The Evolution of Cooperation: Interacting Phenotypes among Social Partners.

Models of cooperation among nonkin suggest that social assortment is important for the evolution of cooperation. Theory predicts that interacting phenotypes, whereby an individual's behavior depends on the behavior of its social partners, can drive such social assortment. We measured repeated indirect genetic effects (IGEs) during cooperative predator inspection in eight populations of Trinidadian guppies (Poecilia reticulata) that vary in their evolutionary history of predation. Four broad patterns emerged that were dependent on river, predation history, and sex: (i) current partner behavior had the largest effect on focal behavior, with fish from low-predation habitats responding more to their social partners than fish from high-predation habitats; (ii) different focal/partner behavior combinations can generate cooperation; (iii) some high-predation fish exhibited carryover effects across social partners; and (iv) high-predation fish were more risk averse. These results provide the first large-scale comparison of interacting phenotypes during cooperation across wild animal populations, highlighting the potential importance of IGEs in maintaining cooperation. Intriguingly, while focal fish responded strongly to current social partners, carryover effects between social partners suggest generalized reciprocity (in which one helps anyone if helped by someone) may contribute to the evolution of cooperation in some, but not all, populations of guppies.

The influence of maternal effects on indirect benefits associated with polyandry.

Despite numerous and diverse theoretical models for the indirect benefits of polyandry, empirical support is mixed. One reason for the difficulty in detecting indirect benefits of polyandry may be that these are subtle and are mediated by environmental effects, such as maternal effects. Maternal effects may be especially important if females allocate resources to their offspring depending on the characteristics of their mating partners. We test this hypothesis in the burying beetle Nicrophorus vespilloides, a species that provides extensive and direct parental care to offspring. We used a fully factorial design and mated females to one, two, three, four or five different males and manipulated conditions so that their offspring received reduced (12 h) or full (ca 72 h) maternal care. We found that average offspring fitness increased with full maternal care but there was no significant effect of polyandry or the interaction between the duration of maternal care and the level of polyandry on offspring fitness. Thus, although polyandry could provide a mechanism for biasing paternity towards high quality or compatible males, and variation in parental care matters, we found no evidence that female N. vespilloides gain indirect benefits by using parental care to bias the allocation of resources under different mating conditions.

Evolution of non-kin cooperation: social assortment by cooperative phenotype in guppies.

Cooperation among non-kin constitutes a conundrum for evolutionary biology. Theory suggests that non-kin cooperation can evolve if individuals differ consistently in their cooperative phenotypes and assort socially by these, such that cooperative individuals interact predominantly with one another. However, our knowledge of the role of cooperative phenotypes in the social structuring of real-world animal populations is minimal. In this study, we investigated cooperative phenotypes and their link to social structure in wild Trinidadian guppies (Poecilia reticulata). We first investigated whether wild guppies are repeatable in their individual levels of cooperativeness (i.e. have cooperative phenotypes) and found evidence for this in seven out of eight populations, a result which was mostly driven by females. We then examined the social network structure of one of these populations where the expected fitness impact of cooperative contexts is relatively high, and found assortment by cooperativeness, but not by genetic relatedness. By contrast, and in accordance with our expectations, we did not find assortment by cooperativeness in a population where the expected fitness impact of cooperative contexts is lower. Our results provide empirical support for current theory and suggest that assortment by cooperativeness is important for the evolution and persistence of non-kin cooperation in real-world populations.

Indirect genetic effects influence antipredator behavior in guppies: estimates of the coefficient of interaction psi and the inheritance of reciprocity.

How and why cooperation evolves, particularly among nonrelatives, remains a major paradox for evolutionary biologists and behavioral ecologists. Although much attention has focused on fitness consequences associated with cooperating, relatively little is known about the second component of evolutionary change, the inheritance of cooperation or reciprocity. The genetics of behaviors that can only be expressed in the context of interactions are particularly difficult to describe because the relevant genes reside in multiple social partners. Indirect genetic effects (IGEs) describe the influence of genes carried in social partners on the phenotype of a focal individual and thus provide a novel approach to quantifying the genetics underlying interactions such as reciprocal cooperation. We used inbred lines of guppies and a novel application of IGE theory to describe the dual genetic control of predator inspection and social behavior, both classic models of reciprocity. We identified effects of focal strain, social group strain, and interactions between focal and group strains on variation in focal behavior. We measured psi, the coefficient of the interaction, which describes the degree to which an individual's phenotype is influenced by the phenotype of its social partners. The genetic identity of social partners substantially influences inspection behavior, measures of threat assessment, and schooling and does so in positively reinforcing manner. We therefore demonstrate strong IGEs for antipredator behavior that represent the genetic variation necessary for the evolution of reciprocity.

Are designer guppies inbred? Microsatellite variation in five strains of ornamental guppies, Poecilia reticulata, used for behavioral research.

Inbred lines are an important tool of genetic studies of all traits, including behavior. Independently derived strains of ornamental "designer" guppies are readily available and predicted to be inbred; however, little is known about actual levels of inbreeding in any of these strains or whether these lines differ in genetic traits that have not been under strong directional artificial selection. We genotyped five designer strains of guppies known to vary in their responses to predator cues and a wild reference population to determine whether designer strains show evidence of inbreeding and whether the strains differed from each other at five microsatellite loci. The designer strains exhibited lower allelic diversity and observed heterozygosity than the wild population. Observed heterozygosity departed significantly from expected heterozygosity for most markers in all five strains of designer guppies. Inbreeding coefficient (f) comparisons between the wild reference population and the designer strains show considerable inbreeding in the designer strains. F(is) values for the designer strains also provide evidence of inbreeding. Finally, F(st) values indicate that the designer strains differ significantly from each other and the wild population. We therefore concluded that designer guppies are inbred compared to wild populations and differ among strains, making them useful tools for genetic studies of behavioral or life history traits.

Variation in anti-predator behavior among five strains of inbred guppies, Poecilia reticulata.

Quantitative genetic studies frequently utilize inbred strains of animals as tools for partitioning the direct and indirect effects of genes from environmental effects in generating an observed phenotype, however, this approach is rarely applied to behavioral studies. Guppies, Poecilia reticulata, perform a set of anti-predator behaviors that may provide an ideal system to study how complex behavioral traits are generated. To assess the utility of ornamental guppies in quantitative genetics studies of behavior, we assayed five morphologically distinct strains of ornamental guppies for response to predator cues and for variation in response among strains. Despite individual variation, all five strains responded to predator cues and differences among strains were found for all assayed behaviors, including measures of boldness and predator avoidance.