Publications by year
Weiss MN, Ellis S, Franks DW, Nielsen MLK, Cant MA, Johnstone RA, Ellifrit DK, Balcomb KC, Croft DP
(2023). Costly lifetime maternal investment in killer whales. Curr Biol
Costly lifetime maternal investment in killer whales.
Parents often sacrifice their own future reproductive success to boost the survival of their offspring, a phenomenon referred to as parental investment. In several social mammals, mothers continue to improve the survival of their offspring well into adulthood;1,2,3,4,5 however, whether this extended care comes at a reproductive costs to mothers, and therefore represents maternal investment, is not well understood. We tested whether lifetime maternal care is a form of parental investment in fish-eating "resident" killer whales. Adult killer whales, particularly males, are known to receive survival benefits from their mothers;3 however, whether this comes at a cost to mothers' reproductive success is not known. Using multiple decades of complete census data from the "southern resident" population, we found a strong negative correlation between females' number of surviving weaned sons and their annual probability of producing a viable calf. This negative effect did not attenuate as sons grew older, and the cost of sons could not be explained by long-term costs of lactation or group composition effects, supporting the hypothesis that caring for adult sons is reproductively costly. This is the first direct evidence of lifetime maternal investment in an iteroparous animal, revealing a previously unknown life history strategy. Abstract
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Padget RFB, Cant MA, Thompson FJ
(2023). Us, them, and the others: Testing for discrimination amongst outgroups in a single-piece nesting termite, Zootermopsis angusticollis. Ecol Evol
Us, them, and the others: Testing for discrimination amongst outgroups in a single-piece nesting termite, Zootermopsis angusticollis.
Recognition of group members is an important adaptation in social organisms because it allows help to be directed toward kin or individuals that are likely to reciprocate, and harm to be directed toward members of competing groups. Evidence in a wide range of animals shows that responses to outgroups vary with context, suggesting that cues to group membership also depend on the social or environmental context. In termites, intergroup encounters are frequent and their outcomes highly variable, ranging from destruction of a colony to colony fusion. As well as genetic factors, nestmate recognition in social insects commonly relies on cues that are mediated by environmental factors such as food source. However, single-piece nesting termite colonies share nesting material and food source with rival colonies (their wood substrate serves as both). In principle, the shared environment of single-piece nesting termite colonies could constrain their ability to identify non-nestmates, contributing to some of the variation seen in encounters, but this has not been investigated. In this study, we raised incipient colonies of a single-piece nesting termite, Zootermopsis angusticollis, on two different wood types and conducted behavioral assays to test whether nestmate discrimination can be constrained by common environmental conditions. We found that non-nestmates elicited higher rates of identity checking and defense behavior compared to nestmates, but there was no effect of wood type on the strength of behavioral responses to non-nestmates. We also found that one key cooperative behavior (allogrooming) was performed equally toward both nestmates and non-nestmates. These findings offer no support for the hypothesis that common wood type constrains the nestmate recognition system of single piece nesting termites. We suggest that where groups encounter each other frequently in a common environment, selection will favor discrimination based on genetic and/or higher resolution environmentally mediated cues. Abstract
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(2022). Collective decision-making in the face of intergroup. conflict: theory and tests.
Collective decision-making in the face of intergroup. conflict: theory and tests
Recently many studies have been published that describe and explain how Abstract
groups of social animals make collective decisions and coordinate their actions.
However, these studies mostly focus on isolated groups, and do not consider how
these groups might behave under different social contexts, such as when there
is the threat of fighting with rival groups. In this thesis, I present two
complementary theoretical models that explore how simple differences in
leadership and decision-making dynamics within groups can have large impacts
on the investment and initiation of intergroup conflict.
In Chapter One, I present an agent-based model of intergroup conflict to
investigate how the presence of leaders and followers influences the dynamics
of conflict initiation and conflict investment. I find that changing different
parameters such as maximum group size, migration rate and intergroup
encounter rate cause either between or within group competition to be
emphasised which changes the levels of conflict investment. When between group competition is low, follower investment in conflict is low and leaders are
forced to overcompensate and contribute (“heroic leadership”). However, when
between-group competition is high, follower investment in conflict is high and
leaders can free-ride and do not contribute (“exploitative leadership”). We find
that when followers contribute then leaders are incentivised to behave more
aggressively and initiate more intergroup conflict.
In Chapter Two, I present a theoretical model to investigate how differences in
shared decision-making can influence conflict escalation in groups consisting of
leaders and followers. I find that when the sharing rules of conflict are biased
towards leaders gaining more benefits or paying less costs than followers then
leaders evolve a higher optimum for pursuing aggressive, conflict escalating
strategies. When this is true, increased shared decision-making by allowing for
increased follower control of collective decision-making results in the evolution of
more peaceful intergroup interactions. In the reverse case, when sharing rules
favour followers, then increasing their share of decision-making increases the
aggressive conflict-escalating tendencies of the group. This theoretical model
shows how different decision-making and political structures can be important for
favouring the evolution of war or peace, and demonstrates how democratic peace
theory might apply to non-human animal societies without complex institutions
Green PA, Thompson FJ, Cant MA
(2022). Fighting force and experience combine to determine contest success in a warlike mammal. Proceedings of the National Academy of Sciences
Fighting force and experience combine to determine contest success in a warlike mammal
. Conflicts between social groups or “intergroup contests” are proposed to play a major role in the evolution of cooperation and social organization in humans and some nonhuman animal societies. In humans, success in warfare and other collective conflicts depends on both fighting group size and the presence and actions of key individuals, such as leaders or talismanic warriors. Understanding the determinants of intergroup contest success in other warlike animals may help to reveal the role of these contests in social evolution. Using 19 y of data on intergroup encounters in a particularly violent social mammal, the banded mongoose (
. Mungos mungo
. ), we show that two factors, the number of adult males and the age of the oldest male (the “senior” male), have the strongest impacts on the probability of group victory. The advantage conferred by senior males appears to stem from their fighting experience. However, the galvanizing effect of senior males declines as they grow old until, at very advanced ages, senior males become a liability rather than an asset and can be evicted. As in human conflict, strength in numbers and the experience of key individuals combine to determine intergroup contest success in this animal society. We discuss how selection arising from intergroup contests may explain a suite of features of individual life history and social organization, including male eviction, sex-assortative alloparental care, and adult sex ratio.
Sankey DWE, Hunt KL, Croft DP, Franks DW, Green PA, Thompson FJ, Johnstone RA, Cant MA
(2022). Leaders of war: Modelling the evolution of conflict among heterogeneous groups. Philosophical Transactions of the Royal Society B: Biological Sciences
Leaders of war: Modelling the evolution of conflict among heterogeneous groups
War, in human and animal societies, can be extremely costly but can also offer significant benefits to the victorious group. We might expect groups to go into battle when the potential benefits of victory (V) outweigh the costs of escalated conflict (C); however, V and C are unlikely to be distributed evenly in heterogeneous groups. For example, some leaders who make the decision to go to war may monopolize the benefits at little cost to themselves ( exploitative leaders). By contrast, other leaders may willingly pay increased costs, above and beyond their share of V ( heroic leaders). We investigated conflict initiation and conflict participation in an ecological model where single-leader multiple-follower groups came into conflict over natural resources. We found that small group size, low migration rate and frequent interaction between groups increased intergroup competition and the evolution of exploitative leadership, while converse patterns favoured increased intragroup competition and the emergence of heroic leaders. We also found evidence of an alternative leader/follower shared effort outcome. Parameters that favoured high contributing heroic leaders, and low contributing followers, facilitated transitions to more peaceful outcomes. We outline and discuss the key testable predictions of our model for empiricists studying intergroup conflict in humans and animals. Abstract
Ellis S, Cant M, Weiss M, Brent L, Meniri M, Thompson F, Croft D
(2022). Patterns and consequences of age-linked change in local relatedness in animal societies. Nature Ecology and Evolution
Patterns and consequences of age-linked change in local relatedness in animal societies
The ultimate payoff of behaviours depends not only on their direct impact on an individual but also on the impact on their relatives. Local relatedness – the average relatedness of an individual to their social environment – therefore has profound impacts on social and life history evolution. Recent work has begun to show that local relatedness has the potential to change systematically over an individual’s lifetime, a process called kinship dynamics. However, it is unclear how general these kinship dynamics are, whether they are predictable in real systems and their impacts on behaviour and life history evolution. In this study, we combine modelling with data from real systems to explore the extent and impact of kinship dynamics. We use data from seven group-living mammals with diverse social and mating systems to demonstrate not only that kinship dynamics occur in animal systems, but also that the direction and magnitude of kinship dynamics can be accurately predicted using a simple model. We use a theoretical model to demonstrate that kinship dynamics can profoundly impact lifetime patterns of behaviour and can drive sex differences in helping and harming behaviour across the lifespan in social species. Taken together this work demonstrates that kinship dynamics are likely to be a fundamental dimension of social evolution, especially when considering age-linked changes and sex differences in behaviour and life history. Abstract
Garcia Arasco A, Manser M, Watson SK, Kyabulima S, Radford AN, Cant MA, Garcia M
(2022). Testing the acoustic adaptation hypothesis with vocalizations from three mongoose species. Animal Behaviour
Testing the acoustic adaptation hypothesis with vocalizations from three mongoose species
Acoustic signals degrade and attenuate as they propagate through the environment, thus transmitting information with lower efficiency. The acoustic adaptation hypothesis (AAH) states that selection should shape the vocalizations of a species to maximize transmission through their habitat. A specific prediction of the AAH is that vocalizations will transmit better when emitted in their native habitat versus non-native habitats. We tested this prediction using vocalizations of three mongoose species that dwell in structurally different habitats: banded mongooses, Mungos mungo, dwarf mongooses, Helogale parvula, and meerkats, Suricata suricatta. Representative vocalizations of the three species were broadcast and rerecorded in each habitat at six distances from the source. Rerecorded vocalizations were compared to nondegraded calls through spectrogram correlation. Using generalized linear mixed models, we then quantified the differences in transmission fidelity of each species' vocalizations. Overall, we found partial support for the AAH within the mongoose family: habitat type strongly affected sound transmission, but depending on the species, vocalizations did not always transmit best in their native habitat, suggesting various degrees of acoustic adaptation. Vegetation cover within habitat type was also found to have a significant influence on the transmission properties of vocalizations. In addition, we found evidence that by changing their behaviour, either by producing vocalizations at different amplitudes or by choosing a specific calling location, mongooses can reduce sound degradation and attenuation over distance, thereby enhancing their communication efficiency. Our work highlights how habitat features may be key determinants of vocalization structure in mongooses, and is generalizable to other species living in similar conditions. It also suggests that, given a species and habitat, other selective pressures might prevail and limit acoustic adaptation in animal communication systems. Finally, our study provides insights into how mammals can adjust their vocal behaviour to compensate for environmental constraints on the transmission of their vocalizations. Abstract
Meniri M, Evans E, Thompson FJ, Marshall HH, Nichols HJ, Lewis G, Holt L, Davey E, Mitchell C, Johnstone RA, et al
(2022). Untangling the oxidative cost of reproduction: an analysis in wild banded mongooses. Ecol Evol
Untangling the oxidative cost of reproduction: an analysis in wild banded mongooses.
The cost of reproduction plays a central role in evolutionary theory, but the identity of the underlying mechanisms remains a puzzle. Oxidative stress has been hypothesized to be a proximate mechanism that may explain the cost of reproduction. We examine three pathways by which oxidative stress could shape reproduction. The "oxidative cost" hypothesis proposes that reproductive effort generates oxidative stress, while the "oxidative constraint" and "oxidative shielding" hypotheses suggest that mothers mitigate such costs through reducing reproductive effort or by pre-emptively decreasing damage levels, respectively. We tested these three mechanisms using data from a long-term food provisioning experiment on wild female banded mongooses (Mungos mungo). Our results show that maternal supplementation did not influence oxidative stress levels, or the production and survival of offspring. However, we found that two of the oxidative mechanisms co-occur during reproduction. There was evidence of an oxidative challenge associated with reproduction that mothers attempted to mitigate by reducing damage levels during breeding. This mitigation is likely to be of crucial importance, as long-term offspring survival was negatively impacted by maternal oxidative stress. This study demonstrates the value of longitudinal studies of wild animals in order to highlight the interconnected oxidative mechanisms that shape the cost of reproduction. Abstract
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Nichols HJ, Arbuckle K, Sanderson JL, Vitikainen EIK, Marshall HH, Thompson FJ, Cant MA, Wells DA
(2021). A double pedigree reveals genetic but not cultural inheritance of cooperative personalities in wild banded mongooses. Ecol Lett
A double pedigree reveals genetic but not cultural inheritance of cooperative personalities in wild banded mongooses.
Personality traits, such as the propensity to cooperate, are often inherited from parents to offspring, but the pathway of inheritance is unclear. Traits could be inherited via genetic or parental effects, or culturally via social learning from role models. However, these pathways are difficult to disentangle in natural systems as parents are usually the source of all of these effects. Here, we exploit natural 'cross fostering' in wild banded mongooses to investigate the inheritance of cooperative behaviour. Our analysis of 800 adult helpers over 21 years showed low but significant genetic heritability of cooperative personalities in males but not females. Cross fostering revealed little evidence of cultural heritability: offspring reared by particularly cooperative helpers did not become more cooperative themselves. Our results demonstrate that cooperative personalities are not always highly heritable in wild, and that the basis of behavioural traits can vary within a species (here, by sex). Abstract
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Nielsen M, Ellis S, Towers J, Doniol-Valcroze T, Franks D, Cant M, Weiss M, Johnstone R, III KB, Ellifrit D, et al (2021). A long post-reproductive lifespan is a shared trait among genetically distinct killer whale populations.
Nielsen MLK, Ellis S, Towers JR, Doniol-Valcroze T, Franks DW, Cant MA, Weiss MN, Johnstone RA, Balcomb KC, Ellifrit DK, et al
(2021). A long postreproductive life span is a shared trait among genetically distinct killer whale populations. ECOLOGY AND EVOLUTION
(13), 9123-9136. Author URL
Marshall HH, Johnstone RA, Thompson FJ, Nichols HJ, Wells D, Hoffman JI, Kalema-Zikusoka G, Sanderson JL, Vitikainen EIK, Blount JD, et al
(2021). A veil of ignorance can promote fairness in a mammal society. Nat Commun
A veil of ignorance can promote fairness in a mammal society.
Rawls argued that fairness in human societies can be achieved if decisions about the distribution of societal rewards are made from behind a veil of ignorance, which obscures the personal gains that result. Whether ignorance promotes fairness in animal societies, that is, the distribution of resources to reduce inequality, is unknown. Here we show experimentally that cooperatively breeding banded mongooses, acting from behind a veil of ignorance over kinship, allocate postnatal care in a way that reduces inequality among offspring, in the manner predicted by a Rawlsian model of cooperation. In this society synchronized reproduction leaves adults in a group ignorant of the individual parentage of their communal young. We provisioned half of the mothers in each mongoose group during pregnancy, leaving the other half as matched controls, thus increasing inequality among mothers and increasing the amount of variation in offspring birth weight in communal litters. After birth, fed mothers provided extra care to the offspring of unfed mothers, not their own young, which levelled up initial size inequalities among the offspring and equalized their survival to adulthood. Our findings suggest that a classic idea of moral philosophy also applies to the evolution of cooperation in biological systems. Abstract
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Weiss MN, Franks DW, Giles DA, Youngstrom S, Wasser SK, Balcomb KC, Ellifrit DK, Domenici P, Cant MA, Ellis S, et al
(2021). Age and sex influence social interactions, but not associations, within a killer whale pod. Proc Biol Sci
Age and sex influence social interactions, but not associations, within a killer whale pod.
Social structure is a fundamental aspect of animal populations. In order to understand the function and evolution of animal societies, it is important to quantify how individual attributes, such as age and sex, shape social relationships. Detecting these influences in wild populations under natural conditions can be challenging, especially when social interactions are difficult to observe and broad-scale measures of association are used as a proxy. In this study, we use unoccupied aerial systems to observe association, synchronous surfacing, and physical contact within a pod of southern resident killer whales (Orcinus orca). We show that interactions do not occur randomly between associated individuals, and that interaction types are not interchangeable. While age and sex did not detectably influence association network structure, both interaction networks showed significant social homophily by age and sex, and centrality within the contact network was higher among females and young individuals. These results suggest killer whales exhibit interesting parallels in social bond formation and social life histories with primates and other terrestrial social mammals, and demonstrate how important patterns can be missed when using associations as a proxy for interactions in animal social network studies. Abstract
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Green PA, Briffa M, Cant MA
(2021). Assessment during Intergroup Contests. Trends Ecol Evol
Assessment during Intergroup Contests.
