma E, Mulder E, Wilson A, Verhulst S, Tregenza T (In Press). Telomere length is highly heritable and independent of growth rate manipulated by temperature in field crickets.
Abstract:
Telomere length is highly heritable and independent of growth rate manipulated by temperature in field crickets
AbstractMany organisms are capable of growing faster than they do. Restrained growth rate has functionally been explained by negative effects on lifespan of accelerated growth. However, the underlying mechanisms remain elusive. Telomere attrition has been proposed as a causal agent and has been studied in endothermic vertebrates. We established that telomeres exist as chromosomal-ends in a model insect, the field cricket, using terminal restriction fragment andBal 31methods. Telomeres comprised TTAGGn repeats of 38kb on average, more than four times longer than the telomeres of human infants.Bal 31assays confirmed that telomeric repeats were located at the chromosome-ends. We tested whether rapid growth is achieved at the expense of telomere length by comparing crickets reared at 23°C with their siblings reared at 28°C, which grew three times faster. Surprisingly, neither temperature treatment nor age affected average telomere length. Concomitantly, the broad sense heritability of telomere length was remarkably high at ~100%. Despite high heritability, the evolvability (a mean standardized measure of genetic variance) was low relative to that of body mass. We discuss the different interpretations of these scaling methods in the context of telomere evolution. It is clear that some important features of vertebrate telomere biology are evident in an insect species dating back to the Triassic, but also that there are some striking differences. The apparent lack of an effect of growth rate and the total number of cell divisions on telomere length is puzzling, suggesting that telomere length could be actively maintained during the growth phase. Whether such maintenance of telomere length is adaptive remains elusive and requires further study investigating the links with fitness in the wild.
Abstract.
Kruuk LEB, Wilson AJ (In Press). The challenge of estimating indirect genetic effects on behaviour: a comment on Bailey et al. Behavioral Ecology
McAdam AG, Garant D, Wilson AJ (In Press). The effect of other’s genes: maternal and other indirect genetic effects. In (Ed) Quantitative genetics in natural populations.
Morrissey MB, Parker DJ, Korsten P, Pemberton JM, Kruuk LEB, Wilson AJ (In Press). The prediction of adaptive evolution: empirical application of the secondary theorem of selection and comparison to the breeder's equation. Evolution, 66, 2399-2410.
Royle NJ, Carter M, Wilson A, Moore A (In Press). The role of indirect genetic effects in the evolution of
interacting reproductive behaviors in the burying beetle,
Nicrophorus vespilloides. Ecology and Evolution
Maskrey D, White S, Wilson A, Houslay T (In Press). Who dares doesn’t always win: risk-averse rockpool prawns are better at controlling a limited food resource. Animal Behaviour
2022
Price E, Langford J, Fawcett T, Wilson A, Croft D (2022). Classifying the posture and activity of ewes and lambs using accelerometers and machine learning on a commercial flock.
Applied Animal Behaviour Science,
251, 105630-105630.
Abstract:
Classifying the posture and activity of ewes and lambs using accelerometers and machine learning on a commercial flock
Early decision making in commercial livestock systems is key to maximising animal welfare and production. Detailed information on an animal’s phenotype is needed to facilitate this, but can be difficult to obtain in a commercial setting. Research into the use of bio-logging on sheep to continuously monitor individual behaviour and indirectly inform health and production has seen rapid growth in recent years. Much of this research, however, has been conducted on small numbers of animals in an experimental setting and over limited time periods. Previous studies have also focused on ewes and there has been little research on the potential of bio-logging for collecting behavioural data on lambs, despite clear potential relevance for production. The present study aimed to test the feasibility of deploying accelerometers on a commercial sheep flock at a key point in the annual production cycle (lambing), to validate the viability of automated monitoring of sheep behaviour in a commercial setting. Also, we aimed to develop robust machine learning algorithms that can classify both the posture and physical activity of adult sheep and lambs. We used a Random Forest machine learning algorithm to predict: two mutually exclusive postures in ewes and lambs (standing and lying), achieving average accuracies of 83.7% and 85.9% respectively; four mutually exclusive activities in ewes (grazing, ruminating, inactive and walking), achieving an average accuracy of 70.9%; and three mutually exclusive activities in lambs (inactive, suckling, walking), achieving an average accuracy of 80.8%. These performance accuracies on large numbers of individuals afford the opportunity to provide a detailed understanding of the daily activity budget of ewes and lambs. Monitoring changes in daily patterns across the annual production cycle while capturing changes in environmental conditions such as weather, day length, terrain and management could reveal key indicator metrics that may inform production and health and provide early warning systems for key issues in commercial flocks.
Abstract.
Patrick SC, Réale D, Potts JR, Wilson AJ, Doutrelant C, Teplitsky C, Charmantier A (2022). Differences in the temporal scale of reproductive investment across the slow‐fast continuum in a passerine. Ecology Letters, 25(5), 1139-1151.
Narayan VP, Wilson AJ, Chenoweth SF (2022). Genetic and social contributions to sex differences in lifespan in Drosophila serrata.
J Evol Biol,
35(4), 657-663.
Abstract:
Genetic and social contributions to sex differences in lifespan in Drosophila serrata.
Sex differences in lifespan remain an intriguing puzzle in evolutionary biology. While explanations range from sex differences in selection to sex differences in the expression of recessive lifespan-altering mutations (via X-linkage), little consensus has been reached. One unresolved issue is the extent to which genetic influences on lifespan dimorphism are modulated by the environment. For example, studies have shown that sex differences in lifespan can either increase or decrease depending upon the social environment. Here, we took an experimental approach, manipulating multiple axes of the social environment across inbred long- and short-lived genotypes and their reciprocal F1s in the fly Drosophila serrata. Our results reveal strong genetic effects and subtle yet significant genotype-by-environment interactions for male and female lifespan, specifically due to both population density and mating status. Further, our data do not support the idea that unconditional expression of deleterious X-linked recessive alleles in heterogametic males accounts for lower male lifespan.
Abstract.
Author URL.
Brown A (2022). Mechanisms of age-related change in performance in a wild social bird: parental age effects, cellular senescence, and dominance acquisition.
Abstract:
Mechanisms of age-related change in performance in a wild social bird: parental age effects, cellular senescence, and dominance acquisition
Age-related changes in performance (reproduction and survival) are widespread in nature. In vertebrates, age-related performance trajectories are typically characterised by early-life improvements followed by late-life declines (termed ‘senescence’). However, the mechanisms that underpin such age-related changes in performance are still poorly understood. In this thesis, I combine molecular, cellular, long-term life history, and radio-telemetry data from a population of a cooperatively breeding bird, the white-browed sparrow weaver Plocepasser mahali, to investigate some key shortfalls in our understanding of the mechanistic origins of age-related changes in organismal performance. In Chapter 2, I present the first longitudinal evidence that within-parent changes in age positively predict offspring telomere lengths, an effect that has the potential to positively impact parent and offspring fitness. Then, in Chapter 3, I present the first evidence for within-individual accumulation of senescent cells with advancing age in a natural population. I also demonstrate that these within-individual increases in senescent cell frequency over the short term are not reflected at the population level, suggestive of the selective disappearance of either individuals with high incidences of senescent cells from the population, or of senescent cells within individuals. In Chapter 4, I investigate the effects of age on dominance acquisition, and provide evidence that individuals that are older relative to other potential competitors are more likely to win dominance turnovers. This finding highlights a potentially widespread mechanism by which the costs of cooperation (in terms of increased competition for breeding positions) could be mitigated in cooperatively breeding species. Finally, in Chapter 5, I investigate whether within-group social circumstances influence subordinate dispersal behaviour. Despite finding that individuals do not seem to adjust their dispersal behaviour in response to the expected payoffs of remaining in their current group versus dispersing, I show that individuals tend to disperse to subordinate positions in smaller groups and with fewer same age or older individuals. As living in a larger group entails survival costs, and individuals are more likely to win dominance in groups where they are the oldest subordinate of their sex, these results suggests individuals may ‘trade up’ their social circumstances when they disperse. Together, my findings elucidate some key shortfalls in our understanding of the mechanisms underlying age-related changes in performance.
Abstract.
Qiu S, Yong L, Wilson A, Croft DP, Graham C, Charlesworth D (2022). Partial sex linkage and linkage disequilibrium on the guppy sex chromosome.
Qiu S, Yong L, Wilson A, Croft DP, Graham C, Charlesworth D (2022). Partial sex linkage and linkage disequilibrium on the guppy sex chromosome.
Mol Ecol,
31(21), 5524-5537.
Abstract:
Partial sex linkage and linkage disequilibrium on the guppy sex chromosome.
The guppy Y chromosome has been considered a model system for the evolution of suppressed recombination between sex chromosomes, and it has been proposed that complete sex-linkage has evolved across about 3 Mb surrounding this fish's sex-determining locus, followed by recombination suppression across a further 7 Mb of the 23 Mb XY pair, forming younger "evolutionary strata". Sequences of the guppy genome show that Y is very similar to the X chromosome. Knowing which parts of the Y are completely nonrecombining, and whether there is indeed a large completely nonrecombining region, are important for understanding its evolution. Here, we describe analyses of PoolSeq data in samples from within multiple natural populations from Trinidad, yielding new results that support previous evidence for occasional recombination between the guppy Y and X. We detected recent demographic changes, notably that downstream populations have higher synonymous site diversity than upstream ones and other expected signals of bottlenecks. We detected evidence of associations between sequence variants and the sex-determining locus, rather than divergence under a complete lack of recombination. Although recombination is infrequent, it is frequent enough that associations with SNPs can suggest the region in which the sex-determining locus must be located. Diversity is elevated across a physically large region of the sex chromosome, conforming to predictions for a genome region with infrequent recombination that carries one or more sexually antagonistic polymorphisms. However, no consistently male-specific variants were found, supporting the suggestion that any completely sex-linked region may be very small.
Abstract.
Author URL.
Galluccio E, Lymbery RA, Wilson A, Evans JP (2022). Personality, sperm traits and a test for their combined dependence on male condition in guppies.
ROYAL SOCIETY OPEN SCIENCE,
9(6).
Author URL.
Yong L, Croft DP, Troscianko J, Ramnarine IW, Wilson AJ (2022). Sensory-based quantification of male colour patterns in Trinidadian guppies reveals no support for parallel phenotypic evolution in multivariate trait space.
Mol Ecol,
31(5), 1337-1357.
Abstract:
Sensory-based quantification of male colour patterns in Trinidadian guppies reveals no support for parallel phenotypic evolution in multivariate trait space.
Parallel evolution, in which independent populations evolve along similar phenotypic trajectories, offers insights into the repeatability of adaptive evolution. Here, we revisit a classic example of parallelism, that of repeated evolution of brighter males in the Trinidadian guppy (Poecilia reticulata). In guppies, colonisation of low predation habitats is associated with emergence of 'more colourful' phenotypes since predator-induced viability selection for crypsis weakens while sexual selection by female preference for conspicuousness remains strong. Our study differs from previous investigations in three respects. First, we adopted a multivariate phenotyping approach to characterise parallelism in multitrait space. Second, we used ecologically-relevant colour traits defined by the visual systems of the two selective agents (i.e. guppy, predatory cichlid). Third, we estimated population genetic structure to test for adaptive (parallel) evolution against a model of neutral phenotypic divergence. We find strong phenotypic differentiation that is inconsistent with a neutral model but very limited support for the predicted pattern of greater conspicuousness at low predation. Effects of predation regime on each trait were in the expected direction, but weak, largely nonsignificant, and explained little among-population variation. In multitrait space, phenotypic trajectories of lineages colonising low from high predation regimes were not parallel. Our results are consistent with reduced predation risk facilitating adaptive differentiation, potentially by female choice, but suggest that this proceeds in independent directions of multitrait space across lineages. Pool-sequencing data also revealed SNPs showing greater differentiation than expected under neutrality, among which some are found in genes contributing to colour pattern variation, presenting opportunities for future genetic study.
Abstract.
Author URL.
Boonekamp J, Rodríguez-Muñoz R, Hopwood P, Zuidersma E, Mulder E, Wilson A, Verhulst S, Tregenza T (2022). Telomere length is highly heritable and independent of growth rate manipulated by temperature in field crickets.
Mol Ecol,
31(23), 6128-6140.
Abstract:
Telomere length is highly heritable and independent of growth rate manipulated by temperature in field crickets.
Many organisms are capable of growing faster than they do. Restrained growth rate has functionally been explained by negative effects on lifespan of accelerated growth. However, the underlying mechanisms remain elusive. Telomere attrition has been proposed as a causal agent and has been mostly studied in endothermic vertebrates. We established that telomeres exist as chromosomal-ends in a model insect, the field cricket Gryllus campestris, using terminal restriction fragment and Bal 31 methods. Telomeres comprised TTAGGn repeats of 38 kb on average, more than four times longer than the telomeres of human infants. Bal 31 assays confirmed that telomeric repeats were located at the chromosome-ends. We tested whether rapid growth between day 1, day 65, day 85, and day 125 is achieved at the expense of telomere length by comparing nymphs reared at 23°C with their siblings reared at 28°C, which grew three times faster in the initial 65 days. Surprisingly, neither temperature treatment nor age affected average telomere length. Concomitantly, the broad sense heritability of telomere length was remarkably high at ~100%. Despite high heritability, the evolvability (a mean-standardized measure of genetic variance) was low relative to that of body mass. We discuss our findings in the context of telomere evolution. Some important features of vertebrate telomere biology are evident in an insect species dating back to the Triassic. The apparent lack of an effect of growth rate on telomere length is puzzling, suggesting strong telomere length maintenance during the growth phase. Whether such maintenance of telomere length is adaptive remains elusive and requires further study investigating the links with fitness in the wild.
Abstract.
Author URL.
Sharman P (2022). Understanding the Genetics of Thoroughbred Racehorse Speed.
Abstract:
Understanding the Genetics of Thoroughbred Racehorse Speed
Long before the publication of Darwin’s theory of evolution by natural selection and Mendel’s work on genes, horses were being selectively bred for improved racing performance. This resulted in the creation of a highly specialised breed of racing horse, known as the thoroughbred. Throughout the 19th century the winning times of the most elite thoroughbred races in Great Britain declined, suggesting genetic evolution of faster speed was ongoing in response to selective breeding. However, several studies have reported a slowing of the rate of improvement since early in the 20th century, leading to a consensus amongst scientists and industry experts that thoroughbred speed has reached a selection limit. The broad aims of my PhD thesis are to understand the genetic basis of variation in racehorse speed, and in doing so, to determine if thoroughbreds have indeed reached a genetic limit for how fast they can run. If so, what is constraining further improvement? Moreover, can a better understanding of the factors that determine the rate of improvement in thoroughbred speed allow us to design breeding programmes that would overcome this supposed limit? to do this, I apply quantitative genetic tools, developed for improving livestock since the mid-19th century but largely passed over by thoroughbred breeders, to a vast pedigreed dataset of thoroughbred performances in Great Britain. Firstly, addressing limitations of previous studies, I set out to characterise more accurately the current and historical rate of phenotypic improvement in thoroughbred speed. Secondly, I apply quantitative genetic analysis to determine the extent of heritable variation for this trait and assess whether phenotypic rates of improvement in speed - if still ongoing - are underpinned by a genetic response to selection. Next, I investigate the possibility that maternal and/or paternal age at conception may affect offspring racehorse speed and examine whether parental identity is an important source of variation in offspring performance. If so, is there any genetic basis of maternal or paternal variation identified, and what are the implications for selection response? Finally, in an essay I explore the history of equine (and jockey) welfare concerns in the sport, and consider the role quantitative genetics could play in reducing equine injury susceptibility alongside improving performance. Lastly, I discuss my findings and consider future directions for this research.
Abstract.
Hunter DC, Ashraf B, Bérénos C, Ellis PA, Johnston SE, Wilson AJ, Pilkington JG, Pemberton JM, Slate J (2022). Using genomic prediction to detect microevolutionary change of a quantitative trait.
Proc Biol Sci,
289(1974).
Abstract:
Using genomic prediction to detect microevolutionary change of a quantitative trait.
Detecting microevolutionary responses to natural selection by observing temporal changes in individual breeding values is challenging. The collection of suitable datasets can take many years and disentangling the contributions of the environment and genetics to phenotypic change is not trivial. Furthermore, pedigree-based methods of obtaining individual breeding values have known biases. Here, we apply a genomic prediction approach to estimate breeding values of adult weight in a 35-year dataset of Soay sheep (Ovis aries). Comparisons are made with a traditional pedigree-based approach. During the study period, adult body weight decreased, but the underlying genetic component of body weight increased, at a rate that is unlikely to be attributable to genetic drift. Thus cryptic microevolution of greater adult body weight has probably occurred. Genomic and pedigree-based approaches gave largely consistent results. Thus, using genomic prediction to study microevolution in wild populations can remove the requirement for pedigree data, potentially opening up new study systems for similar research.
Abstract.
Author URL.
2021
Capilla-Lasheras P, Harrison X, Wood EM, Wilson AJ, Young AJ (2021). Altruistic bet-hedging and the evolution of cooperation in a Kalahari bird.
Science Advances,
7(39).
Abstract:
Altruistic bet-hedging and the evolution of cooperation in a Kalahari bird
Striking effects of cooperation on the reproductive variance of relatives help to explain the global biogeography of altruism.
Abstract.
Marjamäki P, Dugdale HL, Delahay R, McDonald R, Wilson A (2021). Data from Marjamaki et al 2021 J Evol Biol, Genetic, social and maternal contributions to Mycobacterium bovis infection status in European badgers (Meles meles).
Okada K, Katsuki M, Sharma MD, Kiyose K, Seko T, Okada Y, Wilson AJ, Hosken DJ (2021). Natural selection increases female fitness by reversing the exaggeration of a male sexually selected trait.
Nature Communications,
12(1).
