Maternal care leads to the evolution of long, slow lives.

Animals, and mammals in particular, vary widely in their "pace of life," with some species living long lives and reproducing infrequently (slow life histories) and others living short lives and reproducing often (fast life histories). These species also vary in the importance of maternal care in offspring fitness: In some species, offspring are fully independent of their mothers following a brief period of nutritional input, while others display a long period of continued dependence on mothers well after nutritional dependence. Here, we hypothesize that these two axes of variation are causally related to each other, such that extended dependence of offspring on maternal presence leads to the evolution of longer lives at the expense of reproduction. We use a combination of deterministic modeling and stochastic agent-based modeling to explore how empirically observed links between maternal survival and offspring fitness are likely to shape the evolution of mortality and fertility. Each of our modeling approaches leads to the same conclusion: When maternal survival has a strong impact on the survival of offspring and grandoffspring, populations evolve longer lives with less frequent reproduction. Our results suggest that the slow life histories of humans and other primates as well as other long-lived, highly social animals such as hyenas, whales, and elephants are partially the result of the strong maternal care that these animals display. We have designed our models to be readily parameterized with demographic data that are routinely collected by long-term researchers, which will facilitate more thorough testing of our hypothesis.

Evolutionary predictors of the specific colors of birds.

Animal coloration is one of the most conspicuous aspects of human-perceived organismal diversity, yet also one of the least understood. In particular, explaining why species have specific colors (e.g., blue vs. red) has proven elusive. Here, we quantify for nearly all bird species, the proportion of the body covered by each of 12 human-visible color categories, and test whether existing theory can predict the direction of color evolution. The most common colors are black, white, gray and brown, while the rarest are green, blue, purple, and red. Males have more blue, purple, red, or black, whereas females have more yellow, brown, or gray. Sexual dichromatism is partly due to sexual selection favoring ornamental colors in males but not in females. However, sexual selection also correlated positively with brown in both sexes. Strong social selection favors red and black, colors used in agonistic signaling, with the strongest effects in females. Reduced predation risk selects against cryptic colors (e.g., brown) and favors specific ornamental colors (e.g., black). Nocturnality is mainly associated with brown. The effects of habitat use support the sensory drive theory for camouflage and signaling. Darker colors are more common in species living in wet and cold climates, matching ecogeographical rules. Our study unambiguously supports existing theories of color evolution across an entire class of vertebrates, but much variation remains unexplained.

Models of animal coalitions and their implications for human evolution.

Social interaction is a prime driver for the evolution of animal behaviour. Dyadic interaction, in particular, has been the focus of intensive research on the evolution of mutualistic, altruistic, selfish or spiteful behaviours. Meanwhile, triadic interaction has been the minimal framework for the study of animal coalition as observed in some species of primates, as well as in carnivores and cetaceans, where two or more individuals act jointly against a third party in a competitive context. Previous mathematical models of animal coalition have either failed to explain the observed diversity in the configuration of coalition or presumed fine-tuned decision-making that may be unrealistic for non-human animals. To approach these issues, the present study develops a new model that is fairly simple, but still able to account for the observed diversity in animal coalitions. Analysis of the model specifies key parameters affecting the predicted types of coalition: the nature of the benefit being contested, the cost-to-benefit ratio associated with fighting and the synergistic effect in coalition formation. Additionally, the model is used to evaluate the social selection hypothesis, which claims that coalition formation induced social selection favouring reduced aggression and lower fighting abilities during human evolution.

The effects of intersexual interactions on survival can drive the evolution of female ornaments in the absence of mate limitation.

The evolution of sexual ornaments in animals is typically attributed to reproductive competition. However, sexual ornaments also arise in contexts where the ornamented sex is neither mate nor gamete limited, and explanations for ornamentation in these cases remain incomplete. In many species, particularly those with slow life histories, lifetime reproductive success depends more strongly on adult survival than fecundity, and survival can depend on intersexual interactions. We develop a population genetic model to investigate how the effect of intersexual interactions on survival may contribute to ornament evolution in the absence of competition for mates. Using female ornamentation in polygynous mating systems as a case study, we show that, indeed, ornaments can evolve when the ornament functions to modify interactions with males in ways that enhance a female's own survival. The evolutionary dynamics depend qualitatively on the specific behavioral mechanism by which the ornament modifies social interactions. In all cases, the ornament's long-term persistence is ultimately determined by the coevolution of the male locus that determines how males affect female survival. We outline the scenarios that are most likely to favor the evolution of female ornaments through the effects of intersexual interactions on survival, and we urge empirical researchers to consider the potential for this social selection mechanism to shape traits of interest across taxa.

