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.     

Molecular evolution of plant immune system genes

Molecular population genetic studies are providing new perspectives on the evolution of genes that confer resistance to pathogens and herbivores. Here, we compare the evolutionary history of different components of the defense response (detection, signaling and response) and of genes with parallel function in plants and Drosophila. A review of the literature indicates that the dominant form of selection acting on defense genes (balancing, positive and purifying) differs among components of defense. Sampling of particular classes of genes and genes from non-model organisms, however, remains limited. Future studies combining molecular evolutionary analyses with ecological genetic and functional analyses should better reveal how natural selection has shaped defense gene evolution.     

The effects of sexual selection and life history on the genetic structure of redfronted lemur, Eulemur fulvus rufus, groups

We examined genetic consequences of basic predictions of life history and sexual selection theory in a wild population of redfronted lemurs. Because group living in lemurs evolved independently from other primates, and because polygynous lemurs deviate in several sexually selected traits from theoretical predictions, data on genetic correlates of their social and mating systems can make important contributions to studies of convergence in social evolution, but such data are not available from wild populations. We extracted DNA from tissue samples obtained from 59 animals living in Kirindy forest, Madagascar, and examined individual variability at several microsatellite loci and the mitochondrial D-loop. We found that closely related females of a single matriline formed the core of the four main study groups. Virtually all haplotypes of adult males differed from those of coresident females, and many male haplotypes were represented by only one or two individuals. Paternity analyses for infants from groups with detailed behavioural data revealed that a disproportionate share of infants were sired by the central, dominant male of a group, despite promiscuous mating. Extragroup paternities were not detected. The skew in male reproductive success cannot be reconciled with the lack of sexual dimorphism and the even adult sex ratios. We therefore conclude that these group-living lemurs converge with many other primates in sex-specific life history trajectories, including female philopatry and male dispersal, but that the observed skew in male reproductive success makes the apparent lack of adaptation to intrasexual selection in certain behavioural, demographic and morphological traits even more puzzling. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Reproductive skew and the origin of sterile castes

Reproductive skew theory has not heretofore formally addressed one of the most important questions in evolutionary biology: How can whole-life sterile castes evolve? We construct a transactional skew model investigating under what conditions a subordinate in a multimember group is favored to develop into a morphologically specialized worker caste. Our model demonstrates that, contrary to former expectations, the ecological and genetic conditions favoring caste differentiation are far more restrictive than those favoring high skew. Caste differentiation cannot be selected in saturated, symmetrical relatedness groups unless the genetic relatedness among group members is extremely high. In contrast, it can be selected in the saturated, asymmetrical relatedness (parent-offspring) groups with complete skew. If we also consider the future reproduction of subordinates, caste differentiation is possible only after the group size reaches a certain critical point. Most importantly, caste differentiation in a parent-offspring group increases its saturated group size. The positive feedback between group size and the degree of caste differentiation can continue in principle until completely sterile worker castes emerge. Thus, at least in the case of parent-offspring groups, group size but not the degree of reproductive skew may be a better index of the level of social complexity. A scheme for the evolution of sterile worker castes that integrates the role of group size into the framework of reproductive skew theory is proposed.     

Evolution of tryptophan biosynthetic pathway in microbial genomes: a comparative genetic study

Biosynthetic pathway evolution needs to consider the evolution of a group of genes that code for enzymes catalysing the multiple chemical reaction steps leading to the final end product. Tryptophan biosynthetic pathway has five chemical reaction steps that are highly conserved in diverse microbial genomes, though the genes of the pathway enzymes show considerable variations in arrangements, operon structure (gene fusion and splitting) and regulation. We use a combined bioinformatic and statistical analyses approach to address the question if the pathway genes from different microbial genomes, belonging to a wide range of groups, show similar evolutionary relationships within and between them. Our analyses involved detailed study of gene organization (fusion/splitting events), base composition, relative synonymous codon usage pattern of the genes, gene expressivity, amino acid usage, etc. to assess inter- and intra-genic variations, between and within the pathway genes, in diverse group of microorganisms. We describe these genetic and genomic variations in the tryptophan pathway genes in different microorganisms to show the similarities across organisms, and compare the same genes across different organisms to find the possible variability arising possibly due to horizontal gene transfers. Such studies form the basis for moving from single gene evolution to pathway evolutionary studies that are important steps towards understanding the systems biology of intracellular pathways.     