Abstract:
Natural selection increases female fitness by reversing the exaggeration of a male sexually selected trait
AbstractTheory shows how sexual selection can exaggerate male traits beyond naturally selected optima and also how natural selection can ultimately halt trait elaboration. Empirical evidence supports this theory, but to our knowledge, there have been no experimental evolution studies directly testing this logic, and little examination of possible associated effects on female fitness. Here we use experimental evolution of replicate populations of broad-horned flour beetles to test for effects of sex-specific predation on an exaggerated sexually selected male trait (the mandibles), while also testing for effects on female lifetime reproductive success. We find that populations subjected to male-specific predation evolve smaller sexually selected mandibles and this indirectly increases female fitness, seemingly through intersexual genetic correlations we document. Predation solely on females has no effects. Our findings support fundamental theory, but also reveal unforseen outcomes—the indirect effect on females—when natural selection targets sex-limited sexually selected characters.
Abstract.
Fokkema RW, Korsten P, Schmoll T, Wilson AJ (2021). Social competition as a driver of phenotype–environment correlations: implications for ecology and evolution.
Biological Reviews,
96(6), 2561-2572.
Abstract:
Social competition as a driver of phenotype–environment correlations: implications for ecology and evolution
While it is universally recognised that environmental factors can cause phenotypic trait variation via phenotypic plasticity, the extent to which causal processes operate in the reverse direction has received less consideration. In fact individuals are often active agents in determining the environments, and hence the selective regimes, they experience. There are several important mechanisms by which this can occur, including habitat selection and niche construction, that are expected to result in phenotype–environment correlations (i.e. non-random assortment of phenotypes across heterogeneous environments). Here we highlight an additional mechanism – intraspecific competition for preferred environments – that may be widespread, and has implications for phenotypic evolution that are currently underappreciated. Under this mechanism, variation among individuals in traits determining their competitive ability leads to phenotype–environment correlation; more competitive phenotypes are able to acquire better patches. Based on a concise review of the empirical evidence we argue that competition-induced phenotype–environment correlations are likely to be common in natural populations before highlighting the major implications of this for studies of natural selection and microevolution. We focus particularly on two central issues. First, competition-induced phenotype–environment correlation leads to the expectation that positive feedback loops will amplify phenotypic and fitness variation among competing individuals. As a result of being able to acquire a better environment, winners gain more resources and even better phenotypes – at the expense of losers. The distinction between individual quality and environmental quality that is commonly made by researchers in evolutionary ecology thus becomes untenable. Second, if differences among individuals in competitive ability are underpinned by heritable traits, competition results in both genotype–environment correlations and an expectation of indirect genetic effects (IGEs) on resource-dependent life-history traits. Theory tells us that these IGEs will act as (partial) constraints, reducing the amount of genetic variance available to facilitate evolutionary adaptation. Failure to recognise this will lead to systematic overestimation of the adaptive potential of populations. To understand the importance of these issues for ecological and evolutionary processes in natural populations we therefore need to identify and quantify competition-induced phenotype–environment correlations in our study systems. We conclude that both fundamental and applied research will benefit from an improved understanding of when and how social competition causes non-random distribution of phenotypes, and genotypes, across heterogeneous environments.
Abstract.
Prentice P (2021). The evolution of animal “intelligence”: Among-individual differences and the heritable basis of cognitive and personality (co)variation in the Trinidadian guppy (Poecilia reticulata).
Abstract:
The evolution of animal “intelligence”: Among-individual differences and the heritable basis of cognitive and personality (co)variation in the Trinidadian guppy (Poecilia reticulata)
Among-individual variation in cognition is common within populations, and has been demonstrated across a range of animal taxa. From an evolutionary perspective, this variation is a pre-requisite for natural selection and genetic variation – both of which are required for adaptive evolution to occur. Selection has been hypothesised to favour high cognitive performance, however directional selection would be expected to erode genetic (and among-individual) variation over time. Furthermore, as selection does not act on traits in isolation, understanding the extent to which cognitive traits covary with other aspects of phenotype (e.g. personality traits) is an important factor. The question of how among-individual variation is maintained is therefore central to our understanding of the adaptive evolution of cognition in the context of the wider phenotype. The overall aim of my PhD thesis was to study the evolutionary biology of among-individual variation in cognitive and personality traits, and to explore the relationship between them in the Trinidadian guppy (Poecilia reticulata). I aimed to characterise among-individual differences in cognitive performance and personality, and investigate the extent to which genetic variation contributes to these, and to relationships between them. Each chapter was intended to obtain novel insights into the mechanisms explaining the existence and maintenance of these two important facets of behaviour across multiple hierarchical levels. I advocate the use of quantitative genetic style modelling approaches throughout, and seek to highlight the value of multivariate approaches to investigating animal cognition and associated behavioural traits. Firstly, relationships between cognition and personality were explored at the among-individual level, using a measure of cognitive performance in a spatial learning task and a stress-related behavioural trait. Secondly, to further scrutinise links between cognition and personality, the multivariate structure of among-individual variation in cognitive performance across different domains was investigated in addition to variation in personality trait ‘boldness’. Next, among-individual and genetic variation in phenotypic ‘predictability’ (within-individual variation) of a stress-related behavioural trait was analysed using a novel form of ‘double hierarchical’ model. I then explored whether genetic variation contributes to among-individual differences in cognitive performance in a detour reaching task, and further investigated whether an interplay by genotype-by-environment interactions contributed to this variation. and finally, I discuss these results and how they contribute to our understanding of the causes of among-individual variation in cognitive performance, in addition to their evolutionary implications and ideas for future work.
Abstract.
Kyle-Henney M (2021). The roles of Green Fluorescent Proteins and photo-acclimation on the physiological and behavioural responses of Anemonia viridis.
Abstract:
The roles of Green Fluorescent Proteins and photo-acclimation on the physiological and behavioural responses of Anemonia viridis
Studying the fundamental relationships between marine organisms is vital in determining the biological implications of changing environments. In many cases, these environments are underpinned by photosynthetic primary production, and directly affected by variation in abiotic stressors such as light condition and temperature. Photosymbiotic relationships between unicellular plants and multicellular animals are well studied, yet their complexity and interspecies variation leaves many questions unanswered. Respirometry is a well-known method for quantifying physiological impacts of these stressors, however, commercially available respirometry equipment has significant limitations. Chapter 1 therefore describes a novel open source (OS) photo-respirometer to reduce these limitations, whilst maintaining comparable precision and accuracy to explore complex ecological relationships. A temperate example of the algae-cnidarian symbiosis was used to showcase the data collection ability of our photo-respirometer. Results suggest that the photosynthetic efficiency of A. viridis – Symbiodinium symbioses may be influenced by light intensity, acclimation condition and the presence or absence of green fluorescent proteins (GFPs). This first study concludes that the photo-respirometer is a viable alternative to commercial systems and would be advantageous as a single base apparatus for multiple metabolic studies within marine contexts. Chapter 2 explores the behavioural implications of GFP expression and acclimation condition on phototactic responses of A. viridis to light intensity gradients. Phototactic responses did not differ between morphs, suggesting that GFP expression may have alternative functions or be a vestigial trait in this species. Acclimation to low light intensity elicited the greatest phototactic responses but is potentially influenced by water flow direction. This suggests that either water movement or oxygen concentration are limiting factors for phototaxis in temperate cnidarian-algal symbioses and should be the focus of future studies.
Abstract.
2020
McCain SC, Kopelic S, Houslay TM, Wilson AJ, Lu H, Earley RL (2020). Choice consequences: Salinity preferences and hatchling survival in the mangrove rivulus fish (Kryptolebias marmoratus).
J Exp BiolAbstract:
Choice consequences: Salinity preferences and hatchling survival in the mangrove rivulus fish (Kryptolebias marmoratus).
In heterogeneous environments, mobile species should occupy habitats in which their fitness is maximized. Mangrove rivulus fish inhabit mangrove ecosystems where salinities range from 0-65 ppt but are most often collected at ∼25 ppt. We examined rivulus' salinity preference in a lateral salinity gradient, in the absence of predators and competitors. Fish could swim freely for 8 hours throughout the gradient with chambers containing salinities from 5-45 ppt (or 25 ppt throughout, control). We defined preference as the salinity in which the fish spent most of their time, and also measured preference strength, latency to begin exploring the arena, and number of transitions between chambers. To determine whether these traits were repeatable, each fish experienced three trials. Rivulus spent a greater proportion of time in salinities lower (5-15 ppt) than they occupy in the wild. Significant among-individual variation in the (multivariate) behavioral phenotype emerged when animals experienced the gradient, indicating strong potential for selection to drive behavioral evolution in areas with diverse salinity microhabitats. We also showed that rivulus had a significantly greater probability of laying eggs in low salinities compared to control or high salinities. Eggs laid in lower salinities also had higher hatching success compared to those laid in higher salinities. Thus, although rivulus can tolerate a wide range of salinities, they prefer low salinities. These results raise questions about factors that prevent rivulus from occupying lower salinities in the wild, whether higher salinities impose energetic costs, and whether fitness changes as a function of salinity.
Abstract.
Author URL.
Lane SM, Briffa M, Wilson AJ, Truebano M, Foster NL (2020). Evidence of fostering in an internally brooding sea anemone.
Ethology,
126(12), 1141-1147.
Abstract:
Evidence of fostering in an internally brooding sea anemone
Evidence of alloparental care during the incubation stage has largely been demonstrated for species that incubate their offspring externally in a nest. Alloparental care in these species generally consists of the rearing of mixed broods which contain a low proportion of “foreign” young alongside the host's own offspring. However, many animals, including sea anemones, incubate offspring either on or within their bodies. The beadlet anemone Actinia equina incubate their young internally, and as many sea anemones are capable of reproducing both sexually and asexually, the origin of these internally brooded young has been the subject of much debate. While genetically identical young are brooded internally under the juvenile stage, it is thought that those produced sexually are released as larvae into the water and must return to the gastric cavity of an adult in order for metamorphosis to occur. As the likelihood of a planula larva finding its way back to its parent is slim, this suggests that alloparental care may play a role in the survival of juveniles in this species, a hypothesis first suggested a century ago but rarely tested. Here, using highly polymorphic microsatellite markers, we find evidence of alloparental care in A. equina. Our results indicate that while a high proportion of juveniles were genetically identical to their brooding adult, the remaining juveniles showed stark genetic differences to their brooding adult. These juveniles shared far fewer alleles with their “parent” than expected under sexual reproduction, indicating that they were not the adult's offspring. Furthermore, we found variation in the genetic composition of broods, which consisted either of (a) entirely genetically identical individuals, (b) a mix of unique individuals and clonemates or (c) entirely unique individuals, that is no shared genotype. Our results thus indicate that adult A. equina tolerate the presence of non-offspring within their gastric cavity and furthermore that they may incubate entirely “foreign” broods.
Abstract.
Bonneaud C, Tardy L, Hill GE, McGraw KJ, Wilson AJ, Giraudeau M (2020). Experimental evidence for stabilizing selection on virulence in a bacterial pathogen.
Evolution Letters,
4(6), 491-501.
Abstract:
Experimental evidence for stabilizing selection on virulence in a bacterial pathogen
Abstract
. The virulence-transmission trade-off hypothesis has provided a dominant theoretical basis for predicting pathogen virulence evolution, but empirical tests are rare, particularly at pathogen emergence. The central prediction of this hypothesis is that pathogen fitness is maximized at intermediate virulence due to a trade-off between infection duration and transmission rate. However, obtaining sufficient numbers of pathogen isolates of contrasting virulence to test the shape of relationships between key pathogen traits, and doing so without the confounds of evolved host protective immunity (as expected at emergence), is challenging. Here, we inoculated 55 isolates of the bacterial pathogen, Mycoplasma gallisepticum, into non-resistant house finches (Haemorhous mexicanus) from populations that have never been exposed to the disease. Isolates were collected over a 20-year period from outbreak in disease-exposed populations of house finches and vary markedly in virulence. We found a positive linear relationship between pathogen virulence and transmission rate to an uninfected sentinel, supporting the core assumption of the trade-off hypothesis. Further, in support of the key prediction, there was no evidence for directional selection on a quantitative proxy of pathogen virulence and, instead, isolates of intermediate virulence were fittest. Surprisingly, however, the positive relationship between virulence and transmission rate was not underpinned by variation in pathogen load or replication rate as is commonly assumed. Our results indicate that selection favors pathogens of intermediate virulence at disease emergence in a novel host species, even when virulence and transmission are not linked to pathogen load.
Abstract.
Langley EJG, Adams G, Beardsworth CE, Dawson DA, Laker PR, van Horik JO, Whiteside MA, Wilson AJ, Madden JR (2020). Heritability and correlations among learning and inhibitory control traits.
Behavioral Ecology,
31(3), 798-806.
Abstract:
Heritability and correlations among learning and inhibitory control traits
AbstractTo understand the evolution of cognitive abilities, we need to understand both how selection acts upon them and their genetic (co)variance structure. Recent work suggests that there are fitness consequences for free-living individuals with particular cognitive abilities. However, our current understanding of the heritability of these abilities is restricted to domesticated species subjected to artificial selection. We investigated genetic variance for, and genetic correlations among four cognitive abilities: inhibitory control, visual and spatial discrimination, and spatial ability, measured on &gt;450 pheasants, Phasianus colchicus, over four generations. Pheasants were reared in captivity but bred from adults that lived in the wild and hence, were subject to selection on survival. Pheasant chicks are precocial and were reared without parents, enabling us to standardize environmental and parental care effects. We constructed a pedigree based on 15 microsatellite loci and implemented animal models to estimate heritability. We found moderate heritabilities for discrimination learning and inhibitory control (h2 = 0.17–0.23) but heritability for spatial ability was low (h2 = 0.09). Genetic correlations among-traits were largely positive but characterized by high uncertainty and were not statistically significant. Principle component analysis of the genetic correlation matrix estimate revealed a leading component that explained 69% of the variation, broadly in line with expectations under a general intelligence model of cognition. However, this pattern was not apparent in the phenotypic correlation structure which was more consistent with a modular view of animal cognition. Our findings highlight that the expression of cognitive traits is influenced by environmental factors which masks the underlying genetic structure.
Abstract.
Okada K, Katsuki M, Sharma MD, Kiyose K, Seko T, Okada Y, Wilson AJ, Hosken DJ (2020). Natural selection reverses the exaggeration of a male sexually selected trait, which increases female fitness.
Wang D, Forstmeier W, Martin K, Wilson A, Kempenaers B (2020). The role of genetic constraints and social environment in explaining female extra-pair mating.
Evolution,
74(3), 544-558.
Abstract:
The role of genetic constraints and social environment in explaining female extra-pair mating.
Why do females of socially monogamous species engage in extra-pair copulations? This long-standing question remains a puzzle, because the benefits of female promiscuous behavior often do not seem to outweigh the costs. Genetic constraint models offer an answer by proposing that female promiscuity emerges through selection favoring alleles that are either beneficial for male reproductive success (intersexual pleiotropy hypothesis) or beneficial for female fecundity (intrasexual pleiotropy hypothesis). A previous quantitative genetic study on captive zebra finches, Taeniopygia guttata, reported support for the first, but not for the second hypothesis. Here, we re-examine both hypotheses based on data from lines selected for high and low male courtship rate. In contrast to previous conclusions, our new analyses clearly reject the hypothesis that male and female promiscuity are genetically homologous traits. We find some support for a positive genetic correlation between female promiscuity and fecundity. This study also shows that the behavioral outcome of extra-pair courtships primarily depends on individual-specific female preferences and not on the "attractiveness" of the social mate. In contrast, patterns of paternity are strongly influenced by the social partner and the pair bond, presumably reflecting variation in copulation behavior, fertility, or sperm competitiveness.
Abstract.
Author URL.
2019
Styga JM, Houslay TM, Wilson AJ, Earley RL (2019). Correction: Development of G: a test in an amphibious fish (Heredity, (2019), 122, 5, (696-708), 10.1038/s41437-018-0152-4).
Heredity,
122(5), 709-710.
Abstract:
Correction: Development of G: a test in an amphibious fish (Heredity, (2019), 122, 5, (696-708), 10.1038/s41437-018-0152-4)
Figure 3 legend has been corrected to state: “Difference matrices for pairwise-trait phenotypic correlations (rP, below diagonal) and pairwise-trait genetic correlations (rG, above diagonal) from 1, 15, and 100 DPH. Differences are color coded by strength and direction. Differences shown in gray are positive and differences shown in black are negative. When ages are similar, the colored square is small; when ages are very different, the colored square fills the cell. EPL Epural length, EPA epural angle, PHPL parahypural length, PHPA parahypural angle, HYPL hypural length, HYPW hypural width, and SL standard length.”.
Abstract.
Evans JP, Wilson AJ, Pilastro A, Garcia-Gonzalez F (2019). Ejaculate-mediated paternal effects: evidence, mechanisms and evolutionary implications.
REPRODUCTION,
157(4), R109-R126.
Author URL.
Bonneaud C, Tardy L, Giraudeau M, Hill GE, McGraw KJ, Wilson AJ (2019). Evolution of both host resistance and tolerance to an emerging bacterial pathogen.
EVOLUTION LETTERS,
3(5), 544-554.
Author URL.
Parry JVC (2019). The Genetic Basis of Phenotypic Plasticity in Maternal Investment: a Quantitative Genetic Study utilising Nutritional Geometry in the Cockroach Naupheota cinerea.
Abstract:
The Genetic Basis of Phenotypic Plasticity in Maternal Investment: a Quantitative Genetic Study utilising Nutritional Geometry in the Cockroach Naupheota cinerea
Phenotypic plasticity is fundamental in the evolutionary process, as it allows a single genotype to display different phenotypes in response to novel environments. There is a large body of research that demonstrates the ways in which phenotypic plasticity can influence evolution, such as by permitting persistence in novel environments and revealing cryptic genetic variation, which can become genetically assimilated into a population. When plastic responses within a population differ among genotypes, a genotype by environment interaction (GxE) will exist and phenotypic plasticity will have a genetic basis of variation. This genetic basis means that plastic traits are heritable and therefore selection can target both the phenotype that plasticity produces and the plastic response itself. By better understanding the genetic basis of plasticity, the scientific community can hope to further our understanding of the evolutionary process, including how plastic traits are inherited across generations.