Social interactions generate complex selection patterns in virtual worlds.

Understanding the influence of social interactions on individual fitness is key to improving our predictions of phenotypic evolution. However, we often overlook the different components of selection regimes arising from interactions among organisms, including social, correlational, and indirect selection. This is due to the challenging sampling efforts required in natural populations to measure phenotypes expressed during interactions and individual fitness. Furthermore, behaviours are crucial in mediating social interactions, yet few studies have explicitly quantified these selection components on behavioural traits. In this study, we capitalize on an online multiplayer video game as a source of extensive data recording direct social interactions among prey, where prey collaborate to escape a predator in realistic ecological settings. We estimate natural and social selection and their contribution to total selection on behavioural traits mediating competition, cooperation, and predator-prey interactions. Behaviours of other prey in a group impact an individual's survival, and thus are under social selection. Depending on whether selection pressures on behaviours are synergistic or conflicting, social interactions enhance or mitigate the strength of natural selection, although natural selection remains the main driving force. Indirect selection through correlations among traits also contributed to the total selection. Thus, failing to account for the effects of social interactions and indirect selection would lead to a misestimation of the total selection acting on traits. Dissecting the contribution of each component to the total selection differential allowed us to investigate the causal mechanisms relating behaviour to fitness and quantify the importance of the behaviours of conspecifics as agents of selection. Our study emphasizes that social interactions generate complex selective regimes even in a relatively simple ecological environment.

Evolution of female colours in birds: The role of female cost of reproduction and paternal care.

Female ornamentation is frequently observed in animal species and is sometimes found as more evolutionary labile than male ornamentation. A complex array of factors may explain its presence and variation. Here we assessed the role of female cost of reproduction and paternal care. Both factors have been pinpointed as important by theoretical studies but have not been investigated yet in details at the interspecific level. We worked on 133 species of North temperate Passeriformes bird species for which both the clutch volume - here taken as the proxy of female cost of reproduction - and amount of paternal care are relatively well known. Using spectrometry, we measured the whole-body coloured plumage patches and quantified three metrics corresponding to brightness (i.e. achromatic component), colour chromaticity (i.e. intensity) and colour volume (i.e. diversity). We found a strong association between male and female colour metrics. Controlling for this association, we found additional small but detectable effects of both cost of reproduction and paternal care. First, females of species with more paternal care were slightly brighter. Second, the interaction between the level of paternal care and egg volume was correlated with female colour intensity: females with more paternal care were more chromatic, with this association mostly present when their investment in reproduction was low. Together these results suggest that female cost of reproduction and paternal care are part of the multiple factors explaining variation of female coloration, besides the strong covariation between male and female coloration.

Does capacity to produce androgens underlie variation in female ornamentation and territoriality in White-shouldered Fairywren (Malurus alboscapulatus)?

Historic bias toward study of sex hormones and sexual ornamentation in males currently constrains our perspective of hormone-behavior-phenotype relationships. Resolving how ornamented female phenotypes evolve is particularly important for understanding the diversity of social signals across taxa. Studies of both males and females in taxa with variable female phenotypes are needed to establish whether sexes share mechanisms underlying expression of signaling phenotypes and behavior. White-shouldered Fairywren (Malurus alboscapulatus) subspecies vary in female ornamentation, baseline circulating androgens, and response to territorial intrusion. The moretoni ornamented female subspecies is characterized by higher female, but lower male baseline androgens, and a stronger pair territorial response relative to pairs from the lorentzi unornamented female subspecies. Here we address whether subspecific differences in female ornamentation, baseline androgens, and pair territoriality are associated with ability to elevate androgens following gonadotropin releasing hormone (GnRH) challenge and in response to simulated territorial intrusion. We find that subspecies do not differ in their capacity to produce androgens in either sex following GnRH or simulated territorial intrusion (STI) challenges. STI-induced androgens were predictive of degree of response to territorial intrusions in females only, but the direction of the effect was mixed. GnRH-induced androgens did not correlate with response to simulated intruders, nor did females sampled during intrusion elevate androgens relative to flushed controls, suggesting that increased androgens are not necessary for the expression of territorial defense behaviors. Collectively, our results suggest that capacity to produce androgens does not underlie subspecific patterns of female ornamentation, territoriality, and baseline plasma androgens.