Research on how competitors assess (i.e. gather information on) fighting ability and contested resources, as well as how assessment impacts on contest processes and outcomes, has been fundamental to the field of dyadic (one-on-one) contests. Despite recent growth in studies of contests between social-living groups, there is limited understanding of assessment during these intergroup contests. We adapt current knowledge of dyadic contest assessment to the intergroup case, describing what traits of groups, group members, and resources are assessed, and how assessment is manifested in contest processes (e.g. behaviors) and outcomes. This synthesis helps to explain the role of individual heterogeneity in assessment and how groups are shaped by the selective pressure of contests. Abstract
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Green PA, Preston EFR, Nicholl MH, Croft DP, Thompson FJ, Cant MA
(2021). Collective defence and behavioural homogeneity during simulated territorial intrusions in banded mongooses (Mungos mungo). ETHOLOGY
(10), 886-896. Author URL
Khera M, Arbuckle K, Hoffman JI, Sanderson JL, Cant MA, Nichols HJ
(2021). Cooperatively breeding banded mongooses do not avoid inbreeding through familiarity-based kin recognition. Behavioral Ecology and Sociobiology
Cooperatively breeding banded mongooses do not avoid inbreeding through familiarity-based kin recognition
Abstract: in species that live in family groups, such as cooperative breeders, inbreeding is usually avoided through the recognition of familiar kin. For example, individuals may avoid mating with conspecifics encountered regularly in infancy, as these likely include parents, siblings, and closely related alloparents. Other mechanisms have also been reported, albeit rarely; for example, individuals may compare their own phenotype to that of others, with close matches representing likely relatives (“phenotype matching”). However, determinants of the primary inbreeding avoidance mechanisms used by a given species remain poorly understood. We use 24 years of life history and genetic data to investigate inbreeding avoidance in wild cooperatively breeding banded mongooses (Mungos mungo). We find that inbreeding avoidance occurs within social groups but is far from maximised (mean pedigree relatedness between 351 breeding pairs = 0.144). Unusually for a group-living vertebrate, we find no evidence that females avoid breeding with males with which they are familiar in early life. This is probably explained by communal breeding; females give birth in tight synchrony and pups are cared for communally, thus reducing the reliability of familiarity-based proxies of relatedness. We also found little evidence that inbreeding is avoided by preferentially breeding with males of specific age classes. Instead, females may exploit as-yet unknown proxies of relatedness, for example, through phenotype matching, or may employ postcopulatory inbreeding avoidance mechanisms. Investigation of species with unusual breeding systems helps to identify constraints against inbreeding avoidance and contributes to our understanding of the distribution of inbreeding across species. Significance statement: Choosing the right mate is never easy, but it may be particularly difficult for banded mongooses. In most social animals, individuals avoid mating with those that were familiar to them as infants, as these are likely to be relatives. However, we show that this rule does not work in banded mongooses. Here, the offspring of several mothers are raised in large communal litters by their social group, and parents seem unable to identify or direct care towards their own pups. This may make it difficult to recognise relatives based on their level of familiarity and is likely to explain why banded mongooses frequently inbreed. Nevertheless, inbreeding is lower than expected if mates are chosen at random, suggesting that alternative pre- or post-copulatory inbreeding avoidance mechanisms are used. Abstract
(2021). Developing methods and applications for the analysis of cetacean social networks.
Developing methods and applications for the analysis of cetacean social networks
Cetaceans, the whales, dolphins, and porpoises, represent a taxon of intense interest for researchers studying non-human social structure. Social network analysis has become a central tool for studying these species, however the collection, analysis, and application of cetacean social network data comes with numerous challenges. In this thesis, I address key research gaps in the study of cetacean social networks, using the well-studied southern resident killer whale populations as my study system. Abstract
In the first chapter, I present a systematic literature review on cetacean social networks, in order to identify open areas for future research and development.
In Chapter 2, I address the question of social complexity and its quantification. Using mixture models, I develop and test measure of social complexity based on relationship diversity that can be derived from association networks.
In Chapter 3, I demonstrate that a commonly used statistical procedure for regression in association networks does not specify a proper null hypothesis, and results in high type I error rates.
In Chapter 4, I use unmanned aerial systems methods to measure association and interaction networks within a group of southern resident killer whales, finding important differences in the structure of these different networks.
In Chapter 5, I use long-term photographic data to model the spread of a novel pathogen over the social network of the endangered southern resident killer whale community to assess overall risk and potential management strategies.
In Chapter 6, I use a multi-decade dataset of social associations, survival, and fecundity to test the link between aspects of the social environment and fitness in the southern resident killer whale population.
In the final chapter, I provide a general discussion and synthesis of my results. and suggest areas for future research, both generally and within the southern. resident population specifically.
Wells DA, Cant MA, Thompson FJ, Marshall HH, Vitikainen EIK, Hoffman JI, Nichols HJ
(2021). Extra-group paternity varies with proxies of relatedness in a social mammal with high inbreeding risk. BEHAVIORAL ECOLOGY
(1), 94-104. Author URL
Sheppard CE, Heaphy R, Cant MA, Marshall HH
(2021). Individual foraging specialization in group-living species. Animal Behaviour
Individual foraging specialization in group-living species
Individual foraging specialization is a widespread occurrence and has numerous causes and consequences associated with it. However, one key area that has remained largely undiscussed, is the presence of such specialization in group-living species. This warrants special consideration as the behaviour of individuals living in groups is strongly influenced by their social environment, and so may result in distinct mechanisms favouring specialization. Here, we synthesize current theories regarding individual specialization and apply these to group-living species. In doing so we develop a set of testable predictions about the causes and consequences of individual foraging specialization in group-living species. In particular, we conclude that increased local competition between conspecifics will drive the development of individual foraging specialization in group-living species. We hypothesize that ‘one-to-one’ learning will promote individual foraging specialization, whereas learning from multiple role models will erode individual specialization through behavioural conformity. This increase in specialization may also make social groups more resilient to environmental change. We argue that testing predicted causes and consequences of individual specialization in group-living species is an important step in developing our understanding of the evolution of animal societies and how they are likely to be affected by a changing environment. Abstract
(2021). Intergenerational costs of reproduction: Comparative and empirical studies in mammals.
Intergenerational costs of reproduction: Comparative and empirical studies in mammals
Life-history theory is built upon the principles of resource allocation and trade-offs. While intraindividual trade-offs have received the most attention, intergenerational trade-offs could be equally essential to our understanding of life-history evolution. One of the most well-studied trade-offs is that of reproduction and survival, known as the ‘cost of reproduction’. Currently, oxidative stress is thought to explain this cost but could be paid for by offspring as well as mothers and possibly transferred via several pathways. If oxidative stress can have negative intergenerational implications, then mothers should make some effort to mitigate against this to maximise their fitness. In this thesis, I explore that possibility using a comparative approach examining the evolutionary transitions and life-history associations of one organ that may be responsible for perpetuating intergenerational effects – the eutherian placenta. Repeated evolutionary transitions away from high levels of placentation and associations between high levels of placentation and smaller body masses/shorter gestation lengths provide some evidence for a protective function of the placenta against negative intergenerational effects. To complement this study, I examined the potentially negative intergenerational consequences of the oxidative cost of reproduction. This was done by testing the oxidative cost, constraint and shielding hypotheses in parallel using a supplementary feeding experiment in wild banded mongooses, Mungos mungo. While we found that supplementary feeding did not influence oxidative state, we were able to find some support for each of these hypotheses. of particular interest was the finding that a specific marker for oxidative damage was lower in pregnant females compared to non-breeders, and negatively associated with pup survival to one year. This is suggestive of a deleterious intergenerational effect as a consequence of oxidative stress and emphasises a need to mitigate against such effects to maximise fitness through mechanisms such as oxidative constraint and shielding. The wide diversity of placentation that we see across mammals may reflect some of the other strategies used by mammals to further minimise negative intergenerational effects and maximise fitness. Ultimately, placentation could play a significant role in the transfer of intergenerational effects and facilitate life-history evolution. Abstract
Croft DP, Weiss MN, Nielsen MLK, Grimes C, Cant MA, Ellis S, Franks DW, Johnstone RA
(2021). Kinship dynamics: patterns and consequences of changes in local relatedness. Proc Biol Sci
Kinship dynamics: patterns and consequences of changes in local relatedness.
Mounting evidence suggests that patterns of local relatedness can change over time in predictable ways, a process termed kinship dynamics. Kinship dynamics may occur at the level of the population or social group, where the mean relatedness across all members of the population or group changes over time, or at the level of the individual, where an individual's relatedness to its local group changes with age. Kinship dynamics are likely to have fundamental consequences for the evolution of social behaviour and life history because they alter the inclusive fitness payoffs to actions taken at different points in time. For instance, growing evidence suggests that individual kinship dynamics have shaped the evolution of menopause and age-specific patterns of helping and harming. To date, however, the consequences of kinship dynamics for social evolution have not been widely explored. Here we review the patterns of kinship dynamics that can occur in natural populations and highlight how taking a kinship dynamics approach has yielded new insights into behaviour and life-history evolution. We discuss areas where analysing kinship dynamics could provide new insight into social evolution, and we outline some of the challenges in predicting and quantifying kinship dynamics in natural populations. Abstract
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Ellis S, Franks DW, Weiss MN, Cant MA, Domenici P, Balcomb KC, Ellifrit DK, Croft DP
(2021). Mixture models as a method for comparative sociality: social networks and demographic change in resident killer whales. Behavioral Ecology and Sociobiology
Mixture models as a method for comparative sociality: social networks and demographic change in resident killer whales
Abstract: in studies of social behaviour, social bonds are usually inferred from rates of interaction or association. This approach has revealed many important insights into the proximate formation and ultimate function of animal social structures. However, it remains challenging to compare social structure between systems or time-points because extrinsic factors, such as sampling methodology, can also influence the observed rate of association. As a consequence of these methodological challenges, it is difficult to analyse how patterns of social association change with demographic processes, such as the death of key social partners. Here we develop and illustrate the use of binomial mixture models to quantitatively compare patterns of social association between networks. We then use this method to investigate how patterns of social preferences in killer whales respond to demographic change. Resident killer whales are bisexually philopatric, and both sexes stay in close association with their mother in adulthood. We show that mothers and daughters show reduced social association after the birth of the daughter’s first offspring, but not after the birth of an offspring to the mother. We also show that whales whose mother is dead associate more with their opposite sex siblings and with their grandmother than whales whose mother is alive. Our work demonstrates the utility of using mixture models to compare social preferences between networks and between species. We also highlight other potential uses of this method such as to identify strong social bonds in animal populations. Significance statement: Comparing patters of social associations between systems, or between the same systems at different times, is challenging due to the confounding effects of sampling and methodological differences. Here we present a method to allow social associations to be robustly classified and then compared between networks using binomial mixture models. We illustrate this method by showing how killer whales change their patterns of social association in response to the birth of calves and the death of their mother. We show that after the birth of her calf, females associate less with their mother. We also show that whales’ whose mother is dead associate more with their opposite sex siblings and grandmothers than whales’ whose mother is alive. This clearly demonstrates how this method can be used to examine fine scale temporal processes in animal social systems. Abstract
Preston EFR, Thompson FJ, Ellis S, Kyambulima S, Croft DP, Cant MA
(2021). Network-level consequences of outgroup threats in banded mongooses: Grooming and aggression between the sexes. JOURNAL OF ANIMAL ECOLOGY
(1), 153-167. Author URL
Taborsky M, Cant M, Komdeur J
(2021). The Evolution of Social Behaviour.
Cambridge, UK, Cambridge University Press.
The Evolution of Social Behaviour
Preston EFR, Thompson FJ, Kyabulima S, Croft DP, Cant MA
(2021). The dynamics of social cohesion in response to simulated intergroup conflict in banded mongooses. ECOLOGY AND EVOLUTION
(24), 18662-18675. Author URL
Johnstone RA, Cant MA, Cram D, Thompson FJ
(2020). Exploitative leaders incite intergroup warfare in a social mammal. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
(47), 29759-29766. Author URL
Wells DA, Cant MA, Hoffman JI, Nichols HJ
(2020). Inbreeding depresses altruism in a cooperative society. ECOLOGY LETTERS
(10), 1460-1467. Author URL
Weiss MN, Franks DW, Balcomb KC, Ellifrit DK, Silk MJ, Cant MA, Croft DP
(2020). Modelling cetacean morbillivirus outbreaks in an endangered killer whale population. BIOLOGICAL CONSERVATION
, 242 Author URL
(2020). The evolution of intergroup discrimination and colony fusion in a primitive termite, Zootermopsis angusticollis.
The evolution of intergroup discrimination and colony fusion in a primitive termite, Zootermopsis angusticollis
Groups of animals interact in a variety of different ways, from lethal conflict to cooperation and fusion. While intergroup conflict is relatively widely studied, the mechanisms and selective forces underpinning cooperation and group fusion are less well understood. The lower termites are a group of eusocial insects that displays a spectrum of intergroup relationships from violent battles to avoidance to colony fusion, making them a valuable model system with which to study intergroup interactions. In Chapter 2, I present a trial of a novel method of marking termites (Visible Implant Elastomer), finding that it causes slight changes to survival and behaviour associated with reproductive disinhibition. In the following chapters, I investigate two aspects of intergroup interactions in a single-piece nesting species of lower termite, Zootermopsis angusticollis: nestmate recognition and soldier caste ratio. In Chapter 3, I investigate the implications of colonies sharing similar nesting material on the ability of Z. angusticollis pseudergates to discriminate between members of their own and a different colony. I find that Z. angusticollis pseudergates discriminate between nestmates and non-nestmates but that this does not appear to be dependent on whether they encounter a non-nestmate raised on the same or a different wood type. Contrary to prediction, I also find that non-nestmates experience the same levels of cooperative allogrooming as nestmates. In Chapter 4, I use a theoretical model to examine the consequences of colony fusion on the sterile caste, the soldiers, at the 1 colony level. This model predicts that the reported increase in soldier number from some studies is supported under a narrow range of cost and benefit parameters, and that termites can benefit from fusion at the colony level under two scenarios: when fusion results in higher net benefit from soldiers, or when a colony can take advantage of the other’s soldiers. This suggests two pathways to the evolution of colony fusion, which might be applicable to lower termites of different ecological habits. Evidence from both Chapter 3 and Chapter 4 suggest that colony fusion in the lower termites could be driven by selection on pseudergates, which can gain direct fitness benefits from fusion. I suggest that this might be a general phenomenon and that the presence of conflict within a group can facilitate cooperation between groups across taxa. Abstract
Thompson F, Hunt K, Wright K, Rosengaus R, Cole E, Birch G, Maune A, Cant M
(2020). Who goes there? Social surveillance as a response to intergroup conflict in a primitive termite. Biology Letters
Who goes there? Social surveillance as a response to intergroup conflict in a primitive termite
Intergroup conflict has been suggested as a major force shaping the evolution of social behaviour in animal groups. A long-standing hypothesis is that groups at risk of attack by rivals should become more socially cohesive, to increase resilience or protect against future attack. However, it is usually unclear how cohesive behaviours (such as grooming or social contacts) function in intergroup conflict. We performed an experiment in which we exposed young colonies of the dampwood termite, Zootermopsis angusticollis, to a rival colony while preventing physical combat with a permeable barrier. We measured social contacts, allogrooming and trophallaxis before, during and after exposure. Termites showed elevated rates of social contacts during exposure to a rival compared to the pre-exposure phase, but rates returned to pre-exposure levels after colonies were separated for 9 days. There was evidence of a delayed effect of conflict on worker trophallaxis. We suggest that social contacts during intergroup conflict function as a form of social surveillance, to check individual identity and assess colony resource holding potential. Intergroup conflict may increase social cohesion in both the short and the long term, improving the effectiveness of groups in competition. Abstract
Birch G, Cant MA, Thompson FJ
(2019). Behavioural response of workers to repeated intergroup encounters in the harvester ant Messor barbarus. Insectes Sociaux
Behavioural response of workers to repeated intergroup encounters in the harvester ant Messor barbarus
The evolution of cooperation in animal societies is often associated with the evolution of hostility towards members of other groups. It is usually predicted that groups under attack from outsiders should respond by becoming more cohesive or cooperative. However, the responses of individuals to real or simulated intergroup encounters vary widely, for reasons that are poorly understood. We tested how groups of workers of the harvester ant, Messor barbarus, responded to exposure to members of a different colony versus members of their own colony, and how previous exposure to an intruder affected the intensity of the within-group response. We found that workers increased in activity and had more contact with one another immediately following exposure to an ant from a different colony, but also showed a similar behavioural response to presentations involving an ant from their own colony. However, exposure to an intruder from a different colony resulted in much stronger behavioural responses to a second intruder, encountered shortly afterwards. Our results are consistent with studies of social vertebrates which suggest that exposure to intruders results in increased social cohesion. Our results also show that exposure to an intruder primes group members to respond more strongly to future intrusions. Our findings highlight a disconnect between the assumptions of theoretical models which study the effect of intergroup conflict on social evolution over many generations, and the short-term behavioural responses that are the usual focus of studies of intergroup conflict in insects and vertebrates. Abstract
Kuijper ALW, Hanson MA, Vitikainen EIK, Marshall H, Ozanne SE, Cant MA (2019). Developing differences: early-life effects and evolutionary medicine. Philosophical Transactions B: Biological Sciences
Silk MJ, Cant MA, Cafazzo S, Natoli E, McDonald RA
(2019). Elevated aggression is associated with uncertainty in a network of dog dominance interactions. Proc Biol Sci
Elevated aggression is associated with uncertainty in a network of dog dominance interactions.
Dominance hierarchies are widespread in animal societies and reduce the costs of within-group conflict over resources and reproduction. Variation in stability across a social hierarchy may result in asymmetries in the benefits obtained from hierarchy formation. However, variation in the stability and behavioural costs of dominance interactions with rank remain poorly understood. Previous theoretical models have predicted that the intensity of dominance interactions and aggression should increase with rank, but these models typically assume high reproductive skew, and so their generality remains untested. Here we show in a pack of free-living dogs with a sex-age-graded hierarchy that the central region of the hierarchy was dominated by more unstable social relationships and associated with elevated aggression. Our results reveal unavoidable costs of ascending a dominance hierarchy, run contrary to theoretical predictions for the relationship between aggression and social rank in high-skew societies, and widen our understanding of how heterogeneous benefits of hierarchy formation arise in animal societies. Abstract
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Johnstone RA, Cant MA (2019). Evolution of Menopause. Current Biology
Cant MA, Croft DP (2019). Grandmothering in space and time. Current Biology
Vitikainen E, Thompson F, Marshall H, Cant MA (2019). Live long and prosper: durable benefits of early-life care in banded mongooses. Philosophical Transactions B: Biological Sciences
Nattrass S, Croft DP, Ellis S, Cant MA, Weiss MN, Wright BM, Stredulinsky E, Doniol-Valcroze T, Ford JKB, Balcomb KC, et al
(2019). Postreproductive killer whale grandmothers improve the survival of their grandoffspring. Proc Natl Acad Sci U S A
Postreproductive killer whale grandmothers improve the survival of their grandoffspring.
