Reproductive inequality in humans and other mammals.

To address claims of human exceptionalism, we determine where humans fit within the greater mammalian distribution of reproductive inequality. We show that humans exhibit lower reproductive skew (i.e., inequality in the number of surviving offspring) among males and smaller sex differences in reproductive skew than most other mammals, while nevertheless falling within the mammalian range. Additionally, female reproductive skew is higher in polygynous human populations than in polygynous nonhumans mammals on average. This patterning of skew can be attributed in part to the prevalence of monogamy in humans compared to the predominance of polygyny in nonhuman mammals, to the limited degree of polygyny in the human societies that practice it, and to the importance of unequally held rival resources to women's fitness. The muted reproductive inequality observed in humans appears to be linked to several unusual characteristics of our species-including high levels of cooperation among males, high dependence on unequally held rival resources, complementarities between maternal and paternal investment, as well as social and legal institutions that enforce monogamous norms.

Norm Dynamics: Interdisciplinary Perspectives on Social Norm Emergence, Persistence, and Change.

Social norms are the glue that holds society together, yet our knowledge of them remains heavily intellectually siloed. This article provides an interdisciplinary review of the emerging field of norm dynamics by integrating research across the social sciences through a cultural-evolutionary lens. After reviewing key distinctions in theory and method, we discuss research on norm psychology-the neural and cognitive underpinnings of social norm learning and acquisition. We then overview how norms emerge and spread through intergenerational transmission, social networks, and group-level ecological and historical factors. Next, we discuss multilevel factors that lead norms to persist, change, or erode over time. We also consider cultural mismatches that can arise when a changing environment leads once-beneficial norms to become maladaptive. Finally, we discuss potential future research directions and the implications of norm dynamics for theory and policy.

The evolution of germ-soma specialization under different genetic and environmental effects.

Division of labor exists at different levels of biological organization - from cell colonies to human societies. One of the simplest examples of the division of labor in multicellular organisms is germ-soma specialization, which plays a key role in the evolution of organismal complexity. Here we formulate and study a general mathematical model exploring the emergence of germ-soma specialization in colonies of cells. We consider a finite population of colonies competing for resources. Colonies are of the same size and are composed by asexually reproducing haploid cells. Each cell can contribute to activity and fecundity of the colony, these contributions are traded-off. We assume that all cells within a colony are genetically identical but gene effects on fecundity and activity are influenced by variation in the microenvironment experienced by individual cells. Through analytical theory and evolutionary agent-based modeling we show that the shape of the trade-off relation between somatic and reproductive functions, the type and extent of variation in within-colony microenvironment, and, in some cases, the number of genes involved, are important predictors of the extent of germ-soma specialization. Specifically, increasing convexity of the trade-off relation, the number of different environmental gradients acting within a colony, and the number of genes (in the case of random microenvironmental effects) promote the emergence of germ-soma specialization. Overall our results contribute towards a better understanding of the role of genetic, environmental, and microenvironmental factors in the evolution of germ-soma specialization.

Ecological Consequences of Intraspecific Variation in Coevolutionary Systems.

AbstractThe patterns and outcomes of coevolution are expected to depend on intraspecific trait variation. Various evolutionary factors can change this variation in time. As a result, modeling coevolutionary processes solely in terms of mean trait values may not be sufficient; one may need to study the dynamics of the whole trait distribution. Here, we develop a theoretical framework for studying the effects of evolving intraspecific variation in two-species coevolutionary systems. In particular, we build and study mathematical models of competition, exploiter-victim interactions, and mutualism in which the strength of within- and between-species interactions depends on the difference in continuously varying traits between individuals reproducing asexually. We use analytical approximations based on the invasion analysis and supplement them with numerical results. We find that intraspecific variation can be maintained if stabilizing selection is weak in at least one species. When intraspecific variation is maintained under competition or mutualism, coexistence in a stable equilibrium is promoted when between-species interactions mostly happen between individuals similar in trait values. In contrast, in exploiter-victim systems coexistence typically requires strong interactions between dissimilar exploiters and victims. We show that trait distributions can become multimodal. Our approach and results contribute to the understanding of the ecological consequences of intraspecific variation in coevolutionary systems by exploring its effects on population densities and trait distributions.