In this thesis, I use nutritional geometry to examine the role that dietary environment plays in the phenotypic plasticity of maternal investment in the cockroach Nauphoeta cinerea. By creating a half-sib pedigree, I was able to use quantitative genetics to control for individual genotypes, allowing half-siblings to be reared in different nutritional environments (a split brood half-sib design) to judge whether maternal investment varies plastically in response to the nutritional environment, and whether this plasticity has a genetic basis. I used diet eaten per day, gestation period, clutch size, and offspring lipid proportion to measure maternal investment in this study. Specifically, I used two holidic (i.e. chemically defined) diets, one with high carbohydrate content and one with low carbohydrate content, to provide different nutritional environments for the female cockroaches in the experiment. It has previously been shown that many reproductive traits, including gestation period, lipid investment into offspring, and clutch size, for N. cinerea are maximised on high carbohydrate diets, and thus I deemed the high carbohydrate diet a ‘high’ nutritional treatment, and the low carbohydrate a ‘low’ nutritional treatment. I found evidence of phenotypic plasticity in all four of the traits I measured, and evidence of a genetic basis for plasticity (GxE) in diet eaten per day and offspring lipid proportion, but not for gestation period or clutch size.
Overall, my thesis provides evidence for a genetic basis of phenotypic plasticity variation in two traits that are fundamentally important for the fitness of an organism, diet eaten per day and offspring lipid proportion. I discovered that maternal investment in N. cinerea responds plastically to the nutritional environment, in that a single genotype can display different phenotypes depending on the diet they receive. As these two traits are linked to fitness and each other, my findings provide evidence that the plastic response to environmental conditions could evolve, producing organisms better able to persist and reproduce in a range of nutritional environments. My findings also support the theory that the role of phenotypic plasticity should be discussed in the Extended Synthesis for the evolutionary process, as these plastic traits are heritable and two show evidence of a basis in the genotype of the organism. Better understanding of the role phenotypic plasticity plays in the evolutionary process could allow us to predict population responses to changing environments, such as those presented by global climate change.
Abstract.
Hosken DJ, Wilson A (2019). The problem of measuring trait-preference correlations without disrupting them. Behavioral Ecology, 30(6), 1518-1521.
White S, Pascall D, Wilson A (2019). Towards a comparative approach to the structure of animal personality variation. Behavioral Ecology
Dall SRX, McNamara JM, Wilson AJ (2019). Ultimate (Re)Thinking for Behavioural Biology. In Hunt J, Hosken DJ, Wedell N (Eds.)
Genes and Behaviour: Beyond Nature-Nurture, Chichester, UK: John Wiley & Sons Ltd, 11-25.
Abstract:
Ultimate (Re)Thinking for Behavioural Biology
Abstract.
2018
Houslay TH, Wilson A (2018). Data from Houslay et al. Title: Habituation and individual variation in the endocrine stress response in the Trinidadian guppy (Poecilia reticulata). General and Comparative Endocrinology.
Hunt J, Rapkin J, Jensen K, House CM, Wilson AJ (2018). Genotype-by-sex-by-diet interactions for nutritional preference, dietary consumption, and lipid deposition in a field cricket.
Heredity (Edinb),
121(4), 361-373.
Abstract:
Genotype-by-sex-by-diet interactions for nutritional preference, dietary consumption, and lipid deposition in a field cricket.
Changes in feeding behaviour, especially the overconsumption of calories, has led to a rise in the rates of obesity, diabetes, and other associated disorders in humans and a range of animals inhabiting human-influenced environments. However, understanding the relative contribution of genes, the nutritional environment, and their interaction to dietary intake and lipid deposition in the sexes still remains a major challenge. By combining nutritional geometry with quantitative genetics, we determined the effect of genes, the nutritional environment, and their interaction on the total nutritional preference (TP), total diet eaten (TE), and lipid mass (LM) of male and female black field crickets (Teleogryllus commodus) fed one of four diet pairs (DPs) differing in the ratio of protein to carbohydrate and total nutritional content. We found abundant additive genetic variance for TP, TE, and LM in both sexes and across all four DPs, with significant genetic correlations between TE and TP and between TP and LM in males. We also found significant genotype-by-DP and genotype-by-sex-by-DP interactions for each trait and significant genotype-by-sex interactions for TE and LM. Complex interactions between genes, sex, and the nutritional environment, therefore, play an important role in nutrient regulation and lipid deposition in T. commodus. This finding may also help explain the increasing rate of obesity and the maintenance of sex differences in obesity observed across many animal species, including humans.
Abstract.
Author URL.
Smithers SP, Rooney R, Wilson A, Stevens M (2018). Rock pool fish use a combination of colour change and substrate choice to improve camouflage.
Animal Behaviour,
144, 53-65.
Abstract:
Rock pool fish use a combination of colour change and substrate choice to improve camouflage
Camouflage can be achieved by both morphological (e.g. colour, brightness and pattern change) and behavioural (e.g. substrate preference) means. Much of the research on behavioural background matching has been conducted on species with fixed coloration and body patterns, while less is known about the role background choice plays in species capable of rapid (within minutes or seconds) colour change. One candidate species is the rock goby, Gobius paganellus, a common rock pool fish capable of rapid changes in colour and brightness when placed on different backgrounds. However, their ability to match different backgrounds is not unbounded, with some colours and brightness being easier to match than others, thus raising the possibility that gobies may use behavioural background matching to make up for their limited ability to match certain backgrounds. We used digital image analysis and a model of predator vision to investigate the ability of rock gobies to match chromatic (beige and greenish-grey) and achromatic (varying brightness) backgrounds. We then conducted choice experiments to determine whether gobies exhibited a behavioural preference for the backgrounds they were best at matching. Gobies rapidly changed their colour and brightness when placed on the different backgrounds. However, the level of camouflage differed between backgrounds: fish were better at matching beige than greenish-grey, and darker than lighter backgrounds. When given the choice, gobies displayed a behavioural preference for the backgrounds they were best at matching. Our findings therefore show that rock gobies, and probably other animals, use a combination of morphological and behavioural means to achieve camouflage and in doing so mitigate limitations in either approach alone.
Abstract.
Houslay TM, Prentice P, White SJ, Young AJ, Earley RL, Wilson AJ (2018). The Quantitative Genetics of Stress Coping Styles in the Trinidadian Guppy.
Author URL.
White S, Wilson A (2018). White and Wilson 2018 Data from Evolutionary genetics of personality in the Trinidadian guppy I.
White S, Houslay T, Wilson A (2018). White et al 2018 Data from Evolutionary genetics of personality in the Trinidadian guppy II.
2017
Maraqa MS, Griffin R, Sharma MD, Wilson AJ, Hunt J, Hosken DJ, House CM (2017). Constrained evolution of the sex comb in Drosophila simulans.
J Evol Biol,
30(2), 388-400.
Abstract:
Constrained evolution of the sex comb in Drosophila simulans.
Male fitness is dependent on sexual traits that influence mate acquisition (precopulatory sexual selection) and paternity (post-copulatory sexual selection), and although many studies have documented the form of selection in one or the other of these arenas, fewer have done it for both. Nonetheless, it appears that the dominant form of sexual selection is directional, although theoretically, populations should converge on peaks in the fitness surface, where selection is stabilizing. Many factors, however, can prevent populations from reaching adaptive peaks. Genetic constraints can be important if they prevent the development of highest fitness phenotypes, as can the direction of selection if it reverses across episodes of selection. In this study, we examine the evidence that these processes influence the evolution of the multivariate sex comb morphology of male Drosophila simulans. To do this, we conduct a quantitative genetic study together with a multivariate selection analysis to infer how the genetic architecture and selection interact. We find abundant genetic variance and covariance in elements of the sex comb. However, there was little evidence for directional selection in either arena. Significant nonlinear selection was detected prior to copulation when males were mated to nonvirgin females, and post-copulation during sperm offence (again with males mated to nonvirgins). Thus, contrary to our predictions, the evolution of the D. simulans sex comb is limited neither by genetic constraints nor by antagonistic selection between pre- and post-copulatory arenas, but nonlinear selection on the multivariate phenotype may prevent sex combs from evolving to reach some fitness maximizing optima.
Abstract.
Author URL.
Hayward AD, Pemberton JM, Berenos C, Wilson AJ, Pilkington JG, Kruuk LEB (2017). EVIDENCE FOR SELECTION-BY-ENVIRONMENT BUT NOT GENOTYPE-BY-ENVIRONMENT INTERACTIONS FOR FITNESS-RELATED TRAITS IN a WILD
MAMMAL POPULATION. Genetics, 208 (1), 349-364.
Cabrera D, Andres D, McLoughlin PD, Debeffe L, Medill SA, Wilson AJ, Poissant J (2017). Island tameness and the repeatability of flight initiation distance in a large herbivore.
CANADIAN JOURNAL OF ZOOLOGY,
95(10), 771-778.
Author URL.
Smithers SP, Wilson A, Stevens M (2017). Rock pool gobies change their body pattern in response to background features. Biological Journal of the Linnean Society, 121, 109-121.
Houslay T, Vierbuchen M, Grimmer AJ, Young AJ, Wilson A (2017). Testing the stability of behavioural coping style across stress contexts in the Trinidadian guppy. Functional Ecology
2016
Benton CH, Delahay RJ, Robertson A, McDonald RA, Wilson AJ, Burke TA, Hodgson D (2016). Blood thicker than water: kinship, disease prevalence and group size drive divergent patterns of infection risk in a social mammal.
Proc Biol Sci,
283(1835).
Abstract:
Blood thicker than water: kinship, disease prevalence and group size drive divergent patterns of infection risk in a social mammal.
The importance of social- and kin-structuring of populations for the transmission of wildlife disease is widely assumed but poorly described. Social structure can help dilute risks of transmission for group members, and is relatively easy to measure, but kin-association represents a further level of population sub-structure that is harder to measure, particularly when association behaviours happen underground. Here, using epidemiological and molecular genetic data from a wild, high-density population of the European badger (Meles meles), we quantify the risks of infection with Mycobacterium bovis (the causative agent of tuberculosis) in cubs. The risk declines with increasing size of its social group, but this net dilution effect conceals divergent patterns of infection risk. Cubs only enjoy reduced risk when social groups have a higher proportion of test-negative individuals. Cubs suffer higher infection risk in social groups containing resident infectious adults, and these risks are exaggerated when cubs and infectious adults are closely related. We further identify key differences in infection risk associated with resident infectious males and females. We link our results to parent-offspring interactions and other kin-biased association, but also consider the possibility that susceptibility to infection is heritable. These patterns of infection risk help to explain the observation of a herd immunity effect in badgers following low-intensity vaccination campaigns. They also reveal kinship and kin-association to be important, and often hidden, drivers of disease transmission in social mammals.
Abstract.
Author URL.
Sharma MD, Wilson AJ, Hosken DJ (2016). Fisher's sons' effect in sexual selection: absent, intermittent or just low experimental power?.
J Evol Biol,
29(12), 2464-2470.
Abstract:
Fisher's sons' effect in sexual selection: absent, intermittent or just low experimental power?
The Fisherian sexual selection paradigm has been called the null model of sexual selection. At its heart is the expectation of a genetic correlation (rG ) between female preference and male trait. However, recent meta-analysis has shown estimated correlations are often extremely weak and not statistically significant. We show here that systematic failure of studies to reject the null hypothesis that rG = 0 is almost certainly due to the low power of most experimental designs used. We provide an easy way to assess experimental power a priori and suggest that current data make it difficult to definitively test a key component of the Fisher effect.
Abstract.
Author URL.
Wilson AJ, Poissant J (2016). Quantitative Genetics in Natural Populations. In (Ed)
Encyclopedia of Evolutionary Biology, 361-371.
Abstract:
Quantitative Genetics in Natural Populations
Abstract.
Pascoal S, Mendrok M, Mitchell C, Wilson AJ, Hunt J, Bailey NW (2016). Sexual selection and population divergence I: the influence of socially flexible cuticular hydrocarbon expression in male field crickets (Teleogryllus oceanicus).
Evolution,
70(1), 82-97.
Abstract:
Sexual selection and population divergence I: the influence of socially flexible cuticular hydrocarbon expression in male field crickets (Teleogryllus oceanicus).
Debates about how coevolution of sexual traits and preferences might promote evolutionary diversification have permeated speciation research for over a century. Recent work demonstrates that the expression of such traits can be sensitive to variation in the social environment. Here, we examined social flexibility in a sexually selected male trait-cuticular hydrocarbon (CHC) profiles-in the field cricket Teleogryllus oceanicus and tested whether population genetic divergence predicts the extent or direction of social flexibility in allopatric populations. We manipulated male crickets' social environments during rearing and then characterized CHC profiles. CHC signatures varied considerably across populations and also in response to the social environment, but our prediction that increased social flexibility would be selected in more recently founded populations exposed to fluctuating demographic environments was unsupported. Furthermore, models examining the influence of drift and selection failed to support a role of sexual selection in driving population divergence in CHC profiles. Variation in social environments might alter the dynamics of sexual selection, but our results align with theoretical predictions that the role social flexibility plays in modulating evolutionary divergence depends critically on whether responses to variation in the social environment are homogeneous across populations, or whether gene by social environment interactions occur.
Abstract.
Author URL.
Mills JA, Teplitsky C, Arroyo B, Charmantier A, Becker PH, Birkhead TR, Bize P, Blumstein DT, Bonenfant C, Boutin S, et al (2016). Solutions for Archiving Data in Long-Term Studies: a Reply to Whitlock et al. Trends in Ecology and Evolution, 31(2), 85-87.
2015
Briffa M, Sneddon LU, Wilson AJ (2015). Animal personality as a cause and consequence of contest behaviour.
Biol Lett,
11(3).
Abstract:
Animal personality as a cause and consequence of contest behaviour.
We review the evidence for a link between consistent among-individual variation in behaviour (animal personality) and the ability to win contests over limited resources. Explorative and bold behaviours often covary with contest behaviour and outcome, although there is evidence that the structure of these 'behavioural syndromes' can change across situations. Aggression itself is typically repeatable, but also subject to high within-individual variation as a consequence of plastic responses to previous fight outcomes and opponent traits. Common proximate mechanisms (gene expression, endocrine control and metabolic rates) may underpin variation in both contest behaviour and general personality traits. Given the theoretical links between the evolution of fighting and of personality, we suggest that longitudinal studies of contest behaviour, combining behavioural and physiological data, would be a useful context for the study of animal personalities.
Abstract.
Author URL.
Mills JA, Teplitsky C, Arroyo B, Charmantier A, Becker PH, Birkhead TR, Bize P, Blumstein DT, Bonenfant C, Boutin S, et al (2015). Archiving Primary Data: Solutions for Long-Term Studies.
Trends Ecol Evol,
30(10), 581-589.
Abstract:
Archiving Primary Data: Solutions for Long-Term Studies.
The recent trend for journals to require open access to primary data included in publications has been embraced by many biologists, but has caused apprehension amongst researchers engaged in long-term ecological and evolutionary studies. A worldwide survey of 73 principal investigators (Pls) with long-term studies revealed positive attitudes towards sharing data with the agreement or involvement of the PI, and 93% of PIs have historically shared data. Only 8% were in favor of uncontrolled, open access to primary data while 63% expressed serious concern. We present here their viewpoint on an issue that can have non-trivial scientific consequences. We discuss potential costs of public data archiving and provide possible solutions to meet the needs of journals and researchers.
Abstract.
Author URL.
Duffield C, Wilson AJ, Thornton A (2015). Desperate Prawns: Drivers of Behavioural Innovation Vary across Social Contexts in Rock Pool Crustaceans.
PLoS One,
10(10).
Abstract:
Desperate Prawns: Drivers of Behavioural Innovation Vary across Social Contexts in Rock Pool Crustaceans.
Innovative behaviour may allow animals to cope with changes in their environment. Innovative propensities are known to vary widely both between and within species, and a growing body of research has begun to examine the factors that drive individuals to innovate. Evidence suggests that individuals are commonly driven to innovate by necessity; for instance by hunger or because they are physically unable to outcompete others for access to resources. However, it is not known whether the factors that drive individuals to innovate are stable across contexts. We examined contextual variation in the drivers of innovation in rock pool prawns (Palaemon spp), invertebrates that face widely fluctuating environments and may, through the actions of tides and waves, find themselves isolated or in groups. Using two novel foraging tasks, we examined the effects of body size and hunger in prawns tested in solitary and group contexts. When tested alone, small prawns were significantly more likely to succeed in a spatial task, and faster to reach the food in a manipulation task, while hunger state had no effect. In contrast, size had no effect when prawns were tested in groups, but food-deprived individuals were disproportionately likely to innovate in both tasks. We suggest that contextual variation in the drivers of innovation is likely to be common in animals living in variable environments, and may best be understood by considering variation in the perception of relative risks and rewards under different conditions.
Abstract.
Author URL.
Boulton K, Couto E, Grimmer AJ, Earley RL, Canario AVM, Wilson AJ, Walling CA (2015). How integrated are behavioral and endocrine stress response traits? a repeated measures approach to testing the stress-coping style model. Ecology and Evolution
Boulton K, Couto E, Grimmer AJ, Earley RL, Canario AVM, Wilson AJ, Walling CA (2015). How integrated are behavioral and endocrine stress response traits? a repeated measures approach to testing the stress-coping style model.
Ecology and Evolution,
5(3), 618-633.
