Sex differences in dispersal and the evolution of helping and harming

In this article, we explore the impact of sex-biased dispersal on local relatedness and on selection for helping and harming behavior among males and females. We show that in a patch-structured population, when there is a marked sex bias in dispersal, selection will almost always favor harming behavior among individuals of the sex more prone to dispersal. This result holds regardless of the effects of mating skew or overlapping generations. Selection may well also favor helping behavior among individuals of the philopatric sex, particularly if there is generational overlap, but this is less likely to occur if individuals of the philopatric sex compete more intensely for fewer breeding opportunities. In this last case, if generational overlap is low and mating skew pronounced, the result may be selection for harming behavior among both males and females. In general, the rate of dispersal and the level of relatedness among individuals of one sex do not reliably predict their level of helping or harming behavior; selection on either males or females depends on the dispersal of both sexes.     

Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal

Hamilton demonstrated that the evolution of cooperative behaviour is favoured by high relatedness, which can arise through kin discrimination or limited dispersal (population viscosity). These two processes are likely to operate with limited overlap: kin discrimination is beneficial when variation in relatedness is higher, whereas limited dispersal results in less variable and higher average relatedness, reducing selection for kin discrimination. However, most empirical work on eukaryotes has focused on kin discrimination. To address this bias, we analysed how kin discrimination and limited dispersal interact to shape helping behaviour across cooperatively breeding vertebrates. We show that kin discrimination is greater in species where the: (i) average relatedness in groups is lower and more variable; (ii) effect of helpers on breeders reproductive success is greater; and (iii) probability of helping was measured, rather than the amount of help provided. There was also an interaction between these effects with the correlation between the benefits of helping and kin discrimination being stronger in species with higher variance in relatedness. Overall, our results suggest that kin discrimination provides a route to indirect benefits when relatedness is too variable within groups to favour indiscriminate cooperation.     

Evolution of reproductive effort in viscous populations: the importance of population dynamics

I present two ecological models for the evolution of reproductive effort in viscous populations with empty sites. In contrast with previous studies, I show that limited dispersal needs not have a positive effect on the evolutionarily stable allocation of resources to fecundity versus survival. Rather, depending on the feedback between the trait and the population dynamics, population viscosity may have no effect or even lead to a decrease in the evolutionarily stable reproductive effort when individuals can degrade their environment during their lifetime. I show that the different evolutionary outcomes can be explained by the asymmetry in the level of kin competition resulting from investing into juveniles or into adults.     

Population viscosity can promote the evolution of altruistic sterile helpers and eusociality

Because it increases relatedness between interacting individuals, population viscosity has been proposed to favour the evolution of altruistic helping. However, because it increases local competition between relatives, population viscosity may also act as a brake for the evolution of helping behaviours. In simple models, the kin selected fecundity benefits of helping are exactly cancelled out by the cost of increased competition between relatives when helping occurs after dispersal. This result has lead to the widespread view, especially among people working with social organisms, that special conditions are required for the evolution of altruism. Here, we re-examine this result by constructing a simple population genetic model where we analyse whether the evolution of a sterile worker caste (i.e. an extreme case of altruism) can be selected for by limited dispersal. We show that a sterile worker caste can be selected for even under the simplest life-cycle assumptions. This has relevant consequences for our understanding of the evolution of altruism in social organisms, as many social insects are characterized by limited dispersal and significant genetic population structure.     

Kin competition,natal dispersal and the moulding of senescence by natural selection

Most theoretical models for the evolution of senescence have assumed a very large, well mixed population. Here, we investigate how limited dispersal and kin competition might influence the evolution of ageing by deriving indicators of the force of selection, similar to Hamilton (Hamilton 1966 J. Theor. Biol. 12, 12–45). Our analytical model describes how the strength of selection on survival and fecundity changes with age in a patchy population, where adults are territorial and a fraction of juveniles disperse between territories. Both parent–offspring competition and sib competition then affect selection on age-specific life-history traits. Kin competition reduces the strength of selection on survival. Mutations increasing mortality in some age classes can even be favoured by selection, but only when fecundity deteriorates rapidly with age. Population structure arising from limited dispersal however selects for a broader distribution of reproduction over the lifetime, potentially slowing down reproductive senescence. The antagonistic effects of limited dispersal on age schedules of fecundity and mortality cast doubts on the generality of conditions allowing the evolution of ‘suicide genes’ that increase mortality rates without other direct pleiotropic effects. More generally, our model illustrates how limited dispersal and social interactions can indirectly produce patterns of antagonistic pleiotropy affecting vital rates at different ages.     

