Social selection acts on behavior and body mass but does not contribute to the total selection differential in eastern chipmunks

Through social interactions, phenotypes of conspecifics can affect an individual's fitness, resulting in social selection. Social selection is assumed to represent a strong and dynamic evolutionary force that can act with or in opposition to natural selection. Few studies, however, have estimated social selection and its contribution to total selection in the wild. We estimated natural and social selection gradients on exploration, docility, and body mass, and their contribution to selection differentials, in a wild eastern chipmunk population (Tamias striatus). We applied trait-based multiple regression models derived from classical phenotypic selection analyses, which allowed us to include several social partners (i.e., neighbors). We detected social selection gradients on female docility and male body mass, indicating that female with docile neighbors and males with large neighbors had lower fitness. In both sexes, social selection gradients varied with the season. However, we found no phenotypic assortment or disassortment for the studied traits. Social selection gradients, therefore, did not contribute to total selection differentials, and natural selection alone could drive phenotypic changes. Evaluating the factors that drive the evolution of the covariance between interacting phenotypes is necessary to understand the role of social selection as an evolutionary force.     

Phenotypic assortment mediates the effect of social selection in a wild beetle population

Social interactions often have major fitness consequences, but little is known about how specific interacting phenotypes affect the strength of natural selection. Social influences on the evolutionary process can be assessed using a multilevel selection approach that partitions the effects of social partner phenotypes on fitness (referred to as social or group selection) from those of the traits of a focal individual (nonsocial or individual selection). To quantify the contribution of social selection to total selection affecting a trait, the patterns of phenotypic association among interactants must also be considered. We estimated selection gradients on male body size in a wild population of forked fungus beetles (Bolitotherus cornutus). We detected positive nonsocial selection and negative social selection on body size operating through differences in copulation success, indicating that large males with small social partners had highest fitness. In addition, we found that, in low-density demes, the phenotypes of focal individuals were negatively correlated with those of their social partners. This pattern reversed the negative effect of group selection on body size and led to stronger positive selection for body size. Our results demonstrate multilevel selection in nature and stress the importance of considering social selection whenever conspecific interactions occur nonrandomly.     

Social structure modulates the evolutionary consequences of social plasticity: A social network perspective on interacting phenotypes

Organisms express phenotypic plasticity during social interactions. Interacting phenotype theory has explored the consequences of social plasticity for evolution, but it is unclear how this theory applies to complex social structures. We adapt interacting phenotype models to general social structures to explore how the number of social connections between individuals and preference for phenotypically similar social partners affect phenotypic variation and evolution. We derive an analytical model that ignores phenotypic feedback and use simulations to test the predictions of this model. We find that adapting previous models to more general social structures does not alter their general conclusions but generates insights into the effect of social plasticity and social structure on the maintenance of phenotypic variation and evolution. Contribution of indirect genetic effects to phenotypic variance is highest when interactions occur at intermediate densities and decrease at higher densities, when individuals approach interacting with all group members, homogenizing the social environment across individuals. However, evolutionary response to selection tends to increase at greater network densities as the effects of an individual's genes are amplified through increasing effects on other group members. Preferential associations among similar individuals (homophily) increase both phenotypic variance within groups and evolutionary response to selection. Our results represent a first step in relating social network structure to the expression of social plasticity and evolutionary responses to selection.     

Characterizing selection in black‐throated blue warblers using a sexual network approach

Our understanding of trait evolution is built upon studies that examine the correlation between traits and fitness, most of which implicitly assume all individuals experience similar selective environments. However, accounting for differences in selective pressures, such as variation in the social environment, can advance our understanding of how selection shapes individual traits and subsequent fitness. In this study, we test whether variation in the social environment affects selection on individual phenotype. We apply a new sexual network framework to quantify each male's social environment as the mean body size of his primary competitors. We test for direct and social selection on male body size using a 10‐year data set on black‐throated blue warblers (Setophaga caerulescens), a territorial species for which body size is hypothesized to mediate competition for mates. We found that direct selection on body size was weak and nonsignificant, as was social selection via the body size of the males' competitors. Analysing both types of selection simultaneously allows us to firmly reject a role for body size in competitive interactions between males and subsequent male fitness in this population. We evaluate the application of the sexual network approach to empirical data and suggest that other phenotypic traits such as song characteristics and plumage may be more relevant than body size for male–male competition in this small passerine bird.     