Emergent social structure is typically not associated with survival in a facultatively social mammal.

For social animals, group social structure has important consequences for disease and information spread. While prior studies showed individual connectedness within a group has fitness consequences, less is known about the fitness consequences of group social structure for the individuals who comprise the group. Using a long-term dataset on a wild population of facultatively social yellow-bellied marmots (Marmota flaviventer), we showed social structure had largely no relationship with survival, suggesting consequences of individual social phenotypes may not scale to the group social phenotype. An observed relationship for winter survival suggests a potentially contrasting direction of selection between the group and previous research on the individual level; less social individuals, but individuals in more social groups experience greater winter survival. This work provides valuable insights into evolutionary implications across social phenotypic scales.

Extreme offspring ornamentation in American coots is favored by selection within families, not benefits to conspecific brood parasites.

Offspring ornamentation typically occurs in taxa with parental care, suggesting that selection arising from social interactions between parents and offspring may underlie signal evolution. American coot babies are among the most ornamented offspring found in nature, sporting vividly orange-red natal plumage, a bright red beak, and other red parts around the face and pate. Previous plumage manipulation experiments showed that ornamented plumage is favored by strong parental choice for chicks with more extreme ornamentation but left unresolved the question as to why parents show the preference. Here we explore natural patterns of variation in coot chick plumage color, both within and between families, to understand the context of parental preference and to determine whose fitness interests are served by the ornamentation. Conspecific brood parasitism is common in coots and brood parasitic chicks could manipulate hosts by tapping into parental choice for ornamented chicks. However, counter to expectation, parasitic chicks were duller (less red) than nonparasitic chicks. This pattern is explained by color variation within families: Chick coloration increases with position in the egg-laying order, but parasitic eggs are usually the first eggs a female lays. Maternal effects influence chick coloration, but coot females do not use this mechanism to benefit the chicks they lay as parasites. However, within families, chick coloration predicts whether chicks become "favorites" when parents begin control over food distribution, implicating a role for the chick ornamentation in the parental life-history strategy, perhaps as a reliable signal of a chick's size or age.

Intraspecific variation and directional casque asymmetry in adult southern cassowaries (Casuarius casuarius).

The cranial casques of modern cassowaries (Casuarius) have long intrigued researchers; however, in-depth studies regarding their morphological variation are scarce. Through visual inspection, it has been recognized that casque variability exists between conspecifics. Understanding casque variation has both evolutionary and ecological importance. Although hypothesized to be targeted by selection, intraspecific casque variation has not been quantified previously. Through a large sample of C. casuarius (n = 103), we compared casque shape (lateral and rostral views) between sexes and between individuals from non-overlapping geographical regions using two-dimensional (2D) geometric morphometrics. We found no statistically significant differences between the casque shape of females and males and few substantial shape differences between individuals from different geographic areas. Much of the intraspecific variation within C. casuarius is due to casque asymmetries (77.5% rightward deviating, 20.7% leftward deviating, and 1.8% non-deviating from the midline; n = 111), which explain the high variability of southern cassowary casque shape, particularly from the rostral aspect. Finally, we discuss how our non-significant findings implicate social selection theory, and we identify the benefits of quantifying such variation for further elucidating casque function(s) and the social biology of cassowaries.

Phenotypic Assortment Changes the Landscape of Selection.

