Publications by category
Journal articles
Francis RK, Catalano KA, Majoris JE, Rueger T, D’Aloia CC, Bogdanowicz S, Buston PM (2022). Characteristics of breeding habitat, genetic mating system, and determinants of male mating success in the sponge-dwelling goby Elacatinus lori.
Behavioral Ecology and Sociobiology,
76(12).
Abstract:
Characteristics of breeding habitat, genetic mating system, and determinants of male mating success in the sponge-dwelling goby Elacatinus lori
Abstract: Determining the patterns and causes of variation in reproductive success is key to understanding mating systems and sexual selection, but they are challenging to study in cryptobenthic coral reef fishes. Here, we investigate characteristics of breeding habitat, the genetic mating system, and correlates of male mating success in the neon goby Elacatinus lori. This fish is primarily found living and breeding within the yellow tube sponge Aplysina fistularis in Belize — it has become a focus of marine population ecology research, but knowledge of its behavioral ecology is lacking. First, we show that sponges occupied by breeding males tend to be larger than those occupied by residents. Second, we show that E. lori males exhibit a polygynous mating system: some males breed with multiple females simultaneously and/or sequentially. Third, we show that male size is positively related to multiple metrics of male mating success: number of days paired with females, number of clutches laid, and total reproductive output. Male size, however, explains only a small proportion of the variation in male mating success, suggesting that other aspects of the males’ phenotype and ecological context need to be quantified to better explain variation in mating success. More generally, our results suggest that when female movements are restricted, it is necessary to measure habitat characteristics and male traits at smaller spatial scales to gain a deeper understanding of their effects on mating systems and sexual selection. Significance statement: Measuring male reproductive success in a wild population is notoriously difficult, particularly in cryptobenthic coral reef fishes. Often, mating success is used as a proxy for reproductive success because it is easier to measure. Variation in mating success is often predicted by characteristics of the individual and its breeding habitat. Here, we simultaneously describe the (i) breeding habitat, (ii) genetic mating system, and (iii) relationship between male traits, habitat characteristics, and mating success in the neon goby Elacatinus lori. By investigating these three elements together, we provide solid foundations for understanding this species’ mating system. More generally, we suggest that investigations of variation in mating success may be improved by approaching analyses at smaller, more biologically relevant, spatial scales. Our findings highlight the challenges and opportunities of investigating mating systems of cryptobenthic coral reef fishes in the wild.
Abstract.
Rueger T, Heatwole SJ, Wong MYL (2022). Social rank and species-specific differences influence cooperation and conflict in anemonefish societies. Animal Behaviour, 187, 105-116.
Rueger T, Buston PM, Bogdanowicz SM, Wong MY (2021). Genetic relatedness in social groups of the emerald coral goby Paragobiodon xanthosoma creates potential for weak kin selection.
Mol Ecol,
30(5), 1311-1321.
Abstract:
Genetic relatedness in social groups of the emerald coral goby Paragobiodon xanthosoma creates potential for weak kin selection.
Animals forming social groups that include breeders and nonbreeders present evolutionary paradoxes; why do breeders tolerate nonbreeders? and why do nonbreeders tolerate their situation? Both paradoxes are often explained with kin selection. Kin selection is, however, assumed to play little or no role in social group formation of marine organisms with dispersive larval phases. Yet, in some marine organisms, recent evidence suggests small-scale patterns of relatedness, meaning that this assumption must always be tested. Here, we investigated the genetic relatedness of social groups of the emerald coral goby, Paragobiodon xanthosoma. We genotyped 73 individuals from 16 groups in Kimbe Bay, Papua New Guinea, at 20 microsatellite loci and estimated pairwise relatedness among all individuals. We found that estimated pairwise relatedness among individuals within groups was significantly higher than the pairwise relatedness among individuals from the same reef, and pairwise relatedness among individuals from the same reef was significantly higher than the pairwise relatedness among individuals from different reefs. This spatial signature suggests that there may be very limited dispersal in this species. The slightly positive relatedness within groups creates the potential for weak kin selection, which may help to resolve the paradox of why breeders tolerate subordinates in P. xanthosoma. The other paradox, why nonbreeders tolerate their situation, is better explained by alternative hypotheses such as territory inheritance, and ecological and social constraints. We show that even in marine animals with dispersive larval phases, kin selection needs to be considered to explain the evolution of complex social groups.