Understanding why females of some mammalian species cease ovulation prior to the end of life is a long-standing interdisciplinary and evolutionary challenge. In humans and some species of toothed whales, females can live for decades after stopping reproduction. This unusual life history trait is thought to have evolved, in part, due to the inclusive fitness benefits that postreproductive females gain by helping kin. In humans, grandmothers gain inclusive fitness benefits by increasing their number of surviving grandoffspring, referred to as the grandmother effect. Among toothed whales, the grandmother effect has not been rigorously tested. Here, we test for the grandmother effect in killer whales, by quantifying grandoffspring survival with living or recently deceased reproductive and postreproductive grandmothers, and show that postreproductive grandmothers provide significant survival benefits to their grandoffspring above that provided by reproductive grandmothers. This provides evidence of the grandmother effect in a nonhuman menopausal species. By stopping reproduction, grandmothers avoid reproductive conflict with their daughters, and offer increased benefits to their grandoffspring. The benefits postreproductive grandmothers provide to their grandoffspring are shown to be most important in difficult times where the salmon abundance is low to moderate. The postreproductive grandmother effect we report, together with the known costs of late-life reproduction in killer whales, can help explain the long postreproductive life spans of resident killer whales. Abstract
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Inzani E, Marshall HH, Thompson FJ, Kalema-Zikusoka G, Cant MA, Vitikainen EIK
(2019). Spontaneous abortion as a response to reproductive conflict in the banded mongoose. BIOLOGY LETTERS
(12). Author URL
Marshall H, Inger R, Jackson AL, McDonald R, Thompson F, Cant MA (2019). Stable isotopes are quantitative indicators of diet and trophic niche. Ecology Letters
Wells DA, Cant MA, Nichols HJ, Hoffman JI
(2018). A high-quality pedigree and genetic markers both reveal inbreeding depression for quality but not survival in a cooperative mammal. MOLECULAR ECOLOGY
(9), 2271-2288. Author URL
Ellis S, Franks DW, Nattrass S, Currie TE, Cant MA, Giles D, Balcomb KC, Croft DP
(2018). Analyses of ovarian activity reveal repeated evolution of post-reproductive lifespans in toothed whales. Sci Rep
Analyses of ovarian activity reveal repeated evolution of post-reproductive lifespans in toothed whales.
In most species the reproductive system ages at the same rate as somatic tissue and individuals continue reproducing until death. However, females of three species - humans, killer whales and short-finned pilot whales - have been shown to display a markedly increased rate of reproductive senescence relative to somatic ageing. In these species, a significant proportion of females live beyond their reproductive lifespan: they have a post-reproductive lifespan. Research into this puzzling life-history strategy is hindered by the difficulties of quantifying the rate of reproductive senescence in wild populations. Here we present a method for measuring the relative rate of reproductive senescence in toothed whales using published physiological data. of the sixteen species for which data are available (which does not include killer whales), we find that three have a significant post-reproductive lifespan: short-finned pilot whales, beluga whales and narwhals. Phylogenetic reconstruction suggests that female post-reproductive lifespans have evolved several times independently in toothed whales. Our study is the first evidence of a significant post-reproductive lifespan in beluga whales and narwhals which, when taken together with the evidence for post-reproductive lifespan in killer whales, doubles the number of non-human mammals known to exhibit post-reproductive lifespans in the wild. Abstract
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Marshall HH, Griffiths DJ, Mwanguhya F, Businge R, Griffiths AGF, Kyabulima S, Mwesige K, Sanderson JL, Thompson FJ, Vitikainen EIK, et al
(2018). Data collection and storage in long-term ecological and evolutionary studies: the Mongoose 2000 system. PLoS One
Data collection and storage in long-term ecological and evolutionary studies: the Mongoose 2000 system.
Studying ecological and evolutionary processes in the natural world often requires research projects to follow multiple individuals in the wild over many years. These projects have provided significant advances but may also be hampered by needing to accurately and efficiently collect and store multiple streams of the data from multiple individuals concurrently. The increase in the availability and sophistication of portable computers (smartphones and tablets) and the applications that run on them has the potential to address many of these data collection and storage issues. In this paper we describe the challenges faced by one such long-term, individual-based research project: the Banded Mongoose Research Project in Uganda. We describe a system we have developed called Mongoose 2000 that utilises the potential of apps and portable computers to meet these challenges. We discuss the benefits and limitations of employing such a system in a long-term research project. The app and source code for the Mongoose 2000 system are freely available and we detail how it might be used to aid data collection and storage in other long-term individual-based projects. Abstract
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Sheppard CE, Marshall HH, Inger R, Thompson FJ, Vitikainen EIK, Barker S, Nichols HJ, Wells DA, McDonald RA, Cant MA, et al (2018). Decoupling of Genetic and Cultural Inheritance in a Wild Mammal. Current Biology, 28(11), 1846-1850.e2.
Thompson F, Cant MA (2018). Dynamic conflict among heterogeneous groups: a comment on Christensen and Radford. Behavioral Ecology
Sheppard CE, Inger R, McDonald RA, Barker S, Jackson AL, Cant MA, Thompson FJ, Vitikainen EIK, Marshall HH (2018). Intragroup competition predicts individual foraging specialisation in a group-living mammal. Ecology Letters, 21(5), 665-673.
Mitchell J, Kyabulima S, Businge R, Cant MA, Nichols HJ
(2018). Kin discrimination via odour in the cooperatively breeding banded mongoose. R Soc Open Sci
Kin discrimination via odour in the cooperatively breeding banded mongoose.
Kin discrimination is often beneficial for group-living animals as it aids in inbreeding avoidance and providing nepotistic help. In mammals, the use of olfactory cues in kin discrimination is widespread and may occur through learning the scents of individuals that are likely to be relatives, or by assessing genetic relatedness directly through assessing odour similarity (phenotype matching). We use scent presentations to investigate these possibilities in a wild population of the banded mongoose Mungos mungo, a cooperative breeder in which inbreeding risk is high and females breed communally, disrupting behavioural cues to kinship. We find that adults show heightened behavioural responses to unfamiliar (extra-group) scents than to familiar (within-group) scents. Interestingly, we found that responses to familiar odours, but not unfamiliar odours, varied with relatedness. This suggests that banded mongooses are either able to use an effective behavioural rule to identify likely relatives from within their group, or that phenotype matching is used in the context of within-group kin recognition but not extra-group kin recognition. In other cooperative breeders, familiarity is used within the group and phenotype matching may be used to identify unfamiliar kin. However, for the banded mongoose this pattern may be reversed, most likely due to their unusual breeding system which disrupts within-group behavioural cues to kinship. Abstract
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Ellis S, Franks DW, Nattrass S, Cant MA, Bradley DL, Giles D, Balcomb KC, Croft DP
(2018). Postreproductive lifespans are rare in mammals. ECOLOGY AND EVOLUTION
(5), 2482-2494. Author URL
Hares MC, Vitikainen EIK, Marshall HH, Thompson FJ, Blount JD, Cant MA
(2018). Telomere dynamics in wild banded mongooses: Evaluating longitudinal and quasi-longitudinal markers of senescence. EXPERIMENTAL GERONTOLOGY
, 67-73. Author URL
O'Brien S, Luján AM, Paterson S, Cant MA, Buckling A
(2017). Adaptation to public goods cheats in Pseudomonas aeruginosa. Proc Biol Sci
Adaptation to public goods cheats in Pseudomonas aeruginosa.
Cooperation in nature is ubiquitous, but is susceptible to social cheats who pay little or no cost of cooperation yet reap the benefits. The effect such cheats have on reducing population productivity suggests that there is selection for cooperators to mitigate the adverse effects of cheats. While mechanisms have been elucidated for scenarios involving a direct association between producer and cooperative product, it is less clear how cooperators may suppress cheating in an anonymous public goods scenario, where cheats cannot be directly identified. Here, we investigate the real-time evolutionary response of cooperators to cheats when cooperation is mediated by a diffusible public good: the production of iron-scavenging siderophores by Pseudomonas aeruginosa We find that siderophore producers evolved in the presence of a high frequency of non-producing cheats were fitter in the presence of cheats, at no obvious cost to population productivity. A novel morphotype independently evolved and reached higher frequencies in cheat-adapted versus control populations, exhibiting reduced siderophore production but increased production of pyocyanin-an extracellular toxin that can also increase the availability of soluble iron. This suggests that cooperators may have mitigated the negative effects of cheats by downregulating siderophore production and upregulating an alternative iron-acquisition public good. More generally, the study emphasizes that cooperating organisms can rapidly adapt to the presence of anonymous cheats without necessarily incurring fitness costs in the environment they evolve in. Abstract
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Vitikainen EIK, Marshall HH, Thompson FJ, Sanderson JL, Bell MBV, Gilchrist JS, Hodge SJ, Nichols HJ, Cant MA
(2017). Biased escorts: offspring sex, not relatedness explains alloparental care patterns in a cooperative breeder. Proc Biol Sci
Biased escorts: offspring sex, not relatedness explains alloparental care patterns in a cooperative breeder.
Kin selection theory predicts that animals should direct costly care where inclusive fitness gains are highest. Individuals may achieve this by directing care at closer relatives, yet evidence for such discrimination in vertebrates is equivocal. We investigated patterns of cooperative care in banded mongooses, where communal litters are raised by adult 'escorts' who form exclusive caring relationships with individual pups. We found no evidence that escorts and pups assort by parentage or relatedness. However, the time males spent escorting increased with increasing relatedness to the other group members, and to the pup they had paired with. Thus, we found no effect of relatedness in partner choice, but (in males) increasing helping effort with relatedness once partner choices had been made. Unexpectedly, the results showed clear assortment by sex, with female carers being more likely to tend to female pups, and male carers to male pups. This sex-specific assortment in helping behaviour has potential lifelong impacts on individual development and may impact the future size and composition of natal groups and dispersing cohorts. Where relatedness between helpers and recipients is already high, individuals may be better off choosing partners using other predictors of the costs and benefits of cooperation, without the need for possibly costly within-group kin discrimination. Abstract
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Thompson FJ, Marshall HH, Vitikainen EIK, Cant MA
(2017). Causes and consequences of intergroup conflict in cooperative banded mongooses. Animal Behaviour
Causes and consequences of intergroup conflict in cooperative banded mongooses
Conflict between groups is a notable feature of many animal societies. Recent theoretical models suggest that violent intergroup conflict can shape patterns of within-group cooperation. However, despite its prevalence in social species, the adaptive significance of violent intergroup conflict has been little explored outside of humans and chimpanzees, Pan troglodytes. A barrier to current understanding of the role of intergroup conflict in the evolution of social behaviour is a lack of information on the causes and consequences of aggression between groups. Here, we examined the causes and fitness consequences of intergroup conflict in the banded mongoose, Mungos mungo, using a 16-year data set of observed intergroup interactions, life history and behaviour. Banded mongooses are cooperative breeders that live in highly territorial groups and engage in frequent, aggressive and violent intergroup interactions. We found that intensified population-wide competition for food and mates increased the probability of intergroup interactions, and that increased intergroup conflict was associated with periods in which groups were growing in size. Intergroup conflict had fitness costs in terms of reduced litter and adult survival but no cost to pregnant females: in fact, females were less likely to abort following an intergroup interaction than when there had been no recent intergroup conflict. Our results suggest that intergroup conflict has measurable costs to both individuals and groups in the long and short term, and that levels of conflict among groups could be high enough to affect patterns of within-group cooperative behaviour. Establishing the consequences of intergroup conflict in cooperative species can shed light on patterns of conflict and cooperation within groups and, in turn, facilitate our understanding of social evolution. Abstract
Marshall HH, Vitikainen EIK, Mwanguhya F, Businge R, Kyabulima S, Hares MC, Inzani E, Kalema-Zikusoka G, Mwesige K, Nichols HJ, et al
(2017). Data supporting Marshall et al. (2017) in Ecology and Evolution.
Data supporting Marshall et al. (2017) in Ecology and Evolution
This data supports the following publication: Abstract
Marshall HH, Vitikainen EIK, Mwanguhya F, Businge R, Kyabulima S, Hares MC, Inzani E, Kalema-Zikusosa G, Mwesige K, Nichols HJ, et al (2017). Lifetime fitness consequences of early-life ecological hardship in a wild mammal population. Ecology and Evolution
Thompson FJ, Cant MA, Marshall HH, Vitikainen EIK, Sanderson JL, Nichols HJ, Gilchrist JS, Bell MBV, Young AJ, Hodge SJ, et al
(2017). Explaining negative kin discrimination in a cooperative mammal society. Proceedings of the National Academy of Sciences
Explaining negative kin discrimination in a cooperative mammal society
. Kin selection theory predicts that animals will direct altruism toward closer genetic relatives and aggression toward more distantly related individuals. Our 18-y study of wild banded mongooses reveals that, unusually, dominant individuals target females who are more closely related to them for violent eviction from the group. This puzzling result can be explained by selection for unrelated individuals to resist eviction and for related individuals to submit more easily. In support of this idea, we show that kin are targeted for aggression only when individuals are capable of resisting. Our results suggest that, where potential victims can oppose aggression, the usual predictions of kin selection theory can be reversed.
Scott K, Heistermann, M, Cant MA, Vitikainen EIK (2017). Group size and visitor number predict faecal glucocorticoid concentrations in zoo meerkats. Royal Society Open Science
Thompson FJ, Marshall HH, Vitikainen EIK, Young AJ, Cant MA
(2017). Individual and demographic consequences of mass eviction in cooperative banded mongooses. Animal Behaviour
Individual and demographic consequences of mass eviction in cooperative banded mongooses
In animal societies, conflict within groups can result in eviction, where individuals are often permanently expelled from their group. To understand the evolution of eviction and its role in the resolution of within-group conflict requires information on the demographic consequences of eviction for individuals and groups. However, such information is usually difficult to obtain because of the difficulty in tracking and monitoring individuals after they are evicted from their natal groups. Here we used a 15-year data set on life history and demography to investigate the consequences of eviction in a tractable cooperatively breeding mammal, the banded mongoose, Mungos mungo. In this species, groups of individuals are periodically evicted en masse and eviction is a primary mechanism by which new groups form in the study population. Following eviction, we found sex differences in dispersal distance: some females established new groups on the study peninsula but males always dispersed away from the study peninsula. Evicted females suffered reduced reproductive success in the year after eviction. For the evicting group, eviction was associated with increased per capita reproductive success for females, suggesting that eviction is successful in reducing reproductive competition. However, eviction was also associated with increased intergroup conflict for the evicting group. Our results suggest that within-group conflict resolution strategies affect group productivity, group interactions and the structure of the population, and hence have fitness impacts that reach beyond the individual evictors and evictees involved in eviction. Abstract
Marshall HH, Vitikainen EIK, Mwanguhya F, Businge R, Kyabulima S, Hares MC, Inzani E, Kalema-Zikusoka G, Mwesige K, Nichols HJ, et al
(2017). Lifetime fitness consequences of early-life ecological hardship in a wild mammal population. Ecology and Evolution
Lifetime fitness consequences of early-life ecological hardship in a wild mammal population
Early-life ecological conditions have major effects on survival and reproduction. Numerous studies in wild systems show fitness benefits of good quality early-life ecological conditions (“silver-spoon” effects). Recently, however, some studies have reported that poor-quality early-life ecological conditions are associated with later-life fitness advantages and that the effect of early-life conditions can be sex-specific. Furthermore, few studies have investigated the effect of the variability of early-life ecological conditions on later-life fitness. Here, we test how the mean and variability of early-life ecological conditions affect the longevity and reproduction of males and females using 14 years of data on wild banded mongooses (Mungos mungo). Males that experienced highly variable ecological conditions during development lived longer and had greater lifetime fitness, while those that experienced poor early-life conditions lived longer but at a cost of reduced fertility. In females, there were no such effects. Our study suggests that exposure to more variable environments in early life can result in lifetime fitness benefits, whereas differences in the mean early-life conditions experienced mediate a life-history trade-off between survival and reproduction. It also demonstrates how early-life ecological conditions can produce different selection pressures on males and females. Abstract
Ellis S, Franks DW, Nattrass S, Cant MA, Weiss MN, Giles D, Balcomb KC, Croft DP
(2017). Mortality risk and social network position in resident killer whales: Sex differences and the importance of resource abundance. Proceedings of the Royal Society B: Biological Sciences
Mortality risk and social network position in resident killer whales: Sex differences and the importance of resource abundance
An individual’s ecological environment affects their mortality risk, which in turn has fundamental consequences for life-history evolution. In many species, social relationships are likely to be an important component of an individual’s environment, and therefore their mortality risk. Here, we examine the relationship between social position and mortality risk in resident killer whales (Orcinus orca) using over three decades of social and demographic data. We find that the social position of male, but not female, killer whales in their social unit predicts their mortality risk. More socially integrated males have a significantly lower risk of mortality than socially peripheral males, particularly in years of low prey abundance, suggesting that social position mediates access to resources. Male killer whales are larger and require more resources than females, increasing their vulnerability to starvation in years of low salmon abundance. More socially integrated males are likely to have better access to social information and food-sharing opportunities which may enhance their survival in years of low salmon abundance. Our results show that observable variation in the social environment is linked to variation in mortality risk, and highlight how sex differences in social effects on survival may be linked to sex differences in life-history evolution. Abstract
Mitchell J, Cant MA, Nichols HJ
(2017). Pregnancy is detected via odour in a wild cooperative breeder. Biol Lett
Pregnancy is detected via odour in a wild cooperative breeder.