The past,present and future of reproductive skew theory and experiments

A major evolutionary question is how reproductive sharing arises in cooperatively breeding species despite the inherent reproductive conflicts in social groups. Reproductive skew theory offers one potential solution: each group member gains or is allotted inclusive fitness equal to or exceeding their expectation from reproducing on their own. Unfortunately, a multitude of skew models with conflicting predictions has led to confusion in both testing and evaluating skew theory. The confusion arises partly because one set of models (the ‘transactional’ type) answer the ultimate evolutionary question of what ranges of reproductive skew can yield fitness‐enhancing solutions for all group members. The second set of models (‘compromise’) give an evolutionarily proximate, game‐theoretic evolutionarily stable state (ESS) solution that determines reproductive shares based on relative competitive abilities. However, several predictions arising from compromise models require a linear payoff to increased competition and do not hold with non‐linear payoffs. Given that for most species it may be very difficult or impossible to determine the true relationship between effort devoted to competition and reproductive share gained, compromise models are much less predictive than previously appreciated. Almost all skew models make one quantitative prediction (e.g. realized skew must fall within ranges predicted by transactional models), and two qualitative predictions (e.g. variation in relatedness or competitive ability across groups affects skew). A thorough review of the data finds that these three predictions are relatively rarely supported. As a general rule, therefore, the evolution of cooperative breeding appears not to be dependent on the ability of group members to monitor relatedness or competitive ability in order to adjust their behaviour dynamically to gain reproductive share. Although reproductive skew theory fails to predict within‐group dynamics consistently, it does better at predicting quantitative differences in skew across populations or species. This suggests that kin selection can play a significant role in the evolution of sociality. To advance our understanding of reproductive skew will require focusing on a broader array of factors, such as the frequency of mistaken identity, delayed fitness payoffs, and selection pressures arising from across‐group competition. We furthermore suggest a novel approach to investigate the sharing of reproduction that focuses on the underlying genetics of skew. A quantitative genetics approach allows the partitioning of variance in reproductive share itself or that of traits closely associated with skew into genetic and non‐genetic sources. Thus, we can determine the heritability of reproductive share and infer whether it actually is the focus of natural selection. We view the ‘animal model’ as the most promising empirical method where the genetics of reproductive share can be directly analyzed in wild populations. In the quest to assess whether skew theory can provide a framework for understanding the evolution of sociality, quantitative genetics will be a central tool in future research.     