The multinomial index: a robust measure of reproductive skew.

Inequality or skew in reproductive success (RS) is common across many animal species and is of long-standing interest to the study of social evolution. However, the measurement of inequality in RS in natural populations has been challenging because existing quantitative measures are highly sensitive to variation in group/sample size, mean RS, and age-structure. This makes comparisons across multiple groups and/or species vulnerable to statistical artefacts and hinders empirical and theoretical progress. Here, we present a new measure of reproductive skew, the multinomial index, M, that is unaffected by many of the structural biases affecting existing indices. M is analytically related to Nonacs' binomial index, B, and comparably accounts for heterogeneity in age across individuals; in addition, M allows for the possibility of diminishing or even highly nonlinear RS returns to age. Unlike B, however, M is not biased by differences in sample/group size. To demonstrate the value of our index for cross-population comparisons, we conduct a reanalysis of male reproductive skew in 31 primate species. We show that a previously reported negative effect of group size on mating skew was an artefact of structural biases in existing skew measures, which inevitably decline with group size; this bias disappears when using M. Applying phylogenetically controlled, mixed-effects models to the same dataset, we identify key similarities and differences in the inferred within- and between-species predictors of reproductive skew across metrics. Finally, we provide an R package, SkewCalc, to estimate M from empirical data.

Collective action and the evolution of social norm internalization.

Human behavior is strongly affected by culturally transmitted norms and values. Certain norms are internalized (i.e., acting according to a norm becomes an end in itself rather than merely a tool in achieving certain goals or avoiding social sanctions). Humans' capacity to internalize norms likely evolved in our ancestors to simplify solving certain challenges-including social ones. Here we study theoretically the evolutionary origins of the capacity to internalize norms. In our models, individuals can choose to participate in collective actions as well as punish free riders. In making their decisions, individuals attempt to maximize a utility function in which normative values are initially irrelevant but play an increasingly important role if the ability to internalize norms emerges. Using agent-based simulations, we show that norm internalization evolves under a wide range of conditions so that cooperation becomes "instinctive." Norm internalization evolves much more easily and has much larger effects on behavior if groups promote peer punishment of free riders. Promoting only participation in collective actions is not effective. Typically, intermediate levels of norm internalization are most frequent but there are also cases with relatively small frequencies of "oversocialized" individuals willing to make extreme sacrifices for their groups no matter material costs, as well as "undersocialized" individuals completely immune to social norms. Evolving the ability to internalize norms was likely a crucial step on the path to large-scale human cooperation.

On the evolution of visual female sexual signalling.

A long-standing evolutionary puzzle surrounds female sexual signals visible around the time of ovulation. Even among just primates, why do some species have substantial sexual swellings and/or bright colorations visible around females' genital regions, while other species are like humans, with no signs of ovulation visible? What is the evolutionary purpose behind not just these signs, but also this great variation seen among species? Here, we examine the evolutionary trade-offs associated with visual ovulation signalling using agent-based modelling. Our model predicts how various factors, including male genetic heterogeneity and reproductive inequality, female physiological costs, group size, and the weighting of genetic versus non-genetic benefits coming from males, each influence the strength of ovulation signalling. Our model also predicts that increasing the impacts of infanticide will increase ovulation signalling. We use comparative primate data to show that, as predicted by our model, larger group size and higher risk of infanticide each correlate with having stronger visual ovulation signs. Overall, our work resolves some old controversies and sheds new light on the evolution of visual female sexual signalling.

Sexually antagonistic epigenetic marks that canalize sexually dimorphic development.