Social interactions with conspecifics can dramatically affect an individual's fitness. The positive or negative consequences of interacting with social partners typically depend on the value of traits that they express. These pathways of social selection connect the traits and genes expressed in some individuals to the fitness realized by others, thereby altering the total phenotypic selection on and evolutionary response of traits across the multivariate phenotype. The downstream effects of social selection are mediated by the patterns of phenotypic assortment between focal individuals and their social partners (the interactant covariance, Cij', or the multivariate form, CI). Depending on the sign and magnitude of the interactant covariance, the direction of social selection can be reinforced, reversed, or erased. We report estimates of Cij' from a variety of studies of forked fungus beetles to address the largely unexplored questions of consistency and plasticity of phenotypic assortment in natural populations. We found that phenotypic assortment of male beetles based on body size or horn length was highly variable among subpopulations, but that those differences also were broadly consistent from year to year. At the same time, the strength and direction of Cij' changed quickly in response to experimental changes in resource distribution and social properties of populations. Generally, interactant covariances were more negative in contexts in which the number of social interactions was greater in both field and experimental situations. These results suggest that patterns of phenotypic assortment could be important contributors to variability in multilevel selection through their mediation of social selection gradients.

Social Selection and the Evolution of Maladaptation.

Evolution by natural selection is often viewed as a process that inevitably leads to adaptation or an increase in population fitness over time. However, maladaptation, an evolved decrease in fitness, may also occur in response to natural selection under some conditions. Social selection, which arises from the effects of social partners on fitness, has been identified as a potential cause of maladaptation, but we lack a general rule identifying when social selection should lead to a decrease in population mean fitness. Here we use a quantitative genetic model to develop such a rule. We show that maladaptation is most likely to occur when social selection is strong relative to nonsocial selection and acts in an opposing direction. In this scenario, the evolution of traits that impose fitness costs on others may outweigh evolved gains in fitness for the individual, leading to a net decrease in population mean fitness. Furthermore, we find that maladaptation may also sometimes occur when phenotypes of interacting individuals negatively covary. We outline the biological situations where maladaptation in response to social selection can be expected, provide both quantitative genetic and phenotypic versions of our derived result, and suggest what empirical work would be needed to test it. We also consider the effect of social selection on inclusive fitness and support previous work showing that inclusive fitness cannot suffer an evolutionary decrease. Taken together, our results show that social selection may decrease population mean fitness when it opposes individual-level selection, even as inclusive fitness increases.

A Synthesis of Game Theory and Quantitative Genetic Models of Social Evolution.

Two popular approaches for modeling social evolution, evolutionary game theory and quantitative genetics, ask complementary questions but are rarely integrated. Game theory focuses on evolutionary outcomes, with models solving for evolutionarily stable equilibria, whereas quantitative genetics provides insight into evolutionary processes, with models predicting short-term responses to selection. Here we draw parallels between evolutionary game theory and interacting phenotypes theory, which is a quantitative genetic framework for understanding social evolution. First, we show how any evolutionary game may be translated into two quantitative genetic selection gradients, nonsocial and social selection, which may be used to predict evolutionary change from a single round of the game. We show that synergistic fitness effects may alter predicted selection gradients, causing changes in magnitude and sign as the population mean evolves. Second, we show how evolutionary games involving plastic behavioral responses to partners can be modeled using indirect genetic effects, which describe how trait expression changes in response to genes in the social environment. We demonstrate that repeated social interactions in models of reciprocity generate indirect effects and conversely, that estimates of parameters from indirect genetic effect models may be used to predict the evolution of reciprocity. We argue that a pluralistic view incorporating both theoretical approaches will benefit empiricists and theorists studying social evolution. We advocate the measurement of social selection and indirect genetic effects in natural populations to test the predictions from game theory and, in turn, the use of game theory models to aid in the interpretation of quantitative genetic estimates.

Understanding the association between material hardship and posttraumatic stress disorder: a test of the social selection and social causation hypotheses and an exploration of gender differences.

PURPOSE: There is a well-established association between poverty and posttraumatic stress disorder (PTSD); however, little research has tested the temporality of the association. METHODS: Using data from Waves IV (2008; N = 14,800) and V (2016-2018; N = 10,685) of the National Longitudinal Study of Adolescent to Adult Health, we examined temporal associations between material hardship (a specific operationalization of poverty) and PTSD, as well as assessed for potential gender differences in associations. We conducted logistic regression and generalized structural equation modeling to examine associations between material hardship and PTSD and assess for mediation and moderation by gender. RESULTS: Prior PTSD diagnoses were associated with an increased likelihood of material hardship (OR = 1.64; 95% CI 1.21, 2.21). The indirect effect of gender on material hardship through PTSD diagnoses was significant. Prior material hardship was associated with an increased likelihood of PTSD diagnoses (OR = 1.81; 95% CI 1.35, 2.42). The indirect effect of gender on PTSD diagnoses through material hardship was significant. There was no evidence of moderation by gender for either association. CONCLUSION: Results suggest reciprocal associations between material hardship and PTSD. Economic policies, as well as improved access to evidence-based PTSD treatments, may reduce the burden of both material hardships and PTSD.