Evolution of helping and harming in heterogeneous populations

There has been much interest in understanding how demographic factors can mediate social evolution in viscous populations. Here, we examine the impact of heterogeneity in patch quality--that is, the availability of reproductive resources for each breeder--upon the evolution of helping and harming behaviors. We find that, owing to a cancellation of relatedness and kin competition effects, the evolution of obligate and facultative helping and harming is not influenced by the degree of viscosity in populations characterized by either spatial or temporal heterogeneity in patch quality. However, facultative helping and harming may be favored when there is both spatial and temporal heterogeneity in patch quality, with helping and harming being favored in both high-quality and low-quality patches. We highlight the prospect for using kin selection theory to explain within-population variation in social behavior, and point to the need for further theoretical and empirical investigation of this topic.     

Reproductive effort in viscous populations

Abstract.— Here I study a kin selection model of reproductive effort, the allocation of resources to fecundity versus survival, in a patch-structured population. Breeding females remain in the same patch for life. Offspring have costly, partial long-distance dispersal and compete for breeding sites, which become vacant upon the death of previous occupants. The main result is that the evolutionarily stable reproductive effort decreases as offspring dispersal rate increases. The result can be understood as follows: In a well-mixed population with global competition, neither adults nor juveniles compete with relatives, but in a patch-structured population with dispersal restricted to the juvenile phase, juveniles experience relatively less competition with relatives than adults, thus making juveniles relatively more valuable. Because this asymmetry between adults and juveniles decreases with the dispersal rate, so does the evolutionarily stable level of allocation to fecundity.     

Cooperation‐mediated plasticity in dispersal and colonization

Kin selection theory predicts that costly cooperative behaviors evolve most readily when directed toward kin. Dispersal plays a controversial role in the evolution of cooperation: dispersal decreases local population relatedness and thus opposes the evolution of cooperation, but limited dispersal increases kin competition and can negate the benefits of cooperation. Theoretical work has suggested that plasticity of dispersal, where individuals can adjust their dispersal decisions according to the social context, might help resolve this paradox and promote the evolution of cooperation. Here, we experimentally tested the hypothesis that conditional dispersal decisions are mediated by a cooperative strategy: we quantified the density‐dependent dispersal decisions and subsequent colonization efficiency from single cells or groups of cells among six genetic strains of the unicellular Tetrahymena thermophila that differ in their aggregation level (high, medium, and low), a behavior associated with cooperation strategy. We found that the plastic reaction norms of dispersal rate relative to density differed according to aggregation level: highly aggregative genotypes showed negative density‐dependent dispersal, whereas low‐aggregation genotypes showed maximum dispersal rates at intermediate density, and medium‐aggregation genotypes showed density‐independent dispersal with intermediate dispersal rate. Dispersers from highly aggregative genotypes had specialized long‐distance dispersal phenotypes, contrary to low‐aggregation genotypes; medium‐aggregation genotypes showing intermediate dispersal phenotype. Moreover, highly aggregation genotypes showed evidence for beneficial kin‐cooperation during dispersal. Our experimental results should help to resolve the evolutionary conflict between cooperation and dispersal: cooperative individuals are expected to avoid kin‐competition by dispersing long distances, but maintain the benefits of cooperation by dispersing in small groups.     

