It takes two to tango: reproductive skew and social correlates of male mating success in a lek-breeding bird

Variance in reproductive success among individuals is a defining characteristic of many social vertebrates. Yet, our understanding of which male attributes contribute to reproductive success is still fragmentary in most cases. Male–male reproductive coalitions, where males jointly display to attract females, are of particular interest to evolutionary biologists because one male appears to forego reproduction to assist the social partner. By examining the relationship between social behaviour and reproductive success, we can elucidate the proximate function of coalitions in the context of mate choice. Here, we use data from a 4-year study of wire-tailed manakins (Pipra filicauda) to provide molecular estimates of reproductive skew and to test the hypothesis that male–male social interactions, in the context of coordinated displays, positively influence a male''s reproductive success. More specifically, we quantify male–male social interactions using network metrics and predict that greater connectivity will result in higher relative reproductive success. Our data show that four out of six leks studied had significant reproductive skew, with success apportioned to very few individuals in each lek. Metrics of male social affiliations derived from our network analysis, especially male connectivity, measured as the number of males with whom the focal male has extended interactions, were strong predictors of the number of offspring sired. Thus, network connectivity is associated with male fitness in wire-tailed manakins. This pattern may be the result of shared cues used by both sexes to assess male quality, or the result of strict female choice for coordinated display behaviour.     

Experimentally induced variation in neuroendocrine processes affects male reproductive behaviour,sperm characteristics and social interactions

While extensive research has focused on how social interactions evolve, the fitness consequences of the neuroendocrine mechanisms underlying these interactions have rarely been documented, especially in the wild. Here, we measure how the neuroendocrine mechanisms underlying male behaviour affect mating success and sperm competition in the ocellated wrasse (Symphodus ocellatus). In this species, males exhibit three alternative reproductive types. “Nesting males” provide parental care, defend territories and form cooperative associations with unrelated “satellites,” who cheat by sneaking fertilizations but help by reducing sperm competition from “sneakers” who do not cooperate or provide care. To measure the fitness consequences of the mechanisms underlying these social interactions, we used “phenotypic engineering” that involved administering an androgen receptor antagonist (flutamide) to wild, free‐living fish. Nesting males treated with flutamide shifted their aggression from sneakers to satellite males and experienced decreased submissiveness by sneaker males (which correlated with decreased nesting male mating success). The preoptic area (POA), a region controlling male reproductive behaviours, exhibited dramatic down‐regulation of androgen receptor (AR) and vasotocin 1a receptor (V1aR) mRNA following experimental manipulation of androgen signalling. We did not find a direct effect of the manipulation on male mating success, paternity or larval production. However, variation in neuroendocrine mechanisms generated by the experimental manipulation was significantly correlated with changes in behaviour and mating success: V1aR expression was negatively correlated with satellite‐directed aggression, and expression of its ligand arginine vasotocin (AVT) was positively correlated with courtship and mating success, thus revealing the potential for sexual selection on these mechanisms.     

Hamilton's inclusive fitness in finite-structured populations

Hamilton''s formulation of inclusive fitness has been with us for 50 years. During the first 20 of those years attention was largely focused on the evolutionary trajectories of different behaviours, but over the past 20 years interest has been growing in the effect of population structure on the evolution of behaviour and that is our focus here. We discuss the evolutionary journey of the inclusive-fitness effect over this epoch, nurtured as it was in an essentially homogeneous environment (that of ‘transitive’ structures) having to adapt in different ways to meet the expectations of heterogeneous structures. We pay particular attention to the way in which the theory has managed to adapt the original constructs of relatedness and reproductive value to provide a formulation of inclusive fitness that captures a precise measure of allele-frequency change in finite-structured populations.     

Social networks in the lek-mating wire-tailed manakin (Pipra filicauda)

How social structure interacts with individual behaviour and fitness remains understudied despite its potential importance to the evolution of cooperation. Recent applications of network theory to social behaviour advance our understanding of the role of social interactions in various contexts. Here we applied network theory to the social system of lek-mating wire-tailed manakins (Pipra filicauda, Pipridae, Aves). We analysed the network of interactions among males in order to begin building a comparative framework to understand where coordinated display behaviour lies along the continuum from solitary to obligately cooperative dual-male displays in the family Pipridae. Network degree (the number of links from a male to others) ranged from 1 to 10, with low mean and high variance, consistent with the theory for the evolution of cooperation within social networks. We also assessed factors that could predict social and reproductive success of males. Four network metrics, degree, eigenvector centrality, information centrality and reach, some of which assess circuitous as well as the shortest (geodesic) paths of male connectivity, predicted male social rise. The duration of a male's territorial tenure during the 4 years of the study predicted his probability of siring offspring.     

