Parental care, cost of reproduction and reproductive skew: a general costly young model

Understanding the mechanisms by which animals resolve conflicts of interest is the key to understanding the basis of cooperation in social species. Conflict over reproductive portioning is the critical type of conflict among cooperative breeders. The costly young model represents an important, but underappreciated, idea about how an individual's intrinsic condition and cost of reproduction should affect the resolution of conflict over the distribution of reproduction within a cooperatively breeding group. However, dominant control in various forms and fixed parental care (offspring fitness dependent solely on total brood size) are assumed in previous versions of costly young models. Here, we develop a general costly young model by relaxing the restrictive assumptions of existing models. Our results show that (1) when the complete-control assumption is relaxed, the costly young model behaves very differently from the original model, and (2) when the fixed parental care assumption is relaxed, the costly young-costly care model displays similar predictions to the tug-of-war model, although the underlying mechanisms causing these similar patterns are different. These results, we believe, help simplify the seemingly divergent predictions of different reproductive skew models and highlight the importance of studying the group members' intrinsic conditions, costs of producing young, and costs of parental care for understanding breeding conflict resolution in cooperatively breeding animals.     

An assessment of Putative Sexually Antagonistic Traits in a Freshwater Amphipod Species

Sexual conflict can result in an ‘evolutionary arms race’ between males and females, with the evolution of sexual antagonistic traits used to resolve the conflict in favor of one sex over the other. We assessed the resolution of sexual conflict in a Hyalella amphipod species by manipulating putative sexually antagonistic traits in males and females and used mate‐guarding duration as our metric of conflict resolution. We discovered that large male posterior gnathopod size increased mate‐guarding duration, which suggests that it is a sexually antagonistic trait in this species. In contrast, female and male body size did not significantly affect mate‐guarding duration. Given that male posterior gnathopods show heightened condition dependence, future investigations should explore the interactive effects of sexual conflict and ecological context on trait evolution, phenotypic divergence, and speciation to elucidate the complex mechanisms involved in the evolution of biological diversity.     

The influence of mating system on the intensity of parent-offspring conflict in primates

An evolutionary conflict of interest exists between parents and their offspring over the partitioning of parental investment (PI) among siblings. When the direct fitness benefits to offspring of increased PI, outweigh the inclusive fitness costs from lost future sibling fitness, selection should favour the evolution of offspring selfishness over altruism. In theory, this conflict is heightened when females are not strictly monogamous, as current offspring should be less altruistic towards future half-siblings than they would be towards full-siblings. Using data collected on foetal growth rate (representing prenatal PI) in primates, I test the prediction from theory that the resolution of the parent-offspring conflict will be closer to the offspring's evolutionary optima in polyandrous species than in more monandrous species. Using phylogenetic comparative analysis, and controlling for allometry, I show that offspring are able to obtain more PI when the probability of future full-siblings decreases, and that this is most pronounced in taxa where there is the opportunity for direct foetal access to the maternal bloodstream. These results support the hypothesis that the resolution of prenatal PI conflict is influenced by both a species' mating system and by its placental structure.     

Parental investment and family dynamics: interactions between theory and empirical tests