Abstract.
Author URL.
Rueger T, Branconi R, Froehlich CYM, Heatwole SJ, Wong MYL, Buston PM (2021). The Next Frontier in Understanding the Evolution of Coral Reef Fish Societies.
Frontiers in Marine Science,
8Abstract:
The Next Frontier in Understanding the Evolution of Coral Reef Fish Societies
Research on sociality in marine fishes is a vibrant field that is providing new insights into social evolution more generally. Here, we review the past two decades of research, identifying knowledge gaps and new directions. Two coral reef fishes, with social systems similar to other cooperative breeders, have emerged as models: the clown anemonefish Amphiprion percula and the emerald goby Paragobiodon xanthosoma. In these systems, non-breeders do not forgo their own reproduction to gain indirect genetic benefits. Rather, they do so because they stand to inherit the territory in the future and there are strong ecological and social constraints. The reasons why breeders tolerate non-breeders remain obscure, though it is plausibly a combination of weak kin selection, bet-hedging, and benefits mediated via mutualistic interactions with cnidarian hosts. The latter is particularly interesting, given the parallels with other social animals with mutualistic partners, such as acacia ants. Looking beyond the two model species, our attention is turning to species with more complex social organization, such as the damselfish Dascyllus aruanus. Here, variable group stability, conflict intensity, and reproductive skew provide opportunities to test theories of social evolution that have only been tested in a few taxa. New methods like social network analysis are enabling us to uncover more subtle effects of ecology on social interactions. More recently, comparative methods have yielded insights into the correlates of interspecific variation in sociality in the genera to which our model species belong. Phylogenetically controlled contrasts within the genus Gobiodon, have revealed the role of ecology, life history traits, and their interaction in sociality: smaller bodied species are more social than larger bodied species, which are only social on large corals. As climate change affects coral reefs, there is a pressing need to understand the many ways in which environmental disturbance influences these unique social systems. In sum, coral reef fishes have enabled us to test the robustness of current theories of social evolution in new taxa and environments, and they have generated new insights into social evolution that are applicable to a wider variety of taxa.
Abstract.
Rueger T, Harrison HB, Buston PM, Gardiner NM, Berumen ML, Jones GP (2020). Natal philopatry increases relatedness within groups of coral reef cardinalfish.
Proceedings of the Royal Society B: Biological Sciences,
287(1930).
Abstract:
Natal philopatry increases relatedness within groups of coral reef cardinalfish
A central issue in evolutionary ecology is how patterns of dispersal influence patterns of relatedness in populations. In terrestrial organisms, limited dispersal of offspring leads to groups of related individuals. By contrast, for most marine organisms, larval dispersal in open waters is thought to minimize kin associations within populations. However, recent molecular evidence and theoretical approaches have shown that limited dispersal, sibling cohesion and/or differential reproductive success can lead to kin association and elevated relatedness. Here, we tested the hypothesis that limited dispersal explains small-scale patterns of relatedness in the pajama cardinalfish Sphaeramia nematoptera. We used 19 microsatellite markers to assess parentage of 233 juveniles and pairwise relatedness among 527 individuals from 41 groups in Kimbe Bay, Papua New Guinea. Our findings support three predictions of the limited dispersal hypothesis: (i) elevated relatedness within groups, compared with among groups and elevated relatedness within reefs compared with among reefs; (ii) a weak negative correlation of relatedness with distance; (iii) more juveniles than would be expected by chance in the same group and the same reef as their parents. We provide the first example for natal philopatry at the group level causing small-scale patterns of genetic relatedness in a marine fish.
Abstract.
Barbasch TA, Rueger T, Srinivasan M, Wong MYL, Jones GP, Buston PM (2020). Substantial plasticity of reproduction and parental care in response to local resource availability in a wild clownfish population.
Oikos,
129(12), 1844-1855.