Nutrition, the visceral immune system, and the evolutionary origins of pathogenic obesity.

The global obesity epidemic is the subject of an immense, diversely specialized research effort. An evolutionary analysis reveals connections among disparate findings, starting with two well-documented facts: Obesity-associated illnesses (e.g., type-2 diabetes and cardiovascular disease), are especially common in: (i) adults with abdominal obesity, especially enlargement of visceral adipose tissue (VAT), a tissue with important immune functions; and (ii) individuals with poor fetal nutrition whose nutritional input increases later in life. I hypothesize that selection favored the evolution of increased lifelong investment in VAT in individuals likely to suffer lifelong malnutrition because of its importance in fighting intraabdominal infections. Then, when increased nutrition violates the adaptive fetal prediction of lifelong nutritional deficit, preferential VAT investment could contribute to abdominal obesity and chronic inflammatory disease. VAT prioritization may help explain several patterns of nutrition-related disease: the paradoxical increase of chronic disease with increased food availability in recently urbanized and migrant populations; correlations between poor fetal nutrition, improved childhood (catch-up) growth, and adult metabolic syndrome; and survival differences between children with marasmus and kwashiorkor malnutrition. Fats and sugars can aggravate chronic inflammation via effects on intestinal bacteria regulating gut permeability to visceral pathogens. The extremes in a nutrition-sensitive trade-off between visceral (immune-function) vs. subcutaneous (body shape) adiposity may have been favored by selection in highly stratified premedicine societies. Altered adipose allocation in populations with long histories of social stratification and malnutrition may be the result of genetic accommodation of developmental responses to poor maternal/fetal conditions, increasing their vulnerability to inflammatory disease.

Gender roles and selection mechanisms across contexts: a comparative analysis of the relationship between unemployment, self-perceived health and gender.

Health literature shows that unemployment has a gendered effect on health. However, whether men or women are more affected and why remains unclear. We assume that unemployment harms women less than men because of two mechanisms: social roles theories and health selection. First, the availability and centrality in individuals' lives of roles other than employment may reduce the detrimental effect of unemployment for women. Second, the gendered impact of unemployment on health results from the different ways selection mechanisms operate across genders. Moreover, these two mechanisms may operate differently in different contexts - for example, across different gender regimes. We investigate this by pursuing a three-step comparative approach. The analysis relies on EU-SILC data covering Italy and Sweden for 2004 to 2015 and SOEP data for Germany (1995-2017) and applies correlated dynamic random-effects probit models. While we find weak support for the role of health selection in shaping the relations between unemployment, health, and gender, our empirical results are in line with the hypothesis of a larger gendered effect in older (vs younger) cohorts, western (vs eastern) Germany and Italy (vs. Sweden). Future empirical research needs to directly address the role of gender regimes in moderating such complex relationships.

Examining Social Influences on Why We Drink: Perceived Drinking Motives in the Social Network Impact Individuals' Own Drinking Motives and Alcohol Use.

Introduction: A significant body of research has investigated the impacts of social influence and social selection on binge drinking and risk factors for binge drinking in emerging adults; however, one risk factor for binge drinking that has yet to be thoroughly investigated in this regard is drinking motives. Preliminary research suggests the motives of others may impact emerging adults' own alcohol use indirectly through their own motives (i.e., social influence). While these are important findings, research to date has been only conducted with adolescents or dyads and has not examined selection (i.e., selecting social network members with similar motives). We filled these gaps with a longitudinal egocentric social network design. Methods: Emerging adults (N = 177) completed measures on their alcohol use, drinking motives, and social networks at baseline (T1) and four-month follow-up (T2). Results: A cross-lagged panel model indicated T1 perceived network drinking motives predicted T2 participant drinking motives (for all motives but social), but T1 participant drinking motives did not predict T2 perceived network drinking motives. Path analysis indicated T1 perceived network drinking motives predicted T2 participant binge drinking frequency indirectly through T2 participant drinking motives for enhancement, coping-with-anxiety, and conformity, but not social or coping-with-depression, motives. Discussion: Results suggests drinking motives of those around emerging adults impact their own drinking motives, and indirectly, their own alcohol use. We found evidence of social influence, but not social selection. Conclusion: It appears that those around emerging adults have the capacity to influence their drinking behaviors and drinking motives.