Adaptations for social cognition in the primate brain

Studies of the factors affecting reproductive success in group-living monkeys have traditionally focused on competitive traits, like the acquisition of high dominance rank. Recent research, however, indicates that the ability to form cooperative social bonds has an equally strong effect on fitness. Two implications follow. First, strong social bonds make individuals'' fitness interdependent and the ‘free-rider’ problem disappears. Second, individuals must make adaptive choices that balance competition and cooperation—often with the same partners. The proximate mechanisms underlying these behaviours are only just beginning to be understood. Recent results from cognitive and systems neuroscience provide us some evidence that many social and non-social decisions are mediated ultimately by abstract, domain-general neural mechanisms. However, other populations of neurons in the orbitofrontal cortex, striatum, amygdala and parietal cortex specifically encode the type, importance and value of social information. Whether these specialized populations of neurons arise by selection or through developmental plasticity in response to the challenges of social life remains unknown. Many brain areas are homologous and show similar patterns of activity in human and non-human primates. In both groups, cortical activity is modulated by hormones like oxytocin and by the action of certain genes that may affect individual differences in behaviour. Taken together, results suggest that differences in cooperation between the two groups are a matter of degree rather than constituting a fundamental, qualitative distinction.     

Strong inbreeding depression in male mating behaviour in a poeciliid fish

The magnitude of inbreeding depression is often larger in traits closely related to fitness, such as survival and fecundity, compared to morphological traits. Reproductive behaviour is also closely associated with fitness, and therefore expected to show strong inbreeding depression. Despite this, little is known about how reproductive behaviour is affected by inbreeding. Here we show that one generation of full‐sib mating results in a decrease in male reproductive performance in the least killifish (Heterandria formosa). Inbred males performed less gonopodial thrusts and thrust attempts than outbred males (δ = 0.38). We show that this behaviour is closely linked with fitness as gonopodial performance correlates with paternity success. Other traits that show inbreeding depression are offspring viability (δ = 0.06) and maturation time of males (δ = 0.19) and females (δ = 0.14). Outbred matings produced a female biased sex ratio whereas inbred matings produced an even sex ratio.     

High indirect fitness benefits for helpers across the nesting cycle in the tropical paper wasp Polistes canadensis

Explaining the evolution of helping behaviour in the eusocial insects where nonreproductive (“worker”) individuals help raise the offspring of other individuals (“queens”) remains one of the most perplexing phenomena in the natural world. Polistes paper wasps are popular study models, as workers retain the ability to reproduce: such totipotency is likely representative of the early stages of social evolution. Polistes is thought to have originated in the tropics, where seasonal constraints on reproductive options are weak and social groups are effectively perennial. Yet, most Polistes research has focused on nontropical species, where seasonality causes family groups to disperse; cofoundresses forming new nests the following spring are often unrelated, leading to the suggestion that direct fitness through nest inheritance is key in the evolution of helping behaviour. Here, we present the first comprehensive genetic study of social structure across the perennial nesting cycle of a tropical Polistes—Polistes canadensis. Using both microsatellites and newly developed single nucleotide polymorphism markers, we show that adult cofoundresses are highly related and that brood production is monopolized by a single female across the nesting cycle. Nonreproductive cofoundresses in tropical Polistes therefore have the potential to gain high indirect fitness benefits as helpers from the outset of group formation, and these benefits persist through the nesting cycle. Direct fitness may have been less important in the origin of Polistes sociality than previously suggested. These findings stress the importance of studying a range of species with diverse life history and ecologies when considering the evolution of reproductive strategies.     

The adaptive value of sociality in mammalian groups

According to behavioural ecology theory, sociality evolves when the net benefits of close association with conspecifics exceed the costs. The nature and relative magnitude of the benefits and costs of sociality are expected to vary across species and habitats. When sociality is favoured, animals may form groups that range from small pair-bonded units to huge aggregations. The size and composition of social groups have diverse effects on morphology and behaviour, ranging from the extent of sexual dimorphism to brain size, and the structure of social relationships. This general argument implies that sociality has fitness consequences for individuals. However, for most mammalian species, especially long-lived animals like primates, there are sizable gaps in the chain of evidence that links sociality and social bonds to fitness outcomes. These gaps reflect the difficulty of quantifying the cumulative effects of behavioural interactions on fitness and the lack of information about the nature of social relationships among individuals in most taxa. Here, I review what is known about the reproductive consequences of sociality for mammals.     