Social systems and life‐history characteristics of mongooses

The diversity of extant carnivores provides valuable opportunities for comparative research to illuminate general patterns of mammalian social evolution. Recent field studies on mongooses (Herpestidae), in particular, have generated detailed behavioural and demographic data allowing tests of assumptions and predictions of theories of social evolution. The first studies of the social systems of their closest relatives, the Malagasy Eupleridae, also have been initiated. The literature on mongooses was last reviewed over 25 years ago. In this review, we summarise the current state of knowledge on the social organisation, mating systems and social structure (especially competition and cooperation) of the two mongoose families. Our second aim is to evaluate the contributions of these studies to a better understanding of mammalian social evolution in general. Based on published reports or anecdotal information, we can classify 16 of the 34 species of Herpestidae as solitary and nine as group‐living; there are insufficient data available for the remainder. There is a strong phylogenetic signal of sociality with permanent complex groups being limited to the genera Crossarchus, Helogale, Liberiictis, Mungos, and Suricata. Our review also indicates that studies of solitary and social mongooses have been conducted within different theoretical frameworks: whereas solitary species and transitions to gregariousness have been mainly investigated in relation to ecological determinants, the study of social patterns of highly social mongooses has instead been based on reproductive skew theory. In some group‐living species, group size and composition were found to determine reproductive competition and cooperative breeding through group augmentation. Infanticide risk and inbreeding avoidance connect social organisation and social structure with reproductive tactics and life histories, but their specific impact on mongoose sociality is still difficult to evaluate. However, the level of reproductive skew in social mongooses is not only determined by the costs and benefits of suppressing each other's breeding attempts, but also influenced by resource abundance. Thus, dispersal, as a consequence of eviction, is also linked to the costs of co‐breeding in the context of food competition. By linking these facts, we show that the socio‐ecological model and reproductive skew theory share some determinants of social patterns. We also conclude that due to their long bio‐geographical isolation and divergent selection pressures, future studies of the social systems of the Eupleridae will be of great value for the elucidation of general patterns in carnivore social evolution.     

GROUP FORMATION AND THE EVOLUTION OF SOCIALITY

In spite of its intrinsic evolutionary instability, altruistic behavior in social groups is widespread in nature, spanning from organisms endowed with complex cognitive abilities to microbial populations. In this study, we show that if social individuals have an enhanced tendency to form groups and fitness increases with group cohesion, sociality can evolve and be maintained in the absence of actively assortative mechanisms such as kin recognition or nepotism toward other carriers of the social gene. When explicitly taken into account in a game‐theoretical framework, the process of group formation qualitatively changes the evolutionary dynamics with respect to games played in groups of constant size and equal grouping tendencies. The evolutionary consequences of the rules underpinning the group size distribution are discussed for a simple model of microbial aggregation by differential attachment, indicating a way to the evolution of sociality bereft of peer recognition.     

A test for the genetic basis of natural selection: an individual-based longitudinal study in a stream-dwelling fish

In addition to the well-studied evolutionary parameters of (1) phenotype-fitness covariance and (2) the genetic basis of phenotypic variation, adaptive evolution by natural selection requires that (3) fitness variation is effected by heritable genetic differences among individuals and (4) phenotype-fitness covariances must be, at least in part, underlain by genetic covariances. These latter two requirements for adaptive evolutionary change are relatively unstudied in natural populations. Absence of the latter requirements could explain stasis of apparently directionally selected heritable traits. We provide complementary analyses of selection and variation at phenotypic and genetic levels for juvenile growth rate in brook charr Salvelinus fontinalis in Freshwater River, Newfoundland, Canada. Contrary to the vast majority of reports in fish, we found very little viability selection of juvenile body size. Large body size appears nonetheless to be selectively advantageous via a relationship with early maturity. Genetic patterns in evolutionary parameters largely reflected phenotypic patterns. We have provided inference of selection based on longitudinal data, which are uncommon in high fecundity organisms. Furthermore we have provided a practicable framework for further studies of the genetic basis of natural selection.     

«Active» selection may participate in the evolution of primates

Selection pressures in the evolution of morphological characters which are exclusive to primates were discussed. While the evolutionary change in some morphological characters of primates can be explained by natural or sexual selection, there are also morphological characters of primates, such as some regions of neocortices, which are involved in social interactions and whose evolutionary changes can hardly be explained by natural or sexual selection alone. Furthermore, recent studies have demonstrated that relative sizes of brain, neocortex and some thalamic nuclei of brains differ significantly by social structure in primates. Based on these and other findings, we propose here that “active” selection pressures may have favored a variety of morphological characters related to social interactions, the selection pressures which are derived from social interactions and are operative within animals or troops. The introduction of concept of active selection will be useful in developing conceptual frameworks for understanding of the mechanism of evolution of primates, in particular, of hominids.     