Social selection is density dependent but makes little contribution to total selection in New Zealand giraffe weevils.

Social selection occurs when traits of interaction partners influence an individual's fitness and can alter total selection strength. However, we have little idea of what factors influence social selection's strength. Further, social selection only contributes to overall selection when there is phenotypic assortment, but simultaneous estimates of social selection and phenotypic assortment are rare. Here, we estimated social selection on body size in a wild population of New Zealand giraffe weevils (Lasiorhynchus barbicornis). We measured phenotypic assortment by body size and tested whether social selection varied with sex ratio, density and interacted with the body size of the focal individual. Social selection was limited and unaffected by sex ratio or the size of the focal individual. However, at high densities social selection was negative for both sexes, consistent with size-based competitive interactions for access to mates. Phenotypic assortment was always close to zero, indicating negative social selection at high densities will not impede the evolution of larger body sizes. Despite its predicted importance, social selection may only influence evolutionary change in specific contexts, leaving direct selection to drive evolutionary change.

Male-like female morphs in hummingbirds: the evolution of a widespread sex-limited plumage polymorphism.

Differences in the way males and females look or behave are common in animals. However, discrete variation within sexes (sex-limited polymorphism) also occurs in several vertebrate and invertebrate lineages. In birds, female-limited polymorphism (FLP) in which some females resemble males in coloration is most prominent in hummingbirds, a group known for its morphological and behavioural sexual dimorphism. Yet, it remains unclear whether this intrasexual colour variation in hummingbirds arises through direct selection on females, or indirectly as a non-adaptive byproduct resulting from selection on males. Here, we analysed specimens from more than 300 hummingbird species to determine the extent, evolutionary history and function of FLP. We found that FLP evolved independently in every major clade and occurs in nearly 25% of hummingbird species. Using phylogenetically informed analyses, we rejected non-adaptive hypotheses that FLP is the result of indirect selection or pleiotropy across species. Instead, FLP is associated with ecology, migratory status, and marginally with social dominance, suggesting a socioecological benefit to females. Ultimately, we show that FLP is not only widespread in hummingbirds and likely adaptive, but may also be useful for understanding the evolution of female ornamentation in systems under strong sexual selection.

Sexual selection and personality: Individual and group-level effects on mating behaviour in red junglefowl.

Despite increasing evidence of the importance of repeatable among-individual differences in behaviour (animal personality) in ecology and evolution, little remains known about the role of animal personalities in sexual selection. Here, we present an investigation of the hypothesis that the personalities of individuals and their sexual partners play a role in different episodes of sexual selection, and the extent to which these effects are modulated by the social environment. We first examined how two repeatable behaviours-exploration and boldness-are associated with pre- and postcopulatory sexual selection in male red junglefowl Gallus gallus, using replicate groups across three experimental sex ratio treatments. We further explored how the social environment modulates relationships between male personality and mating performance, and whether mating is assortative or disassortative with respect to exploration or boldness. Finally, we examined behavioural mechanisms linking personality with mating performance. Across all sex ratios, the fastest and slowest exploring males courted females proportionally less, and faster exploring males associated with females more and received more sexual solicitations. In female-biased groups, the fastest and slowest exploring males experienced the highest mating success and lowest sperm competition intensity. Faster exploring males also obtained more mates in female-biased groups when their competitors were, on average, slower exploring, and the proportion of matings obtained by fast-exploring males decreased with the proportion of fast-exploring males in a group, consistent with negative frequency-dependent sexual selection. While boldness did not predict mating performance, there was a tendency for individuals to mate disassortatively with respect to boldness. Collectively, our results suggest that male exploration can play a role in sexual selection, and that sexual selection on personality is complex and contingent on the social environment.