A genetic analysis of breeding success in the cooperative meerkat (Suricata suricatta)

Measurement of reproductive skew in social groups is fundamentalto understanding the evolution and maintenance of sociality,as it determines the immediate fitness benefits to helpers ofstaying and helping in a group. However, there is a lack ofstudies in natural populations that provide reliable measuresof reproductive skew and the correlates of reproductive success,particularly in vertebrates. We present results of a study thatuses a combination of field and genetic (microsatellite) dataon a cooperatively breeding mongoose, the meerkat (Suricatasuricatta). We sampled 458 individuals from 16 groups at twosites and analyzed parentage of pups in 110 litters with upto 12 microsatellites. We show that there is strong reproductiveskew in favor of dominants, but that the extent of skew differsbetween the sexes and between different sites. Our data suggestthat the reproductive skew arises from incest avoidance andreproductive suppression of the subordinates by the dominants.     

Agonistic behaviour of female Tegenaria atrica in the presence of different aged spiderlings

The agonistic behaviour of adult female T. atrica increases with increasing age of spiderlings until 80 days post-emergence, then decreases. In all cases, cannibalism of spiderlings increases markedly after completion of their pre-dispersal period with a correlation between the switch of behaviour, from tolerance to cannibalism, and a modification of individual’s cuticular compounds. Experiments that compare spiderlings weight and mobility indicate that female agonistic behaviour are always low with spiderlings in pre-dispersal period, and high with spiderlings in post-dispersal period. Female reproductive state and the weight/mobility of spiderlings are not the only factors controlling the adult female’s agonistic behaviour towards spiderlings on her web, as tactochemical information plays an important role in modulating agonistic behaviour after close contact between female spiders and spiderlings. The agonistic behaviour of females appears to correspond with a change in the increase of polar compound levels (methylesters and fatty acids) and the decrease of apolar compound levels (hydrocarbons) in spiderlings of different ages.     

Position in the laying order has sex-specific consequences for reproductive success in adult black-headed gulls

Mothers who produce multiple offspring within one reproductive attempt often allocate resources differentially; some maternally derived substances are preferentially allocated to last-produced offspring and others to first-produced offspring. The combined effect of these different allocation regimes on the overall fitness of offspring produced early or late in the sequence is not well understood, partly because production order is often coupled with birth order, making it difficult-to-separate effects of pre-natal maternal allocation from those of post-natal social environments. In addition, very little is known about the influence of laying order on fitness in later life. In this study, we used a semi-natural captive colony of black-headed gulls to test whether an offspring's position in the laying order affected its early-life survival and later-life reproductive success, independent of its hatching order. Later-laid eggs were less likely to hatch, but among those that did, survival to adulthood was greater than that of first-laid eggs. In adulthood, the laying order of females did not affect their likelihood of breeding in the colony, but male offspring hatched from last-laid eggs were significantly less likely to gain a breeding position than earlier-laid males. In contrast, later-laid female parents hatched lower proportions of their clutches than first-laid females, but hatching success was unrelated to the laying order of male parents. Our results indicate that gull mothers induce complex and sex-specific effects on both the early survival of their offspring and on long-term reproductive success through laying order effects among eggs of the same breeding attempt.     

Individual heterogeneity in fitness in a long‐lived herbivore

Heterogeneity in the intrinsic quality and nutritional condition of individuals affects reproductive success and consequently fitness. Black brant (Branta bernicla nigricans) are long‐lived, migratory, specialist herbivores. Long migratory pathways and short summer breeding seasons constrain the time and energy available for reproduction, thus magnifying life‐history trade‐offs. These constraints, combined with long lifespans and trade‐offs between current and future reproductive value, provide a model system to examine the role of individual heterogeneity in driving life‐history strategies and individual heterogeneity in fitness. We used hierarchical Bayesian models to examine reproductive trade‐offs, modeling the relationships between within‐year measures of reproductive energy allocation and among‐year demographic rates of individual females breeding on the Yukon‐Kuskokwim Delta, Alaska, using capture–recapture and reproductive data from 1988 to 2014. We generally found that annual survival tended to be buffered against variation in reproductive investment, while breeding probability varied considerably over the range of clutch size‐laying date combinations. We provide evidence for relationships between breeding probability and clutch size, breeding probability and nest initiation date, and an interaction between clutch size and initiation date. Average lifetime clutch size also had a weak positive relationship with apparent survival probability. Our results support the use of demographic buffering strategies for black brant. These results also indirectly suggest associations among environmental conditions during growth, fitness, and energy allocation, highlighting the effects of early growth conditions on individual heterogeneity, and subsequently, lifetime reproductive investment.     