Demography of source—sink populations and the evolution of ecological niches

Summary The demography of populations living in variable environments is an important factor molding the evolution of ecological niches, for it determines the relative strength of selection pressures on adaptations to different habitats. Here I consider a coarse-grained environment consisting of two habitat types and investigate how the selection pressure on reproductive success in different habitats depends on their quality and frequency and the dispersal pattern. The results suggest that selection on adaptations to optimal habitats will usually be stronger than on adaptations to poor habitats and the ecological niche will thus tend to be an evolutionarily conservative character. It is because under the habitat choice or limited dispersal that seem to prevail in natural populations, more individuals encounter the better habitat than would be expected solely on the basis of its relative area. This bias results in reduced selection pressure on reproductive success in the poorer habitat. With habitat choice or limited dispersal, selection pressure on reproductive success in the poorer habitat may exceed that on reproductive success in the better habitat only if the poorer habitat is much more frequent in the environment than the better habitat and the difference in their quality is not large.     

Kin-biased dispersal behaviour in the mango shield scale, Milviscutulus mangiferae

When fitness decreases with increasing density in a habitat, dispersal behaviour is expected to evolve. To avoid competition between kin, dispersal behaviour based on kin recognition should be more likely to occur when the individuals in a habitat are closely related. I tested this prediction with first-instar larvae (crawlers) of the mango shield scale, Milviscutulus mangiferae. The body size of adult females, a measure of fecundity, was larger when only one female was present on a leaf than when two were present. When I placed two crawlers on a leaf, they emigrated more frequently when they were siblings than when they were not related. I discuss the implication of the results for kin recognition in thelytokous parthenogenetic animals. Copyright 2000 The Association for the Study of Animal Behaviour.     

Constraints on the origin and maintenance of genetic kin recognition

Kin-recognition mechanisms allow helping behaviors to be directed preferentially toward related individuals, and could be expected to evolve in many cases. However, genetic kin recognition requires a genetic polymorphism on which recognition is based, and kin discriminating behaviors will affect the evolution of such polymorphism. It is unclear whether genetic polymorphisms used in kin recognition should be maintained by extrinsic selection pressures or not, as opposite conclusions have been reached by analytical one-locus models and simulations exploring different population structures. We analyze a two-locus model in a spatially subdivided population following the island model of dispersal between demes of finite size. We find that in the absence of mutation, selection eliminates polymorphism in most cases, except with extreme spatial structure and low recombination. With mutation, the population may reach a stable limit cycle over which both loci are polymorphic; however, the average frequency of conditional helping can be high only under strong structure and low recombination. Finally, we review evidence for extrinsic selection maintaining polymorphism on which kin recognition is based.     

EVOLUTION OF HELPING AND HARMING IN HETEROGENEOUS GROUPS

Social groups are often composed of individuals who differ in many respects. Theoretical studies on the evolution of helping and harming behaviors have largely focused upon genetic differences between individuals. However, nongenetic variation between group members is widespread in natural populations, and may mediate differences in individuals’ social behavior. Here, we develop a framework to study how variation in individual quality mediates the evolution of unconditional and conditional social traits. We investigate the scope for the evolution of social traits that are conditional on the quality of the actor and/or recipients. We find that asymmetries in individual quality can lead to the evolution of plastic traits with different individuals expressing helping and harming traits within the same group. In this context, population viscosity can mediate the evolution of social traits, and local competition can promote both helping and harming behaviors. Furthermore, asymmetries in individual quality can lead to the evolution of competition‐like traits between clonal individuals. Overall, we highlight the importance of asymmetries in individual quality, including differences in reproductive value and the ability to engage in successful social interactions, in mediating the evolution of helping and harming behaviors.     

The evolution of trans-generational altruism: kin selection meets niche construction

A cornerstone result of sociobiology states that limited dispersal can induce kin competition to offset the kin selected benefits of altruism. Several mechanisms have been proposed to circumvent this dilemma but all assume that actors and recipients of altruism interact during the same time period. Here, this assumption is relaxed and a model is developed where individuals express an altruistic act, which results in posthumously helping relatives living in the future. The analysis of this model suggests that kin selected benefits can then feedback on the evolution of the trait in a way that promotes altruistic helping at high rates under limited dispersal. The decoupling of kin competition and kin selected benefits results from the fact that by helping relatives living in the future, an actor is helping individuals that are not in direct competition with itself. A direct consequence is that behaviours which actors gain by reducing the common good of present and future generations can be opposed by kin selection. The present model integrates niche-constructing traits with kin selection theory and delineates demographic and ecological conditions under which altruism can be selected for; and conditions where the 'tragedy of the commons' can be reduced.     