Simulating the Evolution of the Human Family: Cooperative Breeding Increases in Harsh Environments

Verbal and mathematical models that consider the costs and benefits of behavioral strategies have been useful in explaining animal behavior and are often used as the basis of evolutionary explanations of human behavior. In most cases, however, these models do not account for the effects that group structure and cultural traditions within a human population have on the costs and benefits of its members'' decisions. Nor do they consider the likelihood that cultural as well as genetic traits will be subject to natural selection. In this paper, we present an agent-based model that incorporates some key aspects of human social structure and life history. We investigate the evolution of a population under conditions of different environmental harshness and in which selection can occur at the level of the group as well as the level of the individual. We focus on the evolution of a socially learned characteristic related to individuals'' willingness to contribute to raising the offspring of others within their family group. We find that environmental harshness increases the frequency of individuals who make such contributions. However, under the conditions we stipulate, we also find that environmental variability can allow groups to survive with lower frequencies of helpers. The model presented here is inevitably a simplified representation of a human population, but it provides a basis for future modeling work toward evolutionary explanations of human behavior that consider the influence of both genetic and cultural transmission of behavior.     

Monogamy,strongly bonded groups,and the evolution of human social structure

Human social evolution has most often been treated in a piecemeal fashion, with studies focusing on the evolution of specific components of human society such as pair‐bonding, cooperative hunting, male provisioning, grandmothering, cooperative breeding, food sharing, male competition, male violence, sexual coercion, territoriality, and between‐group conflicts. Evolutionary models about any one of those components are usually concerned with two categories of questions, one relating to the origins of the component and the other to its impact on the evolution of human cognition and social life. Remarkably few studies have been concerned with the evolution of the entity that integrates all components, the human social system itself. That social system has as its core feature human social structure, which I define here as the common denominator of all human societies in terms of group composition, mating system, residence patterns, and kinship structures. The paucity of information on the evolution of human social structure poses substantial problems because that information is useful, if not essential, to assess both the origins and impact of any particular aspect of human society.     

Evolution of Primate Social Systems

We review evolutionary processes and mechanisms that gave rise to the diversity of primate social systems. We define social organization, social structure and mating system as distinct components of a social system. For each component, we summarize levels and patterns of variation among primates and discuss evolutionary determinants of this variation. We conclude that conclusive explanations for a solitary life and pair-living are still lacking. We then focus on interactions among the 3 components in order to identify main targets of selection and potential constraints for social evolution. Social organization and mating system are more closely linked to each other than either one is to social structure. Further, we conclude that it is important to seek a priori measures for the effects of presumed selective factors and that the genetic contribution to social systems is still poorly examined. Finally, we examine the role of primate socio-ecology in current evolutionary biology and conclude that primates are not prominently represented because the main questions asked in behavioral ecology are often irrelevant for primate behavior. For the future, we see a rapprochement of these areas as the role of disease and life-history theory are integrated more fully into primate socio-ecology.     

Social plasticity in fish: integrating mechanisms and function

Social plasticity is a ubiquitous feature of animal behaviour. Animals must adjust the expression of their social behaviour to the nuances of daily social life and to the transitions between life‐history stages, and the ability to do so affects their Darwinian fitness. Here, an integrative framework is proposed for understanding the proximate mechanisms and ultimate consequences of social plasticity. According to this framework, social plasticity is achieved by rewiring or by biochemically switching nodes of the neural network underlying social behaviour in response to perceived social information. Therefore, at the molecular level, it depends on the social regulation of gene expression, so that different brain genomic and epigenetic states correspond to different behavioural responses and the switches between states are orchestrated by signalling pathways that interface the social environment and the genotype. At the evolutionary scale, social plasticity can be seen as an adaptive trait that can be under positive selection when changes in the environment outpace the rate of genetic evolutionary change. In cases when social plasticity is too costly or incomplete, behavioural consistency can emerge by directional selection that recruits gene modules corresponding to favoured behavioural states in that environment. As a result of this integrative approach, how knowledge of the proximate mechanisms underlying social plasticity is crucial to understanding its costs, limits and evolutionary consequences is shown, thereby highlighting the fact that proximate mechanisms contribute to the dynamics of selection. The role of teleosts as a premier model to study social plasticity is also highlighted, given the diversity and plasticity that this group exhibits in terms of social behaviour. Finally, the proposed integrative framework to social plasticity also illustrates how reciprocal causation analysis of biological phenomena (i.e. considering the interaction between proximate factors and evolutionary explanations) can be a more useful approach than the traditional proximate–ultimate dichotomy, according to which evolutionary processes can be understood without knowledge on proximate causes, thereby black‐boxing developmental and physiological mechanisms.     