The pattern of parental investment (PI) seen in nature is a product of the simultaneous resolution of conflicts of interest between the members of a family. How these conflicts are resolved depends upon the mating system, the genetic mechanism, on whether extra PI affects current or future offspring, and the behavioural mechanisms underlying supply and demand of PI. Until recently very little empirical work has been done to underpin these key determinants of conflict resolution. This review examines recent empirical progress in understanding both (1) how conflict is resolved and (2) its evolutionary consequences. How offspring demand interacts with parental supply of resources determines how conflict is resolved. Two extremes are: passive parental choice of competing offspring, relating to offspring control of resource allocation, and active parental choice relating to parental control. Although most previous empirical work has tended to conclude or assume that parents primarily control resource allocation decisions, recent studies explicitly examining predictions from theoretical analyses have shown that offspring control of resource allocation is more important than previously realised. The amount of PI supplied at resolution depends not on who controls food allocation, however, but on the nature of the supply and demand mechanisms. These have yet to be established experimentally, but a recent regression model illustrates how this could be achieved in the field. Determination of the effect of supply on demand (ESD) and the effect of demand on supply (EDS) mechanisms is critical to parent–offspring conflict theory, which has not been adequately tested empirically. There is an underlying, and until recently untested, assumption of models of intrafamilial conflict that there is genetic variation for both offspring demand and parental supply behaviours, so that the behaviours can coevolve. Recent studies on great tits, burrower bugs and mice all found evidence for genetic variation in supply and demand behaviours, but the predicted negative correlation between genes expressed in mothers and their offspring (i.e. parent–offspring coevolution), was found only for burrower bugs. The lack of a negative relationship for great tits and mice may have been a consequence of antagonistic coevolution between the sexes (sexual conflict). These studies illustrate the importance of the underlying genetics and mating system in determining conflict resolution, and point to the need for new models (especially of interbrood competition) taking differences in the genetics and the co-evolution of the ESD and EDS mechanisms into account. We also discuss the importance of the comparative approach in determining evolutionary consequences of conflicts, and use the recent work on growth costs of begging to illustrate the difficulties of measuring costs of conflict in an evolutionary currency. The recent growth in empirical work on conflicts in families illustrates an increasing, and increasingly productive, integration between theoreticians and empiricists.     

Costly punishment prevails in intergroup conflict

Understanding how societies resolve conflicts between individual and common interests remains one of the most fundamental issues across disciplines. The observation that humans readily incur costs to sanction uncooperative individuals without tangible individual benefits has attracted considerable attention as a proximate cause as to why cooperative behaviours might evolve. However, the proliferation of individually costly punishment has been difficult to explain. Several studies over the last decade employing experimental designs with isolated groups have found clear evidence that the costs of punishment often nullify the benefits of increased cooperation, rendering the strong human tendency to punish a thorny evolutionary puzzle. Here, we show that group competition enhances the effectiveness of punishment so that when groups are in direct competition, individuals belonging to a group with punishment opportunity prevail over individuals in a group without this opportunity. In addition to competitive superiority in between-group competition, punishment reduces within-group variation in success, creating circumstances that are highly favourable for the evolution of accompanying group-functional behaviours. We find that the individual willingness to engage in costly punishment increases with tightening competitive pressure between groups. Our results suggest the importance of intergroup conflict behind the emergence of costly punishment and human cooperation.     

Conflict, sticks and carrots: war increases prosocial punishments and rewards

Unlike most species, humans cooperate extensively with group members who are not closely related to them, a pattern sustained in part by punishing non-cooperators and rewarding cooperators. Because internally cooperative groups prevail over less cooperative rival groups, it is thought that violent intergroup conflict played a key role in the evolution of human cooperation. Consequently, it is plausible that propensities to punish and reward will be elevated during intergroup conflict. Using experiments conducted before, during and after the 2006 Israel-Hezbollah war, we show that, during wartime, people are more willing to pay costs to punish non-cooperative group members and reward cooperative group members. Rather than simply increasing within-group solidarity, violent intergroup conflict thus elicits behaviours that, writ large, enhance cooperation within the group, thereby making victory more likely.     

Costs and benefits of evolving under experimentally enforced polyandry or monogamy

Reproduction has classically been viewed as a predominantly cooperative process. However, over the last 20 years this concept has steadily yielded ground to one of continual conflict in which the interests of the sexes are typically discordant. Within this framework, males and females are seen to be locked into a perpetual arms race, each adaptation by one sex promoting the evolution of countermeasures in the other sex. However, under strict genetic monogamy, the interests of the sexes become congruent, and hence antagonistic coevolution does not occur. We subjected the fly Sepsis cynipsea, a species with conspicuous sexual conflict, to experimentally enforced monogamy or polyandry for 29 generations and evaluated the microevolutionary consequences. We found that there were longevity costs to females consistent with sexually antagonistic coevolution. However, our measure of female fitness, offspring emergence, did not differ between treatments, even though life-history characters such as fertility and fecundity did. Results are discussed in terms of costs and benefits of sexual selection and sexual conflict.     