Among mammals, scent has long been known to encode oestrus; however, in many species, detecting pregnancy may also be important in terms of both competition and mate-choice. Here, we show, through odour presentation experiments, that pregnancy is discernible via scent by both sexes in the cooperatively breeding banded mongoose, Mungos mungo Males spent more time investigating and were more likely to scent mark the odours of non-pregnant females, compared to pregnant females. Females showed increased levels of scent marking when odours were of the same reproductive state as themselves. These results present the first direct demonstration that pregnancy is detectable via scent in wild cooperative breeders. Detecting pregnancy may be particularly important in cooperative breeders as, in addition to the competition between males for receptive mates, there is also intense competition between females for access to alloparental care. Consequently, dominant females benefit from targeting reproductive suppression towards subordinates that represent direct threats, such as pregnant females. Abstract
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Croft DP, Johnstone RA, Ellis S, Nattrass S, Franks DW, Brent LJN, Mazzi S, Balcomb KC, Ford JKB, Cant MA, et al (2017). Reproductive Conflict and the Evolution of Menopause in Killer Whales. Current Biology, 27(2), 298-304.
Mitchell J, Cant MA, Vitikainen EIK, Nichols HJ
(2017). Smelling fit: scent marking exposes parasitic infection status in the banded mongoose. Curr Zool
Smelling fit: scent marking exposes parasitic infection status in the banded mongoose.
Preference for uninfected mates is presumed beneficial as it minimizes one's risk of contracting an infection and infecting one's offspring. In avian systems, visual ornaments are often used to indicate parasite burdens and facilitate mate choice. However, in mammals, olfactory cues have been proposed to act as a mechanism allowing potential mates to be discriminated by infection status. The effect of infection upon mammalian mate choice is mainly studied in captive rodents where experimental trials support preference for the odors of uninfected mates and some data suggest scent marking is reduced in individuals with high infection burdens. Nevertheless, whether such effects occur in nonmodel and wild systems remains poorly understood. Here, we investigate the interplay between parasite load (estimated using fecal egg counts) and scent marking behavior in a wild population of banded mongooses Mungos mungo. Focusing on a costly protozoan parasite of the genus Isospora and the nematode worm Toxocara, we first show that banded mongooses that engage in frequent, intensive scent marking have lower Isospora loads, suggesting marking behavior may be an indicator trait regarding infection status. We then use odor presentations to demonstrate that banded mongooses mark less in response to odors of opposite sexed individuals with high Isospora and Toxocara loads. As both of these parasites are known to have detrimental effects upon the health of preweaned young in other species, they would appear key targets to avoid during mate choice. Results provide support for scent as an important ornament and mechanism for advertising parasitic infection within wild mammals. Abstract
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Cant MA, Nichols HJ, Thompson FJ, Vitikainen EIK (2016). Banded mongooses: demography, life history, and social behavior. In Koenig WD, Dickinson JL (Eds.) Cooperative breeding in vertebrates: studies of ecology, evolution and behavior, Cambridge: Cambridge University Press, 318-337.
Vitikainen EIK, Cant MA, Sanderson JL, Mitchell C, Nichols HJ, Marshall HH, Thompson FJ, Gilchrist JS, Hodge SJ, Johnstone RA, et al
(2016). Evidence of Oxidative Shielding of Offspring in a Wild Mammal. FRONTIERS IN ECOLOGY AND EVOLUTION
, 4 Author URL
Vitikainen EIK, Cant MA, Sanderson JL, Mitchell C, Nichols HJ, Marshall HH, Thompson FJ, Gilchrist JS, Hodge SJ, Johnstone RA, et al (2016). Evidence of Oxidative Shielding of Offspring in a Wild Mammal. Frontiers in Ecology and Evolution, 4
Inzani E, Marshall HH, Sanderson JL, Nichols HJ, Thompson FJ, Kalema-Zikusoka G, Hodge SJ, Cant MA, Vitikainen EIK
(2016). Female reproductive competition explains variation in prenatal investment in wild banded mongooses. Scientific Reports
Female reproductive competition explains variation in prenatal investment in wild banded mongooses
Female intrasexual competition is intense in cooperatively breeding species where offspring compete locally for resources and helpers. In mammals, females have been proposed to adjust prenatal investment according to the intensity of competition in the postnatal environment (a form of ‘predictive adaptive response’; PAR). We carried out a test of this hypothesis using ultrasound scanning of wild female banded mongooses in Uganda. In this species multiple females give birth together to a communal litter, and all females breed regularly from one year old. Total prenatal investment (size times the number of fetuses) increased with the number of potential female breeders in the group. This relationship was driven by fetus size rather than number. The response to competition was particularly strong in low weight females and when ecological conditions were poor. Increased prenatal investment did not trade off against maternal survival. In fact we found the opposite relationship: females with greater levels of prenatal investment had elevated postnatal maternal survival. Our results support the hypothesis that mammalian prenatal development is responsive to the intensity of postnatal competition. Understanding whether these responses are adaptive requires information on the long-term consequences of prenatal investment for offspring fitness. Abstract
Mitchell J, Vitikainen EIK, Wells DA, Cant MA, Nichols HJ (2016). Heterozygosity but not inbreeding coefficient predicts parasite burdens in the banded mongoose. Journal of Zoology, 302(1), 32-39.
Cooney F, Vitikainen EIK, Marshall HH, van Rooyen W, Smith RL, Cant MA, Goodey N
(2016). Lack of aggression and apparent altruism towards intruders in a primitive termite. Royal Society Open Science
Lack of aggression and apparent altruism towards intruders in a primitive termite
In eusocial insects, the ability to discriminate nestmates from non-nestmates is widespread and ensures that altruistic actions are directed towards kin and agonistic actions are directed towards non-relatives. Most tests of nestmate recognition have focused on hymenopterans, and suggest that cooperation typically evolves in tandem with strong antagonism towards non-nestmates. Here we present evidence from a phylogenetically and behaviourally basal termite species that workers discriminate members of foreign colonies. However, contrary to our expectations, foreign intruders were the recipients of more rather than less cooperative behaviour, and were not subjected to elevated aggression. We suggest that relations between groups may be much more peaceable in basal termites compared to eusocial hymenoptera, owing to energetic and temporal constraints on colony growth, and the reduced incentive that totipotent workers (who may inherit breeding status) have to contribute to self-sacrificial intergroup conflict. Abstract
Blount JD, Vitikainen EIK, Stott I, Cant MA
(2016). Oxidative shielding and the cost of reproduction. Biological Reviews
Oxidative shielding and the cost of reproduction
Life-history theory assumes that reproduction and lifespan are constrained by trade-offs which prevent their simultaneous increase. Recently, there has been considerable interest in the possibility that this cost of reproduction is mediated by oxidative stress. However, empirical tests of this theory have yielded equivocal support. We carried out a meta-analysis to examine associations between reproduction and oxidative damage across markers and tissues. We show that oxidative damage is positively associated with reproductive effort across females of various species. Yet paradoxically, categorical comparisons of breeders versus non-breeders reveal that transition to the reproductive state is associated with a step-change reduction in oxidative damage in certain tissues and markers. Developing offspring may be particularly sensitive to harm caused by oxidative damage in mothers. Therefore, such reductions could potentially function to shield reproducing mothers, gametes and developing offspring from oxidative insults that inevitably increase as a consequence of reproductive effort. According to this perspective, we hypothesise that the cost of reproduction is mediated by dual impacts of maternally-derived oxidative damage on mothers and offspring, and that mothers may be selected to diminish such damage. Such oxidative shielding may explain why many existing studies have concluded that reproduction has little or no oxidative cost. Future advance in life-history theory therefore needs to take account of potential transgenerational impacts of the mechanisms underlying life-history trade-offs. Biological Reviews Abstract
Thompson FJ, Marshall HH, Sanderson JL, Vitikainen EIK, Nichols HJ, Gilchrist JS, Young AJ, Hodge SJ, Cant MA
(2016). Reproductive competition triggers mass eviction in cooperative banded mongooses. Proceedings of the Royal Society B: Biological Sciences
Reproductive competition triggers mass eviction in cooperative banded mongooses
. In many vertebrate societies, forced eviction of group members is an important determinant of population structure, but little is known about what triggers eviction. Three main explanations are: (i) the reproductive competition hypothesis, (ii) the coercion of cooperation hypothesis, and (iii) the adaptive forced dispersal hypothesis. The last hypothesis proposes that dominant individuals use eviction as an adaptive strategy to propagate copies of their alleles through a highly structured population. We tested these hypotheses as explanations for eviction in cooperatively breeding banded mongooses (
. Mungos mungo
. ), using a 16-year dataset on life history, behaviour and relatedness. In this species, groups of females, or mixed-sex groups, are periodically evicted
. en masse
. Our evidence suggests that reproductive competition is the main ultimate trigger for eviction for both sexes. We find little evidence that mass eviction is used to coerce helping, or as a mechanism to force dispersal of relatives into the population. Eviction of females changes the landscape of reproductive competition for remaining males, which may explain why males are evicted alongside females. Our results show that the consequences of resolving within-group conflict resonate through groups and populations to affect population structure, with important implications for social evolution.
Franks DW, Nattrass S, Brent LJN, Whitehead H, Foote AD, Mazzi S, Ford JKB, Balcomb KC, Cant MA, Croft DP, et al (2016). The significance of postreproductive lifespans in killer whales: a comment on Robeck et al.: Table 1. Journal of Mammalogy, 97(3), 906-909.
Marshall HH, Sanderson JL, Mwanghuya F, Businge R, Kyabulima S, Hares MC, Inzani E, Kalema-Zikusoka G, Mwesige K, Thompson FJ, et al
(2016). Variable ecological conditions promote male helping by changing banded mongoose group composition. Behav Ecol
Variable ecological conditions promote male helping by changing banded mongoose group composition.
Ecological conditions are expected to have an important influence on individuals' investment in cooperative care. However, the nature of their effects is unclear: both favorable and unfavorable conditions have been found to promote helping behavior. Recent studies provide a possible explanation for these conflicting results by suggesting that increased ecological variability, rather than changes in mean conditions, promote cooperative care. However, no study has tested whether increased ecological variability promotes individual-level helping behavior or the mechanisms involved. We test this hypothesis in a long-term study population of the cooperatively breeding banded mongoose, Mungos mungo, using 14 years of behavioral and meteorological data to explore how the mean and variability of ecological conditions influence individual behavior, body condition, and survival. Female body condition was more sensitive to changes in rainfall leading to poorer female survival and pronounced male-biased group compositions after periods of high rainfall variability. After such periods, older males invested more in helping behavior, potentially because they had fewer mating opportunities. These results provide the first empirical evidence for increased individual helping effort in more variable ecological conditions and suggest this arises because of individual differences in the effect of ecological conditions on body condition and survival, and the knock-on effect on social group composition. Individual differences in sensitivity to environmental variability, and the impacts this has on the internal structure and composition of animal groups, can exert a strong influence on the evolution and maintenance of social behaviors, such as cooperative care. Abstract
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Nichols HJ, Cant MA, Sanderson JL
(2015). Adjustment of costly extra-group paternity according to inbreeding risk in a cooperative mammal. Behavioral Ecology
Adjustment of costly extra-group paternity according to inbreeding risk in a cooperative mammal
Females of many animal species seek mating opportunities with multiple males, despite being able to obtain sufficient sperm to father their offspring from a single male. In animals that live in stable social groups, females often choose to mate outside their group resulting in extra-group paternity (EGP). One reason proposed to explain female choice for extra-group males is to obtain compatible genes, for example, in order to avoid inbreeding depression in offspring. The benefits of such extra-group paternities could be substantial if they result in fitter, outbred offspring. However, avoiding inbreeding in this way could be costly for females, for example, through retaliation by cuckolded males or through receiving aggression while prospecting for extra-group mating opportunities. We investigate the costs and benefits of EGP in the banded mongoose Mungos mungo, a cooperatively breeding mammal in which within-group mates are sometimes close relatives. We find that pups born to females that mate with extra-group males are more genetically heterozygous are heavier and are more likely to survive to independence than pups born to females that mate within their group. However, extra-group matings also involve substantial costs as they occur during violent encounters that sometimes result in injury and death. This appears to lead femalebanded mongooses to adaptively adjust EGP levels according to the current risk of inbreeding associated with mating within the group. For group-living animals, the costs of intergroup interactions may help to explain variation in both inbreeding rates and EGP within and between species. Abstract
Sanderson JL, Wang J, Vitikainen EIK, Cant MA, Nichols HJ (2015). Banded mongooses avoid inbreeding when mating with members of the same natal group. Molecular Ecology, 24(14), 3738-3751.
Brent LJN, Franks DW, Foster EA, Balcomb KC, Cant MA, Croft DP (2015). Ecological Knowledge, Leadership, and the Evolution of Menopause in Killer Whales. Current Biology, 25(6), 746-750.
Sanderson JL, Nichols HJ, Marshall HH, Vitikainen EIK, Thompson FJ, Walker SL, Cant MA, Young AJ
(2015). Elevated glucocorticoid concentrations during gestation predict reduced reproductive success in subordinate female banded mongooses. Biol Lett
Elevated glucocorticoid concentrations during gestation predict reduced reproductive success in subordinate female banded mongooses.
Dominant females in social species have been hypothesized to reduce the reproductive success of their subordinates by inducing elevated circulating glucocorticoid (GC) concentrations. However, this 'stress-related suppression' hypothesis has received little support in cooperatively breeding species, despite evident reproductive skews among females. We tested this hypothesis in the banded mongoose (Mungos mungo), a cooperative mammal in which multiple females conceive and carry to term in each communal breeding attempt. As predicted, lower ranked females had lower reproductive success, even among females that carried to term. While there were no rank-related differences in faecal glucocorticoid (fGC) concentrations prior to gestation or in the first trimester, lower ranked females had significantly higher fGC concentrations than higher ranked females in the second and third trimesters. Finally, females with higher fGC concentrations during the third trimester lost a greater proportion of their gestated young prior to their emergence from the burrow. Together, our results are consistent with a role for rank-related maternal stress in generating reproductive skew among females in this cooperative breeder. While studies of reproductive skew frequently consider the possibility that rank-related stress reduces the conception rates of subordinates, our findings highlight the possibility of detrimental effects on reproductive outcomes even after pregnancies have become established. Abstract
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Cant MA (2015). Reproductive suppression. In Whelehan P, Bolin A (Eds.) The International Encyclopedia of Human Sexuality, Oxford: John Wiley and Sons Ltd.
Croft DP, Brent LJN, Franks DW, Cant MA
(2015). The evolution of prolonged life after reproduction. Trends Ecol Evol
The evolution of prolonged life after reproduction.
Why females of some species cease ovulation before the end of their natural lifespan is a longstanding evolutionary puzzle. For many species in captivity, post-reproductive life is simply an epiphenomenon of lengthened lifespan. Yet in natural populations of humans as well as some cetaceans and insects, reproductive senescence occurs much faster than somatic aging and females exhibit prolonged post-reproductive lifespans (PRLSs). Determining the mechanisms and functions that underpin PRLSs has proved a significant challenge. Here we bring together both classic and modern hypotheses proposed to explain PRLSs and discuss their application to both human and nonhuman animals. By taking an integrative and broad taxonomic approach we highlight the need to consider multiple interacting explanations for the evolution of PRLSs. Abstract
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Sanderson JL, Stott I, Young AJ, Vitikainen EIK, Hodge SJ, Cant MA
(2015). The origins of consistent individual differences in cooperation in wild banded mongooses, Mungos mungo. Animal Behaviour
The origins of consistent individual differences in cooperation in wild banded mongooses, Mungos mungo
Individual differences in contributions to cooperation can be strikingly consistent over time giving rise to alternative cooperative phenotypes within animal societies. Following the social niche specialization hypothesis, these consistent differences may be driven by social conflict over reproductive opportunities if individuals specializing as 'breeders' and 'nonbreeders' experience a beneficial reduction in social conflict and differential costs associated with cooperating. This hypothesis gives three testable predictions: (1) consistent individual differences in cooperative behaviour will be accompanied by consistent individual differences in reproductive behaviour, (2) individuals contributing heavily to reproduction will contribute relatively little to cooperative behaviours within the same breeding attempt and vice versa, and (3) individuals that consistently contribute heavily to reproduction over their lifetime will also consistently contribute less to cooperative behaviours and vice versa. We tested these predictions with a 15-year investigation into the lifetime patterns of mate guarding and two forms of cooperative offspring care ('babysitting' and 'escorting') in a wild population of banded mongooses. We found significant repeatability of individual contributions to both cooperative behaviours, as well as significant repeatability of individual levels of mate guarding. However, we found no evidence of negative covariance between contributions to cooperative and reproductive behaviours either within breeding attempts or across lifetimes. This suggests that the observed consistent individual differences in both cooperative behaviour and reproduction are not associated; there is no evidence of a trade-off between reproduction and cooperation. However, we found a significant positive covariance between babysitting and escorting when estimated both within breeding attempts and across lifetimes, which suggests that some group members are generally more cooperative than others, contributing more to both behaviours over their lifetimes. The drivers of this consistent individual variation in contributions to cooperation remain unknown. Abstract
Donaldson L, Thompson FJ, Field J, Cant MA
(2014). Do paper wasps negotiate over helping effort?. Behavioral Ecology
Do paper wasps negotiate over helping effort?