Social traits,social networks and evolutionary biology

The social environment is both an important agent of selection for most organisms, and an emergent property of their interactions. As an aggregation of interactions among members of a population, the social environment is a product of many sets of relationships and so can be represented as a network or matrix. Social network analysis in animals has focused on why these networks possess the structure they do, and whether individuals’ network traits, representing some aspect of their social phenotype, relate to their fitness. Meanwhile, quantitative geneticists have demonstrated that traits expressed in a social context can depend on the phenotypes and genotypes of interacting partners, leading to influences of the social environment on the traits and fitness of individuals and the evolutionary trajectories of populations. Therefore, both fields are investigating similar topics, yet have arrived at these points relatively independently. We review how these approaches are diverged, and yet how they retain clear parallelism and so strong potential for complementarity. This demonstrates that, despite separate bodies of theory, advances in one might inform the other. Techniques in network analysis for quantifying social phenotypes, and for identifying community structure, should be useful for those studying the relationship between individual behaviour and group‐level phenotypes. Entering social association matrices into quantitative genetic models may also reduce bias in heritability estimates, and allow the estimation of the influence of social connectedness on trait expression. Current methods for measuring natural selection in a social context explicitly account for the fact that a trait is not necessarily the property of a single individual, something the network approaches have not yet considered when relating network metrics to individual fitness. Harnessing evolutionary models that consider traits affected by genes in other individuals (i.e. indirect genetic effects) provides the potential to understand how entire networks of social interactions in populations influence phenotypes and predict how these traits may evolve. By theoretical integration of social network analysis and quantitative genetics, we hope to identify areas of compatibility and incompatibility and to direct research efforts towards the most promising areas. Continuing this synthesis could provide important insights into the evolution of traits expressed in a social context and the evolutionary consequences of complex and nuanced social phenotypes.     

Reducing environmental bias when measuring natural selection

Abstract.— Crucial to understanding the process of natural selection is characterizing phenotypic selection. Measures of phenotypic selection can be biased by environmental variation among individuals that causes a spurious correlation between a trait and fitness. One solution is analyzing genotypic data, rather than phenotypic data. Genotypic data, however, are difficult to gather, can be gathered from few species, and typically have low statistical power. Environmental correlations may act through traits other than through fitness itself. A path analytic framework, which includes measures of such traits, may reduce environmental bias in estimates of selection coefficients. We tested the efficacy of path analysis to reduce bias by re-analyzing three experiments where both phenotypic and genotypic data were available. All three consisted of plant species (Impatiens capensis, Arabidopsis thaliana , and Raphanus sativus) grown in experimental plots or the greenhouse. We found that selection coefficients estimated by path analysis using phenotypic data were highly correlated with those based on genotypic data with little systematic bias in estimating the strength of selection. Although not a panacea, using path analysis can substantially reduce environmental biases in estimates of selection coefficients. Such confidence in phenotypic selection estimates is critical for progress in the study of natural selection.     

Predation risk as a driving force for phenotypic assortment: a cross-population comparison

Frequency-dependent predation has been proposed as a general mechanism driving the phenotypic assortment of social groups via the ‘oddity effect’, which occurs when the presence of odd individuals in a group allows a predator to fixate on a single prey item, increasing the predator''s attack-to-kill ratio. However, the generality of the oddity effect has been debated and, previously, there has not been an ecological assessment of the role of predation risk in driving the phenotypic assortment of social groups. Here, we compare the levels of body length assortment of social groups between populations of the Trinidadian guppy (Poecilia reticulata) that experience differences in predation risk. As predicted by the oddity effect hypothesis, we observe phenotypic assortment by body length to be greater under high predation risk. However, we found that a number of low-predation populations were also significantly assorted by body length, suggesting that other mechanisms may have a role to play.     

MEASURING NATURAL SELECTION ON PHENOTYPIC PLASTICITY

To understand natural selection we need to integrate its measure across environments. We present a method for measuring phenotypic selection that combines the potential for both environmental variation and phenotypic plasticity. The method uses path analysis and a measure of selection that is analogous to selection on breeding values. For individuals growing in alternative environments, paths are created that represent potential changes in the environment. The probabilities for these changes are then multiplied by the path coefficients to calculate selection coefficients. Selection on plasticity is measured as the difference in selection within each environment. We illustrate these methods using data on selection in an experimental population of Arabidopsis thaliana. Individuals from 36 families were grown in one of four environments, a factorial combination of shaded/open and early/late shading. For final height of the inflorescence, there was positive selection in both the open and shaded environments and negative selection on plasticity of height. For bolting time, there was also positive selection in both environments, but no selection on plasticity. We show how to use this information to examine how selection would change with changes in environmental frequencies and their transition probabilities. These methods can be expanded to encompass continuous traits and continuous environments as well as other complexities of natural selection.     