Cooperation and conflict: field experiments in Northern Ireland

The idea that cohesive groups, in which individuals help each other, have a competitive advantage over groups composed of selfish individuals has been widely suggested as an explanation for the evolution of cooperation in humans. Recent theoretical models propose the coevolution of parochial altruism and intergroup conflict, when in-group altruism and out-group hostility contribute to the group''s success in these conflicts. However, the few empirical attempts to test this hypothesis do not use natural groups and conflate measures of in-group and unbiased cooperative behaviour. We conducted field experiments based on naturalistic measures of cooperation (school/charity donations and lost letters'' returns) with two religious groups with an on-going history of conflict—Catholics and Protestants in Northern Ireland. Conflict was associated with reduced donations to out-group schools and the return of out-group letters, but we found no evidence that it influences in-group cooperation. Rather, socio-economic status was the major determinant of cooperative behaviour. Our study presents a challenge to dominant perspectives on the origins of human cooperation, and has implications for initiatives aiming to promote conflict resolution and social cohesion.     

Influence of number of pollinations and pollen load size on maternal fitness costs in Collinsia heterophylla: implications for existence of a sexual conflict over timing of stigma receptivity

Costs related to pollen competition have rarely been considered, but are expected in the case of sexual conflict where male and female sexual functions have opposing evolutionary interests. In Collinsia heterophylla, delayed stigma receptivity is beneficial as it enhances pollen competition. A sexual conflict over timing of stigma receptivity has been proposed in this species as early pollination, following one-time pollinations, is advantageous to pollen donors at a cost of reduced maternal seed set (measured as seed number). In this study, we explored whether the maternal cost was still present following an additional pollination. We hypothesized that the cost is caused either by harm related to early pollen presence or by factors unrelated to harm. We performed pollinations at different stages of floral development, either one or two pollinations (24-h time lag), and varied the size of the first pollen load in the latter category. Early pollination reduced seed biomass also after two-time pollinations, suggesting a persistent maternal cost of early pollen presence. Further, pollen load size modified seed production, possibly indicating that dose-dependent harm influences the maternal cost of early fertilization. Our results strongly suggest negative effects of pollen competition on maternal fitness following early pollination, which is consistent with the existence of a sexual conflict over timing of stigma receptivity. In conclusion, we propose that much could be gained if more plant studies considered the potential for fitness costs in relation to sexual conflict, particularly those investigating pollen-pistil interactions.     

The ecology of cooperative breeding behaviour

Ecology is a fundamental driving force for the evolutionary transition from solitary living to breeding cooperatively in groups. However, the fact that both benign and harsh, as well as stable and fluctuating, environments can favour the evolution of cooperative breeding behaviour constitutes a paradox of environmental quality and sociality. Here, we propose a new model – the dual benefits framework – for resolving this paradox. Our framework distinguishes between two categories of grouping benefits – resource defence benefits that derive from group‐defended critical resources and collective action benefits that result from social cooperation among group members – and uses insider–outsider conflict theory to simultaneously consider the interests of current group members (insiders) and potential joiners (outsiders) in determining optimal group size. We argue that the different grouping benefits realised from resource defence and collective action profoundly affect insider–outsider conflict resolution, resulting in predictable differences in the per capita productivity, stable group size, kin structure and stability of the social group. We also suggest that different types of environmental variation (spatial vs. temporal) select for societies that form because of the different grouping benefits, thus helping to resolve the paradox of why cooperative breeding evolves in such different types of environments.     

Facing the crowd: intruder pressure,within‐group competition,and the resolution of conflicts over group‐membership

Recent theory in social evolution has been mainly concerned with competition and cooperation within social groups of animals and their impact on the stability of those groups. Much less attention has been paid to conflicts arising as a result of solitary floaters (outsiders) attempting to join groups of established residents (insiders). We model such conflicts over group‐membership using a demographically explicit approach in which the rates of births and deaths in a population determine the availability of group‐vacancies and the number of floaters competing over these vacancies. We find that the outcome of within‐group competition, reflected in the partitioning of reproduction among group members, exerts surprisingly little influence on the resolution of insider‐outsider conflict. The outcome of such conflict is also largely unaffected by differences in resource holding potential between insiders and outsiders. By contrast, whether or not groups form is mainly determined by demographic factors (variation in vital rates such as fecundity and mortality) and the resulting population dynamics. In particular, at high floater densities territory defense becomes too costly, and groups form because insiders give in to the intruder pressure imposed on them by outsiders. We emphasize the importance of insider‐outsider conflicts in social evolution theory and highlight avenues for future research.     