Future social rank: forecasting status in the green anole (Anolis carolinensis)

Predicting the future social standing of an individual without aggressive social interaction may seem contradictory, as formation of social rank depends on agonistic interactions. In the lizard Anolis carolinensis, predicting social rank is possible using latency to eyespot formation (sympathetic darkening of postorbital skin from green to black during stressful agonistic interactions), because they form more rapidly in male lizards that become dominant. Darkened eyespots also inhibit aggressive behavior. As the timing of eyespot formation appears to be an important component of stress responsiveness and future social status, we hypothesized that a proactive disposition toward non-aggressive behavior, such as feeding and courtship, would be associated with aggressiveness. We assessed the relationship between rank and the temporal dynamics of eyespot formation, latencies to aggressive display, feeding, and reproductive behavior. Male lizards that became dominant were faster to respond to all types of stimuli tested (aggression, feeding, and courtship). The temporal dynamics of the neuroendocrine stress response appear to influence the motivation for behavioral response. Animals that recover from stress more quickly also eat, court, and fight more readily. In summary, this work suggests that latencies to aggressive, reproductive, and feeding behavior, as well as eyespot signals, are reliable predictors of future social status of individual male A. carolinensis.     

Morph‐dependent fitness and directional change of morph frequencies over time in a Dutch population of Common buzzards Buteo buteo

How genetic polymorphisms are maintained in a population is a key question in evolutionary ecology. Previous work on a plumage colour polymorphism in the common buzzard Buteo buteo suggested heterozygote advantage as the mechanism maintaining the co‐existence of three morphs (light, intermediate and dark). We took advantage of 20 years of life‐history data collected in a Dutch population to replicate earlier studies on the relationship between colour morph and fitness in this species. We examined differences between morphs in adult apparent survival, breeding success, annual number of fledglings produced and cumulative reproductive success. We found that cumulative reproductive success differed among morphs, with the intermediate morph having highest fitness. We also found assortative mating for colour morph, whereby assortative pairs were more likely to produce offspring and had longer‐lasting pair bonds than disassortative pairs. Over the 20‐year study period, the proportion of individuals with an intermediate morph increased. This apparent evolutionary change did not just arise from selection on individual phenotypes, but also from fitness benefits of assortative mating. The increased frequency of intermediates might also be due to immigration or drift. We hypothesize that genetic variation is maintained through spatial variation in selection pressures. Further studies should investigate morph‐dependent dispersal behaviour and habitat choice.     

Fitness conflicts and the costs of sociality in communal egg layers: a theoretical model and empirical tests

Individuals within complex social groups often experience reduced reproduction owing to coercive or suppressive actions of other group members. However, the nature of social and ecological environments that favour individual acceptance of such costs of sociality is not well understood. Taxa with short periods of direct social interaction, such as some communal egg layers, are interesting models for study of the cost of social interaction because opportunities to control reproduction of others are limited to brief periods of reproduction. To understand the conditions under which communal egg layers are in fitness conflict and thus likely to influence each other's reproduction, we develop an optimality model involving a brood guarding 'host' and a nonguarding disperser, or 'egg dumper'. The model shows that when, where intermediate-sized broods have highest survival, lifetime inclusive fitnesses of hosts and dumpers are often optimized with different numbers of dumped eggs. We hypothesize that resolution of this conflict may involve attempts by one party to manipulate the other's reproduction. To test model predictions we used a lace bug (Heteroptera: Tingidae) that shows both hosts and egg dumpers as well as increased offspring survival in response to communal egg laying. We found that egg-dumping lace bugs oviposit a number of eggs that very closely matches predicted fitness optimum for hosts rather than predicted optimum of dumpers. This result suggests that dumpers pay a social cost for communal egg laying, a cost that may occur through host suppression of dumper reproduction. Although dumper allocation of eggs is thus sub-optimal for dumpers, previous models show that the decision to egg dump is nevertheless evolutionarily stable, possibly because hosts permit just enough dumper oviposition to encourage commitment to the behaviour.     