Abstract:
Substantial plasticity of reproduction and parental care in response to local resource availability in a wild clownfish population
Plasticity, the capacity of individuals to respond to changing environments by modifying traits, may be critically important for population persistence by allowing for adaptive responses on shorter timescales than genetic change. Here, we use the clown anemonefish Amphiprion percula, whose access to resources is constrained by their anemones, to test the role of plasticity in generating variation in reproductive success among groups. We surveyed a wild clownfish population and found positive correlations between anemone area, fish size, reproduction and parental care. We used structural equation modeling to test the hypothesis that these correlations emanate from variation in anemone area and found support for a pathway linking anemone area to female investment, female investment to male investment and male investment to embryo survival. Next, we experimentally tested whether plasticity in response to resource availability can result in variation in parental traits using a feeding manipulation and found substantial plasticity in reproduction and parental care in response to changes in the availability of food resources. The results of this study reveal the role of plasticity in response to local resource availability in generating variation among individuals in reproductive strategies, linking studies of behavior and demography in this model species, and ultimately contributing to our ability to predict how populations might cope with environmental changes.
Abstract.
Rueger T, Harrison HB, Gardiner NM, Berumen ML, Jones GP (2019). Extra‐pair mating in a socially monogamous and paternal mouth‐brooding cardinalfish. Molecular Ecology, 28(10), 2625-2635.
Giffin AL, Rueger T, Jones GP (2019). Ontogenetic shifts in microhabitat use and coral selectivity in three coral reef fishes. Environmental Biology of Fishes, 102(1), 55-67.
Rueger T, Barbasch TA, Wong MYL, Srinivasan M, Jones GP, Buston PM (2018). Reproductive control via the threat of eviction in the clown anemonefish.
Proceedings of the Royal Society B: Biological Sciences,
285(1891), 20181295-20181295.
Abstract:
Reproductive control via the threat of eviction in the clown anemonefish
. In social groups, high reproductive skew is predicted to arise when the reproductive output of a group is limited, and dominant individuals can suppress subordinate reproductive efforts. Reproductive suppression is often assumed to occur via overt aggression or the threat of eviction. It is unclear, however, whether the threat of eviction alone is sufficient to induce reproductive restraint by subordinates. Here, we test two assumptions of the restraint model of reproductive skew by investigating whether resource limitation generates reproductive competition and whether the threat of eviction leads to reproductive restraint in the clown anemonefish
. Amphiprion percula
. First, we use a feeding experiment to test whether reproduction is resource limited, which would create an incentive for the dominant pair to suppress subordinate reproduction. We show that the number of eggs laid increased in the population over the study period, but the per cent increase in fed groups was more than twice that in unfed groups (205% and 78%, respectively). Second, we use an eviction experiment to test whether the dominant pair evicts mature subordinates, which would create an incentive for the subordinates to forgo reproduction. We show that mature subordinates are seven times more likely to be evicted than immature subordinates of the same size. In summary, we provide experimental support for the assumptions of the restraint model by showing that resource limitation creates reproductive competition and a credible threat of eviction helps explain why subordinates forego reproduction. Transactional models of reproductive skew may apply well to this and other simple systems.
.
Abstract.
Rueger T, Gardiner NM, Jones GP (2017). Site fidelity facilitates pair formation in aggregations of coral reef cardinalfish. Oecologia, 186(2), 425-434.
Rueger T, Gardiner NM, Jones GP (2016). Homing is not for everyone: displaced cardinalfish find a new place to live. Journal of Fish Biology, 89(4), 2182-2188.
Rueger T, Gardiner NM, Jones GP (2016). Size matters: male and female mate choice leads to size-assortative pairing in a coral reef cardinalfish. Behavioral Ecology, arw082-arw082.
Rueger T, Harrison HB, Jones GP, Mansour H, Berumen ML (2015). Resolving genealogical relationships in the Pyjama cardinalfish, Sphaeramia nematoptera (Apogonidae) with 23 novel microsatellite markers. Conservation Genetics Resources, 7(3), 623-626.
Rueger T, Gardiner NM, Jones GP (2014). Relationships between pair formation, site fidelity and sex in a coral reef cardinalfish. Behavioural Processes, 107, 119-126.
Rüger T, Sommer U (2012). Warming does not always benefit the small – Results from a plankton experiment. Aquatic Botany, 97(1), 64-68.