Two girls for every boy: The effects of group size and composition on the reproductive success of male and female white-faced capuchins

Many factors have been hypothesized to affect the size and adult sex ratios of primate groups and these, in turn, have been argued to influence birth rates. Using park-wide census data collected on a population of capuchins over a 25-year period, we examined whether group size and adult sex ratio affect the per capita reproductive success of male and female white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica. We found that the reproductive success of females (measured as the observed minus the expected ratio of immatures to adult females in the group) decreased with increasing group size, whereas that of males was independent of group size. The proportion of adult males residing in groups had significant, yet contrasting effects on males and females. Male reproductive success was negatively associated with the proportion of males residing in groups whereas female reproductive success increased with the proportion of males. The latter finding supports the intersexual conflict hypothesis, which suggests that a conflict of interest occurs between males and females over adult sex ratios. The effects of group size and composition on the reproductive success of capuchins, a male-dispersed omnivorous species, are similar to those reported for howlers, a bisexually-dispersed folivorous species. One common factor between these taxa is that groups with low ratios of males to females are at greater risk of takeovers and resultant infanticide. Our results suggest that regardless of dietary preference and dispersal pattern, the threat of infanticide can constrain primate group size and composition.     

Sexual conflict in wing size and shape in Drosophila melanogaster

Intralocus sexual conflict occurs when opposing selection pressures operate on loci expressed in both sexes, constraining the evolution of sexual dimorphism and displacing one or both sexes from their optimum. We eliminated intralocus conflict in Drosophila melanogaster by limiting transmission of all major chromosomes to males, thereby allowing them to win the intersexual tug‐of‐war. Here, we show that this male‐limited (ML) evolution treatment led to the evolution (in both sexes) of masculinized wing morphology, body size, growth rate, wing loading, and allometry. In addition to more male‐like size and shape, ML evolution resulted in an increase in developmental stability for males. However, females expressing ML chromosomes were less developmentally stable, suggesting that being ontogenetically more male‐like was disruptive to development. We suggest that sexual selection over size and shape of the imago may therefore explain the persistence of substantial genetic variation in these characters and the ontogenetic processes underlying them.     

Adaptation and the genetics of social behaviour

In recent years much progress has been made towards understanding the selective forces involved in the evolution of social behaviour including conflicts over reproduction among group members. Here, I argue that an important additional step necessary for advancing our understanding of the resolution of potential conflicts within insect societies is to consider the genetics of the behaviours involved. First, I discuss how epigenetic modifications of behaviour may affect conflict resolution within groups. Second, I review known natural polymorphisms of social organization to demonstrate that a lack of consideration of the genetic mechanisms involved may lead to erroneous explanations of the adaptive significance of behaviour. Third, I suggest that, on the basis of recent genetic studies of sexual conflict in Drosophila, it is necessary to reconsider the possibility of within-group manipulation by means of chemical substances (i.e. pheromones). Fourth, I address the issue of direct versus indirect genetic effects, which is of particular importance for the study of behaviour in social groups. Fifth, I discuss the issue of how a genetic influence on dominance hierarchies and reproductive division of labour can have secondary effects, for example in the evolution of promiscuity. Finally, because the same sets of genes (e.g. those implicated in chemical signalling and the responses that are triggered) may be used even in species as divergent as ants, cooperative breeding birds and primates, an integration of genetic mechanisms into the field of social evolution may also provide unifying ideas.     

Parent–Offspring Conflict in Primates

Parent–offspring conflict (POC) theory (Trivers, 1974) has stimulated controversy in evolutionary biology and behavioral ecology. The theory has been criticized by some primate behavioral researchers on both conceptual and empirical grounds. First, it has been argued that it would be more advantageous to mothers and offspring to agree over the allocation of parental investment and to cooperate rather than to disagree and engage in conflict. Second, some studies have provided data suggesting that primate mothers and offspring engage in behavioral conflict over the scheduling of their activities rather than parental investment. In reality, parent–offspring interactions are likely to involve both cooperation and conflict, and the hypothesis that mothers and infants squabble over the scheduling of their activities is not incompatible with POC theory. Furthermore, the predictions of POC theory are supported by a number of empirical studies of primates. POC theory has enhanced our understanding of the dynamics of parent–offspring relationships in many animal species, and it is very likely that future studies of primates will continue to benefit from using POC theory as an explanatory framework.     