Spite and the scale of competition

In recent years there has been a large body of theoretical work examining how local competition can reduce and even remove selection for altruism between relatives. However, it is less well appreciated that local competition favours selection for spite, the relatively neglected ugly sister of altruism. Here, we use extensions of social evolution theory that were formulated to deal with the consequences for altruism of competition between social partners, to illustrate several points on the evolution of spite. Specifically, we show that: (i) the conditions for the evolution of spite are less restrictive than previously assumed; (ii) previous models which have demonstrated selection for spite often implicitly assumed local competition; (iii) the scale of competition must be allowed for when distinguishing different forms of spite (Hamiltonian vs. Wilsonian); (iv) local competition can enhance the spread of spiteful greenbeards; and (v) the theory makes testable predictions for how the extent of spite should vary dependent upon population structure and average relatedness.     

Testing the molecular and evolutionary causes of a 'leapfrog' pattern of geographical variation in coloration

Understanding the mechanisms accounting for the evolution of phenotypic diversity is central to evolutionary biology. We use molecular and phenotypic data to test hypotheses for 'leapfrog' patterns of geographical variation, in which phenotypically similar, disjunct populations are separated by distinct populations of the same species. Phylogenetic reconstructions revealed independent evolution of melanic plumage characters in different populations in the Neotropical avian genus Arremon. Thus, phenotypic similarities between distant populations cannot be explained by close phylogenetic affinity. Nor can they be attributed to recurring mutations in the MC1R gene, a locus involved in melanic pigmentation. A coalescent analysis indicates that plumage traits have become fixed at a faster rate than expected under genetic drift, suggesting that selection underlies their repeated evolution. In contrast to views that genetic drift drives phenotypic differentiation in Neotropical montane birds, our results imply that geographical variation preceding speciation may reflect the action of deterministic selective processes.     

Assortative mating but no evidence of genetic divergence in a species characterized by a trophic polymorphism

Disruptive selection is a process that can result in multiple subgroups within a population, which is referred to as diversification. Foraging‐related diversification has been described in many taxa, but many questions remain about the contribution of such diversification to reproductive isolation and potentially sympatric speciation. Here, we use stable isotope analysis of diet and morphological analysis of body shape to examine phenotypic divergence between littoral and pelagic foraging ecomorphs in a population of pumpkinseed sunfish (Lepomis gibbosus). We then examine reproductive isolation between ecomorphs by comparing the isotopic compositions of nesting males to eggs from their nests (a proxy for maternal diet) and use nine microsatellite loci to examine genetic divergence between ecomorphs. Our data support the presence of distinct foraging ecomorphs in this population and indicate that there is significant positive assortative mating based on diet. We did not find evidence of genetic divergence between ecomorphs, however, indicating that isolation is either relatively recent or is not strong enough to result in genetic divergence at the microsatellite loci. Based on our findings, pumpkinseed sunfish represent a system in which to further explore the mechanisms by which natural and sexual selection contribute to diversification, prior to the occurrence of sympatric speciation.     

Selection for individual recognition and the evolution of polymorphic identity signals in Polistes paper wasps

Individual recognition (IR) requires individuals to uniquely identify their social partners based on phenotypic variation. Because IR is so specific, distinctive phenotypes that stand out from the crowd facilitate efficient recognition. Over time, the benefits of unique appearances are predicted to produce a correlation between IR and phenotypic variation. Here, we test whether there is an association between elevated phenotypic polymorphism and IR in paper wasps. Previous work has shown that Polistes fuscatus use variable colour patterns for IR. We test whether two less variable wasp species, Polistes dominulus and Polistes metricus, are capable of IR. As predicted, neither species is capable of IR, suggesting that highly variable colour patterns are confined to Polistes species with IR. This association suggests that elevated phenotypic variation in taxa with IR may be the result of selection for identity signals rather than neutral processes. Given that IR is widespread among social taxa, selection for identity signalling may be an underappreciated mechanism for the origin and maintenance of polymorphism.     