Publications by year
2022
Francis RK, Catalano KA, Majoris JE, Rueger T, D’Aloia CC, Bogdanowicz S, Buston PM (2022). Characteristics of breeding habitat, genetic mating system, and determinants of male mating success in the sponge-dwelling goby Elacatinus lori.
Behavioral Ecology and Sociobiology,
76(12).
Abstract:
Characteristics of breeding habitat, genetic mating system, and determinants of male mating success in the sponge-dwelling goby Elacatinus lori
Abstract: Determining the patterns and causes of variation in reproductive success is key to understanding mating systems and sexual selection, but they are challenging to study in cryptobenthic coral reef fishes. Here, we investigate characteristics of breeding habitat, the genetic mating system, and correlates of male mating success in the neon goby Elacatinus lori. This fish is primarily found living and breeding within the yellow tube sponge Aplysina fistularis in Belize — it has become a focus of marine population ecology research, but knowledge of its behavioral ecology is lacking. First, we show that sponges occupied by breeding males tend to be larger than those occupied by residents. Second, we show that E. lori males exhibit a polygynous mating system: some males breed with multiple females simultaneously and/or sequentially. Third, we show that male size is positively related to multiple metrics of male mating success: number of days paired with females, number of clutches laid, and total reproductive output. Male size, however, explains only a small proportion of the variation in male mating success, suggesting that other aspects of the males’ phenotype and ecological context need to be quantified to better explain variation in mating success. More generally, our results suggest that when female movements are restricted, it is necessary to measure habitat characteristics and male traits at smaller spatial scales to gain a deeper understanding of their effects on mating systems and sexual selection. Significance statement: Measuring male reproductive success in a wild population is notoriously difficult, particularly in cryptobenthic coral reef fishes. Often, mating success is used as a proxy for reproductive success because it is easier to measure. Variation in mating success is often predicted by characteristics of the individual and its breeding habitat. Here, we simultaneously describe the (i) breeding habitat, (ii) genetic mating system, and (iii) relationship between male traits, habitat characteristics, and mating success in the neon goby Elacatinus lori. By investigating these three elements together, we provide solid foundations for understanding this species’ mating system. More generally, we suggest that investigations of variation in mating success may be improved by approaching analyses at smaller, more biologically relevant, spatial scales. Our findings highlight the challenges and opportunities of investigating mating systems of cryptobenthic coral reef fishes in the wild.
Abstract.
Rueger T, Heatwole SJ, Wong MYL (2022). Social rank and species-specific differences influence cooperation and conflict in anemonefish societies. Animal Behaviour, 187, 105-116.
2021
Rueger T, Buston PM, Bogdanowicz SM, Wong MY (2021). Genetic relatedness in social groups of the emerald coral goby Paragobiodon xanthosoma creates potential for weak kin selection.
Mol Ecol,
30(5), 1311-1321.
Abstract:
Genetic relatedness in social groups of the emerald coral goby Paragobiodon xanthosoma creates potential for weak kin selection.
Animals forming social groups that include breeders and nonbreeders present evolutionary paradoxes; why do breeders tolerate nonbreeders? and why do nonbreeders tolerate their situation? Both paradoxes are often explained with kin selection. Kin selection is, however, assumed to play little or no role in social group formation of marine organisms with dispersive larval phases. Yet, in some marine organisms, recent evidence suggests small-scale patterns of relatedness, meaning that this assumption must always be tested. Here, we investigated the genetic relatedness of social groups of the emerald coral goby, Paragobiodon xanthosoma. We genotyped 73 individuals from 16 groups in Kimbe Bay, Papua New Guinea, at 20 microsatellite loci and estimated pairwise relatedness among all individuals. We found that estimated pairwise relatedness among individuals within groups was significantly higher than the pairwise relatedness among individuals from the same reef, and pairwise relatedness among individuals from the same reef was significantly higher than the pairwise relatedness among individuals from different reefs. This spatial signature suggests that there may be very limited dispersal in this species. The slightly positive relatedness within groups creates the potential for weak kin selection, which may help to resolve the paradox of why breeders tolerate subordinates in P. xanthosoma. The other paradox, why nonbreeders tolerate their situation, is better explained by alternative hypotheses such as territory inheritance, and ecological and social constraints. We show that even in marine animals with dispersive larval phases, kin selection needs to be considered to explain the evolution of complex social groups.