Recent theory and empirical studies of avian biparental systems suggest that animals resolve conflict over parental care via a process of behavioral negotiation or "rules for responding." Less is known, however, about whether negotiation over helping effort occurs in cooperatively breeding animal societies or whether behavioral negotiation requires a relatively large brain. In this study, we tested whether negotiation over help occurs in a social insect, the paper wasp Polistes dominulus, by recording individual responses to both observed and experimentally induced foraging returns by other group members. In our experiments, we manipulated food delivery to the nest in 2 ways: 1) by catching departing foragers and giving them larval food to take back to the nest and 2) by giving larval food directly to wasps on the nest, which they then fed to larvae, so increasing food delivery independently of helper effort. We found no evidence from Experiment 1 that helpers adjusted their own foraging effort according to the foraging effort of other group members. However, when food was provided directly to the nest, wasps did respond by reducing their own foraging effort. One interpretation of this result is that paper wasp helpers adjust their helping effort according to the level of offspring need rather than the work rate of other helpers. Negotiation based on indicators of demand rather than work rate is a likely mechanism to resolve conflict over investment in teams where helpers cannot observe each other's work rate directly, as is commonly the case in insect and vertebrate societies. © the Author 2013. Abstract
Thompson FJ, Donaldson L, Johnstone RA, Field J, Cant MA
(2014). Dominant aggression as a deterrent signal in paper wasps. Behavioral Ecology
Dominant aggression as a deterrent signal in paper wasps
Low-level social aggression is a conspicuous feature of cooperative animal societies, but its precise function is usually unclear. One long-standing hypothesis is that aggressive displays by dominant individuals serve to reduce uncertainty about relative strength and deter subordinates from starting fights that they are unlikely to win. However, most formal theoretical models of this idea do not consider how the credibility of deterrent signals might change over time in social groups. We developed a simple model of dominant aggression as a deterrent signal, which takes into account how credibility changes over time and how selection should act on receiver memory. We then carried out an experimental test of the predictions of our model on a field population of the paper wasp, Polistes dominulus. The match between our theoretical and empirical results suggests that low-level social aggression can help to maintain the stability and productivity of cooperative associations in this species. Moreover, our work suggests that rates of aggression in animal societies and the robustness of social memories are likely to be intimately related. © 2014 the Author. Abstract
Nichols HJ, Cant MA, Hoffman JI, Sanderson JL
(2014). Evidence for frequent incest in a cooperatively breeding mammal. Biology Letters
Evidence for frequent incest in a cooperatively breeding mammal
As breeding between relatives often results in inbreeding depression, inbreeding avoidance is widespread in the animal kingdom. However, inbreeding avoidance may entail fitness costs. For example, dispersal away from relatives may reduce survival. How these conflicting selection pressures are resolved is challenging to investigate, but theoretical models predict that inbreeding should occur frequently in some systems. Despite this, few studies have found evidence of regular incest in mammals, even in social species where relatives are spatio-temporally clustered and opportunities for inbreeding frequently arise. We used genetic parentage assignments together with relatedness data to quantify inbreeding rates in a wild population of banded mongooses, a cooperatively breeding carnivore. We show that females regularly conceive to close relatives, including fathers and brothers. We suggest that the costs of inbreeding avoidance may sometimes outweigh the benefits, even in cooperatively breeding species where strong within-group incest avoidance is considered to be the norm. Abstract
Sanderson JL, Young AJ, Hodge SJ, Kyabulima S, Walker SL, Cant MA
(2014). Hormonal mediation of a carry-over effect in a wild cooperative mammal. Functional Ecology
Hormonal mediation of a carry-over effect in a wild cooperative mammal
Recent research has shown that parental investment in one breeding attempt often has a profound negative impact on the level of parental investment in subsequent breeding attempts. However, the mechanistic underpinnings that mediate such carry-over effects are poorly understood. Here, we hypothesise that carry-over effects arise because energetic losses lead to elevated levels of glucocorticoid 'stress' hormones which inhibit future investment and thereby maintain energetic homeostasis. We investigate this hypothesis through a detailed investigation of a carry-over effect of (allo-) parental investment in the cooperatively breeding banded mongoose (Mungos mungo). Using a combination of non-invasive hormone monitoring and feeding experiments, we demonstrate (i) that high glucocorticoid concentrations prior to breeding predict reduced alloparental investment; (ii) that energetic losses associated with high alloparental investment lead to an increase in glucocorticoid concentrations during the breeding attempt; and (iii) that elevated glucocorticoid concentrations persist into a time period that is known to affect future investment, although high pup mortality meant that we could not measure effects on subsequent alloparental investment directly. Together, our results provide strong evidence for the hypothesis that carry-over effects on parental investment are mediated by circulating glucocorticoid concentrations. Since an individual's stress physiology is shaped by early-life and social factors, our findings may help to explain how these factors contribute to individual variation in parental investment and lifetime reproductive success. Abstract
Cant MA, Nichols HJ, Johnstone RA, Hodge SJ
(2014). Policing of reproduction by hidden threats in a cooperative mammal. Proc Natl Acad Sci U S A
Policing of reproduction by hidden threats in a cooperative mammal.
The evolution of cooperation in animal and human societies is associated with mechanisms to suppress individual selfishness. In insect societies, queens and workers enforce cooperation by "policing" selfish reproduction by workers. Insect policing typically takes the form of damage limitation after individuals have carried out selfish acts (such as laying eggs). In contrast, human policing is based on the use of threats that deter individuals from acting selfishly in the first place, minimizing the need for damage limitation. Policing by threat could in principle be used to enforce reproductive suppression in animal societies, but testing this idea requires an experimental approach to simulate reproductive transgression and provoke out-of-equilibrium behavior. We carried out an experiment of this kind on a wild population of cooperatively breeding banded mongooses (Mungos mungo) in Uganda. In this species, each group contains multiple female breeders that give birth to a communal litter, usually on the same day. In a 7-y experiment we used contraceptive injections to manipulate the distribution of maternity within groups, triggering hidden threats of infanticide. Our data suggest that older, socially dominant females use the threat of infanticide to deter selfish reproduction by younger females, but that females can escape the threat of infanticide by synchronizing birth to the same day as older females. Our study shows that reproduction in animal societies can be profoundly influenced by threats that remain hidden until they are triggered experimentally. Coercion may thus extend well beyond the systems in which acts of infanticide are common. Abstract
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Port M, Cant MA
(2014). Reproductive Competition Among Males in Multimale Groups of Primates: Modeling the Costs and Effectiveness of Conflict. International Journal of Primatology
Reproductive Competition Among Males in Multimale Groups of Primates: Modeling the Costs and Effectiveness of Conflict
Multimale groups of primates are characterized by strong reproductive competition among males, generally resulting in an uneven division of male reproductive success (reproductive skew). The observed patterns of conflict and reproductive skew have often been attributed to the so-called tug-of-war model. We show, however, that two important assumptions of this model are not met in male primates. First, the tug-of-war model assumes that reproductive conflict reduces overall group productivity, but in male primates (and most other vertebrates) conflict likely involves mortality rather than fecundity costs. Second, the tug-of-war model does not account for the possibility that male primates can achieve some reproductive success without engagement in open conflict, such as when a single male cannot guard several receptive females at the same time. We therefore develop a dynamic version of the tug-of-war model, in which reproductive competition causes mortality costs, and in which individuals can gain uncontested shares of reproduction dependent on the degree of female receptive overlap. This model differs substantially from the original tug-of-war model, and derives a new and rich set of comparative predictions. For instance, it predicts that the level of conflict among males declines as the queuing success of subordinate males increases (as survival increases), and also, as their uncontested share of reproduction increases, e.g. as female receptive overlap increases. Our model shows how male-male conflict and female receptive overlap collectively determine the level of reproductive skew among male primates, and illustrates that this relationship is more complex than previously thought. © 2013 Springer Science+Business Media New York. Abstract
Bell MBV, Cant MA, Borgeaud C, Thavarajah N, Samson J, Clutton-Brock TH
(2014). Suppressing subordinate reproduction provides benefits to dominants in cooperative societies of meerkats. Nat Commun
Suppressing subordinate reproduction provides benefits to dominants in cooperative societies of meerkats.
In many animal societies, a small proportion of dominant females monopolize reproduction by actively suppressing subordinates. Theory assumes that this is because subordinate reproduction depresses the fitness of dominants, yet the effect of subordinate reproduction on dominant behaviour and reproductive success has never been directly assessed. Here, we describe the consequences of experimentally preventing subordinate breeding in 12 groups of wild meerkats (Suricata suricatta) for three breeding attempts, using contraceptive injections. When subordinates are prevented from breeding, dominants are less aggressive towards subordinates and evict them less often, leading to a higher ratio of helpers to dependent pups, and increased provisioning of the dominant's pups by subordinate females. When subordinate breeding is suppressed, dominants also show improved foraging efficiency, gain more weight during pregnancy and produce heavier pups, which grow faster. These results confirm the benefits of suppression to dominants, and help explain the evolution of singular breeding in vertebrate societies. Abstract
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Green JP, Cant MA, Field J
(2014). Using social parasitism to test reproductive skew models in a primitively eusocial wasp. Proc Biol Sci
Using social parasitism to test reproductive skew models in a primitively eusocial wasp.
Remarkable variation exists in the distribution of reproduction (skew) among members of cooperatively breeding groups, both within and between species. Reproductive skew theory has provided an important framework for understanding this variation. In the primitively eusocial Hymenoptera, two models have been routinely tested: concessions models, which assume complete control of reproduction by a dominant individual, and tug-of-war models, which assume on-going competition among group members over reproduction. Current data provide little support for either model, but uncertainty about the ability of individuals to detect genetic relatedness and difficulties in identifying traits conferring competitive ability mean that the relative importance of concessions versus tug-of-war remains unresolved. Here, we suggest that the use of social parasitism to generate meaningful variation in key social variables represents a valuable opportunity to explore the mechanisms underpinning reproductive skew within the social Hymenoptera. We present a direct test of concessions and tug-of-war models in the paper wasp Polistes dominulus by exploiting pronounced changes in relatedness and power structures that occur following replacement of the dominant by a congeneric social parasite. Comparisons of skew in parasitized and unparasitized colonies are consistent with a tug-of-war over reproduction within P. dominulus groups, but provide no evidence for reproductive concessions. Abstract
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Cant MA, Vitikainen E, Nichols HJ (2013). Chapter Six Demography and Social Evolution of Banded Mongooses. In (Ed) , 407-445.
Cant MA (2013). Cooperative breeding. In (Ed) The Princeton Guide to Evolution, Princeton: Princeton University Press.
Cant MA, Vitikainen E, Nichols HJ
(2013). Demography and social evolution of banded mongooses.
Demography and social evolution of banded mongooses
Long-term studies of cooperatively breeding vertebrates offer excellent opportunities to test theories about the evolution of cooperation and the demographic consequences of social behavior. Here we draw together over a decade of research on an unusually tractable cooperative mammal system, the banded mongoose (Mungos mungo) and compare our results against advances in social evolution theory that have occurred over the same period. We report recent data on the demographic and genetic structure of the population, and then focus on the main conflictual and cooperative features of the breeding system. Groups are founded by unrelated dispersal coalitions of males and females and consist of multiple male and female breeders. Genetic relatedness between breeding males and females increases with the number of years since group founding, but breeders nevertheless appear to avoid inbreeding. Reproductive competition between females is intense, but young females can escape infanticide by synchronizing birth to the same day as older, socially dominant females. Dominant females respond to reproductive competition by evicting subordinate females en masse. Helping behavior takes two main forms: "babysitting" offspring at the den in the early weeks of life, and "escorting" particular offspring after they emerge from the den. Males contribute most to both babysitting and escorting, particularly the low-ranking males that are excluded from breeding. The way that conflict over reproduction is resolved in this system has a strong influence on patterns of eviction and dispersal. Like many other cooperative vertebrates, each banded mongoose group represents a small, highly viscous population embedded within a larger "metapopulation". Our research highlights the links between within-group conflict, demography, and the evolution of cooperative life histories. © 2013 Elsevier Inc. Abstract
Port M, Cant MA
(2013). Longevity suppresses conflict in animal societies. Biol Lett
Longevity suppresses conflict in animal societies.
Models of social conflict in animal societies generally assume that within-group conflict reduces the value of a communal resource. For many animals, however, the primary cost of conflict is increased mortality. We develop a simple inclusive fitness model of social conflict that takes this cost into account. We show that longevity substantially reduces the level of within-group conflict, which can lead to the evolution of peaceful animal societies if relatedness among group members is high. By contrast, peaceful outcomes are never possible in models where the primary cost of social conflict is resource depletion. Incorporating mortality costs into models of social conflict can explain why many animal societies are so remarkably peaceful despite great potential for conflict. Abstract
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Cant MA, Young AJ
(2013). Resolving social conflict among females without overt aggression. Philos Trans R Soc Lond B Biol Sci
Resolving social conflict among females without overt aggression.
Members of animal societies compete over resources and reproduction, but the extent to which such conflicts of interest are resolved peacefully (without recourse to costly or wasteful acts of aggression) varies widely. Here, we describe two theoretical mechanisms that can help to understand variation in the incidence of overt behavioural conflict: (i) destruction competition and (ii) the use of threats. The two mechanisms make different assumptions about the degree to which competitors are socially sensitive (responsive to real-time changes in the behaviour of their social partners). In each case, we discuss how the model assumptions relate to biological reality and highlight the genetic, ecological and informational factors that are likely to promote peaceful conflict resolution, drawing on empirical examples. We suggest that, relative to males, reproductive conflict among females may be more frequently resolved peacefully through threats of punishment, rather than overt acts of punishment, because (i) offspring are more costly to produce for females and (ii) reproduction is more difficult to conceal. The main need now is for empirical work to test whether the mechanisms described here can indeed explain how social conflict can be resolved without overt aggression. Abstract
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Jansen DAWAM, Cant MA, Manser MB
(2013). Testing for vocal individual discrimination in adult banded mongooses. Journal of Zoology
Testing for vocal individual discrimination in adult banded mongooses
The ability to individually recognize conspecifics is acknowledged as one of the prerequisites for the development of sophisticated social relationships in group-living species. It has been hypothesized that the discrimination of individual identities is crucial for the maintenance of social relationships and cooperation based on repeated interactions, and for the evolution of many social behaviours. Previous studies have shown that the close calls of the cooperatively breeding banded mongoose Mungos mungo are individually distinct. For instance, banded mongoose pups are able to distinguish between close calls of their escort and of a non-escort. In this study, we used playbacks based on the recently proposed violation-of-expectation paradigm and a dominance/age class recognition setup to investigate whether adult banded mongooses use the individual signature of close calls to distinguish among adult group members. We found no evidence that the individual signature in close calls is used to discriminate identity in banded mongooses. Based on the previous work, we suggest that this is not because banded mongooses are incapable of using signatures as a means of individual discrimination, but because the benefits of such discrimination are low. The study highlights the importance of understanding the function of a signal (e.g. the expected response), timing and the biology of the species when designing and performing playback experiments. © 2013 the Zoological Society of London. Abstract
Cant MA, Gilchrist JS (2013). The banded mongoose (Mungos Mungo). In Kingdon J, Happold D, Butynski TM, Hoffmann M, Happold M, Kalina J (Eds.) The Mammals of Africa V: Carnivores, Pangolins, Equids and Rhinoceroses, London: a & C Black Publishers, 354-360.
Cant MA (2012). Cooperative breeding systems. In Royle NJ, Smiseth PT, Koelliker M (Eds.) The Evolution of Parental Care, Oxford: Oxford University Press, 206-225.
Nichols HJ, Jordan NR, Jamie GA, Cant MA, Hoffman JI
(2012). Fine-scale spatiotemporal patterns of genetic variation reflect budding dispersal coupled with strong natal philopatry in a cooperatively breeding mammal. Molecular Ecology
Fine-scale spatiotemporal patterns of genetic variation reflect budding dispersal coupled with strong natal philopatry in a cooperatively breeding mammal
The relatedness structure of animal populations is thought to be a critically important factor underlying the evolution of mating systems and social behaviours. While previous work has shown that population structure is shaped by many biological processes, few studies have investigated how these factors vary over time. Consequently, we explored the fine-scale spatiotemporal genetic structure of an intensively studied population of cooperatively breeding banded mongooses (Mungos mungo) over a 10-year period. Overall population structure was strong (average FST = 0.129) but groups with spatially overlapping territories were not more genetically similar to one another than noncontiguous groups. Instead, genetic differentiation was associated with historical group-fission (budding) events, with new groups diverging from their parent groups over time. Within groups, relatedness was high within but not between the sexes, although the latter increased over time since group formation due to group founders being replaced by philopatric young. This trend was not mirrored by a decrease in average offspring heterozygosity over time, suggesting that close inbreeding may often be avoided, even when immigration into established groups is virtually absent and opportunities for extra-group matings are rare. Fine-scale spatiotemporal population structure could have important implications in social species, where relatedness between interacting individuals is a vital component in the evolution of patterns of inbreeding avoidance, reproductive skew and kin-selected helping and harming. © 2012 Blackwell Publishing Ltd. Abstract
Nichols HJ, Amos W, Bell MBV, Mwanguhya F, Kyabulima S, Cant MA
(2012). Food availability shapes patterns of helping effort in a cooperative mongoose. Animal Behaviour
Food availability shapes patterns of helping effort in a cooperative mongoose
In cooperatively breeding vertebrate societies, contributions to offspring care can vary greatly between group members. Kin selection theory predicts that cooperation will be favoured when directed towards relatives and when the cost to benefit ratio is low. The fitness costs of helping in turn depend on the impact of energetic investments in care on future reproductive success, which is likely to vary between helpers. For example, investments may impact more on a young helper, which needs to invest energy in growth and is an inexperienced forager. We investigated how a key predictor of cost, food availability (estimated using rainfall), influences helping behaviour in the banded mongoose, Mungos mungo. In this cooperative carnivore, a variable number of group members breed while almost all help to rear the communal litter. Nonbreeding females and juvenile males helped less when food was scarce, reflecting the potentially high costs of weight loss and reduced growth on survival and future reproductive success. In contrast, adult males maintained their investment in care as food supply decreased, probably because body condition has relatively little impact on male reproductive success in this species. Breeding females (with pups in the communal litter) also maintained their helping effort as food supply decreased. Although mothers invested highly in care, there was no evidence that they preferentially cared for their own pups, probably because synchronized birthing scrambles maternity cues. Patterns of care in the banded mongoose thus seem to reflect the benefits gained from helping and the long-term fitness costs to the helper. © 2012 the Association for the Study of Animal Behaviour. Abstract
Nichols HJ, Bell MBV, Hodge SJ, Cant MA
(2012). Resource limitation moderates the adaptive suppression of subordinate breeding in a cooperatively breeding mongoose. Behavioral Ecology
Resource limitation moderates the adaptive suppression of subordinate breeding in a cooperatively breeding mongoose
Social animal species show considerable variation in the way in which reproduction is distributed among group members. Recent attempts to explain this variation have proposed that differences in reproductive skew are attributable to differences in the net benefits group members receive from suppressing each other's breeding attempts. Despite receiving relatively little theoretical and empirical attention, the availability of resources required for successful breeding may have an important influence in determining the costs and benefits of suppressing reproduction and thus influence reproductive skew within social groups. Here, we test this possibility using a long-term study of female reproductive success in the banded mongoose Mungos mungo. We find that females experience greater costs of co-breeding when resources are in short supply and that older, more dominant females respond to this cost by suppressing subordinate breeding. This results in differing patterns of reproductive success for females of different competitive abilities, with the oldest, most dominant females breeding regardless of resource availability and younger, subordinate females breeding only when resources are abundant. Our findings highlight the role of resource limitation in determining the distribution of reproductive opportunities within social groups. © 2012 the Author. Abstract
Jansen DAWAM, Cant MA, Manser MB
(2012). Segmental concatenation of individual signatures and context cues in banded mongoose (Mungos mungo) close calls. BMC Biol
Segmental concatenation of individual signatures and context cues in banded mongoose (Mungos mungo) close calls.