Evolutionary stability and the rarity of grandmothering

The provision of intergenerational care, via the Grandmother Hypothesis, has been implicated in the evolution of postfertile longevity, particularly in humans. However, if grandmothering does provide fitness benefits, a key question is why has it evolved so infrequently? We investigate this question with a combination of life‐history and evolutionary game theory. We derive simple eligibility and stability thresholds, both of which must be satisfied if intergenerational care is first to evolve and then to persist in a population. As one threshold becomes easier to fulfill, the other becomes more difficult, revealing a conflict between the two. As such, we suggest that, in fact, we should expect the evolution of grandmothering to be rare.     

Natural 'poor start' does not increase mortality over the lifetime

Poor nutrition and other challenges during infancy can impose delayed costs, and it has been proposed that expression of costs during adulthood should involve increased mortality rather than reduced reproduction. Demonstrations of delayed costs come mostly from experimental manipulations of the diet and hormones of captive infants of short-lived species, and we know very little about how natural poor starts in life affect wild animals over their lifetimes. In the blue-footed booby, sibling conflict obliges younger brood members to grow up suffering aggressive subordination, food deprivation and elevated stress hormone, but surviving fledglings showed no deficit in reproduction over the first 5-10 years. A study of 7927 individuals from two-fledgling and singleton broods from 20 cohorts found no significant evidence of a higher rate of mortality nor a lower rate of recruitment in younger fledglings than in elder fledglings or singletons at any age over the 20 year lifespan. Development of boobies may be buffered against the three challenges of subordination. Experimental challenges to neonates that result in delayed costs have usually been more severe, more prolonged and more abruptly suspended, and it is unclear which natural situations they mimic.     

Sex-dependent selection differentially shapes genetic variation on and off the guppy Y chromosome

Because selection is often sex-dependent, alleles can have positive effects on fitness in one sex and negative effects in the other, resulting in intralocus sexual conflict. Evolutionary theory predicts that intralocus sexual conflict can drive the evolution of sex limitation, sex-linkage, and sex chromosome differentiation. However, evidence that sex-dependent selection results in sex-linkage is limited. Here, we formally partition the contribution of Y-linked and non-Y-linked quantitative genetic variation in coloration, tail, and body size of male guppies (Poecilia reticulata)-traits previously implicated as sexually antagonistic. We show that these traits are strongly genetically correlated, both on and off the Y chromosome, but that these correlations differ in sign and magnitude between both parts of the genome. As predicted, variation in attractiveness was found to be associated with the Y-linked, rather than with the non-Y-linked component of genetic variation in male ornamentation. These findings show how the evolution of Y-linkage may be able to resolve sexual conflict. More generally, they provide unique insight into how sex-specific selection has the potential to differentially shape the genetic architecture of fitness traits across different parts of the genome.     

Does reproductive isolation evolve faster in larger populations via sexually antagonistic coevolution?

Sexual conflict over reproductive investment can lead to sexually antagonistic coevolution and reproductive isolation. It has been suggested that, unlike most models of allopatric speciation, the evolution of reproductive isolation through sexually antagonistic coevolution will occur faster in large populations as these harbour greater levels of standing genetic variation, receive larger numbers of mutations and experience more intense sexual selection. We tested this in bruchid beetle populations (Callosobruchus maculatus) by manipulating population size and standing genetic variability in replicated lines derived from founders that had been released from sexual conflict for 90 generations. We found that after 19 generations of reintroduced sexual conflict, none of our treatments had evolved significant overall reproductive isolation among replicate lines. However, as predicted, measures of reproductive isolation tended to be greater among larger populations. We discuss our methodology, arguing that reproductive isolation is best examined by performing a matrix of allopatric and sympatric crosses whereas measurement of divergence requires crosses with a tester line.