Social heterosis and the maintenance of genetic diversity

Genetic diversity in species is often high in spite of directional selection or strong genetic drift. One resolution to this paradox may be through fitness benefits arising from interactions of genetically diverse individuals. Advantageous phenotypes that are impossible in single individuals (e.g. being simultaneously bold and shy) can be expressed by groups composed of genetically different individuals. Genetic diversity, therefore, can produce mutualistic benefits shared by all group members. We define this effect as 'social heterosis', and mathematically demonstrate maintenance of allelic diversity when diverse groups or neighbourhoods are more reproductively successful than homogenous ones. Through social heterosis, genetic diversity persists without: frequency dependence within groups, migration, balancing selection, genetic linkages, overdominance, antagonistic pleiotropy or nonrandom allele assortment. Social heterosis may also offer an alternative evolutionary pathway to cooperation that does not require clustering of related individuals, nepotistic favouritism towards kin, or overt reciprocity.     

Similar preferences for ornamentation in opposite‐ and same‐sex choice experiments

Selection due to social interactions comprises competition over matings (sexual selection stricto sensu) plus other forms of social competition and cooperation. Sexual selection explains sex differences in ornamentation and in various other phenotypes, but does not easily explain cases where those phenotypes are similar in males and females. Understanding such similarities requires knowing how phenotypes influence nonsexual social interactions as well, which can be very important in gregarious animals, but whose role for phenotypic evolution has been overlooked. For example, ‘mate choice’ experiments often found preferences for ornamentation, but have not assessed whether those are strictly sexual or are general social preferences. Using choice experiments with a gregarious and mutually ornamented finch, the common waxbill (Estrilda astrild), we show that preferences for ornamentation in the opposite‐sex also extend to same‐sex interactions. Waxbills discriminated between opposite‐ and same‐sex individuals, but most preferences for colour traits were similar when interacting with either sex. Similar preferences in sexual and nonsexual associations may be widespread in nature, either as social adaptations or as by‐product of mate preferences. In either case, such preferences may set the stage for the evolution of mutual ornamentation and of various other similarities between the sexes.     

Socially flexible female choice differs among populations of the Pacific field cricket: geographical variation in the interaction coefficient psi (Ψ)

Indirect genetic effects (IGEs) occur when genes expressed in one individual affect the phenotype of a conspecific. Theoretical models indicate that the evolutionary consequences of IGEs critically depend on the genetic architecture of interacting traits, and on the strength and direction of phenotypic effects arising from social interactions, which can be quantified by the interaction coefficient Ψ. In the context of sexually selected traits, strong positive Ψ tends to exaggerate evolutionary change, whereas negative Ψ impedes sexual trait elaboration. Despite its theoretical importance, whether and how Ψ varies among geographically distinct populations is unknown. Such information is necessary to evaluate the potential for IGEs to contribute to divergence among isolated or semi-isolated populations. Here, we report substantial variation in Ψ for a behavioural trait involved in sexual selection in the field cricket Teleogryllus oceanicus: female choosiness. Both the strength and direction of Ψ varied among geographically isolated populations. Ψ also changed over time. In a contemporary population of crickets from Kauai, experience of male song increased female choosiness. In contrast, experience of male song decreased choosiness in an ancestral population from the same location. This rapid change corroborates studies examining the evolvability of Ψ and demonstrates how interpopulation variation in the interaction coefficient might influence sexual selection and accelerate divergence of traits influenced by IGEs that contribute to reproductive isolation in nascent species or subspecies.     

Learned social preference in zebrafish

How social aggregations arise and persist is central to our understanding of evolution, behavior, and psychology. When social groups arise within a species, evolutionary divergence and speciation can result. To understand this diversifying role of social behavior, we must examine the internal and external influences that lead to nonrandom assortment of phenotypes. Many fishes form aggregations called shoals that reduce predation risk while enhancing foraging and reproductive success. Thus, shoaling is adaptive, and signals that maintain shoals are likely to evolve under selection. Given the diversity of pigment patterns among Danio fishes, visual signals might be especially important in mediating social behaviors in this group. Our understanding of pigment pattern development in the zebrafish D. rerio allows integrative analyses of how molecular variation leads to morphological variation among individuals and how morphological variation influences social interactions. Here, we use the zebrafish pigment mutant nacre/mitfa to test roles for genetic and environmental determinants in the development of shoaling preference. We demonstrate that individuals discriminate between shoals having different pigment pattern phenotypes and that early experience determines shoaling preference. These results suggest a role for social learning in pigment pattern diversification in danios.     