BACKGROUND: all animals are anatomically constrained in the number of discrete call types they can produce. Recent studies suggest that by combining existing calls into meaningful sequences, animals can increase the information content of their vocal repertoire despite these constraints. Additionally, signalers can use vocal signatures or cues correlated to other individual traits or contexts to increase the information encoded in their vocalizations. However, encoding multiple vocal signatures or cues using the same components of vocalizations usually reduces the signals' reliability. Segregation of information could effectively circumvent this trade-off. In this study we investigate how banded mongooses (Mungos mungo) encode multiple vocal signatures or cues in their frequently emitted graded single syllable close calls. RESULTS: the data for this study were collected on a wild, but habituated, population of banded mongooses. Using behavioral observations and acoustical analysis we found that close calls contain two acoustically different segments. The first being stable and individually distinct, and the second being graded and correlating with the current behavior of the individual, whether it is digging, searching or moving. This provides evidence of Marler's hypothesis on temporal segregation of information within a single syllable call type. Additionally, our work represents an example of an identity cue integrated as a discrete segment within a single call that is independent from context. This likely functions to avoid ambiguity between individuals or receivers having to keep track of several context-specific identity cues. CONCLUSIONS: Our study provides the first evidence of segmental concatenation of information within a single syllable in non-human vocalizations. By reviewing descriptions of call structures in the literature, we suggest a general application of this mechanism. Our study indicates that temporal segregation and segmental concatenation of vocal signatures or cues is likely a common, but so far neglected, dimension of information coding in animal vocal communication. We argue that temporal segregation of vocal signatures and cues evolves in species where communication of multiple unambiguous signals is crucial, but is limited by the number of call types produced. Abstract
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Johnstone RA, Cant MA, Field J
(2012). Sex-biased dispersal, haplodiploidy and the evolution of helping in social insects. Proceedings of the Royal Society B: Biological Sciences
Sex-biased dispersal, haplodiploidy and the evolution of helping in social insects
In his famous haplodiploidy hypothesis, W. D. Hamilton proposed that high sister-sister relatedness facilitates the evolution of kin-selected reproductive altruism among Hymenopteran females. Subsequent analyses, however, suggested that haplodiploidy cannot promote altruism unless altruists capitalize on relatedness asymmetries by helping to raise offspring whose sex ratio is more female-biased than the population at large. Here, we show that haplodiploidy is in fact more favourable than is diploidy to the evolution of reproductive altruism on the part of females, provided only that dispersal is male-biased (no sex-ratio bias or active kin discrimination is required). The effect is strong, and applies to the evolution both of sterile female helpers and of helping among breeding females. Moreover, a review of existing data suggests that female philopatry and non-local mating are widespread among nest-building Hymenoptera. We thus conclude that Hamilton was correct in his claim that 'family relationships in the Hymenoptera are potentially very favourable to the evolution of reproductive altruism'. © 2011 the Royal Society. Abstract
(2012). Suppression of social conflict and evolutionary transitions to cooperation. Am Nat
Suppression of social conflict and evolutionary transitions to cooperation.
Evolutionary conflict arises at all levels of biological organization and presents a barrier to the evolution of cooperation. This barrier can be overcome by mechanisms that reduce the disparity between the fitness optima of subunits, sometimes called the "battleground" of conflict. An alternative, unstudied possibility is that effort invested in conflict is unprofitable. This possibility has received little attention because most existing models of social conflict assume that fitness depends on the ratio of players' conflict efforts, so that "peaceful" outcomes featuring zero conflict effort are evolutionarily unstable. Here I show that peaceful outcomes are stable where success depends on the difference rather than the ratio of efforts invested in conflict. These difference form models are particularly appropriate to model strategies of suppression or policing. The model suggests that incomplete information and asymmetries in strength can act to eliminate costly conflict within groups, even among unrelated individuals, and thereby facilitate the evolution of cooperation. Abstract
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Bell MBV, Nichols HJ, Gilchrist JS, Cant MA, Hodge SJ
(2012). The cost of dominance: Suppressing subordinate reproduction affects the reproductive success of dominant female banded mongooses. Proceedings of the Royal Society B: Biological Sciences
The cost of dominance: Suppressing subordinate reproduction affects the reproductive success of dominant female banded mongooses
Social species show considerable variation in the extent to which dominant females suppress subordinate reproduction. Much of this variation may be influenced by the cost of active suppression to dominants, who may be selected to balance the need to maximize the resources available for their own offspring against the costs of interfering with subordinate reproduction. To date, the cost of reproductive suppression has received little attention, despite its potential to influence the outcome of conflict over the distribution of reproduction in social species. Here, we investigate possible costs of reproductive suppression in banded mongooses, where dominant females evict subordinates from their groups, thereby inducing subordinate abortion. We show that evicting subordinate females is associated with substantial costs to dominant females: pups born to females who evicted subordinates while pregnant were lighter than those born after undisturbed gestations; pups whose dependent period was disrupted by an eviction attained a lower weight at independence; and the proportion of a litter that survived to independence was reduced if there was an eviction during the dependent period. To our knowledge, this is the first empirical study indicating a possible cost to dominants in attempting to suppress subordinate breeding, and we argue that much of the variation in reproductive skew both within and between social species may be influenced by adaptive variation in the effort invested in suppression by dominants. © 2011 the Royal Society. Abstract
Abbot P, Abe J, Alcock J, Alizon S, Alpedrinha JAC, Andersson M, Andre JB, Van Baalen M, Balloux F, Balshine S, et al (2011). Inclusive fitness theory and eusociality. Nature, 471(7339).
Furrer RD, Kyabulima S, Willems EP, Cant MA, Manser MB
(2011). Location and group size influence decisions in simulated intergroup encounters in banded mongooses. Behavioral Ecology
Location and group size influence decisions in simulated intergroup encounters in banded mongooses
In social species that cooperatively defend territories the decision to retreat or attack in contests between groups is likely to depend on ecological and social factors. Previous studies have emphasized the importance of the encounter location or the size of competing groups on the outcome. In addition, the identity of the intruder, whether familiar or stranger, may also play a role. To test whether the same factors affect the resident group's decisions already at the beginning of contests, we simulated intergroup encounters in banded mongooses (Mungos mungo). When spotting rival groups banded mongooses emit "screeching calls" which lead group members to bunch up. With playbacks of these calls, we tested how the groups' response was affected by the following factors: 1) the location of the playback in relation to their territory (exclusive use vs. overlap); 2) the number of resident individuals; and 3) the origin of calls (neighbor vs. stranger) used. Subjects were more likely to approach the loudspeakers and arrive within 1 m of the speakers in the exclusive use zone than in the overlap zone. Moreover, larger groups tended to be more likely to move toward the loudspeakers and were also more likely to arrive there. The origin of calls used in the playbacks did not affect the groups' responses. These findings exemplify the importance of the combined effect of location and group size on group decisions during impending intergroup contest. © the Author 2011. Abstract
Hodge SJ, Bell MBV, Cant MA
(2011). Reproductive competition and the evolution of extreme birth synchrony in a cooperative mammal. Biology Letters
Reproductive competition and the evolution of extreme birth synchrony in a cooperative mammal
Reproductive events in animal societies often show a high degree of temporal clustering, but the evolutionary causes of this synchronization are poorly understood. Here, we suggest that selection to avoid the negative effects of competition with other females has given rise to a remarkable degree of birth synchrony in the communal-breeding banded mongoose (Mungos mungo). Within banded mongoose groups, births are highly synchronous, with 64 per cent of females giving birth on exactly the same night. Our results indicate that this extreme synchrony arises because offspring suffer an increased risk of infanticide if their mother gives birth before other females, but suffer in competition with older littermates if their mother gives birth after them. These findings highlight the important influence that reproductive competition can have for the evolution of reproductive synchrony. This journal is © 2010 the Royal Society. Abstract
Jordan NR, Manser MB, Mwanguhya F, Kyabulima S, Rüedi P, Cant MA
(2011). Scent marking in wild banded mongooses: 1. Sex-specific scents and overmarking. Animal Behaviour
Scent marking in wild banded mongooses: 1. Sex-specific scents and overmarking
Overmarking occurs when one individual places its scent mark directly on top of the scent mark of another individual. Although it is almost ubiquitous among terrestrial mammals, we know little about the function of overmarking and detailed field observations are rare. We investigated the chemical composition of scents and patterns of overmarking by wild banded mongooses, Mungos mungo. Chemical analyses of anal gland secretions showed that scents were sexually dimorphic. Both male and female adults were more likely to overmark the scents of same-sex individuals. An analysis of responses to two scents on the same site suggested that the sex of the top or most recent scent was more important than that of the bottom or original scent in determining overmarking response. Juveniles also overmarked scents at high rates, but did not respond to scents in a sex-specific way. Same-sex-specific patterns within groups have not been described in any other species, and may reflect a social system with intense intrasexual competition for reproduction within both sexes. Banded mongooses live in large mixed-sex groups, with intense competition between males for females, owing to the heavily male-biased adult sex ratio and highly synchronized oestrous cycles. Oestrous synchronization may also promote intrasexual competition for males within females, as females compete simultaneously for high-quality males. Female competition for males may also be enhanced by the rewards of male-biased parental care. This investigation highlights the need for detailed studies of overmarking in the natural context, to confirm and expand upon laboratory findings. © 2010 the Association for the Study of Animal Behaviour. Abstract
Jordan NR, Mwanguhya F, Furrer RD, Kyabulima S, Rüedi P, Cant MA
(2011). Scent marking in wild banded mongooses: 2. Intrasexual overmarking and competition between males. Animal Behaviour
Scent marking in wild banded mongooses: 2. Intrasexual overmarking and competition between males
Sexual selection has resulted in the elaboration of secondary sexual characteristics in many animals. Although mammalian scent glands, secretions and marking behaviour are commonly sexually dimorphic, these traits have received little attention compared to avian plumage and mammalian weaponry. Overmarking, when one individual places a scent mark directly over that of another individual, is of particular interest. Owing to the costs of repeatedly monitoring and covering the scent marks of rivals, overmarking may provide an honest indication of a male's resource-holding potential, perhaps explaining why female rodents exposed to experimental overmarks subsequently prefer to associate with males whose scent mark was on top. This study on wild banded mongooses, Mungos mungo, suggests that overmarking may primarily affect behavioural mating success through male competition not by female mate choice. First, chemical analyses of anal gland secretions demonstrated that males had individually distinctive scents, and a field experiment confirmed that mongooses were able to discriminate between scents from different individuals. Observations of overmarking patterns showed a relationship between overmarking score and behavioural mating success, but we found no evidence that females actively chose to mate with males with high overmarking scores. Instead, we found that males with higher overmarking scores first mate-guarded females at a significantly younger age than males with lower overmarking scores. Since mate-guarding males obtain the vast majority of matings, this suggests that overmarking may be an important component of intrasexual competition for mating opportunities in this species. © 2010 the Association for the Study of Animal Behaviour. Abstract
Jordan NR, Mwanguhya F, Kyabulima S, Rüedi P, Hodge SJ, Cant MA
(2011). Scent marking in wild banded mongooses: 3. Intrasexual overmarking in females. Animal Behaviour
Scent marking in wild banded mongooses: 3. Intrasexual overmarking in females
In contrast to numerous studies of scent marking in male mammals, studies of female scent marking are relatively rare. We have previously shown that communally breeding female banded mongooses, Mungos mungo, are more likely to overmark the scent of other females. Here we describe female overmarking patterns in more detail, and discuss these results in relation to hypotheses potentially explaining such 'female intrasexual overmarking'. To our knowledge, this is the first study to investigate female overmarking in any wild mammal. First, although we found some evidence of individually distinctive scent marks in females, we found no evidence to suggest that female intrasexual overmarking was related to competition for food, as feeding competition was infrequent, and unrelated to overmarking scores. We also found no evidence to suggest that intrasexual overmarking in females was involved in reproductive suppression. Females with the highest and lowest overmarking scores in each group were mate-guarded by males for similar durations. Finally, we found little evidence to suggest that female intrasexual overmarking was involved in competition for males. Although the female with the highest overmarking score in each group tended to be mate-guarded by males in better condition than the female with the lowest overmarking score, a female's overmarking score affected neither the amount of harassment she received from males nor the frequency of mating attempts received. These results are discussed in light of these and other untested hypotheses for female overmarking. © 2010 the Association for the Study of Animal Behaviour. Abstract
(2011). The role of threats in animal cooperation. Proc Biol Sci
The role of threats in animal cooperation.
In human societies, social behaviour is strongly influenced by threats of punishment, even though the threats themselves rarely need to be exercised. Recent experimental evidence suggests that similar hidden threats can promote cooperation and limit within-group selfishness in some animal systems. In other animals, however, threats appear to be ineffective. Here I review theoretical and empirical studies that help to understand the evolutionary causes of these contrasting patterns, and identify three factors-impact, accuracy and perception-that together determine the effectiveness of threats to induce cooperation. Abstract
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Müller CA, Cant MA
(2010). Imitation and traditions in wild banded mongooses. Current Biology
Imitation and traditions in wild banded mongooses
Evidence has accumulated in recent years indicating that traditions are not a unique feature of human societies but may be common in primates and some other mammals [1-8]. However, most documented cases remain contentious because observational studies of free-living animals suffer from interpretive weaknesses [9, 10], whereas social diffusion experiments performed in captivity (e.g. [6-8]) may not reflect conditions found in nature [2, 10]. Here we use experiments under natural conditions to demonstrate that wild banded mongooses (Mungos mungo) pass preferences for one of two possible foraging techniques on to the next generation through contextual imitation. Notably, both techniques coexisted within the same groups and were transmitted concurrently between adults and pups, which form close one-to-one associations during the period of pup dependency. This experimental demonstration of a foraging tradition in wild mammals provides critical evidence to support previous accounts of traditions in nonhuman animals based on distribution patterns of natural behaviors [1-4]. Moreover, our data provide the first experimental demonstration of imitation in wild mammals and, contrary to common assumption [9, 11], show that social learning need not lead to an increased behavioral homogeneity within groups. © 2010 Elsevier Ltd. Abstract
Cant MA, Hodge SJ, Bell MBV, Gilchrist JS, Nichols HJ
(2010). Reproductive control via eviction (but not the threat of eviction) in banded mongooses. Proc Biol Sci
Reproductive control via eviction (but not the threat of eviction) in banded mongooses.