Microevolution of S-allele frequencies in wild cherry populations: respective impacts of negative frequency dependent selection and genetic drift

Negative frequency dependent selection (NFDS) is supposed to be the main force controlling allele evolution at the gametophytic self-incompatibility locus (S-locus) in strictly outcrossing species. Genetic drift also influences S-allele evolution. In perennial sessile organisms, evolution of allelic frequencies over two generations is mainly shaped by individual fecundities and spatial processes. Using wild cherry populations between two successive generations, we tested whether S-alleles evolved following NFDS qualitative and quantitative predictions. We showed that allelic variation was negatively correlated with parental allelic frequency as expected under NFDS. However, NFDS predictions in finite population failed to predict more than half S-allele quantitative evolution. We developed a spatially explicit mating model that included the S-locus. We studied the effects of self-incompatibility and local drift within populations due to pollen dispersal in spatially distributed individuals, and variation in male fecundity on male mating success and allelic frequency evolution. Male mating success was negatively related to male allelic frequency as expected under NFDS. Spatial genetic structure combined with self-incompatibility resulted in higher effective pollen dispersal. Limited pollen dispersal in structured distributions of individuals and genotypes and unequal pollen production significantly contributed to S-allele frequency evolution by creating local drift effects strong enough to counteract the NFDS effect on some alleles.     

Fluctuating populations and kin interaction in mammals

Kin selection in animals favors less aggressive interaction among related individuals. If the genetic relatedness among neighbors changes with population structure and density, behavioral interaction may also change according to the population structure. Charnov and Finerty proposed a hypothesis that kin selection in voles causes population cycles if the relatedness among neighbors decreases as density increases. Field experiments have recently tested this hypothesis. Furthermore, field studies of social interaction in voles have increased in number, so that the effects of kinship on reproductive success can be reviewed. These studies indicate that although kin interaction might be an important factor affecting social behavior and reproductive success in voles, the relationships both between kinship and degree of amicable behavior or reproductive rate, and between relatedness among neighbors and population density, are far less simple than had been supposed.     

Mating system, philopatry and patterns of kinship in the cooperatively breeding subdesert mesite Monias benschi

In the first molecular study of a member of the threatened avian family, Mesitornithidae, we used nine polymorphic microsatellite loci to elucidate parentage, patterns of within-group kinship and occurrence of extra-group paternity in the subdesert mesite Monias benschi, of southwest Madagascar. We found this cooperatively breeding species to have a very fluid mating system. There was evidence of genetic monogamy and polygynandry: of the nine groups with multiple offspring, six contained one breeding pair with unrelated helpers and three contained multiple male and female breeders with related helpers. Although patterns of within-group kinship varied, there was a strong positive relationship between group size and relatedness, suggesting that groups form by natal philopatry. There was also a strong positive correlation between within-sex and between-sex relatedness, indicating that unlike most cooperatively breeding birds, philopatry involved both sexes. In contrast to predictions of kin selection and reproductive skew models, all monogamous groups contained unrelated individuals, while two of the three polygynandrous groups were families. Moreover, although between-group variation in seasonal reproductive success was related to within-group female relatedness, relatedness among males and between the sexes had no bearing on a group's reproductive output. While kin selection may underlie helping behaviour in females, factors such as direct long-term fitness benefits of group living probably determine helping in males. Of the 14 offspring produced by fully sampled groups, at least two were sired by males from neighbouring groups: one by a breeding male and one by a nonbreeding male, suggesting that males may augment their reproductive success through extra-group paternity.     