The sexes share the same autosomal genomes, yet sexual dimorphism is common due to sex-specific gene expression. When present, XX and XY karyotypes trigger alternate regulatory cascades that determine sex-specific gene expression profiles. In mammals, secretion of testosterone (T) by the testes during foetal development is the master switch influencing the gene expression pathways (male vs. female) that will be followed, but many genes have sex-specific expression prior to T secretion. Environmental factors, like endocrine disruptors and mimics, can interfere with sexual development. However, sex-specific ontogeny can be canalized by the production of epigenetic marks (epimarks) generated during early ontogeny that increase sensitivity of XY embryos to T and decrease sensitivity of XX embryos. Here, we integrate and synthesize the evidence indicating that canalizing epimarks are produced during early ontogeny. We will also describe the evidence that such epimarks sometimes carry over across generations and produce mosaicism in which some traits are discordant with the gonad. Such carryover epimarks are sexually antagonistic because they benefit the individual in which they were formed (via canalization) but harm opposite-sex offspring when they fail to erase across generations and produce gonad-trait discordances. SA-epimarks have the potential to: i) magnify phenotypic variation for many sexually selected traits, ii) generate overlap along many dimensions of the masculinity/femininity spectrum, and iii) influence medically important gonad-trait discordances like cryptorchidism, hypospadias and idiopathic hirsutism.

War, space, and the evolution of Old World complex societies.

How did human societies evolve from small groups, integrated by face-to-face cooperation, to huge anonymous societies of today, typically organized as states? Why is there so much variation in the ability of different human populations to construct viable states? Existing theories are usually formulated as verbal models and, as a result, do not yield sharply defined, quantitative predictions that could be unambiguously tested with data. Here we develop a cultural evolutionary model that predicts where and when the largest-scale complex societies arose in human history. The central premise of the model, which we test, is that costly institutions that enabled large human groups to function without splitting up evolved as a result of intense competition between societies-primarily warfare. Warfare intensity, in turn, depended on the spread of historically attested military technologies (e.g., chariots and cavalry) and on geographic factors (e.g., rugged landscape). The model was simulated within a realistic landscape of the Afroeurasian landmass and its predictions were tested against a large dataset documenting the spatiotemporal distribution of historical large-scale societies in Afroeurasia between 1,500 BCE and 1,500 CE. The model-predicted pattern of spread of large-scale societies was very similar to the observed one. Overall, the model explained 65% of variance in the data. An alternative model, omitting the effect of diffusing military technologies, explained only 16% of variance. Our results support theories that emphasize the role of institutions in state-building and suggest a possible explanation why a long history of statehood is positively correlated with political stability, institutional quality, and income per capita.

Homosexuality via canalized sexual development: a testing protocol for a new epigenetic model.

We recently synthesized and reinterpreted published studies to advance an epigenetic model for the development of homosexuality (HS). The model is based on epigenetic marks laid down in response to the XX vs. XY karyotype in embryonic stem cells. These marks boost sensitivity to testosterone in XY fetuses and lower it in XX fetuses, thereby canalizing sexual development. Our model predicts that a subset of these canalizing epigenetic marks stochastically carry over across generations and lead to mosaicism for sexual development in opposite-sex offspring--the homosexual phenotype being one such outcome. Here, we begin by outlining why HS has been under-appreciated as a commonplace phenomenon in nature, and how this trend is currently being reversed in the field of neurobiology. We next briefly describe our epigenetic model of HS, develop a set of predictions, and describe how epigenetic profiles of human stem cells can provide for a strong test of the model.

On the evolutionary origins of the egalitarian syndrome.

The evolutionary emergence of the egalitarian syndrome is one of the most intriguing unsolved puzzles related to the origins of modern humans. Standard explanations and models for cooperation and altruism--reciprocity, kin and group selection, and punishment--are not directly applicable to the emergence of egalitarian behavior in hierarchically organized groups that characterized the social life of our ancestors. Here I study an evolutionary model of group-living individuals competing for resources and reproductive success. In the model, the differences in fighting abilities lead to the emergence of hierarchies where stronger individuals take away resources from weaker individuals and, as a result, have higher reproductive success. First, I show that the logic of within-group competition implies under rather general conditions that each individual benefits if the transfer of the resource from a weaker group member to a stronger one is prevented. This effect is especially strong in small groups. Then I demonstrate that this effect can result in the evolution of a particular, genetically controlled psychology causing individuals to interfere in a bully-victim conflict on the side of the victim. A necessary condition is a high efficiency of coalitions in conflicts against the bullies. The egalitarian drive leads to a dramatic reduction in within-group inequality. Simultaneously it creates the conditions for the emergence of inequity aversion, empathy, compassion, and egalitarian moral values via the internalization of behavioral rules imposed by natural selection. It also promotes widespread cooperation via coalition formation.