Considerable research has focused on understanding variation in reproductive skew in cooperative animal societies, but the pace of theoretical development has far outstripped empirical testing of the models. One major class of model suggests that dominant individuals can use the threat of eviction to deter subordinate reproduction (the 'restraint' model), but this idea remains untested. Here, we use long-term behavioural and genetic data to test the assumptions of the restraint model in banded mongooses (Mungos mungo), a species in which subordinates breed regularly and evictions are common. We found that dominant females suffer reproductive costs when subordinates breed, and respond to these costs by evicting breeding subordinates from the group en masse, in agreement with the assumptions of the model. We found no evidence, however, that subordinate females exercise reproductive restraint to avoid being evicted in the first place. This means that the pattern of reproduction is not the result of a reproductive 'transaction' to avert the threat of eviction. We present a simple game theoretical analysis that suggests that eviction threats may often be ineffective to induce pre-emptive restraint among multiple subordinates and predicts that threats of eviction (or departure) will be much more effective in dyadic relationships and linear hierarchies. Transactional models may be more applicable to these systems. Greater focus on testing the assumptions rather than predictions of skew models can lead to a better understanding of how animals control each other's reproduction, and the extent to which behaviour is shaped by overt acts versus hidden threats. Abstract
. Author URL
Jordan NR, Mwanguhya F, Kyabulima S, Rueedi P, Cant MA
(2010). Scent marking within and between groups of wild banded mongooses. JOURNAL OF ZOOLOGY
(1), 72-83. Author URL
Johnstone RA, Cant MA
(2010). The evolution of menopause in cetaceans and humans: the role of demography. Proceedings of the Royal Society B: Biological Sciences
The evolution of menopause in cetaceans and humans: the role of demography
Human females stop reproducing long before they die. Among other mammals, only pilot and killer whales exhibit a comparable period of post-reproductive life. The grandmother hypothesis suggests that kin selection can favour post-reproductive survival when older females help their relatives to reproduce. But although there is an evidence that grandmothers can provide such assistance, it is puzzling why menopause should have evolved only among the great apes and toothed whales. We have previously suggested (Cant & Johnstone 2008 Proc. Natl Acad. Sci. USA 105, 5332-5336 (doi:10.1073/pnas. 0711911105)) that relatedness asymmetries owing to female-biased dispersal in ancestral humans would have favoured younger females in reproductive competition with older females, predisposing our species to the evolution of menopause. But this argument appears inapplicable to menopausal cetaceans, which exhibit philopatry of both sexes combined with extra-group mating. Here, we derive general formulae for 'kinship dynamics', the agerelated changes in local relatedness that occur in long-lived social organisms as a consequence of dispersal and mortality. We show that the very different social structures of great apes and menopausal whales both give rise to an increase in local relatedness with female age, favouring late-life helping. Our analysis can therefore help to explain why, of all long-lived, social mammals, it is specifically among the great apes and toothed whales that menopause and post-reproductive helping have evolved. © 2010 the Royal Society. Abstract
Nichols HJ, Amos W, Cant MA, Bell MBV, Hodge SJ
(2010). Top males gain high reproductive success by guarding more successful females in a cooperatively breeding mongoose. Animal Behaviour
Top males gain high reproductive success by guarding more successful females in a cooperatively breeding mongoose
Of key importance for understanding cooperative societies is the way in which reproductive opportunities are distributed among group members. Traditionally, skew has been thought of as a product of intrasexual competition. However, cooperatively breeding species often live in mixed-sex groups, so the behaviour of one sex has the potential to influence skew in the other. We addressed the importance of inter- and intrasexual conflict in determining reproductive skew through a study of paternity sharing in the cooperatively breeding banded mongoose, Mungus mungo. Unlike banded mongoose females, where reproductive skew is low, males exhibited high skew, with 85% of paternities being assigned to the three oldest males in each group. Individual males appeared unable to monopolize reproduction because females come into oestrus in synchrony and mate multiply. Instead, older males increased their success by mate guarding the oldest, most fecund females. Our findings therefore highlight the importance of mate choice in males and reveal the behavioural differences between the sexes that generate reproductive skew. They also emphasize the considerable influence that female behaviour can have on male reproductive skew. © 2010 the Association for the Study of Animal Behaviour. Abstract
Cant MA, Johnstone RA
(2009). How threats influence the evolutionary resolution of within-group conflict. American Naturalist
How threats influence the evolutionary resolution of within-group conflict
Most examples of cooperation in nature share a common feature: individuals can interact to produce a productivity benefit or fitness surplus, but there is conflict over how these gains are shared. A central question is how threats to exercise outside options influence the resolution of conflict within such cooperative associations. Here we show how a simple principle from economic bargaining theory, the outside option principle, can help to solve this problem in biological systems. According to this principle, outside options will affect the resolution of conflict only when the payoff of taking up these options exceeds the payoffs individuals can obtain from bargaining or negotiating within the group; otherwise, threats to exercise outside options are not credible and are therefore irrelevant. We show that previous attempts to incorporate outside options in synthetic models of reproductive conflict fail to distinguish between credible and incredible threats, and then we use the outside option principle to develop credible synthetic models in two contexts: reproductive skew and biparental care. A striking prediction of our analysis is that outside options are least relevant to the resolution of conflict in cooperative groups of kin and are most relevant in transient associations or interactions among nonrelatives. Our analysis shows a way to link the resolution of within-group conflict to the environmental setting in which it occurs, and it illuminates the role of threats in the evolution of social behavior. © 2009 by the University of Chicago. Abstract
Johnstone RA, Cant, M.A.
(2009). Models of reproductive skew: outside options and the resolution of reproductive conflict. In Hager R, Jones CB (Eds.) Reproductive Skew in Vertebrates
, Cambridge: Cambridge University Press, 3-23.
Models of reproductive skew: outside options and the resolution of reproductive conflict.
Cant MA, Johnstone RA, Russell AF
(2009). Reproductive conflict and the evolution of menopause. In Hager R, Jones CB (Eds.) Reproductive Skew in Vertebrates
, in Reproductive Skew in Vertebrates: Cambridge University Press, 24-52.
Reproductive conflict and the evolution of menopause.
Field J, Cant, M.A.
(2009). Reproductive skew in primitively eusocial insects: lessons for vertebrates. In Hager R, Jones CB (Eds.) Reproductive Skew in Vertebrates
, Cambridge: Cambridge University Press, 305-334.
Reproductive skew in primitively eusocial insects: lessons for vertebrates.
Field J, Cant MA
(2009). Social stability and helping in small animal societies. Philosophical Transactions of the Royal Society B: Biological Sciences
Social stability and helping in small animal societies
In primitively eusocial societies, all individuals can potentially reproduce independently. The key fact that we focus on in this paper is that individuals in such societies instead often queue to inherit breeding positions. Queuing leads to systematic differences in expected future fitness. We first discuss the implications this has for variation in behaviour. For example, because helpers nearer to the front of the queue have more to lose, they should work less hard to rear the dominant's offspring. However, higher rankers may be more aggressive than low rankers, even if they risk injury in the process, if aggression functions to maintain or enhance queue position. Second, we discuss how queuing rules may be enforced through hidden threats that rarely have to be carried out. In fishes, rule breakers face the threat of eviction from the group. In contrast, subordinate paper wasps are not injured or evicted during escalated challenges against the dominant, perhaps because they are more valuable to the dominant. We discuss evidence that paper-wasp dominants avoid escalated conflicts by ceding reproduction to subordinates. Queuing rules appear usually to be enforced by individuals adjacent in the queue rather than by dominants. Further manipulative studies are required to reveal mechanisms underlying queue stability and to elucidate what determines queue position in the first place. © 2009 the Royal Society. Abstract
Cant MA, Johnstone RA
(2008). Reproductive conflict and the separation of reproductive generations in humans. Proc Natl Acad Sci U S A
Reproductive conflict and the separation of reproductive generations in humans.
An enduring puzzle of human life history is why women cease reproduction midway through life. Selection can favor postreproductive survival because older females can help their offspring to reproduce. But the kin-selected fitness gains of helping appear insufficient to outweigh the potential benefits of continued reproduction. Why then do women cease reproduction in the first place? Here, we suggest that early reproductive cessation in humans is the outcome of reproductive competition between generations, and we present a simple candidate model of how this competition will be resolved. We show that among primates exhibiting a postreproductive life span, humans exhibit an extraordinarily low degree of reproductive overlap between generations. The rapid senescence of the human female reproductive system coincides with the age at which, in natural fertility populations, women are expected to encounter reproductive competition from breeding females of the next generation. Several lines of evidence suggest that in ancestral hominids, this younger generation typically comprised immigrant females. In these circumstances, relatedness asymmetries within families are predicted to give younger females a decisive advantage in reproductive conflict with older females. A model incorporating both the costs of reproductive competition and the benefits of grandmothering can account for the timing of reproductive cessation in humans and so offers an improved understanding of the evolution of menopause. Abstract
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Johnstone RA, Cant MA
(2008). Sex differences in dispersal and the evolution of helping and harming. Am Nat
Sex differences in dispersal and the evolution of helping and harming.
In this article, we explore the impact of sex-biased dispersal on local relatedness and on selection for helping and harming behavior among males and females. We show that in a patch-structured population, when there is a marked sex bias in dispersal, selection will almost always favor harming behavior among individuals of the sex more prone to dispersal. This result holds regardless of the effects of mating skew or overlapping generations. Selection may well also favor helping behavior among individuals of the philopatric sex, particularly if there is generational overlap, but this is less likely to occur if individuals of the philopatric sex compete more intensely for fewer breeding opportunities. In this last case, if generational overlap is low and mating skew pronounced, the result may be selection for harming behavior among both males and females. In general, the rate of dispersal and the level of relatedness among individuals of one sex do not reliably predict their level of helping or harming behavior; selection on either males or females depends on the dispersal of both sexes. Abstract
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Field J, Cant MA (2007). Direct fitness, reciprocity and helping: a perspective from primitively eusocial wasps. Behavioural Processes, 76(2), 160-162.
Buston PM, Reeve HK, Cant MA, Vehrencamp SL, Emlen ST
(2007). Reproductive skew and the evolution of group dissolution tactics: a synthesis of concession and restraint models. Animal Behaviour
Reproductive skew and the evolution of group dissolution tactics: a synthesis of concession and restraint models
Reproductive skew theory provides a compelling explanation for the partitioning of reproduction among individuals within animal societies. One constructive criticism of the theory is that there are too many models, all of which have different assumptions and predictions, which makes it difficult to know what to test. Here we begin the process of tackling this problem, by re-examining the assumptions and predictions of basic concession and restraint models, two transactional models that are often tested as alternatives. Concession models assume that the dominant has complete control over the allocation of reproduction but may yield some of the group's reproduction to prevent the subordinate from voluntarily departing. Restraint models assume that the subordinate has complete control over the allocation of reproduction but may not claim all of the group's reproduction to prevent the dominant from forcibly evicting it. We show that the group dissolution tactics that individuals use (forcible eviction or voluntary departure) need not be an assumption of the model, but rather they can be predicted using Hamilton's rule and the standard variables of skew models. We reveal that the assumption that one individual (dominant or subordinate) has complete control over the allocation of reproduction is an idea common to both models, and we resolve this semantic difference by calling this individual 'the allocator'. We show that, regardless of the group dissolution tactics that individuals adopt, the allocator's share of the reproduction always increases as relatedness increases, as group productivity increases, and as constraints on leaving to breed elsewhere intensify. We conclude that concession and restraint type models make qualitatively similar predictions, and should not be tested as alternatives. In summary, this study makes the transactional framework of reproductive skew more general, by eliminating restrictive assumptions, and more amenable to testing in the field, by clarifying assumptions and predictions. © 2007 the Association for the Study of Animal Behaviour. Abstract
Buston PM, Cant MA
(2006). A new perspective on size hierarchies in nature: Patterns, causes, and consequences. Oecologia
A new perspective on size hierarchies in nature: Patterns, causes, and consequences
Many plant and animal aggregations have size hierarchies within which a variety of sizes of individuals, from large to small, can be found. Size hierarchies are thought to indicate the existence of competition amongst individuals within the aggregation, but determining their exact cause is difficult. The key to understanding size hierarchies lies in first quantifying the pattern of size and growth of individuals. We conducted a quantitative investigation of pattern in the size hierarchy of the clown anemonefish Amphiprion percula, in Madang Lagoon, Papua New Guinea. Here, groups of A. percula occupy sea anemones (Heteractis magnifica) that provide protection from predators. Within each anemone there is a single group composed of a breeding pair and zero to four non-breeders. Within each group there is a single size hierarchy; the female is largest (rank 1), the male is second largest (rank 2), and the non-breeders get progressively smaller (ranks 3-6). We demonstrate that individuals adjacent in rank are separated by body size ratios whose distribution is significantly different from the distribution expected under a null model-the growth of individuals is regulated such that each dominant ends up being about 1.26 times the size of its immediate subordinate. We show that it is decisions about growth at the individual level that generate the size hierarchy at the group level, and thereby determine maximum group size and population size. This study provides a new perspective on the pattern, causes and consequences of size hierarchies. © Springer-Verlag 2006. Abstract
(2006). A tale of two theories: Parent-offspring conflict and reproductive skew. Animal Behaviour
A tale of two theories: Parent-offspring conflict and reproductive skew
The recent development of reproductive skew (RS) theory shows striking parallels with that of parent-offspring conflict (POC) theory a decade earlier. In particular, the concept of 'battleground' and 'resolution' models in POC theory is equally relevant to RS theory. The battleground of conflict in POC and RS has been defined by different constraints (which I term 'optimization' and 'group stability' constraints, respectively). This distinction is not inherent but arises simply because POC models assume that the fitness benefits of an increasing share of resource show diminishing returns, whereas skew models assume a linear relation between reproductive share and fitness. Incorporating diminishing returns into skew models reveals a simple and almost wholly neglected explanation for reproductive sharing. Models of POC have moved on from simply defining the battleground to consider how conflict within it is resolved. The development of analogous models for RS theory is at a relatively early stage. In particular, more work is needed to understand the manner and extent to which overt aggression can mediate reproductive control. Lessons learned from attempts to test POC theory can help guide tests of RS theory, and provide information on both the nature of the battleground over reproduction and the mechanism by which conflicts are resolved. © 2006 the Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Abstract
Cant MA, Shen SF
(2006). Endogenous timing in competitive interactions among relatives. Proceedings of the Royal Society B: Biological Sciences
Endogenous timing in competitive interactions among relatives
Most evolutionary game theory models solve for equilibrium levels of some behaviour on the restrictive assumptions that players choose their actions simultaneously, and that a player cannot change its action after observing that of its opponent. An alternative framework is provided by sequential or 'Stackelberg' games in which one player commits to a 'first move' and the other has an opportunity to observe this move before choosing its response. Recent interest in the economic literature has focused on Stackelberg games which exhibit 'endogenous timing', i.e. games in which a leader and a follower arise spontaneously as a consequence of each player attempting to maximize its reward. Here, we provide the first demonstration of endogenous timing in an evolutionary context using a simple model of resource competition (the 'tug-of-war' model). We show that whenever two related individuals compete for a share of communal resources, both do best to adopt distinct roles in a sequential game rather than engage in simultaneous competition. Somewhat counterintuitively, the stable solution is for the weaker individual to act as leader and commit to a first move, because this arrangement leads to a lower total effort invested in competition. Endogenous timing offers a new explanation for the spontaneous emergence of leaders and followers in social groups, and highlights the benefits of commitment in social interaction. © 2005 the Royal Society. Abstract
Cant MA, English S, Reeve HK, Field J
(2006). Escalated conflict in a social hierarchy. Proc Biol Sci
Escalated conflict in a social hierarchy.
Animals that live in cooperative societies form hierarchies in which dominant individuals reap disproportionate benefits from group cooperation. The stability of these societies requires subordinates to accept their inferior status rather than engage in escalated conflict with dominants over rank. Applying the logic of animal contests to these cases predicts that escalated conflict is more likely where subordinates are reproductively suppressed, where group productivity is high, relatedness is low, and where subordinates are relatively strong. We tested these four predictions in the field on co-foundress associations of the paper wasp Polistes dominulus by inducing contests over dominance rank experimentally. Subordinates with lower levels of ovarian development, and those in larger, more productive groups, were more likely to escalate in conflict with their dominant, as predicted. Neither genetic relatedness nor relative body size had significant effects on the probability of escalation. The original dominant emerged as the winner in all except one escalated contest. The results provide the first evidence that reproductive suppression of subordinates increases the threat of escalated conflict, and hence that reproductive sharing can promote stability of the dominant-subordinate relationship. Abstract
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Field J, Cant MA (2006). Helping effort in primitively eusocial wasps. Annales Zoologici Fennici, 43, 481-487.
Cant, Llop, Field (2006). Individual Variation in Social Aggression and the Probability of Inheritance: Theory and a Field Test. The American Naturalist, 167(6), 837-837.
Cant MA, Llop JB, Field J
(2006). Individual variation in social aggression and the probability of inheritance: theory and a field test. Am Nat
Individual variation in social aggression and the probability of inheritance: theory and a field test.