Leadership and Path Characteristics during Walks Are Linked to Dominance Order and Individual Traits in Dogs

Movement interactions and the underlying social structure in groups have relevance across many social-living species. Collective motion of groups could be based on an “egalitarian” decision system, but in practice it is often influenced by underlying social network structures and by individual characteristics. We investigated whether dominance rank and personality traits are linked to leader and follower roles during joint motion of family dogs. We obtained high-resolution spatio-temporal GPS trajectory data (823,148 data points) from six dogs belonging to the same household and their owner during 14 30–40 min unleashed walks. We identified several features of the dogs'' paths (e.g., running speed or distance from the owner) which are characteristic of a given dog. A directional correlation analysis quantifies interactions between pairs of dogs that run loops jointly. We found that dogs play the role of the leader about 50–85% of the time, i.e. the leader and follower roles in a given pair are dynamically interchangable. However, on a longer timescale tendencies to lead differ consistently. The network constructed from these loose leader–follower relations is hierarchical, and the dogs'' positions in the network correlates with the age, dominance rank, trainability, controllability, and aggression measures derived from personality questionnaires. We demonstrated the possibility of determining dominance rank and personality traits of an individual based only on its logged movement data. The collective motion of dogs is influenced by underlying social network structures and by characteristics such as personality differences. Our findings could pave the way for automated animal personality and human social interaction measurements.     

Parental provisioning behaviour plays a key role in linking personality with reproductive success

Repeatable behavioural traits (‘personality’) have been shown to covary with fitness, but it remains poorly understood how such behaviour–fitness relationships come about. We applied a multivariate approach to reveal the mechanistic pathways by which variation in exploratory and aggressive behaviour is translated into variation in reproductive success in a natural population of blue tits, Cyanistes caeruleus. Using path analysis, we demonstrate a key role for provisioning behaviour in mediating the link between personality and reproductive success (number of fledged offspring). Aggressive males fed their nestlings at lower rates than less aggressive individuals. At the same time, their low parental investment was associated with increased female effort, thereby positively affecting fledgling production. Whereas male exploratory behaviour was unrelated to provisioning behaviour and reproductive success, fast-exploring females fed their offspring at higher rates and initiated breeding earlier, thus increasing reproductive success. Our findings provide strong support for specific mechanistic pathways linking components of behavioural syndromes to reproductive success. Importantly, relationships between behavioural phenotypes and reproductive success were obscured when considering simple bivariate relationships, underlining the importance of adopting multivariate views and statistical tools as path analysis to the study of behavioural evolution.     

Estimating individual fitness in the wild using capture–recapture data

The concept of Darwinian fitness is central in evolutionary ecology, and its estimation has motivated the development of several approaches. However, measuring individual fitness remains challenging in empirical case studies in the wild. Measuring fitness requires a continuous monitoring of individuals from birth to death, which is very difficult to get in part because individuals may or may not be controlled at each reproductive event and recovered at death. Imperfect detection hampers keeping track of mortality and reproductive events over the whole lifetime of individuals. We propose a new statistical approach to estimate individual fitness while accounting for imperfect detection. Based on hidden process modelling of longitudinal data on marked animals, we show that standard metrics to quantify fitness, namely lifetime reproductive success, individual growth rate and lifetime individual contribution to population growth, can be extended to cope with imperfect detection inherent to most monitoring programs in the wild. We illustrate our approach using data collected on individual roe deer in an intensively monitored population.     

Structure and function in mammalian societies

Traditional interpretations of the evolution of animal societies have suggested that their structure is a consequence of attempts by individuals to maximize their inclusive fitness within constraints imposed by their social and physical environments. In contrast, some recent re-interpretations have argued that many aspects of social organization should be interpreted as group-level adaptations maintained by selection operating between groups or populations. Here, I review our current understanding of the evolution of mammalian societies, focusing, in particular, on the evolution of reproductive strategies in societies where one dominant female monopolizes reproduction in each group and her offspring are reared by other group members. Recent studies of the life histories of females in these species show that dispersing females often have little chance of establishing new breeding groups and so are likely to maximize their inclusive fitness by helping related dominants to rear their offspring. As in eusocial insects, increasing group size can lead to a progressive divergence in the selection pressures operating on breeders and helpers and to increasing specialization in their behaviour and life histories. As yet, there is little need to invoke group-level adaptations in order to account for the behaviour of individuals or the structure of mammalian groups.