Human origins and the transition from promiscuity to pair-bonding.

A crucial step in recent theories of human origins is the emergence of strong pair-bonding between males and females accompanied by a dramatic reduction in the male-to-male conflict over mating and an increased investment in offspring. How such a transition from promiscuity to pair-bonding could be achieved is puzzling. Many species would, indeed, be much better off evolutionarily if the effort spent on male competition over mating was redirected to increasing female fertility or survivorship of offspring. Males, however, are locked in a "social dilemma," where shifting one's effort from "appropriation" to "production" would give an advantage to free-riding competitors and therefore, should not happen. Here, I first consider simple models for four prominent scenarios of the human transition to pair-bonding: communal care, mate guarding, food for mating, and mate provisioning. I show that the transition is not feasible under biologically relevant conditions in any of these models. Then, I show that the transition can happen if one accounts for male heterogeneity, assortative pair formation, and evolution of female choice and faithfulness. This process is started when low-ranked males begin using an alternative strategy of female provisioning. At the end, except for the top-ranked individuals, males invest exclusively in provisioning females who have evolved very high fidelity to their mates. My results point to the crucial importance of female choice and emphasize the need for incorporating between-individual variation in theoretical and empirical studies of social dilemmas and behaviors.

The genomic signature of parallel adaptation from shared genetic variation.

Parallel adaptation is common and may often occur from shared genetic variation, but the genomic consequences of this process remain poorly understood. We first use individual-based simulations to demonstrate that comparisons between populations adapted in parallel to similar environments from shared variation reveal a characteristic genomic signature around a selected locus: a low-divergence valley centred at the locus and flanked by twin peaks of high divergence. This signature is initiated by the hitchhiking of haplotype tracts differing between derived populations in the broader neighbourhood of the selected locus (driving the high-divergence twin peaks) and shared haplotype tracts in the tight neighbourhood of the locus (driving the low-divergence valley). This initial hitchhiking signature is reinforced over time because the selected locus acts as a barrier to gene flow from the source to the derived populations, thus promoting divergence by drift in its close neighbourhood. We next empirically confirm the peak-valley-peak signature by combining targeted and RAD sequence data at three candidate adaptation genes in multiple marine (source) and freshwater (derived) populations of threespine stickleback. Finally, we use a genome-wide screen for the peak-valley-peak signature to discover additional genome regions involved in parallel marine-freshwater divergence. Our findings offer a new explanation for heterogeneous genomic divergence and thus challenge the standard view that peaks in population divergence harbour divergently selected loci and that low-divergence regions result from balancing selection or localized introgression. We anticipate that genome scans for peak-valley-peak divergence signatures will promote the discovery of adaptation genes in other organisms.

Models of speciation: where are we now?

Theory building is an integral part of biological research, in general, and of speciation research, in particular. Here, I review the modeling work on speciation done in the last 10 years or so, assessing the progress made and identifying areas where additional effort is required. Specific topics considered include evolutionary dynamics of genetic incompatibilities, spatial and temporal patterns of speciation, links to neutral theory of biodiversity, effects of multidimensionality of phenotype, sympatric and parapatric speciation, adaptive radiation, speciation by sexual conflict, and models tailored for specific biological systems. Particularly challenging questions for future theoretical research identified here are 1) incorporating gene regulatory networks in models describing accumulation of genetic incompatibilities; 2) integrating models of community ecology with those developed in speciation theory; 3) building models providing better insights on the dynamics of parapatric speciation; 4) modeling speciation in multidimensional ecological niches with mating preferences based on multidimensional mating cues and sexual characters; 5) linking microevolutionary processes with macroevolutionary patterns as observed in adaptive radiations and paleontological record; 6) modeling speciation in specific systems studied by empirical biologists; and 7) modeling human origins. The insights from dynamic models of speciation should be useful in developing statistical tools that would enable empiricists to infer the history of past evolutionary divergence and speciation from genomic data.