Abstract:
How integrated are behavioral and endocrine stress response traits? a repeated measures approach to testing the stress-coping style model
It is widely expected that physiological and behavioral stress responses will be integrated within divergent stress-coping styles (SCS) and that these may represent opposite ends of a continuously varying reactive-proactive axis. If such a model is valid, then stress response traits should be repeatable and physiological and behavioral responses should also change in an integrated manner along a major axis of among-individual variation. While there is some evidence of association between endocrine and behavioral stress response traits, few studies incorporate repeated observations of both. To test this model, we use a multivariate, repeated measures approach in a captive-bred population of Xiphophorus birchmanni. We quantify among-individual variation in behavioral stress response to an open field trial (OFT) with simulated predator attack (SPA) and measure waterborne steroid hormone levels (cortisol, 11-ketotestosterone) before and after exposure. Under the mild stress stimulus (OFT), (multivariate) behavioral variation among individuals was consistent with a strong axis of personality (shy-bold) or coping style (reactive-proactive) variation. However, behavioral responses to a moderate stressor (SPA) were less repeatable, and robust statistical support for repeatable endocrine state over the full sampling period was limited to 11-ketotestosterone. Although post hoc analysis suggested cortisol expression was repeatable over short time periods, qualitative relationships between behavior and glucocorticoid levels were counter to our a priori expectations. Thus, while our results clearly show among-individual differences in behavioral and endocrine traits associated with stress response, the correlation structure between these is not consistent with a simple proactive-reactive axis of integrated stress-coping style. Additionally, the low repeatability of cortisol suggests caution is warranted if single observations (or indeed repeat measures over short sampling periods) of glucocorticoid traits are used in ecological or evolutionary studies focussed at the individual level.
Abstract.
Thornton A, Wilson AJ (2015). In search of the Darwinian Holy Trinity in cognitive evolution: a comment on Croston et al. Behavioral Ecology, 26(6), 1460-1461.
Taylor ML, Skeats A, Wilson AJ, Price TAR, Wedell N (2015). Opposite environmental and genetic influences on body size in North American Drosophila pseudoobscura Evolutionary ecology and behaviour.
BMC Evolutionary Biology,
15(1).
Abstract:
Opposite environmental and genetic influences on body size in North American Drosophila pseudoobscura Evolutionary ecology and behaviour
Background: Populations of a species often differ in key traits. However, it is rarely known whether these differences are associated with genetic variation and evolved differences between populations, or are instead simply a plastic response to environmental differences experienced by the populations. Here we examine the interplay of plasticity and direct genetic control by investigating temperature-size relationships in populations of Drosophila pseudoobscura from North America. We used 27 isolines from three populations and exposed them to four temperature regimes (16°C, 20°C, 23°C, 26°C) to examine environmental, genetic and genotype-by-environment sources of variance in wing size. Results: By far the largest contribution to variation in wing size came from rearing temperature, with the largest flies emerging from the coolest temperatures. However, we also found a genetic signature that was counter to this pattern as flies originating from the northern, cooler population were consistently smaller than conspecifics from more southern, warmer populations when reared under the same laboratory conditions. Conclusions: We conclude that local selection on body size appears to be acting counter to the environmental effect of temperature. We find no evidence that local adaptation in phenotypic plasticity can explain this result, and suggest indirect selection on traits closely linked with body size, or patterns of chromosome inversion may instead be driving this relationship.
Abstract.
2014
Wilson AJ (2014). Competition as a source of constraint on life history evolution in natural populations.
Heredity (Edinb),
112(1), 70-78.
Abstract:
Competition as a source of constraint on life history evolution in natural populations.
Competition among individuals is central to our understanding of ecology and population dynamics. However, it could also have major implications for the evolution of resource-dependent life history traits (for example, growth, fecundity) that are important determinants of fitness in natural populations. This is because when competition occurs, the phenotype of each individual will be causally influenced by the phenotypes, and so the genotypes, of competitors. Theory tells us that indirect genetic effects arising from competitive interactions will give rise to the phenomenon of 'evolutionary environmental deterioration', and act as a source of evolutionary constraint on resource-dependent traits under natural selection. However, just how important this constraint is remains an unanswered question. This article seeks to stimulate empirical research in this area, first highlighting some patterns emerging from life history studies that are consistent with a competition-based model of evolutionary constraint, before describing several quantitative modelling strategies that could be usefully applied. A recurrent theme is that rigorous quantification of a competition's impact on life history evolution will require an understanding of the causal pathways and behavioural processes by which genetic (co)variance structures arise. Knowledge of the G-matrix among life history traits is not, in and of itself, sufficient to identify the constraints caused by competition.
Abstract.
Author URL.
Sakaluk SK, Wilson AJ, Bowers EK, Johnson LS, Masters BS, Johnson BGP, Vogel LA, Forsman AM, Thompson CF (2014). Genetic and environmental variation in condition, cutaneous immunity, and haematocrit in house wrens.
BMC EVOLUTIONARY BIOLOGY,
14 Author URL.
Boulton K, Grimmer AJ, Rosenthal GG, Walling CA, Wilson AJ (2014). How stable are personalities? a multivariate view of behavioural variation over long and short timescales in the sheepshead swordtail, Xiphophorus birchmanni.
Behavioral Ecology and Sociobiology,
68(5), 791-803.
Abstract:
How stable are personalities? a multivariate view of behavioural variation over long and short timescales in the sheepshead swordtail, Xiphophorus birchmanni
Many studies have revealed repeatable (among-individual) variance in behavioural traits consistent with variation in animal personality; however, these studies are often conducted using data collected over single sampling periods, most commonly with short time intervals between observations. Consequently, it is not clear whether population-level patterns of behavioural variation are stable across longer timescales and/or multiple sampling periods or whether individuals maintain consistent ranking of behaviours (and/or personality) over their lifetimes. Here, we address these questions in a captive-bred population of a tropical freshwater poeciliid fish, Xiphophorus birchmanni. Using a multivariate approach, we estimate the among-individual variance-covariance matrix (I), for a set of behavioural traits repeatedly assayed in two different experimental contexts (open-field trials, emergence and exploration trials) over long-term (56 days between observations) and short-term (4-day observation interval) time periods. In both long- and short-term data sets, we find that traits are repeatable and the correlation structure of I is consistent with a latent axis of variation in boldness. While there are some qualitative differences in the way individual traits contribute to boldness and a tendency towards higher repeatabilities in the short-term study, overall, we find that population-level patterns of among-individual behavioural (co)variance to be broadly similar over both time frames. At the individual level, we find evidence that short-term studies can be informative for an individual's behavioural phenotype over longer (e.g. lifetime) periods. However, statistical support is somewhat mixed and, at least for some observed behaviours, relative rankings of individual performance change significantly between data sets. © 2014 Springer-Verlag Berlin Heidelberg.
Abstract.
Boulton K, Grimmer AJ, Rosenthal GG, Walling CA, Wilson AJ (2014). How stable are personalities? a multivariate view of behavioural variation over long and short timescales in the sheepshead swordtail, Xiphophorus birchmanni. Behavioral Ecology and Sociobiology, 1-13.
Hayward AD, Nussey DH, Wilson AJ, Berenos C, Pilkington JG, Watt KA, Pemberton JM, Graham AL (2014). Natural Selection on Individual Variation in Tolerance of Gastrointestinal Nematode Infection.
PLoS Biology,
12(7), 1-13.
Abstract:
Natural Selection on Individual Variation in Tolerance of Gastrointestinal Nematode Infection
Hosts may mitigate the impact of parasites by two broad strategies: resistance, which limits parasite burden, and tolerance, which limits the fitness or health cost of increasing parasite burden. The degree and causes of variation in both resistance and tolerance are expected to influence host-parasite evolutionary and epidemiological dynamics and inform disease management, yet very little empirical work has addressed tolerance in wild vertebrates. Here, we applied random regression models to longitudinal data from an unmanaged population of Soay sheep to estimate individual tolerance, defined as the rate of decline in body weight with increasing burden of highly prevalent gastrointestinal nematode parasites. On average, individuals lost weight as parasite burden increased, but whereas some lost weight slowly as burden increased (exhibiting high tolerance), other individuals lost weight significantly more rapidly (exhibiting low tolerance). We then investigated associations between tolerance and fitness using selection gradients that accounted for selection on correlated traits, including body weight. We found evidence for positive phenotypic selection on tolerance: on average, individuals who lost weight more slowly with increasing parasite burden had higher lifetime breeding success. This variation did not have an additive genetic basis. These results reveal that selection on tolerance operates under natural conditions. They also support theoretical predictions for the erosion of additive genetic variance of traits under strong directional selection and fixation of genes conferring tolerance. Our findings provide the first evidence of selection on individual tolerance of infection in animals and suggest practical applications in animal and human disease management in the face of highly prevalent parasites. © 2014 Hayward et al.
Abstract.
Hayward AD, Nussey DH, Wilson AJ, Berenos C, Pilkington JG, Watt KA, Pemberton JM, Graham AL (2014). Natural selection on individual variation in tolerance of gastrointestinal nematode infection.
PLoS Biol,
12(7).
Abstract:
Natural selection on individual variation in tolerance of gastrointestinal nematode infection.
Hosts may mitigate the impact of parasites by two broad strategies: resistance, which limits parasite burden, and tolerance, which limits the fitness or health cost of increasing parasite burden. The degree and causes of variation in both resistance and tolerance are expected to influence host-parasite evolutionary and epidemiological dynamics and inform disease management, yet very little empirical work has addressed tolerance in wild vertebrates. Here, we applied random regression models to longitudinal data from an unmanaged population of Soay sheep to estimate individual tolerance, defined as the rate of decline in body weight with increasing burden of highly prevalent gastrointestinal nematode parasites. On average, individuals lost weight as parasite burden increased, but whereas some lost weight slowly as burden increased (exhibiting high tolerance), other individuals lost weight significantly more rapidly (exhibiting low tolerance). We then investigated associations between tolerance and fitness using selection gradients that accounted for selection on correlated traits, including body weight. We found evidence for positive phenotypic selection on tolerance: on average, individuals who lost weight more slowly with increasing parasite burden had higher lifetime breeding success. This variation did not have an additive genetic basis. These results reveal that selection on tolerance operates under natural conditions. They also support theoretical predictions for the erosion of additive genetic variance of traits under strong directional selection and fixation of genes conferring tolerance. Our findings provide the first evidence of selection on individual tolerance of infection in animals and suggest practical applications in animal and human disease management in the face of highly prevalent parasites.
Abstract.
Author URL.
Roff DA, Wilson AJ (2014). Quantifying Genotype‐by‐Environment Interactions in Laboratory Systems. In (Ed) Genotype-by-Environment Interactions and Sexual Selection, 100-136.
Edward DA, Poissant J, Wilson AJ, Chapman T (2014). Sexual conflict and interacting phenotypes: a quantitative genetic analysis of fecundity and copula duration in drosophila melanogaster. Evolution
Edward DA, Poissant J, Wilson AJ, Chapman T (2014). Sexual conflict and interacting phenotypes: a quantitative genetic analysis of fecundity and copula duration in drosophila melanogaster.
Evolution,
68(6), 1651-1660.
Abstract:
Sexual conflict and interacting phenotypes: a quantitative genetic analysis of fecundity and copula duration in drosophila melanogaster
Many reproductive traits that have evolved under sexual conflict may be influenced by both sexes. Investigation of the genetic architecture of such traits can yield important insight into their evolution, but this entails that the heritable component of variation is estimated for males and females-as an interacting phenotype. We address the lack of research in this area through an investigation of egg production and copula duration in the fruit fly, Drosophila melanogaster. Despite egg production rate being determined by both sexes, which may cause sexual conflict, an assessment of this trait as an interacting phenotype is lacking. It is currently unclear whether copula duration is determined by males and/or females. We found significant female, but not male, genetic variance for egg production rate that may indicate reduced potential for ongoing sexually antagonistic coevolution. In contrast, copula duration was determined by significant genetic variance in both sexes. We also identified genetic variation in egg retention among virgin females. Although previously identified in wild populations, it is unclear why this should be present in a laboratory stock. This study provides a novel insight into the shared genetic architecture of reproductive traits that are the subject of sexual conflict. © 2014 the Society for the Study of Evolution.
Abstract.
Royle NJ, Russell AF, Wilson AJ (2014). The evolution of flexible parenting.
Science,
345(6198), 776-781.
Abstract:
The evolution of flexible parenting.
Parenting behaviors, such as the provisioning of food by parents to offspring, are known to be highly responsive to changes in environment. However, we currently know little about how such flexibility affects the ways in which parenting is adapted and evolves in response to environmental variation. This is because few studies quantify how individuals vary in their response to changing environments, especially social environments created by other individuals with which parents interact. Social environmental factors differ from nonsocial factors, such as food availability, because parents and offspring both contribute and respond to the social environment they experience. This interdependence leads to the coevolution of flexible behaviors involved in parenting, which could, paradoxically, constrain the ability of individuals to rapidly adapt to changes in their nonsocial environment.
Abstract.
Author URL.
2013
Wilson AJ, Grimmer A, Rosenthal GG (2013). Causes and consequences of contest outcome: Aggressiveness, dominance and growth in the sheepshead swordtail, Xiphophorus birchmanni.
Behavioral Ecology and Sociobiology,
67(7), 1151-1161.
Abstract:
Causes and consequences of contest outcome: Aggressiveness, dominance and growth in the sheepshead swordtail, Xiphophorus birchmanni
Although our understanding of how animal personality affects fitness is incomplete, one general hypothesis is that personality traits (e.g. boldness and aggressiveness) contribute to competitive ability. If so, then under resource limitation, personality differences will generate variation in life history traits crucial to fitness, like growth. Here, we test this idea using data from same-sex dyadic interaction trials of sheepshead swordtails (Xiphophorus birchmanni). In males, there was evidence of repeatable variation across a suite of agonistic contest behaviours, while repeatable opponent effects on focal behaviour were also detected. A single vector explains 80 % of the among-individual variance in multivariate phenotype and can be viewed as aggressiveness. We also find that aggressiveness predicts dominance-the repeatable tendency to win food in competition-and dominant individuals show faster post-trial weight gain (independently of initial size). In females, a dominance hierarchy predictive of weight gain was also found, but there was no evidence of variation in aggressiveness. While size often predicts contest outcome, our results show that individuals may sometimes grow larger because they are behaviourally dominant rather than vice versa. When resources are limited, personality traits such as aggression can influence growth, life history, and fitness through impacts on resource acquisition. © 2013 Springer-Verlag Berlin Heidelberg.
Abstract.
Wilson AJ, Grimmer A, Rosenthal GG (2013). Causes and consequences of contest outcome: aggressiveness, dominance and growth in the sheepshead swordtail, Xiphophorus birchmanni. Behavioral Ecology and Sociobiology, 1-11.
Schuett W, Dall SRX, Wilson AJ, Royle NJ (2013). Environmental transmission of a personality trait: Foster parent exploration behaviour predicts offspring exploration behaviour in zebra finches.
Biology Letters,
9(4).
Abstract:
Environmental transmission of a personality trait: Foster parent exploration behaviour predicts offspring exploration behaviour in zebra finches
Consistent behavioural differences between individuals are common in many species and can have important effects on offspring fitness. To understand the evolution of such personality variation it is important to determine the mode of inheritance, but this has been quantified for only a few species. Here, we report results from a breeding experiment in captive zebra finches, Taeniopygia guttata, in which we cross-fostered offspring to disentangle the importance of genetic and non-genetic transmission of behaviour. Genetic and foster-parents’ exploratory type was measured in a novel environment pre-breeding and offspring exploratory type was assessed at adulthood. Offspring exploratory type was predicted by the exploratory behaviour of the foster but not the genetic parents, whereas offspring size was predicted by genetic but not foster parents’ size. Other aspects of the social environment, such as rearing regime (uni- versus biparental), hatching position, brood size, or an individual’s sex did not influence offspring exploration. Our results therefore indicate that non-genetic transmission of behaviour can play an important role in shaping animal personality variation.
Abstract.
Hayward AD, Wilson AJ, Pilkington JG, Clutton-Brock TH, Pemberton JM, Kruuk LEB (2013). Reproductive senescence in female Soay sheep: Variation across traits and contributions of individual ageing and selective disappearance.
Functional Ecology,
27(1), 184-195.
Abstract:
Reproductive senescence in female Soay sheep: Variation across traits and contributions of individual ageing and selective disappearance
Although senescence in reproductive success has been observed in a number of wild animal populations, longitudinal analyses determining the actual processes responsible for population-level patterns of ageing, and in particular, the relative contributions of within-individual senescence vs. selective mortality, are rare. Furthermore, many studies also only consider single traits in isolation, despite evidence that different aspects of physiology and fitness may show varying patterns of senescence. We used data from an unmanaged population of Soay sheep on the islands of St Kilda, NW Scotland to analyse age-related change in four aspects of female reproductive performance: annual fecundity, twinning rate and the maternally influenced offspring traits of lamb birth weight and early survival. We present the results of three analytical techniques, which attempt to disentangle the contributions of within-individual ageing, selective mortality and terminal effects to the observed population-level patterns of age-specific change. All four traits showed considerable age-related change, but population-level trajectories varied markedly across them. Population-level patterns were underpinned by considerable within-individual senescence including within-individual terminal declines in performance occurring only in the final year of life. However, at the population level, these processes were also masked to some extent by selective disappearance (mortality) of poor breeders. The contributions of individual-level ageing and selective mortality to population-level ageing patterns varied considerably between traits, as did the nature of individual-level senescence. We did not observe detectable significant late-life declines in all four traits: in particular, there was no evidence of senescence in twinning rate. The results indicate that senescence may not be ubiquitous across all aspects of reproductive performance within a population. © 2012 the Authors. Functional Ecology © 2012 British Ecological Society.
Abstract.
2012
Koch M, Wilson AJ, Kerschbaumer M, Wiedl T, Sturmbauer C (2012). Additive genetic variance of quantitative traits in natural and pond-bred populations of the Lake Tanganyika cichlid Tropheus moorii.