Recent theory suggests that much of the wide variation in individual behavior that exists within cooperative animal societies can be explained by variation in the future direct component of fitness, or the probability of inheritance. Here we develop two models to explore the effect of variation in future fitness on social aggression. The models predict that rates of aggression will be highest toward the front of the queue to inherit and will be higher in larger, more productive groups. A third prediction is that, in seasonal animals, aggression will increase as the time available to inherit the breeding position runs out. We tested these predictions using a model social species, the paper wasp Polistes dominulus. We found that rates of both aggressive "displays" (aimed at individuals of lower rank) and aggressive "tests" (aimed at individuals of higher rank) decreased down the hierarchy, as predicted by our models. The only other significant factor affecting aggression rates was date, with more aggression observed later in the season, also as predicted. Variation in future fitness due to inheritance rank is the hidden factor accounting for much of the variation in aggressiveness among apparently equivalent individuals in this species. Abstract
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Cant MA, Johnstone RA
(2006). Self-serving punishment and the evolution of cooperation. J Evol Biol
(5), 1383-1385. Author URL
Cant MA, English S
(2006). Stable group size in cooperative breeders: the role of inheritance and reproductive skew. Behavioral Ecology
Stable group size in cooperative breeders: the role of inheritance and reproductive skew
Recent studies of reproductive skew have revealed great variation in the distribution of direct fitness among group members, yet there have been surprisingly few attempts to explore the consequences of such variation for stable group size, and none that take into account the future benefits of group membership to nonbreeders. This means that the existing theory is not suited to explain the group size of most cooperatively breeding vertebrates and primitively social insects in which group membership involves substantial future benefits. Here we model the group size of such species as social queues in which nonbreeders can inherit a breeding position if they outlive those ahead of them in the queue. We demonstrate, however, that the results can be generalized to systems in which inheritance occurs via scramble competition, rather than via a strict queue. The model predicts that stable group size will depend on the number of breeding positions in the group and the mortality rates of breeders and nonbreeders, but not on the distribution of reproduction among the pool of breeders. This is because deaths occur at random, so that each individual has the same chance of surviving to reach each breeding position. We tested a specific prediction of the model using data on ovarian development in the paper wasp, Polistes dominulus. We found a positive correlation between group size and the proportion of females with fully developed eggs, as predicted. Our results clarify the interaction between the dominance structure and size of animal groups and add to the growing recognition of the potential for inheritance as a major determinant of both individual behavior and group-level characteristics of animal societies. © the Author 2006. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. Abstract
Cant MA, Field J
(2005). Helping effort in a dominance hierarchy. Behavioral Ecology
Helping effort in a dominance hierarchy
In many cooperatively breeding species, group members form a dominance hierarchy or queue to inherit the position of breeder. Models aimed at understanding individual variation in helping behavior, however, rarely take into account the effect of dominance rank on expected future reproductive success and thus the potential direct fitness costs of helping. Here we develop a kin-selection model of helping behavior in multimember groups in which only the highest ranking individual breeds. Each group member can invest in the dominant's offspring at a cost to its own survivorship. The model predicts that lower ranked subordinates, who have a smaller probability of inheriting the group, should work harder than higher ranked subordinates. This prediction holds regardless of whether the intrinsic mortality rate of subordinates increases or decreases with rank. The prediction does not necessarily hold, however, where the costs of helping are higher for lower ranked individuals: a situation that may be common in vertebrates. The model makes two further testable predictions: that the helping effort of an individual of given rank should be lower in larger groups, and the reproductive success of dominants should be greater where group members are more closely related. Empirical evidence for these predictions is discussed. We argue that the effects of rank on stable helping effort may explain why attempts to correlate individual helping effort with relatedness in cooperatively breeding species have met with limited success. © the Author 2005. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. Abstract
Shreeves G, Cant MA, Bolton A, Field J
(2003). Insurance-based advantages for subordinate co-foundresses in a temperate paper wasp. Proceedings of the Royal Society B: Biological Sciences
Insurance-based advantages for subordinate co-foundresses in a temperate paper wasp
Recent explanations for the evolution of eusociality, focusing more on costs and benefits than relatedness, are largely untested. We validate one such model by showing that helpers in foundress groups of the paper wasp Polistes dominulus benefit from an insurance-based mechanism known as Assured Fitness Returns (AFRs). Experimental helper removals left remaining group members with more offspring than they would normally rear. Reduced groups succeeded in preserving the dead helpers' investment by rearing these extra offspring, even when helper removals occurred long before worker emergence. While helpers clearly gained from AFRs, offspring of lone foundresses failed after foundress death, so that AFRs represent a true advantage for helpers. Smaller, less valuable offspring were probably sacrificed to feed larger offspring, but reduced groups did not preferentially attract joiners or increase their foraging effort to compensate for their smaller workforce. We failed to detect a second insurance-based advantage, Survivorship Insurance, in which larger groups are less likely to fail than smaller groups. We suggest that through their use of small offspring as a food store to cope with temporary shortages, wasps may be less susceptible than vertebrates to offspring failure following the death of group members. Abstract
(2003). Patterns of helping effort in co-operatively breeding banded mongooses (Mungos mungo). Journal of Zoology
Patterns of helping effort in co-operatively breeding banded mongooses (Mungos mungo)
In most co-operative breeding species, some individuals contribute much more to helping behaviour than others. The most well-established explanation of such variation is based on kin selection and suggests that, in the absence of detectable differences in relatedness, individuals who suffer lower costs for a given level of help should contribute more. Differences in helping effort between dominance/sex categories were investigated in co-operatively breeding banded mongooses Mungos mungo in Uganda. The most conspicuous form of help in this species is provided by individuals who babysit offspring at the den while the rest of the pack goes off to forage. Across eight groups, the survival rate of pups increased with the average number of babysitters guarding them, consistent with the hypothesis that helpers benefit the brood that they guard. There was no difference between dominant males, subordinate males and breeding females in total contributions to babysitting. Subordinate males, however, contributed more to babysitting in the mornings, which were the longest and presumably the most energetically expensive sessions of the day. In six litters in one well-studied pack, dominant males and breeding females reduced their contribution to babysitting for the period that females were in oestrus. By contrast, subordinate males increased their contribution to become the main babysitters during this time. These results are consistent with the hypothesis that, where helping conflicts with breeding, individuals with little chance of direct reproduction can help at a lower fitness cost than those with a high probability of successful reproduction. Abstract
Cant, Reeve (2002). Female Control of the Distribution of Paternity in Cooperative Breeders. The American Naturalist, 160(5), 602-602.
Cant MA, Reeve HK
(2002). Female control of the distribution of paternity in cooperative breeders. American Naturalist
Female control of the distribution of paternity in cooperative breeders
Models of reproductive skew have shed light on why animal societies vary in the partitioning of reproduction among group members. However, their application to cooperative vertebrate societies remains controversial. A particular problem is that previous models assume that skew in paternity is determined by interactions among males and males only. This conflicts with observations from many species that indicate that females exert control over the distribution of paternity. Here we address this shortfall in the current theory by developing two models to explore the expected patterns of skew in three member groups in which a female controls the allocation of paternity among two males. The first "staying incentive" model extends previous "transactional" (or "concession") models to examine the conditions where females will be willing to share reproduction among a dominant and a subordinate male to retain the subordinate in the group. The second "work incentive" model explores patterns of skew where females allocate paternity in order to maximize the amount of care their offspring receive. The models make contrasting predictions about the nature of male-female conflict over reproduction and also about the relationships between skew and relatedness, ecological constraints, the relative quality of the subordinate male, and the relative cost of care for the two males. These divergent predictions provide a schema by which the evolutionary causes of variation in skew among males can be evaluated. Abstract
Cant MA, Otali E, Mwanguhya F
(2002). Fighting and mating between groups in a cooperatively breeding mammal, the banded mongoose. Ethology
Fighting and mating between groups in a cooperatively breeding mammal, the banded mongoose
Many cooperatively breeding animals actively defend a territory containing resources such as food and shelter, which are essential for reproduction. Some observations, however, indicate that conflicts between groups are often triggered by the attempts of males or females, or both, to gain extra-group copulations. We studied interactions between 12 groups of banded mongooses (Mungos mungo) in Uganda to test whether the frequency of inter-group encounters was linked to the reproductive status of females, and conducted an experiment to examine the responses of individuals to mongooses from other groups. The rate at which focal groups fought with other groups was higher when its females were in estrous, suggesting that many fights take place over access to mates. Both males and estrous females were instrumental in instigating encounters with rival groups, and extra-group copulation in the midst of a fight was observed on three occasions. We experimentally simulated encounters with foreign individuals by presenting each of six groups with cages containing a male and a female from a rival group. Subordinate males were the first to investigate these 'intruders', spent more time around the intruders' cages, and were more aggressive to the intruders than either dominant males or females. Subordinate males directed more attention and aggression towards the male intruder than the female intruder. We suggest that male banded mongooses actively seek extra-group copulations in pursuit of paternity, while females may actively seek extra-group copulations as a way of reducing inbreeding depression. Abstract
Cant MA, Otali E, Mwanguhya F
(2001). Eviction and dispersal in co-operatively breeding banded mongooses (Mungos mungo). Journal of Zoology
Eviction and dispersal in co-operatively breeding banded mongooses (Mungos mungo)
The mode by which individuals disperse, and the cost of dispersal, are of great importance in attempts to understand variation in reproductive skew in animal societies. In this paper we report detailed information on dispersal and pack formation in banded mongooses Mungos mungo. Six pack fission events were recorded among 11 packs over 22 months. Pack fission occurred under two distinct circumstances. First, groups of individuals were evicted from their natal group as a result of intense aggression from other group members. A small fraction of group members was responsible for most of the aggression. Both sexes helped to attack and evict individuals from the group, and both males and females were driven out of their natal groups en masse. The second mode of pack fission occurred when groups of same-sex individuals left their natal group voluntarily to join dispersing individuals of the opposite sex, thereby forming new packs. Dispersing groups were more frequently involved in fights with rival packs of mongooses compared to established groups, and in one instance these fights seemed to be responsible for severe injury and increased mortality among members of a dispersing group. The observations of eviction provide one line of evidence that the presence of subordinates is sometimes detrimental to dominants, contrary to the assumptions of concession models of reproductive skew. Abstract
Cant MA, Field J
(2001). Helping effort and future fitness in cooperative animal societies. Proceedings of the Royal Society B: Biological Sciences
Helping effort and future fitness in cooperative animal societies
Little attention has been paid to a conspicuous and universal feature of animal societies: the variation between individuals in helping effort. Here, we develop a multiplayer kin-selection model that assumes that subordinates face a trade-off because current investment in help reduces their own future reproductive success. The model makes two predictions: (i) subordinates will work less hard the closer they are to inheriting breeding status; and (ii) for a given dominance rank, subordinates will work less hard in larger groups. The second prediction reflects the larger pay-off from inheriting a larger group. Both predictions were tested through a field experiment on the paper wasp Polistes dominulus. First, we measured an index of helping effort among subordinates, then we removed successive dominants to reveal the inheritance ranks of the subordinates: their positions in the queue to inherit dominance. We found that both inheritance rank and group size had significant effects on helping effort, in the manner predicted by our model. The close match between our theoretical and empirical results suggests that individuals adjust their helping effort according to their expected future reproductive success. This relationship has probably remained hidden in previous studies that have focused on variation in genetic relatedness. Abstract
Cant, Johnstone (2000). Power Struggles, Dominance Testing, and Reproductive Skew. The American Naturalist, 155(3), 406-406.
Cant MA, Johnstone RA
(2000). Power Struggles, Dominance Testing, and Reproductive Skew. Am Nat
Power Struggles, Dominance Testing, and Reproductive Skew.
Models of reproductive skew are concerned with the partitioning of reproduction between dominant and subordinate members of a group. In an interesting extension of these models, Reeve and Ratnieks briefly considered whether it might benefit subordinates to engage in aggressive behavior to test the fighting ability of a dominant. Their analysis suggested that such testing should be more probable in groups that feature high skew and, hence, perhaps among closer relatives (because high relatedness favors high skew). Here we explore in more detail the possibility of dominance testing. Three models that differ in the outcome of fights over dominance are presented: in the first model, the loser of the challenge is killed; in the second model, the loser is evicted from the nest; and, in the third model, the loser becomes (or remains) subordinate. In each case we consider the independent effects of the parameters that determine skew (namely, relatedness, group productivity, and ecological constraints) on the predicted level of dominance testing. We then construct an amalgamated model to examine situations where fights may lead to any one of the three outcomes. Our analysis reveals that, in the majority of cases, higher relatedness will in fact lead to lower levels of aggression. Moreover, dominance testing need not be associated with high skew. Rather, the relationship between skew and dominance testing will depend on which factor (relatedness, group productivity, or level of ecological constraints) is principally responsible for variation in the distribution of reproduction. Abstract
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(2000). Social control of reproduction in banded mongooses. Anim Behav
Social control of reproduction in banded mongooses.
Recent theoretical work suggests that the distribution of reproduction, or degree of reproductive skew, in animal societies depends crucially on (1) whether dominant individuals can fully control subordinate reproduction, and (2) how subordinate reproduction affects the fitness of dominants. I investigated these two factors in cooperatively breeding banded mongooses, Mungos mungo. Female packmates entered oestrus together and were closely guarded by dominant males. These males were aggressive to subordinate males who attempted to mate, but females still managed to mate with males other than their mate guard. Older females were guarded and mated a few days before their younger packmates, yet all females usually gave birth on the same day, suggesting that older females may have a longer gestation period. Moreover, older females carried more fetuses. Overall, ca. 83% of adult females conceived in each breeding attempt and 71% carried to term. These results indicate that, among males, dominant individuals did not have full control over the mating attempts of subordinates (since they could not fully control the mating behaviour of the females they guarded), while among females there was little or no attempt to prevent subordinates from breeding (at least, prior to parturition). Two within-group infanticides by males suggested that some control over reproduction may be exercised postpartum. Per capita survivorship of young in the den increased with the number of females who gave birth. Thus, dominant females may benefit from subordinate reproduction, providing a possible explanation for the lack of reproductive suppression among females in this species. Copyright 2000 the Association for the Study of Animal Behaviour. Abstract
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Cant MA, Johnstone RA
(1999). Costly young and reproductive skew in animal societies. Behavioral Ecology
Costly young and reproductive skew in animal societies
Many recent models of reproductive skew explain subordinate reproduction as a staying incentive offered by dominants, who can produce more young with a helper present than without. Here, we present a new, alternative explanation for subordinate reproduction, which applies whenever the fitness cost to a parent of producing young is an accelerating function of the number produced (as commonly assumed in optimal clutch size theory). Under these circumstances, a dominant individual may be selected to offer a share of reproduction to a related subordinate, not as an incentive to stay, but because additional offspring that would be expensive for the dominant to produce are cheap for the subordinate. 'Beneficial sharing' of this kind is more likely the more closely related the subordinate is to the dominant, so that the model predicts a negative relationship between skew and relatedness. This result runs directly counter to the positive relationship predicted by previous incentive-based models. We explore the interaction of these contrasting effects by developing an integrated model that allows for both beneficial sharing and staying incentives. When offspring are cheap to produce, this integrated model predicts that the incentive effect will dominate, and skew will increase with relatedness. When young are costly, in contrast, beneficial sharing will be of greater importance, and skew will decrease with relatedness. Abstract
Johnstone RA, Cant MA
(1999). Reproductive skew and indiscriminate infanticide. Anim Behav
Reproductive skew and indiscriminate infanticide.
In communally breeding animals, there is an evolutionary conflict over the partitioning of reproduction within the group. If dominant group members do not have complete control over subordinate reproduction, this conflict may favour the evolution of infanticidal behaviour (by either subordinates or dominants or both). Elimination of offspring, however, is likely to be constrained by the difficulty of discriminating between an individual's own progeny and those of cobreeders. Here, we develop an evolutionarily stable strategy (ESS) model of reproductive partitioning, which demonstrates that killing of young can be favoured, even if such discrimination is not possible. The model predicts that infanticide will typically be associated with elevated levels of offspring production, and is most likely to prove evolutionarily stable when the coefficient of relatedness between cobreeders is low, and offspring are cheap to produce. The effect of infanticide is to release subordinates from the reproductive restraint they would otherwise be forced to exercise, leading to reduced reproductive skew. When infanticide is possible, addition of numerous young to the joint brood will not lower overall productivity, because progeny in excess of the most productive brood size are eliminated. Subordinates are thus free to contribute more young to the brood than would otherwise be the case. In addition, we show that the possibility of infanticide may influence the pattern of reproduction within a group even if no offspring are actually killed at equilibrium. Copyright 1999 the Association for the Study of Animal Behaviour. Abstract
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Johnstone RA, Cant MA
(1999). Reproductive skew and the threat of eviction: a new perspective. Proceedings of the Royal Society B: Biological Sciences
Reproductive skew and the threat of eviction: a new perspective
Most recent models of the partitioning of reproduction attempt to explain patterns of skew on the assumption that dominant individuals have complete control over breeding opportunities within the group, but may nevertheless concede a share of direct reproduction to subordinates as an incentive to remain peacefully in the association. Although these models may be applicable to some animal societies, we argue that they fail to provide a comprehensive theory of skew. Instead, we suggest that subordinates may often be able to claim unsanctioned reproduction for themselves, but will be forced to excercise a degree of reproductive restraint lest they incite ejection by the dominant. Reproductive skew, in other words, may reflect the threat of ejection (inducing subordinate restraint) rather that the threat of subordinate departure (inducing reproductive concessions by dominants). We present a simple evolutionarily stable strategy model of reproductive skew under these circumstances, which demonstrates that a shift in emphasis from reproductive concession by dominants to reproductive restraint on the part of subordinates, radically alters the predictions of skew models. High group productivity, high relatedness and (when group members are related) strong ecological constraints are all expected to lead to reduced skew (the opposite conclusions to those of previous, concession-based analyses). The reason is that these factors reduce the benefits (or increase the costs) of ejection to the dominant, who therefore does best to tolerate more subordinate reproduction. Abstract
Johnstone RA, Woodroffe R, Cant MA, Wright J
(1999). Reproductive skew in multimember groups. American Naturalist
Reproductive skew in multimember groups
Cooperative societies vary in the extent to which reproduction is skewed toward one or a few socially dominant animals. Many recent models attempt to explain this variation on the basis that a dominant who benefits from the presence of subordinates may offer them incentives, in the form of reproductive opportunities, to remain in the group. While most societies contain multiple members, however, these models have considered only the relationship between a dominant and a single subordinate or have assumed that all subordinates are identical. We develop an incentive-based evolutionary stable strategy model of reproductive skew in three-member groups, in which subordinates may vary in their opportunities for independent reproduction, their contribution to group productivity, and in their relatedness both to the dominant and to one another. Our model demonstrates that the conclusions of two-member models cannot all be generalized to larger groups. For example, relatedness among group members can influence whether or not the dominant does best to offer staying incentives to subordinates in a three-member, but not a two-member, group. Both the degree of skew and group stability depend on the relatedness between subordinates as well as on the relatedness of each to the dominant, and the incentives that each individual subordinate receives are influenced by the traits of the other. Whether such effects increase or decrease skew and group stability depends crucially on whether a third group member increases group productivity to a greater or lesser extent than the first. Abstract
(1998). A model for the evolution of reproductive skew without reproductive suppression. Animal Behaviour
A model for the evolution of reproductive skew without reproductive suppression
Reproductive skew is a measure of the way breeding is distributed among the members of an animal society or group. Up to now, explanations of patterns of skew have been limited to one particular model, which assumes that a single dominant has full control over the distribution of subordinate reproduction. If this control is incomplete or absent, however, unsanctioned breeding by subordinate females will increase the total number of young produced. Here I present a new model for the evolution of skew that considers the effect of brood size on the inclusive fitness of dominants and subordinates. By augmenting brood size, a subordinate female reduces the per capita fitness of a dominant's offspring, so the net benefits of producing young are lower for related subordinates. I consider the stable level of skew when both dominant and subordinate attempt to maximize their inclusive fitness under two conditions: (1) when the dominant is unable to anticipate that a subordinate will add to her brood; and (2) the dominant does anticipate subordinate reproduction and can respond by adjusting her own brood size. In the first case, the model predicts that reproductive skew will increase with relatedness between breeders, because related subordinates are selected to add fewer young to the dominant's brood. In the second case, the dominant's optimal response to the presence of a second breeder exaggerates the relationship between relatedness and skew: dominants should produce more young when breeding with related compared with unrelated subordinates. Abstract
McLachlan A, Cant M (1995). Small males are more symmetrical: mating success in the midge Chironomus plumosus (Diptera:Chrinomidae). Animal Behaviour, 50, 748-755.
McLachlan A, Cant M (1995). Small males are more symmetrical: mating success in the midge Chironomus plumosus L. (Diptera: Chironomidae). Animal Behaviour, 50(3), 841-846.