Abstract.
Author URL.
Rueger T, Branconi R, Froehlich CYM, Heatwole SJ, Wong MYL, Buston PM (2021). The Next Frontier in Understanding the Evolution of Coral Reef Fish Societies.
Frontiers in Marine Science,
8Abstract:
The Next Frontier in Understanding the Evolution of Coral Reef Fish Societies
Research on sociality in marine fishes is a vibrant field that is providing new insights into social evolution more generally. Here, we review the past two decades of research, identifying knowledge gaps and new directions. Two coral reef fishes, with social systems similar to other cooperative breeders, have emerged as models: the clown anemonefish Amphiprion percula and the emerald goby Paragobiodon xanthosoma. In these systems, non-breeders do not forgo their own reproduction to gain indirect genetic benefits. Rather, they do so because they stand to inherit the territory in the future and there are strong ecological and social constraints. The reasons why breeders tolerate non-breeders remain obscure, though it is plausibly a combination of weak kin selection, bet-hedging, and benefits mediated via mutualistic interactions with cnidarian hosts. The latter is particularly interesting, given the parallels with other social animals with mutualistic partners, such as acacia ants. Looking beyond the two model species, our attention is turning to species with more complex social organization, such as the damselfish Dascyllus aruanus. Here, variable group stability, conflict intensity, and reproductive skew provide opportunities to test theories of social evolution that have only been tested in a few taxa. New methods like social network analysis are enabling us to uncover more subtle effects of ecology on social interactions. More recently, comparative methods have yielded insights into the correlates of interspecific variation in sociality in the genera to which our model species belong. Phylogenetically controlled contrasts within the genus Gobiodon, have revealed the role of ecology, life history traits, and their interaction in sociality: smaller bodied species are more social than larger bodied species, which are only social on large corals. As climate change affects coral reefs, there is a pressing need to understand the many ways in which environmental disturbance influences these unique social systems. In sum, coral reef fishes have enabled us to test the robustness of current theories of social evolution in new taxa and environments, and they have generated new insights into social evolution that are applicable to a wider variety of taxa.
Abstract.
2020
Rueger T, Harrison HB, Buston PM, Gardiner NM, Berumen ML, Jones GP (2020). Natal philopatry increases relatedness within groups of coral reef cardinalfish.
Proceedings of the Royal Society B: Biological Sciences,
287(1930).
Abstract:
Natal philopatry increases relatedness within groups of coral reef cardinalfish
A central issue in evolutionary ecology is how patterns of dispersal influence patterns of relatedness in populations. In terrestrial organisms, limited dispersal of offspring leads to groups of related individuals. By contrast, for most marine organisms, larval dispersal in open waters is thought to minimize kin associations within populations. However, recent molecular evidence and theoretical approaches have shown that limited dispersal, sibling cohesion and/or differential reproductive success can lead to kin association and elevated relatedness. Here, we tested the hypothesis that limited dispersal explains small-scale patterns of relatedness in the pajama cardinalfish Sphaeramia nematoptera. We used 19 microsatellite markers to assess parentage of 233 juveniles and pairwise relatedness among 527 individuals from 41 groups in Kimbe Bay, Papua New Guinea. Our findings support three predictions of the limited dispersal hypothesis: (i) elevated relatedness within groups, compared with among groups and elevated relatedness within reefs compared with among reefs; (ii) a weak negative correlation of relatedness with distance; (iii) more juveniles than would be expected by chance in the same group and the same reef as their parents. We provide the first example for natal philopatry at the group level causing small-scale patterns of genetic relatedness in a marine fish.
Abstract.
Barbasch TA, Rueger T, Srinivasan M, Wong MYL, Jones GP, Buston PM (2020). Substantial plasticity of reproduction and parental care in response to local resource availability in a wild clownfish population.
Oikos,
129(12), 1844-1855.