Antagonistic multilevel selection on size and architecture in variable density settings

In some ecological settings, an individual's fitness depends on both its own phenotype (individual-level selection) as well as the phenotype of the individuals with which it interacts (group-level selection). Using contextual analysis to measure multilevel selection in experimental stands of Arabidopsis thaliana, we detected significant linear selection that reversed across individual versus group levels for two composite phenotypic traits, "size" and "elongation." In both cases, selection at the individual level acted to increase values of these traits, presumably due to their positive effect on resource acquisition. Group selection favored decreased values of the same traits. Nonlinear selection was weak but significant in several cases, including stabilizing selection on developmental rate; individuals with very rapid development likely had lower than average fitness due to their reduced resource level at reproduction, while very delayed reproduction may have resulted in lower fitness if prolonged competition for resources reduced overall environmental quality and fitness of all individuals in a group. Under this scenario, stabilizing selection on individual traits is evidence of selection at the group level. Significant density-dependent selection suggests that a threshold density must be reached before group selection acts. Below this threshold, selection at the individual level affects phenotypic evolution more strongly than group selection. A second experiment measured multilevel selection in progeny stands of the original experimental plants. Multilevel selection again acted antagonistically on a composite trait that included size and elongation as well as on an architectural trait, branch production. The magnitude of individual versus group selection was relatively similar in the progeny generation, and the observed balance of individual versus group selection across densities is generally consistent with the hypotheses that multilevel selection can contribute to phenotypic evolution and to important demographic phenomena, including soft selection and the "law of constant yield."     

Selection on body size and sexual size dimorphism differs between host species in a seed-feeding beetle

Sexual size dimorphism varies substantially among populations and species but we have little understanding of the sources of selection generating this variation. We used path analysis to study how oviposition host affects selection on body size in a seed-feeding beetle (Stator limbatus) in which males contribute large ejaculates (nuptial gifts) to females. Females use nutrients in these ejaculates for egg production. Male body size, which affects ejaculate size, affects female fecundity and is thus under fecundity selection similar in magnitude to the fecundity selection on female body size. We show that when eggs are laid on a host on which larval mortality is low (seeds of Acacia greggii) fecundity predicts fitness very well and fecundity selection is the major source of selection on both male and female adult size. In contrast, when eggs are laid on a host on which larval mortality is high (seeds of Parkinsonia florida) fecundity poorly predicts fitness such that fecundity selection is relaxed on both male and female size. However, because egg size affects larval mortality on this poor host (P. florida) there is selection on female size via the female size --> egg size --> fitness path; this selection via egg size offsets the reduction in fecundity selection on female, but not male, body size. Thus, differences in host suitability (due to differences in larval mortality) affect the relative importance of two sources of selection on adult body size; fecundity selection on both male and female body size is lower on the poor quality host (P. florida) relative to the high quality host (A. greggii) whereas selection on female body size via effects of egg size on offspring survival (body size --> egg size --> fitness) is greater on the poor quality host relative to the high quality host. Because selection via the egg size path affects only females the difference in larval survival between hosts shifts the relative magnitude of selection on female vs. male size. Researchers working on other study systems should be alerted to the possible importance of subtle, but consequential, indirect selection on their study organisms.     

How mammalian sex chromosomes acquired their peculiar gene content

It has become increasingly evident that gene content of the sex chromosomes is markedly different from that of the autosomes. Both sex chromosomes appear enriched for genes related to sexual differentiation and reproduction; but curiously, the human X chromosome also seems to bear a preponderance of genes linked to brain and muscle functions. In this review, we will synthesize several evolutionary theories that may account for this nonrandom assortment of genes on the sex chromosomes, including 1) asexual degeneration, 2) sexual antagonism, 3) constant selection, and 4) hemizygous exposure. Additionally, we will speculate on how the evolution of sex-chromosome gene content might have impacted on the phenotypic evolution of mammals and particularly humans. Our discussion will focus on the mammalian sex chromosomes, but will cross reference other species where appropriate.