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.     

Evolution of the capacity to evolve

Abstract During the past two decades, the fields of molecular biology and genetics have enabled study of far broader and more detailed aspects of evolutionary change than were possible when the evolutionary synthesis was elaborated in the mid‐twentieth century. The capacity for complete sequencing of both genes and proteins of all groups of organisms provide, simultaneously, the means to determine both the patterns and processes of evolution throughout the history of life. Increased knowledge of the genome documents the changing nature of its composition, mode of transmission, and the nature of the units of selection. Advances in evolutionary developmental biology demonstrate the conservation of genetic elements throughout multicellular organisms, and explain how control of the timing, position and nature of their expression has produced the extraordinary diversity of living plants and animals. The next generation of evolutionary biologists will benefit greatly from the increased integration of these new fields of research with those that are currently emphasized in the standard textbooks and journals.     

Quantitative genetic versions of Hamilton's rule with empirical applications

Hamilton''s theory of inclusive fitness revolutionized our understanding of the evolution of social interactions. Surprisingly, an incorporation of Hamilton''s perspective into the quantitative genetic theory of phenotypic evolution has been slow, despite the popularity of quantitative genetics in evolutionary studies. Here, we discuss several versions of Hamilton''s rule for social evolution from a quantitative genetic perspective, emphasizing its utility in empirical applications. Although evolutionary quantitative genetics offers methods to measure each of the critical parameters of Hamilton''s rule, empirical work has lagged behind theory. In particular, we lack studies of selection on altruistic traits in the wild. Fitness costs and benefits of altruism can be estimated using a simple extension of phenotypic selection analysis that incorporates the traits of social interactants. We also discuss the importance of considering the genetic influence of the social environment, or indirect genetic effects (IGEs), in the context of Hamilton''s rule. Research in social evolution has generated an extensive body of empirical work focusing—with good reason—almost solely on relatedness. We argue that quantifying the roles of social and non-social components of selection and IGEs, in addition to relatedness, is now timely and should provide unique additional insights into social evolution.     

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 F_ST = 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.     

Structure trees and species trees: what they say about morphological development and evolution

The evolutionary history of morphological structures generally is equated with that of the taxa that carry them. It is argued here that, analogous to genes, developmental genetic pathways underlying morphological structures may be subject to developmental evolutionary changes that result, for instance, in duplication (serial homology analogous to gene duplication and paralogy). Entities that undergo evolution are expected to be related to each other as a tree. Just as with molecular evolution, "structure trees" and species trees sometimes may be incongruent, with implications for morphological homology concepts. Detection of structure trees through morphological evolutionary analyses may point to an entity that is maintained through evolution, possibly in part because it is a developmentally integrated structure ("individualized"). This idea is illustrated in a morphological evolutionary analysis of leaf primordia. These analyses suggest that leaf primordia in monocots and close relatives are related to each other as a tree and, therefore, are developmentally integrated, evolving entities. Among monocot primordia this tree structure breaks down, and it is concluded that there is no entity, the "monocot leaf primordium." However, one group of primordia is identified within monocots that have uniform characteristics and that are well represented by model species maize and rice. Such analyses of structure trees can facilitate the extrapolation and interpretation of results from molecular developmental and other comparative studies.