Abstract:
Substantial plasticity of reproduction and parental care in response to local resource availability in a wild clownfish population
Plasticity, the capacity of individuals to respond to changing environments by modifying traits, may be critically important for population persistence by allowing for adaptive responses on shorter timescales than genetic change. Here, we use the clown anemonefish Amphiprion percula, whose access to resources is constrained by their anemones, to test the role of plasticity in generating variation in reproductive success among groups. We surveyed a wild clownfish population and found positive correlations between anemone area, fish size, reproduction and parental care. We used structural equation modeling to test the hypothesis that these correlations emanate from variation in anemone area and found support for a pathway linking anemone area to female investment, female investment to male investment and male investment to embryo survival. Next, we experimentally tested whether plasticity in response to resource availability can result in variation in parental traits using a feeding manipulation and found substantial plasticity in reproduction and parental care in response to changes in the availability of food resources. The results of this study reveal the role of plasticity in response to local resource availability in generating variation among individuals in reproductive strategies, linking studies of behavior and demography in this model species, and ultimately contributing to our ability to predict how populations might cope with environmental changes.
Abstract.
2019
Rueger T, Harrison HB, Gardiner NM, Berumen ML, Jones GP (2019). Extra‐pair mating in a socially monogamous and paternal mouth‐brooding cardinalfish. Molecular Ecology, 28(10), 2625-2635.
Giffin AL, Rueger T, Jones GP (2019). Ontogenetic shifts in microhabitat use and coral selectivity in three coral reef fishes. Environmental Biology of Fishes, 102(1), 55-67.
2018
Rueger T, Barbasch TA, Wong MYL, Srinivasan M, Jones GP, Buston PM (2018). Reproductive control via the threat of eviction in the clown anemonefish.
Proceedings of the Royal Society B: Biological Sciences,
285(1891), 20181295-20181295.
Abstract:
Reproductive control via the threat of eviction in the clown anemonefish
. In social groups, high reproductive skew is predicted to arise when the reproductive output of a group is limited, and dominant individuals can suppress subordinate reproductive efforts. Reproductive suppression is often assumed to occur via overt aggression or the threat of eviction. It is unclear, however, whether the threat of eviction alone is sufficient to induce reproductive restraint by subordinates. Here, we test two assumptions of the restraint model of reproductive skew by investigating whether resource limitation generates reproductive competition and whether the threat of eviction leads to reproductive restraint in the clown anemonefish
. Amphiprion percula
. First, we use a feeding experiment to test whether reproduction is resource limited, which would create an incentive for the dominant pair to suppress subordinate reproduction. We show that the number of eggs laid increased in the population over the study period, but the per cent increase in fed groups was more than twice that in unfed groups (205% and 78%, respectively). Second, we use an eviction experiment to test whether the dominant pair evicts mature subordinates, which would create an incentive for the subordinates to forgo reproduction. We show that mature subordinates are seven times more likely to be evicted than immature subordinates of the same size. In summary, we provide experimental support for the assumptions of the restraint model by showing that resource limitation creates reproductive competition and a credible threat of eviction helps explain why subordinates forego reproduction. Transactional models of reproductive skew may apply well to this and other simple systems.
.
Abstract.
2017
Rueger T, Gardiner NM, Jones GP (2017). Site fidelity facilitates pair formation in aggregations of coral reef cardinalfish. Oecologia, 186(2), 425-434.
2016
Rueger T, Gardiner NM, Jones GP (2016). Homing is not for everyone: displaced cardinalfish find a new place to live. Journal of Fish Biology, 89(4), 2182-2188.
Rueger T, Gardiner NM, Jones GP (2016). Size matters: male and female mate choice leads to size-assortative pairing in a coral reef cardinalfish. Behavioral Ecology, arw082-arw082.
2015
Rueger T, Harrison HB, Jones GP, Mansour H, Berumen ML (2015). Resolving genealogical relationships in the Pyjama cardinalfish, Sphaeramia nematoptera (Apogonidae) with 23 novel microsatellite markers. Conservation Genetics Resources, 7(3), 623-626.
2014
Rueger T, Gardiner NM, Jones GP (2014). Relationships between pair formation, site fidelity and sex in a coral reef cardinalfish. Behavioural Processes, 107, 119-126.
2012
Rüger T, Sommer U (2012). Warming does not always benefit the small – Results from a plankton experiment. Aquatic Botany, 97(1), 64-68.