Hydrobiologia,
682(1), 131-141.
Abstract:
Additive genetic variance of quantitative traits in natural and pond-bred populations of the Lake Tanganyika cichlid Tropheus moorii
Quantitative genetic studies in natural populations are of growing interest to speciation research since divergence is often believed to arise through micro-evolutionary change, caused by natural selection on functional morphological traits. The species flock of cichlid fishes in Africa's oldest lake, Lake Tanganyika, offers a rare opportunity to study this process. Using the cichlid species Tropheus moorii, we assessed the potential for microevolution in a set of morphological traits by estimating their quantitative genetic basis of variation. Two approaches were employed: (1) estimation of trait heritabilities (h 2) in situ from a sample of wild caught fish, and (2) estimation of h 2 from first generation offspring produced in a semi-natural breeding experiment. In both cases, microsatellite data were used to infer pedigree structure among the sampled individuals and estimates of h 2 were made using an animal model approach. Although power was limited by the pedigree structures estimated (particularly in the wild caught sample), we nonetheless demonstrate the presence of significant additive genetic variance for aspects of morphology that, in the cichlid species Tropheus moorii, are expected to be functionally and ecologically important, and therefore likely targets of natural selection. We hypothesize that traits showing significant additive genetic variance, such as the mouth position have most likely played a key role in the adaptive evolution of the cichlid fish Tropheus moorii. © 2011 the Author(s).
Abstract.
Morrissey MB, Walling CA, Wilson AJ, Pemberton JM, Clutton-Brock TH, Kruuk LEB (2012). Genetic Analysis of Life-History Constraint and Evolution in a Wild Ungulate Population.
AMERICAN NATURALIST,
179(4), E97-E114.
Author URL.
Morrissey MB, Walling CA, Wilson AJ, Pemberton JM, Clutton-Brock TH, Kruuk LEB (2012). Genetic analysis of life-history constraint and evolution in a wild ungulate population.
Am Nat,
179(4), E97-114.
Abstract:
Genetic analysis of life-history constraint and evolution in a wild ungulate population.
Trade-offs among life-history traits are central to evolutionary theory. In quantitative genetic terms, trade-offs may be manifested as negative genetic covariances relative to the direction of selection on phenotypic traits. Although the expression and selection of ecologically important phenotypic variation are fundamentally multivariate phenomena, the in situ quantification of genetic covariances is challenging. Even for life-history traits, where well-developed theory exists with which to relate phenotypic variation to fitness variation, little evidence exists from in situ studies that negative genetic covariances are an important aspect of the genetic architecture of life-history traits. In fact, the majority of reported estimates of genetic covariances among life-history traits are positive. Here we apply theory of the genetics and selection of life histories in organisms with complex life cycles to provide a framework for quantifying the contribution of multivariate genetically based relationships among traits to evolutionary constraint. We use a Bayesian framework to link pedigree-based inference of the genetic basis of variation in life-history traits to evolutionary demography theory regarding how life histories are selected. Our results suggest that genetic covariances may be acting to constrain the evolution of female life-history traits in a wild population of red deer Cervus elaphus: genetic covariances are estimated to reduce the rate of adaptation by about 40%, relative to predicted evolutionary change in the absence of genetic covariances. Furthermore, multivariate phenotypic (rather than genetic) relationships among female life-history traits do not reveal this constraint.
Abstract.
Author URL.
Boulton K, Sinderman B, Pearce MR, Earley RL, Wilson AJ (2012). He who dares only wins sometimes: Physiological stress and contest behaviour in Xiphophorus helleri.
Behaviour,
149(9), 977-1002.
Abstract:
He who dares only wins sometimes: Physiological stress and contest behaviour in Xiphophorus helleri
While many factors influence contest outcome and social dominance in animals, there is increasing interest in behavioural-physiological stress-coping styles. Causality, however, is often ambiguous; is physiological state determined by contest outcome or vice versa? Furthermore, experimental protocols may themselves induce stress responses that impact individual behaviour and, thus, potentially contest outcome. Here we test whether latency to recover from acute stress, measured both physiologically and behaviourally, predicts who initiates and who wins dyadic contests between pairs of male green swordtails (Xiphophorous helleri). In line with our predictions, animals that recovered faster (behaviourally) from disturbance created by the experimental protocol prior to meeting an opponent were more likely to initiate contests; however, they were not more likely to win and, contrary to expectations, had higher pre-contest Cortisol levels than their opponents. They also showed greater physiological stress responses to the experiment as determined from the difference between pre- and post-contest Cortisol levels. Moreover, stress response was independent of whether a contest escalated. In contradiction to evidence found in other taxa and fish systems, the suite of traits that we measured were not correlated in a manner that allowed classification of the animals into the usual reactive and proactive stress-coping styles. Our results suggest that coping style may play a key role in determining which individual initiates a contest, but that other factors govern contest outcome. © 2012 Koninklijke Brill NV, Leiden.
Abstract.
Hammerschmidt K, Deines P, Wilson AJ, Rolff J (2012). Quantitative genetics of immunity and life history under different photoperiods.
HEREDITY,
108(5), 569-576.
Author URL.
2011
Wilson AJ, Reale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LEB, Nussey DH (2011). An ecologist's guide to the animal model (vol 79, pg 13, 2010).
JOURNAL OF ANIMAL ECOLOGY,
80(5), 1109-1109.
Author URL.
Hadfield JD, Wilson AJ, Kruuk LEB (2011). Cryptic evolution: does environmental deterioration have a genetic basis?.
Genetics,
187(4), 1099-1113.
Abstract:
Cryptic evolution: does environmental deterioration have a genetic basis?
Cryptic evolution has been defined as adaptive evolutionary change being masked by concurrent environmental change. Empirical studies of cryptic evolution have usually invoked a changing climate and/or increasing population density as the form of detrimental environmental change experienced by a population undergoing cryptic evolution. However, Fisher (1958) emphasized that evolutionary change in itself is likely to be an important component of "environmental deterioration," a point restated by Cooke et al. (1990) in the context of intraspecific competition. In this form, environmental deterioration arises because a winning lineage has to compete against more winners in successive generations as the population evolves. This "evolutionary environmental deterioration" has different implications for the selection and evolution of traits influenced by resource competition than general environmental change. We reformulate Cooke's model as a quantitative genetic model to show that it is identical in form to more recent developments proposed by quantitative geneticists. This provides a statistical framework for discriminating between the alternative hypotheses of environmental change and environmental deterioration caused by evolutionary change. We also demonstrate that in systems where no phenotypic change has occurred, there are many reasonable biological processes that will generate patterns in predicted breeding values that are consistent with what has been interpreted as cryptic evolution, and care needs to be taken when interpreting these patterns. These processes include mutation, sib competition, and invisible fractions.
Abstract.
Author URL.
Vale PF, Wilson AJ, Best A, Boots M, Little TJ (2011). Epidemiological, Evolutionary, and Coevolutionary Implications of Context-Dependent Parasitism.
AMERICAN NATURALIST,
177(4), 510-521.
Author URL.
Graham AL, Shuker DM, Pollitt LC, Auld SKJR, Wilson AJ, Little TJ (2011). Fitness consequences of immune responses: Strengthening the empirical framework for ecoimmunology.
Functional Ecology,
25(1), 5-17.
Abstract:
Fitness consequences of immune responses: Strengthening the empirical framework for ecoimmunology
1.Ecoimmunologists aim to understand the costs, benefits, and net fitness consequences of different strategies for immune defense. 2.Measuring the fitness consequences of immune responses is difficult, partly because of complex relationships between host fitness and the within-host density of parasites and immunological cells or molecules. In particular, neither the strongest immune responses nor the lowest parasite densities necessarily maximize host fitness. 3.Here, we propose that ecoimmunologists should routinely endeavour to measure three intertwined parameters: host fitness, parasite density, and relevant immune responses. We further propose that analyses of relationships among these traits would benefit from the statistical machinery used for analyses of phenotypic plasticity and/or methods that are robust to the bi-directional causation inherent in host-parasite relationships. For example, analyses of how host fitness depends upon parasite density, which is an evolutionary ecological definition of tolerance, would benefit from these more robust methods. 4.Together, these steps promote rigorous quantification of the fitness consequences of immune responses. Such quantification is essential if ecoimmunologists are to decipher causes of immune polymorphism in nature and predict trajectories of natural selection on immune defense. © 2010 the Authors. Functional Ecology © 2010 British Ecological Society.
Abstract.
Wilson AJ, Morrissey MB, Adams MJ, Walling CA, Guinness FE, Pemberton JM, Clutton-Brock TH, Kruuk LEB (2011). Indirect genetics effects and evolutionary constraint: an analysis of social dominance in red deer, Cervus elaphus.
J Evol Biol,
24(4), 772-783.
Abstract:
Indirect genetics effects and evolutionary constraint: an analysis of social dominance in red deer, Cervus elaphus.
By determining access to limited resources, social dominance is often an important determinant of fitness. Thus, if heritable, standard theory predicts mean dominance should evolve. However, dominance is usually inferred from the tendency to win contests, and given one winner and one loser in any dyadic contest, the mean proportion won will always equal 0.5. Here, we argue that the apparent conflict between quantitative genetic theory and common sense is resolved by recognition of indirect genetic effects (IGEs). We estimate selection on, and genetic (co)variance structures for, social dominance, in a wild population of red deer Cervus elaphus, on the Scottish island of Rum. While dominance is heritable and positively correlated with lifetime fitness, contest outcomes depend as much on the genes carried by an opponent as on the genotype of a focal individual. We show how this dependency imposes an absolute evolutionary constraint on the phenotypic mean, thus reconciling theoretical predictions with common sense. More generally, we argue that IGEs likely provide a widespread but poorly recognized source of evolutionary constraint for traits influenced by competition.
Abstract.
Author URL.
Wilson AJ, de Boer M, Arnott G, Grimmer A (2011). Integrating personality research and animal contest theory: aggressiveness in the green swordtail Xiphophorus helleri. PLoS One
Martin JGA, Nussey DH, Wilson AJ, Reale D (2011). Measuring individual differences in reaction norms in field and experimental studies: a power analysis of random regression models.
METHODS IN ECOLOGY AND EVOLUTION,
2(4), 362-374.
Author URL.
Hayward AD, Wilson AJ, Pilkington JG, Clutton-Brock TH, Pemberton JM, Kruuk LEB (2011). Natural selection on a measure of parasite resistance varies across ages and environmental conditions in a wild mammal.
J Evol Biol,
24(8), 1664-1676.
Abstract:
Natural selection on a measure of parasite resistance varies across ages and environmental conditions in a wild mammal.
Parasites detrimentally affect host fitness, leading to expectations of positive selection on host parasite resistance. However, as immunity is costly, host fitness may be maximized at low, but nonzero, parasite infection intensities. These hypotheses are rarely tested on natural variation in free-living populations. We investigated selection on a measure of host parasite resistance in a naturally regulated Soay sheep population using a longitudinal data set and found negative correlations between parasite infection intensity and annual fitness in lambs, male yearlings and adult females. However, having accounted for confounding effects of body weight, the effect was only significant in lambs. Associations between fitness and parasite resistance were environment-dependent, being strong during low-mortality winters, but negligible during harsher high-mortality winters. There was no evidence for stabilizing selection. Our findings reveal processes that may shape variation in parasite resistance in natural populations and illustrate the importance of accounting for correlated traits in selection analysis.
Abstract.
Author URL.
2010
Wilson AJ, Réale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LEB, Nussey DH (2010). An ecologist's guide to the animal model.
J Anim Ecol,
79(1), 13-26.
Abstract:
An ecologist's guide to the animal model.
1. Efforts to understand the links between evolutionary and ecological dynamics hinge on our ability to measure and understand how genes influence phenotypes, fitness and population dynamics. Quantitative genetics provides a range of theoretical and empirical tools with which to achieve this when the relatedness between individuals within a population is known. 2. A number of recent studies have used a type of mixed-effects model, known as the animal model, to estimate the genetic component of phenotypic variation using data collected in the field. Here, we provide a practical guide for ecologists interested in exploring the potential to apply this quantitative genetic method in their research. 3. We begin by outlining, in simple terms, key concepts in quantitative genetics and how an animal model estimates relevant quantitative genetic parameters, such as heritabilities or genetic correlations. 4. We then provide three detailed example tutorials, for implementation in a variety of software packages, for some basic applications of the animal model. We discuss several important statistical issues relating to best practice when fitting different kinds of mixed models. 5. We conclude by briefly summarizing more complex applications of the animal model, and by highlighting key pitfalls and dangers for the researcher wanting to begin using quantitative genetic tools to address ecological and evolutionary questions.
Abstract.
Author URL.
Hegyi G, Herényi M, Wilson AJ, Garamszegi LZ, Rosivall B, Eens M, Török J (2010). Breeding experience and the heritability of female mate choice in collared flycatchers.
PLoS ONE,
5(11).
Abstract:
Breeding experience and the heritability of female mate choice in collared flycatchers
Background: Heritability in mate preferences is assumed by models of sexual selection, and preference evolution may contribute to adaptation to changing environments. However, mate preference is difficult to measure in natural populations as detailed data on mate availability and mate sampling are usually missing. Often the only available information is the ornamentation of the actual mate. The single long-term quantitative genetic study of a wild population found low heritability in female mate ornamentation in Swedish collared flycatchers. One potentially important cause of low heritability in mate ornamentation at the population level is reduced mate preference expression among inexperienced individuals. Methodology/Principal Findings: Applying animal model analyses to 21 years of data from a Hungarian collared flycatcher population, we found that additive genetic variance was 50 percent and significant for ornament expression in males, but less than 5 percent and non-significant for mate ornamentation treated as a female trait. Female breeding experience predicted breeding date and clutch size, but mate ornamentation and its variance components were unrelated to experience. Although we detected significant area and year effects on mate ornamentation, more than 85 percent of variance in this trait remained unexplained. Moreover, the effects of area and year on mate ornamentation were also highly positively correlated between inexperienced and experienced females, thereby acting to remove difference between the two groups. Conclusions/Significance: the low heritability of mate ornamentation was apparently not explained by the presence of inexperienced individuals. Our results further indicate that the expression of mate ornamentation is dominated by temporal and spatial constraints and unmeasured background factors. Future studies should reduce unexplained variance or use alternative measures of mate preference. The heritability of mate preference in the wild remains a principal but unresolved question in evolutionary ecology. © 2010 Hegyi et al.
Abstract.
Husby A, Nussey DH, Visser ME, Wilson AJ, Sheldon BC, Kruuk LEB (2010). Contrasting patterns of phenotypic plasticity in reproductive traits in two great tit (Parus major) populations.
Evolution,
64(8), 2221-2237.
Abstract:
Contrasting patterns of phenotypic plasticity in reproductive traits in two great tit (Parus major) populations
Phenotypic plasticity is an important mechanism via which populations can respond to changing environmental conditions, but we know very little about how natural populations vary with respect to plasticity. Here we use random-regression animal models to understand the multivariate phenotypic and genetic patterns of plasticity variation in two key life-history traits, laying date and clutch size, using data from long-term studies of great tits in the Netherlands (Hoge Veluwe [HV]) and UK (Wytham Woods [WW]). We show that, while population-level responses of laying date and clutch size to temperature were similar in the two populations, between-individual variation in plasticity differed markedly. Both populations showed significant variation in phenotypic plasticity (IxE) for laying date, but IxE was significantly higher in HV than in WW. There were no significant genotype-by-environment interactions (GxE) for laying date, yet differences in GxE were marginally nonsignificant between HV and WW. For clutch size, we only found significant IxE and GxE in WW but no significant difference between populations. From a multivariate perspective, plasticity in laying date was not correlated with plasticity in clutch size in either population. Our results suggest that generalizations about the form and cause of any response to changing environmental conditions across populations may be difficult. © 2010 the Author(s). Journal compilation © 2010 the Society for the Study of Evolution.
Abstract.
Gratten J, Wilson AJ, McRae AF, Beraldi D, Visscher PM, Pemberton JM, Slate J (2010). No evidence for warming climate theory of coat colour change in Soay sheep: a comment on Maloney et al. Biology Letters, 6(5), 678-679.
Morrissey MB, Wilson AJ (2010). Pedantics: an r package for pedigree-based genetic simulation and pedigree manipulation, characterization and viewing.
Molecular Ecology Resources,
10(4), 711-719.
Abstract:
Pedantics: an r package for pedigree-based genetic simulation and pedigree manipulation, characterization and viewing
Analyses of pedigrees and pedigree-derived parameters (e.g. relatedness and fitness) provide some of the most informative types of studies in evolutionary biology. The r package pedantics implements tools to facilitate power and sensitivity analyses of pedigree-related studies of natural populations. Functions are available to permute pedigree data in various ways with the goal of mimicking patterns of pedigree errors and missingness that occur in studies of natural populations. Another set of functions simulates genetic and phenotypic data based on arbitrary pedigrees. Finally, functions are also available with which visual and numerical representations of pedigree structure can be generated. © 2009 Blackwell Publishing Ltd.
Abstract.
Poissant J, Wilson AJ, Coltman DW (2010). Sex-specific genetic variance and the evolution of sexual dimorphism: a systematic review of cross-sex genetic correlations.
Evolution,
64(1), 97-107.
Abstract:
Sex-specific genetic variance and the evolution of sexual dimorphism: a systematic review of cross-sex genetic correlations
The independent evolution of the sexes may often be constrained if male and female homologous traits share a similar genetic architecture. Thus, cross-sex genetic covariance is assumed to play a key role in the evolution of sexual dimorphism (SD) with consequent impacts on sexual selection, population dynamics, and speciation processes. We compiled cross-sex genetic correlations (rMF) estimates from 114 sources to assess the extent to which the evolution of SD is typically constrained and test several specific hypotheses. First, we tested if rMF differed among trait types and especially between fitness components and other traits. We also tested the theoretical prediction of a negative relationship between rMF and SD based on the expectation that increases in SD should be facilitated by sex-specific genetic variance. We show that rMF is usually large and positive but that it is typically smaller for fitness components. This demonstrates that the evolution of SD is typically genetically constrained and that sex-specific selection coefficients may often be opposite in sign due to sub-optimal levels of SD. Most importantly, we confirm that sex-specific genetic variance is an important contributor to the evolution of SD by validating the prediction of a negative correlation between rMF and SD. © 2009 the Society for the Study of Evolution.