Modelling social norms: an integration of the norm-utility approach with beliefs dynamics.

We review theoretical approaches for modelling the origin, persistence and change of social norms. The most comprehensive models describe the coevolution of behaviours, personal, descriptive and injunctive norms while considering influences of various authorities and accounting for cognitive processes and between-individual differences. Models show that social norms can improve individual and group well-being. Under some conditions though, deleterious norms can persist in the population through conformity, preference falsification and pluralistic ignorance. Polarization in behaviour and beliefs can be maintained, even when societal advantages of particular behaviours or belief systems over alternatives are clear. Attempts to change social norms can backfire through cognitive processes including cognitive dissonance and psychological reactance. Under some conditions social norms can change rapidly via tipping point dynamics. Norms can be highly susceptible to manipulation, and network structure influences their propagation. Future models should incorporate network structure more thoroughly, explicitly study online norms, consider cultural variations and be applied to real-world processes. This article is part of the theme issue 'Social norm change: drivers and consequences'.

Social norm change: drivers and consequences.

Social norms research is booming. In recent years, several experts have recommended using social norms (unwritten rules that prescribe what people ought or ought not to do) to confront the societal, environmental and health challenges our societies face. If we are to do so, a better understanding is required of how social norms themselves emerge, evolve and respond to these challenges. Social norms have long been used as post hoc explanations of behaviour or are seen as stable social constructs. Yet norms evolve dynamically with the changing group processes (e.g. political polarization, kinship structures) and societal challenges (e.g. pandemics, climate change) for which they are presented as solutions. The Theme Issue 'Social norm change: drivers and consequences' contains 14 contributions that present state-of-the-art approaches to understand what generates social norm change and how this impacts our societies. Contributions give insight into (i) the identification of norms, norm change and their effect on behaviour; (ii) drivers and consequences of spontaneous norm change; and (iii) how norm change can be engineered to promote desired behavioural change. This article is part of the theme issue 'Social norm change: drivers and consequences'.

Evolution of mate choice and the so-called magic traits in ecological speciation.

Non-random mating provides multiple evolutionary benefits and can result in speciation. Biological organisms are characterised by a myriad of different traits, many of which can serve as mating cues. We consider multiple mechanisms of non-random mating simultaneously within a unified modelling framework in an attempt to understand better which are more likely to evolve in natural populations going through the process of local adaptation and ecological speciation. We show that certain traits that are under direct natural selection are more likely to be co-opted as mating cues, leading to the appearance of magic traits (i.e. phenotypic traits involved in both local adaptation and mating decisions). Multiple mechanisms of non-random mating can interact so that trait co-evolution enables the evolution of non-random mating mechanisms that would not evolve alone. The presence of magic traits may suggest that ecological selection was acting during the origin of new species.

Evolution of manipulated behavior.

Many social behaviors are triggered by social partners. For example, cells in a multicellular organism often become soma via extrinsically regulated differentiation, while individuals in a eusocial colony often become helpers via extrinsic caste determination. One explanation for social triggering is that it informs when it is beneficial to express the behavior. Alternatively, social triggering can represent manipulation where social partners partially or completely control the focal individual's behavior. For instance, caste determination in primitively eusocial taxa is typically accomplished via differential feeding or dominance hierarchies, suggesting some manipulation. However, selection would favor resistance if manipulation is detrimental to manipulated parties, and the outcome of the manipulation conflict remains intricate. We analyze the coevolution of manipulation and resistance in a simple but general setting. We show that, despite possible resistance, manipulated behavior can be established under less stringent conditions than spontaneous (i.e., nonmanipulated) behavior because of resistance costs. The existence of this advantage might explain why primitive eusocial behavior tends to be triggered socially and coercively. We provide a simple condition for the advantage of manipulated behavior that may help infer whether a socially triggered behavior is manipulated. We illustrate our analysis with a hypothetical example of maternal manipulation relevant to primitive eusociality.