No evidence for divergence in male harmfulness or female resistance in response to changes in the opportunity for dispersal

The outcome of sexual conflict can depend on the social environment, as males respond to changes in the inclusive fitness payoffs of harmfulness and harm females less when they compete with familiar relatives. Theoretical models also predict that if limited male dispersal predictably enhances local relatedness while maintaining global competition, kin selection can produce evolutionary divergences in male harmfulness among populations. Experimental tests of these predictions, however, are rare. We assessed rates of dispersal in female and male seed beetles Callosobruchus maculatus, a model species for studies of sexual conflict, in an experimental setting. Females dispersed significantly more often than males, but dispersing males travelled just as far as dispersing females. Next, we used experimental evolution to test whether limiting dispersal allowed the action of kin selection to affect divergence in male harmfulness and female resistance. Populations of C. maculatus were evolved for 20 and 25 generations under one of three dispersal regimens: completely free dispersal, limited dispersal and no dispersal. There was no divergence among treatments in female reproductive tract scarring, ejaculate size, mating behaviour, fitness of experimental females mated to stock males or fitness of stock females mated to experimental males. We suggest that this is likely due to insufficient strength of kin selection rather than a lack of genetic variation or time for selection. Limited dispersal alone is therefore not sufficient for kin selection to reduce male harmfulness in this species, consistent with general predictions that limited dispersal will only allow kin selection if local relatedness is independent of the intensity of competition among kin.     

The Impact of male reproductive skew on kin structure and sociality in multi‐male groups

Patterns of within‐group relatedness are expected to affect the prospects for cooperation among group members through kin selection. It has long been established that dispersal patterns determine the availability of kin and there is ample evidence of matrilineal kin biases in social behavior across primate species. However, in 1979, Jeanne Altmann¹ suggested that mating patterns also influence the structure of within‐group relatedness; high male reproductive skew and the frequent replacement of breeding males leads to relatively high levels of paternal relatedness and age‐structured paternal sibships within groups. As a consequence of frequent replacement of breeding males, relatedness among offspring of a given female will be reduced to the half‐ rather than full‐sibling level. Depending on the number of sires and degree of relatedness among mothers, members of the same birth cohort may be as closely related as maternal siblings. If animals are able to recognize their paternal kin and exhibit biases in favor of them, this may influence the distribution of cooperation and the intensity of competition within groups of primates. Here, I summarize the evidence that serves as the basis for Altmann's predictions and review evidence regarding whether or not the availability of paternal kin also leads to paternal kin bias among primates.     

Demography, altruism, and the benefits of budding

It is now widely appreciated that competition between kin inhibits the evolution of altruism. In standard population genetics models, it is difficult for indiscriminate altruism towards social partners to be favoured at all. The reason is that while limited dispersal increases the kinship of social partners it also intensifies local competition. One solution that has received very little attention is if individuals disperse as groups (budding dispersal), as this relaxes local competition without reducing kinship. Budding behaviour is widespread through all levels of biological organization, from early protocellular life to cooperatively breeding vertebrates. We model the effects of individual dispersal, budding dispersal, soft selection and hard selection to examine the conditions under which altruism is favoured. More generally, we examine how these various demographic details feed into relatedness and scale of competition parameters that can be included into Hamilton's rule.     

Fine‐scale genetic structure and helping decisions in a cooperatively breeding bird

In animal societies, characteristic demographic and dispersal patterns may lead to genetic structuring of populations, generating the potential for kin selection to operate. However, even in genetically structured populations, social interactions may still require kin discrimination for cooperative behaviour to be directed towards relatives. Here, we use molecular genetics and long‐term field data to investigate genetic structure in an adult population of long‐tailed tits Aegithalos caudatus, a cooperative breeder in which helping occurs within extended kin networks, and relate this to patterns of helping with respect to kinship. Spatial autocorrelation analyses reveal fine‐scale genetic structure within our population, such that related adults of either sex are spatially clustered following natal dispersal, with relatedness among nearby males higher than that among nearby females, as predicted by observations of male‐biased philopatry. This kin structure creates opportunities for failed breeders to gain indirect fitness benefits via redirected helping, but crucially, most close neighbours of failed breeders are unrelated and help is directed towards relatives more often than expected by indiscriminate helping. These findings are consistent with the effective kin discrimination mechanism known to exist in long‐tailed tits and support models identifying kin selection as the driver of cooperation.