Abstract.
Morrissey MB, Kruuk LEB, Wilson AJ (2010). The danger of applying the breeder's equation in observational studies of natural populations.
J Evol Biol,
23(11), 2277-2288.
Abstract:
The danger of applying the breeder's equation in observational studies of natural populations.
The breeder's equation, which predicts evolutionary change when a phenotypic covariance exists between a heritable trait and fitness, has provided a key conceptual framework for studies of adaptive microevolution in nature. However, its application requires strong assumptions to be made about the causation of fitness variation. In its univariate form, the breeder's equation assumes that the trait of interest is not correlated with other traits having causal effects on fitness. In its multivariate form, the validity of predicted change rests on the assumption that all such correlated traits have been measured and incorporated into the analysis. Here, we (i) highlight why these assumptions are likely to be seriously violated in studies of natural, rather than artificial, selection and (ii) advocate wider use of the Robertson-Price identity as a more robust, and less assumption-laden, alternative to the breeder's equation for applications in evolutionary ecology.
Abstract.
Author URL.
Hadfield JD, Wilson AJ, Garant D, Sheldon BC, Kruuk LEB (2010). The misuse of BLUP in ecology and evolution.
Am Nat,
175(1), 116-125.
Abstract:
The misuse of BLUP in ecology and evolution.
Best linear unbiased prediction (BLUP) is a method for obtaining point estimates of a random effect in a mixed effect model. Over the past decade it has been used extensively in ecology and evolutionary biology to predict individual breeding values and reaction norms. These predictions have been used to infer natural selection, evolutionary change, spatial-genetic patterns, individual reaction norms, and frailties. In this article we show analytically and through simulation and example why BLUP often gives anticonservative and biased estimates of evolutionary and ecological parameters. Although some concerns with BLUP methodology have been voiced before, the scale and breadth of the problems have probably not been widely appreciated. Bias arises because BLUPs are often used to estimate effects that are not explicitly accounted for in the model used to make the predictions. In these cases, predicted breeding values will often say more about phenotypic patterns than the genetic patterns of interest. An additional problem is that BLUPs are point estimates of quantities that are usually known with little certainty. Failure to account for this uncertainty in subsequent tests can lead to both bias and extreme anticonservatism. We demonstrate that restricted maximum likelihood and Bayesian solutions exist for these problems and show how unbiased and powerful tests can be derived that adequately quantify uncertainty. of particular utility is a new test for detecting evolutionary change that not only accounts for prediction error in breeding values but also accounts for drift. To illustrate the problem, we apply these tests to long-term data on the Soay sheep (Ovis aries) and the great tit (Parus major) and show that previously reported temporal trends in breeding values are not supported.
Abstract.
Author URL.
Brommer JE, Rattiste K, Wilson AJ (2010). The rate of ageing in a long-lived bird is not heritable. Heredity, 104, 363-370.
Wilson AJ, Nussey DH (2010). What is individual quality? an evolutionary perspective.
Trends Ecol Evol,
25(4), 207-214.
Abstract:
What is individual quality? an evolutionary perspective.
In studies of population ecology, demography and life history evolution, among-individual differences in traits associated with survival and reproduction are often attributed to variation in 'individual quality'. However, often intuitive quality is rarely defined explicitly, and we argue that this can result in ambiguity about what quality actually is. Here we consider the various ways in which the concept of quality is currently applied, and show that subtle differences in intended meaning have very important consequences when the goal is to draw evolutionary inferences. We also propose a novel approach that is consistent with all current ecological uses, but also allows the concept of quality to be integrated with existing evolutionary theory.
Abstract.
Author URL.
2009
Hayward AD, Wilson AJ, Pilkington JG, Pemberton JM, Kruuk LEB (2009). Ageing in a variable habitat: environmental stress affects senescence in parasite resistance in St Kilda Soay sheep.
Proc Biol Sci,
276(1672), 3477-3485.
Abstract:
Ageing in a variable habitat: environmental stress affects senescence in parasite resistance in St Kilda Soay sheep.
Despite widespread empirical evidence for a general deterioration in the majority of traits with advancing age, it is unclear whether the progress of senescence is chronologically determined, or whether factors such as environmental conditions experienced over the lifespan are more important. We explored the relative importance of 'chronological' and 'environmental' measures of age to changes in parasite resistance across the lifespan of free-living Soay sheep. Our results show that individuals experience an increase in parasite burden, as indicated by gastrointestinal helminth faecal egg count (FEC) with chronological age. However, chronological age fails to fully explain changes in FEC because a measure of environmental age, cumulative environmental stress, predicts an additional increase in FEC once chronological age has been accounted for. Additionally, we show that in females age-specific changes are dependent upon the environmental conditions experienced across individuals' life histories: increases in FEC with age were greatest among individuals that had experienced the highest degree of stress. Our results illustrate that chronological age alone may not always correspond to biological age, particularly in variable environments. In these circumstances, measures of age that capture the cumulative stresses experienced by an individual may be useful for understanding the process of senescence.
Abstract.
Author URL.
Wilson AJ, Gelin U, Perron M-C, Réale D (2009). Indirect genetic effects and the evolution of aggression in a vertebrate system.
Proc Biol Sci,
276(1656), 533-541.
Abstract:
Indirect genetic effects and the evolution of aggression in a vertebrate system.
Aggressive behaviours are necessarily expressed in a social context, such that individuals may be influenced by the phenotypes, and potentially the genotypes, of their social partners. Consequently, it has been hypothesized that indirect genetic effects (IGEs) arising from the social environment will provide a major source of heritable variation on which selection can act. However, there has been little empirical scrutiny of this to date. Here we test this hypothesis in an experimental population of deer mice (Peromyscus maniculatus). Using quantitative genetic models of five aggression traits, we find repeatable and heritable differences in agonistic behaviours of focal individuals when presented with an opponent mouse. For three of the traits, there is also support for the presence of IGEs, and estimated correlations between direct and indirect genetic (rAO,F) effects were high. As a consequence, any selection for aggression in the focal individuals should cause evolution of the social environment as a correlated response. In two traits, strong positive rAO,F will cause the rapid evolution of aggression, while in a third case changes in the phenotypic mean will be constrained by negative covariance between direct and IGEs. Our results illustrate how classical analyses may miss important components of heritable variation, and show that a full understanding of evolutionary dynamics requires explicit consideration of the genetic component of the social environment.
Abstract.
Author URL.
Wilson AJ (2009). Maternal effects in ungulates. In Maestripieri D, Mateo JM (Eds.)
Maternal Effects in Mammals, University of Chicago Press.
Abstract:
Maternal effects in ungulates
Abstract.
Sawalha RM, Bell L, Brotherstone S, White I, Wilson AJ, Villanueva B (2009). Scrapie-resistant sheep show certain coat colour characteristics.
Genet Res (Camb),
91(1), 39-46.
Abstract:
Scrapie-resistant sheep show certain coat colour characteristics.
Susceptibility to scrapie is known to be associated with polymorphisms at the prion protein (PrP) gene, and this association is the basis of current selective programmes implemented to control scrapie in many countries. However, these programmes might have unintended consequences for other traits that might be associated with PrP genotype. The objective of this study was to investigate the relationship between PrP genotype and coat colour characteristics in two UK native sheep breeds valued for their distinctive coat colour patterns. Coat colour pattern, darkness and spotting and PrP genotype records were available for 11 674 Badgerfaced Welsh Mountain and 2338 Shetland sheep. The data were analysed with a log-linear model using maximum likelihood. Results showed a strong significant association of PrP genotype with coat colour pattern in Badgerfaced Welsh Mountain and Shetland sheep and with the presence of white spotting in Shetland sheep. Animals with the ARR/ARR genotype (the most scrapie resistant) had higher odds of having a light dorsum and a dark abdomen than the reverse pattern. The implication of these associations is that selection to increase resistance to scrapie based only on PrP genotype could result in change in morphological diversity and affect other associated traits such as fitness.
Abstract.
Author URL.
Robinson MR, Wilson AJ, Pilkington JG, Clutton-Brock TH, Pemberton JM, Kruuk LEB (2009). The impact of environmental heterogeneity on genetic architecture in a wild population of Soay sheep.
Genetics,
181(4), 1639-1648.
Abstract:
The impact of environmental heterogeneity on genetic architecture in a wild population of Soay sheep.
This work demonstrates that environmental conditions experienced by individuals can shape their development and affect the stability of genetic associations. The implication of this observation is that the environmental response may influence the evolution of traits in the wild. Here, we examined how the genetic architecture of a suite of sexually dimorphic traits changed as a function of environmental conditions in an unmanaged population of Soay sheep (Ovis aries) on the island of Hirta, St. Kilda, northwest Scotland. We examined the stability of phenotypic, genetic, and environmental (residual) covariance in males during the first year of life between horn length, body weight, and parasite load in environments of different quality. We then examined the same covariance structures across environments within and between the adult sexes. We found significant genotype-by-environment interactions for lamb male body weight and parasite load, leading to a change in the genetic correlation among environments. Horn length was genetically correlated with body weight in males but not females and the genetic correlation among traits within and between the sexes was dependent upon the environmental conditions experienced during adulthood. Genetic correlations were smaller in more favorable environmental conditions, suggesting that in good environments, loci are expressed that have sex-specific effects. The reduction in genetic correlation between the sexes may allow independent evolutionary trajectories for each sex. This study demonstrates that the genetic architecture of traits is not stable under temporally varying environments and highlights the fact that evolutionary processes may depend largely upon ecological conditions.
Abstract.
Author URL.
Reed TE, Warzybok P, Wilson AJ, Bradley RW, Wanless S, Sydeman WJ (2009). Timing is everything: flexible phenology and shifting selection in a colonial seabird.
J Anim Ecol,
78(2), 376-387.
Abstract:
Timing is everything: flexible phenology and shifting selection in a colonial seabird.
1. In order to reproduce successfully in a temporally varying environment, iteroparous animals must exhibit considerable behavioural flexibility across their lifetimes. By adjusting timing of breeding each year, parents can ensure optimal overlap between the energy intensive period of offspring production and the seasonal peak in favourable environmental conditions, thereby increasing their chances of successfully rearing young. 2. Few studies investigate variation among individuals in how they respond to fluctuating conditions, or how selection acts on these individual differences, but this information is essential for understanding how populations will cope with rapid environmental change. 3. We explored inter-annual trends in breeding time and individual responses to environmental variability in common guillemots Uria aalge, an important marine top predator in the highly variable California Current System. Complex, nonlinear relationships between phenology and oceanic and climate variables were found at the population level. Using a novel application of a statistical technique called random regression, we showed that individual females responded in a nonlinear fashion to environmental variability, and that reaction norm shape differed among females. 4. The pattern and strength of selection varied substantially over a 34-year period, but in general, earlier laying was favoured. Females deviating significantly from the population mean laying date each year also suffered reduced breeding success, with the strength of nonlinear selection varying in relation to environmental conditions. 5. We discuss our results in the wider context of an emerging literature on the evolutionary ecology of individual-level plasticity in the wild. Better understanding of how species-specific factors and local habitat features affect the timing and success of breeding will improve our ability to predict how populations will respond to climate change.
Abstract.
Author URL.
Wilson AJ, Pemberton JM, Pilkington JG, Clutton-Brock TH, Kruuk LEB (2009). Trading offspring size for number in a variable environment: selection on reproductive investment in female Soay sheep.
J Anim Ecol,
78(2), 354-364.
Abstract:
Trading offspring size for number in a variable environment: selection on reproductive investment in female Soay sheep.
1. Given energetic constraints, female reproductive strategy is expected to be shaped by a trade-off between offspring size and offspring number, the optimal resolution of which may vary with environmental conditions. 2. We tested the hypothesis that selection will favour the production of larger litters, even at some expense to offspring size, under good conditions (and vice versa in harsh environments) using data from a long-term study of an unmanaged population of Soay sheep on the islands of St Kilda, NW Scotland. 3. Both litter size (which is either 1 or 2) and offspring birth weight are under positive selection through female annual fitness, but the strength of selection varies systematically with environmental conditions. Age effects were also detected, with selection weakening as female age increases. 4. Consistent with theoretical predictions, the selective trade-off between litter and offspring size is shifted in favour of the latter under poor environmental conditions. Thus, direct selection on offspring birth weight increases under harsh environmental conditions, particularly for females producing twins. 5. However, singletons are only favoured when environmental conditions are very poor, and offspring weight is constrained to be low. Thus, the current low incidence of twinning (13.5% of litters produced since 1985) appears to be suboptimal with respect to the empirically estimated selection regime. Thus, litter size, a trait known to be heritable, may be expected to evolve upwards in this population. 6. Our study highlights the necessity of incorporating environmental heterogeneity and age structure into analyses of natural selection, and suggests that the common assumption of optimality used in models of life history may sometimes be problematic.
Abstract.
Author URL.
2008
Ward PI, Wilson AJ, Reim C (2008). A cost of cryptic female choice in the yellow dung fly.
Genetica,
134(1), 63-67.
Abstract:
A cost of cryptic female choice in the yellow dung fly
Female dung flies Scathophaga stercoraria (L.) store sperm from several males in three or four spermathecae. Selection on the number of spermathecae was successful and the morphological intermediate stages in the evolution from three to four spermathecae are illustrated. The genetic quality of a male from a female's perspective depends on an interaction between their genotypes and the microhabitat in which the offspring will grow. Females influence the paternity pattern of their offspring, and do this differently in different microhabitats. Females with four spermathecae are better able to influence paternity than are those with three spermathecae. However, there must be a cost to building and maintaining an extra spermatheca. We estimate, using the animal model on pedigree data, that this cost is approximately five eggs per clutch, i.e. around 8% of the mean clutch size. This is a substantial cost and such costs should not be ignored in discussions of the benefits to females of assessing the genetic qualities of their mating partners. We suggest that the number of spermathecae in the study population is stable because the relative benefits in quality of offspring through cryptic female choice is balanced by the costs in total numbers of offspring. © 2007 Springer Science+Business Media B.V.
Abstract.
Gratten J, Wilson AJ, McRae AF, Beraldi D, Visscher PM, Pemberton JM, Slate J (2008). A localized negative genetic correlation constrains microevolution of coat color in wild sheep.
Science,
319(5861), 318-320.
Abstract:
A localized negative genetic correlation constrains microevolution of coat color in wild sheep
The evolutionary changes that occur over a small number of generations in natural populations often run counter to what is expected on the basis of the heritability of traits and the selective forces acting upon them. In Soay sheep, dark coat color is associated with large size, which is heritable and positively correlated with fitness, yet the frequency of dark sheep has decreased. This unexpected microevolutionary trend is explained by genetic linkage between the causal mutation underlying the color polymorphism and quantitative trait loci with antagonistic effects on size and fitness. As a consequence, homozygous dark sheep are large, but have reduced fitness relative to phenotypically indistinguishable dark heterozygotes and light sheep. This result demonstrates the importance of understanding the genetic basis of fitness variation when making predictions about the microevolutionary consequences of selection.
Abstract.
Pettay JE, Charmantier A, Wilson AJ, Lummaa V (2008). Age-specific genetic and maternal effects in fecundity of preindustrial Finnish women.
Evolution,
62(9), 2297-2304.
Abstract:
Age-specific genetic and maternal effects in fecundity of preindustrial Finnish women
A population's potential for evolutionary change depends on the amount of genetic variability expressed in traits under selection. Studies attempting to measure this variability typically do so over the life span of individuals, but theory suggests that the amount of additive genetic variance can change during the course of individuals' lives. Here we use pedigree data from historical Finns and a quantitative genetic framework to investigate how female fecundity, throughout an individual's reproductive life, is influenced by "maternal" versus additive genetic effects. We show that although maternal effects explain variation in female fecundity early in life, these effects wane with female age. Moreover, this decline in maternal effects is associated with a concomitant increase in additive genetic variance with age. Our results thus highlight that single over-lifetime estimates of trait heritability may give a misleading view of a trait's potential to respond to changing selection pressures. © 2008 the Author(s).
Abstract.
Pujol B, Wilson AJ, Ross RIC, Pannell JR (2008). Are Q<inf>ST</inf>-F<inf>ST</inf> comparisons for natural populations meaningful?.
Molecular Ecology,
17(22), 4782-4785.
Abstract:
Are QST-FST comparisons for natural populations meaningful?
Comparisons between putatively neutral genetic differentiation amongst populations, FST, and quantitative genetic variation, QST, are increasingly being used to test for natural selection. However, we find that approximately half of the comparisons that use only data from wild populations confound phenotypic and genetic variation. We urge the use of a clear distinction between narrow-sense QST, which can be meaningfully compared with FST, and phenotypic divergence measured between populations, PST, which is inadequate for comparisons in the wild. We also point out that an unbiased estimate of QST can be found using the so-called 'animal model' of quantitative genetics. © 2008 the Authors.
Abstract.
Wilson AJ, Rambaut A (2008). Breeding racehorses: What price good genes?.
Biology Letters,
4(2), 173-175.
Abstract:
Breeding racehorses: What price good genes?
Horse racing is a multi-million pound industry, in which genetic information is increasingly used to optimize breeding programmes. To maximize the probability of producing a successful offspring, the owner of a mare should mate her with a high-quality stallion. However, stallions with big reputations command higher stud fees and paying these is only a sensible strategy if, (i) there is a genetic variation for success on the racecourse and (ii) stud fees are an honest signal of a stallion's genetic quality. Using data on thoroughbred racehorses, and lifetime earnings from prize money (LE) as a measure of success, we performed quantitative genetic analyses within an animal model framework to test these two conditions. Although LE is heritable (V A=0.299±0.108, Pr=0.002), there is no genetic variance for stud fee and the genetic correlation between traits is therefore zero. This result is supported by an absence of any relationship between stud fees for currently active stallions and the predicted LE for their (hypothetical) offspring. Thus, while there are good genes to be bought, a stallion's fees are not an honest signal of his genetic quality and are a poor predictor of a foal's prize winning potential. © 2007 the Royal Society.
Abstract.
Wilson AJ, Charmantier A, Hadfield JD (2008). Evolutionary genetics of ageing in the wild: Empirical patterns and future perspectives.
Functional Ecology,
22(3), 431-442.
Abstract:
Evolutionary genetics of ageing in the wild: Empirical patterns and future perspectives
1. Classical evolutionary theory states that senescence should arise as a consequence of the declining force of selection late in life. Although the quantitative genetic predictions of hypotheses derived from this theory have been extensively tested in laboratory studies of invertebrate systems, relatively little is known about the genetics of ageing in the wild. 2. Data from long-term ecological studies is increasingly allowing quantitative genetic approaches to be used in studies of senescence in free-living populations of vertebrates. We review work to date and argue that the patterns are broadly consistent with theoretical predictions, although there is also a clear need for more empirical work. 3. We argue that further advances in this field of research might be facilitated by increased use of reaction norm models, and a decreased emphasis on attempting to discriminate between mutation accumulation and antagonistic pleiotropy models of senescence. We also suggest a framework for the better integration of environmental and genetic effects on ageing. 4. Finally, we discuss some of the difficulties in applying quantitative genetic models to studies of senescence outside the laboratory. In particular we highlight the problems that viability selection can cause for an accurate estimation of parameters used in the prediction of age-trajectory evolution. © 2008 the Authors.
Abstract.
Brommer JE, Rattiste K, Wilson AJ (2008). Exploring plasticity in the wild: Laying date-temperature reaction norms in the common gull Larus canus.
Proceedings of the Royal Society B: Biological Sciences,
275(1635), 687-693.
Abstract:
Exploring plasticity in the wild: Laying date-temperature reaction norms in the common gull Larus canus
Exploration of causal components of plasticity is important for insight into evolutionary dynamics and an organism's ability to respond to climate change. Among individuals, variation in plasticity can be due to genotype-environment interaction (G×E) or a result from environmental effects associated with an individual. We investigated plasticity for laying date in the common gulls Larus canus, using data collected in Estonia during 37 years (n=11624 records on 2262 females, with 472 relatives). We used a sliding window approach to find the period in spring during which mean temperature best explained the annual mean laying date. Then, considering the spring temperature as a quantitative description of the environment, we used pedigree information and a random regression animal model to determine the variation in plasticity for the laying date-temperature relationship. We found that individuals differ in the plasticity of laying date (such that there is increased variation among individuals for the laying date in warmer springs), and that approximately 11% of variation in the laying date is heritable, but we found no statistical support for G×E. Plasticity in this species is not constrained by warmer springs. © 2008 the Royal Society.
Abstract.
Breitling LPH, Wilson AJ, Raiko A, Lagog M, Siba P, Shaw MA, Quinnell RJ (2008). Heritability of human hookworm infection in Papua New Guinea.
Parasitology,
135(12), 1407-1415.
Abstract:
Heritability of human hookworm infection in Papua New Guinea
Hookworms infect approximately 740 million humans worldwide and are an important cause of morbidity. The present study examines the role of additive genetic effects in determining the intensity of hookworm infection in humans, and whether these effects vary according to the sex of the host. Parasitological and epidemiological data for a population of 704 subjects in Papua New Guinea were used in variance components analysis. The 'narrow-sense' heritability of hookworm infection was estimated as 0.15±0.04 (P
Abstract.
Kruuk LEB, Slate J, Wilson AJ (2008). New answers for old questions: the evolutionary quantitative genetics of wild animal populations.
Annual Review of Ecology, Evolution, and Systematics,
39, 525-548.
Abstract:
New answers for old questions: the evolutionary quantitative genetics of wild animal populations
Recent years have seen a rapid expansion in the scope of quantitative genetic analyses undertaken in wild populations. We illustrate here the potential for such studies to address fundamental evolutionary questions about the maintenance of genetic diversity and to reveal hidden genetic conflicts or constraints not apparent at the phenotypic level. Trade-offs between different components of fitness, sexually-antagonistic genetic effects, maternal effects, genotype-by-environment interactions, genotype-by-age interactions, and variation between different regions of the genome in localized genetic correlations may all prevent the erosion of genetic variance. We consider ways in which complex interactions between ecological conditions and the expression of genetic variation can be elucidated, and emphasize the benefits of conducting selection analyses within a quantitative genetic framework. We also review potential developments associated with rapid advances in genomic technology, in particular the increased availability of extensive marker information. Our conclusions highlight the complexity of processes contributing to the maintenance of genetic diversity in wild populations, and underline the value of a quantitative genetic approach in parameterizing models of life-history evolution. Copyright © 2008 by Annual Reviews. All rights reserved.
Abstract.
Adams CE, Wilson AJ, Ferguson MM (2008). Parallel divergence of sympatric genetic and body size forms of Arctic charr, Salvelinus alpinus, from two Scottish lakes.
Biological Journal of the Linnean Society,
95(4), 748-757.
Abstract:
Parallel divergence of sympatric genetic and body size forms of Arctic charr, Salvelinus alpinus, from two Scottish lakes
FST and RST estimates for Arctic charr from six microsatelite markers collected from two neighbouring Scottish lakes, Loch Maree and Loch Stack, confirm the presence of two distinct genetic groupings representing separate populations within each lake. In both lakes, there was also a clear body size dimorphism, with large and small body size forms that segregated according to genetic grouping. There was evidence of only subtle foraging ecology differences between morphs, with the small body size morph in both lakes being more generalist in its foraging in the summer (consuming mostly plankton but also some macrobenthos) than the large body size morph, which specialized on planktonic prey. Trophic morphology (head and mouth shape) did not differ significantly between morphs (although the small sample size for Maree makes this a preliminary finding). Cluster analysis of the microsatelite data and the presence of private alleles showed that morphologically similar forms in different lakes were not genetically similar, as would be expected under a multiple invasion hypothesis. Thus, the data do not support a hypothesis of a dual invasion of both lakes by two common ancestors but instead suggest an independent origin of the two forms in each lake. Thus parallel sympatric divergence as a result of common selection pressures in both lakes is the most parsimonious explanation of the evolutionary origin of these polymorphisms. © 2008 the Linnean Society of London.
Abstract.
Poissant J, Wilson AJ, Festa-Bianchet M, Hogg JT, Coltman DW (2008). Quantitative genetics and sex-specific selection on sexually dimorphic traits in bighorn sheep.
Proceedings of the Royal Society B: Biological Sciences,
275(1635), 623-628.
Abstract:
Quantitative genetics and sex-specific selection on sexually dimorphic traits in bighorn sheep
Sexual conflict at loci influencing traits shared between the sexes occurs when sex-specific selection pressures are antagonistic relative to the genetic correlation between the sexes. To assess whether there is sexual conflict over shared traits, we estimated heritability and intersexual genetic correlations for highly sexually dimorphic traits (horn volume and body mass) in a wild population of bighorn sheep (Ovis canadensis) and quantified sex-specific selection using estimates of longevity and lifetime reproductive success. Body mass and horn volume showed significant additive genetic variance in both sexes, and intersexual genetic correlations were 0.24±0.28 for horn volume and 0.63±0.30 for body mass. For horn volume, selection coefficients did not significantly differ from zero in either sex. For body weight, selection coefficients were positive in females but did not differ from zero in males. The absence of detectable sexually antagonistic selection suggests that currently there are no sexual conflicts at loci influencing horn volume and body mass. © 2008 the Royal Society.
Abstract.
Nussey DH, Wilson AJ, Morris A, Pemberton J, Clutton-Brock T, Kruuk LEB (2008). Testing for genetic trade-offs between early- and late-life reproduction in a wild red deer population.
Proceedings of the Royal Society B: Biological Sciences,
275(1635), 745-750.
Abstract:
Testing for genetic trade-offs between early- and late-life reproduction in a wild red deer population
The antagonistic pleiotropy (AP) theory of ageing predicts genetically based trade-offs between investment in reproduction in early life and survival and performance in later life. Laboratory-based research has shown that such genetic trade-offs exist, but little is currently known about their prevalence in natural populations. We used random regression 'animal model' techniques to test the genetic basis of trade-offs between early-life fecundity (ELF) and maternal performance in late life in a wild population of red deer (Cervus elaphus) on the Isle of Rum, Scotland. Significant genetic variation for both ageing rates in a key maternal performance measure (offspring birth weight) and ELF was present in this population. We found some evidence for a negative genetic covariance between the rate of ageing in offspring birth weight and ELF, and also for a negative environmental covariance. Our results suggest rare support for the AP theory of ageing from a wild population. © 2008 the Royal Society.
Abstract.
Wilson AJ (2008). Why h<sup>2</sup> does not always equal V<inf>A</inf>/V<inf>P</inf>?.
Journal of Evolutionary Biology,
21(3), 647-650.
Abstract:
Why h2 does not always equal VA/VP?
Over the last decade, there has been a rapid growth in the application of quantitative genetic techniques to evolutionary studies of natural populations. Whereas this work yields enormous insight into evolutionary processes in the wild, the use of modelling techniques and strategies adopted from animal breeders means that estimates of trait heritabilities (h2) are highly vulnerable to misinterpretation. Specifically, when estimated using animal models, h2 will not generally be comparable across studies and must be interpreted as being conditioned on any fixed effects included in the model. Failure to realize the model dependency of published h2 estimates will give a very misleading, and in most cases upwardly biased, impression of the potential for trait evolution. © 2008 the Author.
Abstract.
2007
Morrissey MB, Wilson AJ, Pemberton JM, Ferguson MM (2007). A framework for power and sensitivity analyses for quantitative genetic studies of natural populations, and case studies in Soay sheep (Ovis aries).
J Evol Biol,
20(6), 2309-2321.
Abstract:
A framework for power and sensitivity analyses for quantitative genetic studies of natural populations, and case studies in Soay sheep (Ovis aries).
Studies of the quantitative genetics of natural populations have contributed greatly to evolutionary biology in recent years. However, while pedigree data required are often uncertain (i.e. incomplete and partly erroneous) and limited, means to evaluate the effects of such uncertainties have not been developed. We have therefore developed a general framework for power and sensitivity analyses of such studies. We propose that researchers first generate a set of pedigree data that they wish to use in a quantitative genetic study, as well as data regarding errors that occur in that pedigree. This pedigree is then permuted using the data regarding errors to generate hypothetical 'true' and 'assumed' pedigrees that differ so as to mimic pedigree errors that might occur in the study system under consideration. Phenotypic data are then simulated across the true pedigree (according to user-defined genetic and environmental covariance structures), before being analysed with standard quantitative genetic techniques in conjunction with the 'assumed' pedigree data. To illustrate this approach, we conducted power and sensitivity analyses in a well-known study of Soay sheep (Ovis aries). We found that, although the estimation of simple genetic (co)variance structures is fairly robust to pedigree errors, some potentially serious biases were detected under more complex scenarios involving maternal effects. Power analyses also showed that this study system provides high power to detect heritabilities as low as about 0.09. Given this range of results, we suggest that such power and sensitivity analyses could greatly complement empirical studies, and we provide the computer program PEDANTICS to aid in their application.
Abstract.
Author URL.
Wilson AJ, Nussey DH, Pemberton JM, Pilkington JG, Morris A, Pelletier F, Clutton-Brock TH, Kruuk LEB (2007). Evidence for a genetic basis of aging in two wild vertebrate populations.
Curr Biol,
17(24), 2136-2142.
Abstract:
Evidence for a genetic basis of aging in two wild vertebrate populations.
Aging, or senescence, defined as a decline in physiological function with age, has long been a focus of research interest for evolutionary biologists. How has natural selection failed to remove genetic effects responsible for such reduced fitness among older individuals? Current evolutionary theory explains this phenomenon by showing that, as a result of the risk of death from environmental causes that individuals experience, the force of selection inevitably weakens with age. This in turn means that genetic mutations having detrimental effects that are only felt late in life might persist in a population. Although widely accepted, this theory rests on the assumption that there is genetic variation for aging in natural systems, or (equivalently), that genotype-by-age interactions (GxA) occur for fitness. To date, empirical support for this assumption has come almost entirely from laboratory studies on invertebrate systems, most notably Drosophila and C. elegans, whereas tests of genetic variation for aging are largely lacking from natural populations. By using data from two wild mammal populations, we perform quantitative genetic analyses of fitness and provide the first evidence for a genetic basis of senescence to come from a study in the natural environment. We find evidence that genetic differences among individuals cause variation in their rates of aging and that additive genetic variance for fitness increases with age, as predicted by the evolutionary theory of senescence.
Abstract.
Author URL.
Brommer JE, Wilson AJ, Gustafsson L (2007). Exploring the genetics of aging in a wild passerine bird.
American Naturalist,
170(4), 643-650.
Abstract:
Exploring the genetics of aging in a wild passerine bird
Senescence is the decline in survival and reproduction as an organism ages and is known to occur in collared flycatchers Ficedula albicollis. We consider annual fitness (the estimated genetic contribution that an individual makes to next year's gene pool) as a measure of age-specific fitness. We apply a restricted maximum likelihood linear mixed-model approach on 25 years of data on 3,844 male and 4,992 female collared flycatchers. Annual fitness had a significant additive genetic component (h2 of about 4%). Annual fitness declined at later ages in both sexes. Using a random regression animal model, we show that the observed age-related phenotypic changes in annual fitness were not present on the additive genetic level, contrary to predictions of genetic hypotheses of senescence. Our study suggests that patterns of aging in the wild need to be interpreted with caution in terms of underlying genetics because they may be largely determined by environmental processes. © 2007 by the University of Chicago. All rights reserved.
Abstract.
Hadfield JD, Wilson AJ (2007). Multilevel selection 3: modeling the effects of interacting individuals as a function of group size.
Genetics,
177(1), 667-668.
Abstract:
Multilevel selection 3: modeling the effects of interacting individuals as a function of group size.
Bijma et al. (2007a,b) presented a quantitative genetic theory of multilevel selection and showed how to estimate the relevant parameters using standard restricted maximum-likelihood (REML) methodology. Extending their results we develop a wider class of models that provide a more realistic framework for capturing the effects of interacting individuals. These models also make use of standard REML techniques and include the original model as a special case.
Abstract.
Author URL.
Adams CE, Fraser D, Wilson AJ, Alexander G, Ferguson MM, Skulason S (2007). Patterns of phenotypic and genetic variability show hidden diversity in Scottish Arctic charr.
Ecology of Freshwater Fish,
16(1), 78-86.
Abstract:
Patterns of phenotypic and genetic variability show hidden diversity in Scottish Arctic charr
This study examined the degree and pattern of variability in trophic morphology in Arctic charr (Salvelinus alpinus L.) at three spatial scales: across 22 populations from Scotland and between and within two adjacent catchments (Laxford and Shin) in northern Scotland. In addition, the variability at six microsatellite loci between and within the Laxford and Shin systems was determined. Habitat use by charr differed significantly between populations. The pattern of variability in trophic morphology, known to influence foraging ability in charr, showed a very high degree of between-population variation with at least 52% of population pairs showing significant differences in head shape. Trophic morphology and genetic variation was also high over small geographical scales; variation being as high between charr from lakes within the same catchment, as between adjacent catchments. The pattern of both phenotypic and genotypic variation suggests a mosaic of variation across populations with geographically close populations often as distinct from each other as populations with much greater separation. Very low levels of effective migrants between populations, even within the same catchment, suggest that this variation is being maintained by very low straying rates between phenotypically and genetically distinct populations, even when there is no apparent barrier to movement. We conclude that the genetic and phenotypic integrity of charr populations across Scotland is high and that this adaptive radiation constitutes a 'hidden' element of diversity in northern freshwater systems. Two consequences of this are that the population (rather than the species) makes a more rational unit for the consideration of conservation strategies and that the habitat requirements and therefore management needs may differ significantly between populations. © 2007 Blackwell Munksgaard.
Abstract.
Wilson AJ, Pemberton JM, Pilkington JG, Clutton-Brock TH, Coltman DW, Kruuk LEB (2007). Quantitative genetics of growth and cryptic evolution of body size in an island population.
Evolutionary Ecology,
21(3), 337-356.
Abstract:
Quantitative genetics of growth and cryptic evolution of body size in an island population
While evolution occurs when selection acts on a heritable trait, empirical studies of natural systems have frequently reported phenotypic stasis under these conditions. We performed quantitative genetic analyses of weight and hindleg length in a free-living population of Soay sheep (Ovis aries) to test whether genetic constraints can explain previously reported stasis in body size despite evidence for strong positive directional selection. Genetic, maternal and environmental covariance structures were estimated across ontogeny using random regression animal models. Heritability increased with age for weight and hindleg length, though both measures of size were highly heritable across ontogeny. Genetic correlations among ages were generally strong and uniformly positive, and the covariance structures were also highly integrated across ontogeny. Consequently, we found no constraint to the evolution of larger size itself. Rather we expect size at all ages to increase in response to positive selection acting at any age. Consistent with expectation, predicted breeding values for age-specific size traits have increased over a twenty-year period, while maternal performance for offspring size has declined. Re-examination of the phenotypic data confirmed that sheep are not getting larger, but also showed that there are significant negative trends in size at all ages. The genetic evolution is therefore cryptic, with the response to selection presumably being masked at the phenotypic level by a plastic response to changing environmental conditions. Density-dependence, coupled with systematically increasing population size, may contribute to declining body size but is insufficient to completely explain it. Our results demonstrate that an increased understanding of the genetic basis of quantitative traits, and of how plasticity and microevolution can occur simultaneously, is necessary for developing predictive models of phenotypic change in nature. © 2006 Springer Science+Business Media B.V.
Abstract.
Nussey DH, Wilson AJ, Brommer JE (2007). The evolutionary ecology of individual phenotypic plasticity in wild populations.
Journal of Evolutionary Biology,
20(3), 831-844.
Abstract:
The evolutionary ecology of individual phenotypic plasticity in wild populations
The ability of individual organisms to alter morphological and life-history traits in response to the conditions they experience is an example of phenotypic plasticity which is fundamental to any population's ability to deal with short-term environmental change. We currently know little about the prevalence, and evolutionary and ecological causes and consequences of variation in life history plasticity in the wild. Here we outline an analytical framework, utilizing the reaction norm concept and random regression statistical models, to assess the between-individual variation in life history plasticity that may underlie population level responses to the environment at both phenotypic and genetic levels. We discuss applications of this framework to date in wild vertebrate populations, and illustrate how natural selection and ecological constraint may alter a population's response to the environment through their effects at the individual level. Finally, we present future directions and challenges for research into individual plasticity. © 2007 the Authors.
Abstract.
2006
Adams CE, Hamilton DJ, Mccarthy I, Wilson AJ, Grant A, Alexander G, Waldron S, Snorasson SS, Ferguson MM, Skúlason S, et al (2006). Does breeding site fidelity drive phenotypic and genetic sub-structuring of a population of arctic charr?.
Evolutionary Ecology,
20(1), 11-26.
Abstract:
Does breeding site fidelity drive phenotypic and genetic sub-structuring of a population of arctic charr?
There is now increasing acceptance that divergence of phenotypic traits, and the genetic structuring that underlie such divergence, can occur in sympatry. Here we report the serendipitous discovery of a sympatric polymorphism in the upper Forth catchment, Scotland, in a species for which high levels of phenotypic variation have been reported previously, the Arctic charr, Salvelinus alpinus. Attempting to determine the proximate mechanisms through which this pattern of phenotypic variation is maintained, we examine the use of the available feeding resource and the genotypic and phenotypic structure of charr in this system. We show clear differences in head morphology between charr from three very closely connected lakes with no barrier to movement (Lochs Doine, Voil and Lubnaig) and also differences in muscle stable isotope signatures and in stomach contents. There were significant differences at 6 microsatelite loci (between Lubnaig and the other two lochs) and very low estimates of effective migration between populations. We conclude that, despite living in effective sympatry, strong genetic and phenotypic sub-structuring is likely maintained by very high levels of site fidelity, especially during spawning, resulting in functional allopatric divergence of phenotype. © Springer 2006.
Abstract.
Wilson AJ, Pemberton JM, Pilkington JG, Coltman DW, Mifsud DV, Clutton-Brock TH, Kruuk LEB (2006). Environmental coupling of selection and heritability limits evolution.
PLoS Biol,
4(7).
Abstract:
Environmental coupling of selection and heritability limits evolution.
There has recently been great interest in applying theoretical quantitative genetic models to empirical studies of evolution in wild populations. However, while classical models assume environmental constancy, most natural populations exist in variable environments. Here, we applied a novel analytical technique to a long-term study of birthweight in wild sheep and examined, for the first time, how variation in environmental quality simultaneously influences the strength of natural selection and the genetic basis of trait variability. In addition to demonstrating that selection and genetic variance vary dramatically across environments, our results show that environmental heterogeneity induces a negative correlation between these two parameters. Harsh environmental conditions were associated with strong selection for increased birthweight but low genetic variance, and vice versa. Consequently, the potential for microevolution in this population is constrained by either a lack of heritable variation (in poor environments) or by a reduced strength of selection (in good environments). More generally, environmental dependence of this nature may act to limit rates of evolution, maintain genetic variance, and favour phenotypic stasis in many natural systems. Assumptions of environmental constancy are likely to be violated in natural systems, and failure to acknowledge this may generate highly misleading expectations for phenotypic microevolution.
Abstract.
Author URL.
Wilson AJ, Pemberton JM, Pilkington JG, Coltman DW, Mifsud DV, Clutton-Brock TH, Kruuk LE (2006). Environmental coupling of selection and heritability limits evolution.
PLoS biology,
4(7).
Abstract:
Environmental coupling of selection and heritability limits evolution.
There has recently been great interest in applying theoretical quantitative genetic models to empirical studies of evolution in wild populations. However, while classical models assume environmental constancy, most natural populations exist in variable environments. Here, we applied a novel analytical technique to a long-term study of birthweight in wild sheep and examined, for the first time, how variation in environmental quality simultaneously influences the strength of natural selection and the genetic basis of trait variability. In addition to demonstrating that selection and genetic variance vary dramatically across environments, our results show that environmental heterogeneity induces a negative correlation between these two parameters. Harsh environmental conditions were associated with strong selection for increased birthweight but low genetic variance, and vice versa. Consequently, the potential for microevolution in this population is constrained by either a lack of heritable variation (in poor environments) or by a reduced strength of selection (in good environments). More generally, environmental dependence of this nature may act to limit rates of evolution, maintain genetic variance, and favour phenotypic stasis in many natural systems. Assumptions of environmental constancy are likely to be violated in natural systems, and failure to acknowledge this may generate highly misleading expectations for phenotypic microevolution.
Abstract.
Wilson AJ, Reale D (2006). Ontogeny of additive and maternal genetic effects: lessons from domestic mammals.
Am Nat,
167(1), E23-E38.
Abstract:
Ontogeny of additive and maternal genetic effects: lessons from domestic mammals.
Evolution of size and growth depends on heritable variation arising from additive and maternal genetic effects. Levels of heritable (and nonheritable) variation might change over ontogeny, increasing through "variance compounding" or decreasing through "compensatory growth." We test for these processes using a meta-analysis of age-specific weight traits in domestic ungulates. Generally, mean standardized variance components decrease with age, consistent with compensatory growth. Phenotypic convergence among adult sheep occurs through decreasing environmental and maternal genetic variation. Maternal variation similarly declines in cattle. Maternal genetic effects are thus reduced with age (both in absolute and relative terms). Significant trends in heritability (decreasing in cattle, increasing in sheep) result from declining maternal and environmental components rather than from changing additive variation. There was no evidence for increasing standardized variance components. Any compounding must therefore be masked by more important compensatory processes. While extrapolation of these patterns to processes in natural population is difficult, our results highlight the inadequacy of assuming constancy in genetic parameters over ontogeny. Negative covariance between direct and maternal genetic effects was common. Negative correlations with additive and maternal genetic variances indicate that antagonistic pleiotropy (between additive and maternal genetic effects) may maintain genetic variance and limit responses to selection.
Abstract.
Author URL.
2005
Wilson AJ, Coltman DW, Pemberton JM, Overall ADJ, Byrne KA, Kruuk LEB (2005). Maternal genetic effects set the potential for evolution in a free-living vertebrate population.
J Evol Biol,
18(2), 405-414.
Abstract:
Maternal genetic effects set the potential for evolution in a free-living vertebrate population.
Heritable maternal effects have important consequences for the evolutionary dynamics of phenotypic traits under selection, but have only rarely been tested for or quantified in evolutionary studies. Here we estimate maternal effects on early-life traits in a feral population of Soay sheep (Ovis aries) from St Kilda, Scotland. We then partition the maternal effects into genetic and environmental components to obtain the first direct estimates of maternal genetic effects in a free-living population, and furthermore test for covariance between direct and maternal genetic effects. Using an animal model approach, direct heritabilities (h2) were low but maternal genetic effects (m2) represented a relatively large proportion of the total phenotypic variance for each trait (birth weight m2=0.119, birth date m2=0.197, natal litter size m2=0.211). A negative correlation between direct and maternal genetic effects was estimated for each trait, but was only statistically significant for natal litter size (ram= -0.714). Total heritabilities (incorporating variance from heritable maternal effects and the direct-maternal genetic covariance) were significant for birth weight and birth date but not for natal litter size. Inadequately specified models greatly overestimated additive genetic variance and hence direct h2 (by a factor of up to 6.45 in the case of birth date). We conclude that failure to model heritable maternal variance can result in over- or under-estimation of the potential for traits to respond to selection, and advocate an increased effort to explicitly measure maternal genetic effects in evolutionary studies.
Abstract.
Author URL.
Wilson AJ, Kruuk LEB, Coltman DW (2005). Ontogenetic patterns in heritable variation for body size: using random regression models in a wild ungulate population.
Am Nat,
166(6), E177-E192.
Abstract:
Ontogenetic patterns in heritable variation for body size: using random regression models in a wild ungulate population.
Body size is an important determinant of fitness in many organisms. While size will typically change over the lifetime of an individual, heritable components of phenotypic variance may also show ontogenetic variation. We estimated genetic (additive and maternal) and environmental covariance structures for a size trait (June weight) measured over the first 5 years of life in a natural population of bighorn sheep Ovis canadensis. We also assessed the utility of random regression models for estimating these structures. Additive genetic variance was found for June weight, with heritability increasing over ontogeny because of declining environmental variance. This pattern, mirrored at the phenotypic level, likely reflects viability selection acting on early size traits. Maternal genetic effects were significant at ages 0 and 1, having important evolutionary implications for early weight, but declined with age being negligible by age 2. Strong positive genetic correlations between age-specific traits suggest that selection on June weight at any age will likely induce positively correlated responses across ontogeny. Random regression modeling yielded similar results to traditional methods. However, by facilitating more efficient data use where phenotypic sampling is incomplete, random regression should allow better estimation of genetic (co)variances for size and growth traits in natural populations.
Abstract.
Author URL.
Wilson AJ, Pilkington JG, Pemberton JM, Coltman DW, Overall ADJ, Byrne KA, Kruuk LEB (2005). Selection on mothers and offspring: whose phenotype is it and does it matter?.
Evolution,
59(2), 451-463.
Abstract:
Selection on mothers and offspring: whose phenotype is it and does it matter?
Reproductive and early life-history traits can be considered aspects of either offspring or maternal phenotype, and their evolution will therefore depend on selection operating through offspring and maternal components of fitness. Furthermore, selection at these levels may be antagonistic, with optimal offspring and maternal fitness occurring at different phenotypic values. We examined selection regimes on the correlated traits of birth weight, birth date, and litter size in Soay sheep (Ovis aries) using data from a long-term study of a free-living population on the archipelago of St. Kilda, Scotland. We tested the hypothesis that selective constraints on the evolution of the multivariate phenotype arise through antagonistic selection, either acting at offspring and maternal levels, or on correlated aspects of phenotype. All three traits were found to be under selection through variance in short-term and lifetime measures of fitness. Analysis of lifetime fitness revealed strong positive directional selection on birth weight and weaker selection for increased birth date at both levels. However, there was also evidence for stabilizing selection on these traits at the maternal level, with reduced fitness at high phenotypic values indicating lower phenotypic optima for mothers than for offspring. Additionally, antagonistic selection was found on litter size. From the offspring's point of view it is better to be born a singleton, whereas maternal fitness increases with average litter size. The decreased fitness of twins is caused by their reduced birth weight; therefore, this antagonistic selection likely results from trade-offs between litter size and birth weight that have different optimal resolutions with respect to offspring and maternal fitness. Our results highlight how selection regimes may vary depending on the assignment of reproductive and early life-history traits to either offspring or maternal phenotype.
Abstract.
Author URL.
Morrissey MB, Wilson AJ (2005). The potential costs of accounting for genotypic errors in molecular parentage analyses. Molecular Ecology, 14, 4111-4121.
2004
Wilson AJ, Hutchings JA, Ferguson MM (2004). Dispersal in a stream dwelling salmonid: Inferences from tagging and microsatellite studies.
Conservation Genetics,
5(1), 25-37.
Abstract:
Dispersal in a stream dwelling salmonid: Inferences from tagging and microsatellite studies
We used both direct (mark-recapture) and indirect (microsatellite analysis) methodologies to investigate dispersal between two putative populations of brook charr (Salvelinus fontinalis) in Freshwater River, Cape Race, Newfoundland, Canada. Over a 5-year study period, mark-recapture data revealed some movement by fish, but the proportion of recaptured fish migrating from one population area to another was low (0-4.1%). Additionally, during sampling periods in the spawning seasons, no fish was found in the alternate population area to that of its first capture. Despite this pattern of limited movement, microsatellite analysis based on sixteen polymorphic loci provided no evidence of genetic differentiation. Indirect estimates of dispersal parameters varied greatly between different methods of analysis. While use of a coalescent-based model yielded estimated migration rates congruent with the results of the mark-recapture study, other methods resulted in much higher estimates of migration between the populations. In particular, the lack of genetic differentiation coupled with likely violations of the assumed island model prevented generation of meaningful estimates of dispersal using Fst. The disparities between migration rates estimated from the mark-recapture work and from the different indirect methods highlight the difficulties of using indirect methods to estimate dispersal on an ecological timescale. However, mark-recapture methods can fail to detect historical or episodic movement that is important in an evolutionary context, and we therefore argue that a combination of direct and indirect methods can provide a more complete picture of dispersal than either approach alone.
Abstract.
Wilson AJ, Gíslason D, Skúlason S, Snorrason SS, Adams CE, Alexander G, Danzmann RG, Ferguson MM (2004). Population genetic structure of Arctic charr, Salvelinus alpinus from northwest Europe on large and small spatial scales.
Mol Ecol,
13(5), 1129-1142.
Abstract:
Population genetic structure of Arctic charr, Salvelinus alpinus from northwest Europe on large and small spatial scales.
To examine the population genetic structure of lake-resident Arctic charr, Salvelinus alpinus from northwest Europe on multiple spatial scales, 2367 individuals from 43 lakes located in three geographical regions (Iceland, the British Isles and Scandinavia) were genotyped at six microsatellite loci. On a large scale, data provided little evidence to support clustering of populations according to geographical region. Hierarchical analysis of molecular variance indicated that, although statistically significant, only 2.17% of the variance in allelic frequencies was partitioned at the among-region level. Within regions, high levels of genetic differentiation were typically found between lakes regardless of the geographical distance separating them. These results are consistent with the hypothesis of rapid postglacial recolonization of all of northwest Europe from a single charr lineage, with subsequent restriction of gene flow. On a smaller scale, there was evidence for close genetic relationships among lakes from within common drainage basins in Scotland. Thus, interlake genetic structure reflects localized patterns of recent (or contemporary) gene flow superimposed onto a larger scale structure that is largely a result of historical processes. There was also evidence for widespread genetic structuring at the within-lake level, with sympatric populations detected in 10 lakes, and multilocus heterozygote deficits found in 23 lakes. This evidence of the Wahlund effect was found in all lakes known to contain discrete phenotypic morphs, as well as many others, suggesting that morphs may often represent separate breeding populations, and also that the phenomenon of polymorphism in this species may be more widespread than is currently realized.
Abstract.
Author URL.
2003
Wilson AJ, McDonald G, Moghadam HK, Herbinger CM, Ferguson MM (2003). Marker-assisted estimation of quantitative genetic parameters in rainbow trout, Oncorhynchus mykiss.
Genetical Research,
81(2), 145-156.
Abstract:
Marker-assisted estimation of quantitative genetic parameters in rainbow trout, Oncorhynchus mykiss
Estimation of quantitative genetic parameters conventionally requires known pedigree structure. However, several methods have recently been developed to circumvent this requirement by inferring relationship structure from molecular marker data. Here, two such marker-assisted methodologies were used and compared in an aquaculture population of rainbow trout (Oncorhynchus mykiss). Firstly a regression-based model employing estimates of pairwise relatedness was applied, and secondly a Markov Chain Monte Carlo (MCMC) procedure was employed to reconstruct full-sibships and hence an explicit pedigree. While both methods were effective in detecting significant components of genetic variance and covariance for size and spawning time traits, the regression model resulted in estimates that were quantitatively unreliable, having both significant bias and low precision. This result can be largely attributed to poor performance of the pairwise relatedness estimator. In contrast, genetic parameters estimated from the reconstructed pedigree showed close agreement with ideal values obtained from the true pedigree. Although not significantly biased, parameters based on the reconstructed pedigree were underestimated relative to ideal values. This was due to the complex structure of the true pedigree in which high numbers of half-sibling relationships resulted in inaccurate partitioning of full-sibships, and additional unrecognized relatedness between families.
Abstract.
Wilson AJ, Hutchings JA, Ferguson MM (2003). Selective and genetic constraints on the evolution of body size in a stream-dwelling salmonid fish.
J Evol Biol,
16(4), 584-594.
Abstract:
Selective and genetic constraints on the evolution of body size in a stream-dwelling salmonid fish.
To examine constraints on evolution of larger body size in two stunted populations of brook charr (Salvelinus fontinalis) from a single river in Cape Race, Newfoundland, Canada, we measured viability selection acting on length-at-age traits, and estimated quantitative genetic parameters in situ (following reconstruction of pedigree information from microsatellite data). Furthermore we tested for phenotypic differentiation between the populations, and for association of high juvenile growth with early maturity that is predicted by life history theory. Within each population, selection differentials and estimates of heritabilities for length-at-age traits suggested that evolution of larger size is prevented by both selective and genetic constraints. Between the populations, phenotypic differentiation was found in length-at-age and age of maturation traits, whereas early maturation was associated with increased juvenile growth (relative to adult growth) both within and between populations. The results suggest an adaptive plastic response in age of maturation to juvenile growth rates that have a largely environmental basis of determination.
Abstract.
Author URL.
2002
Wilson AJ, Ferguson MM (2002). Molecular pedigree analysis in natural populations of fishes: approaches, applications, and practical considerations. Canadian Journal of Fisheries and Aquatic Sciences(59), 1696-1707.
