Invasion of sibmating genes in diploid and haplodiploid populations

Summary Existing genetic models of the evolution of sibmating behaviour in diploids incorporate inbreeding depression in terms of reduced fecundity of consanguineous mating pairs rather than reduced survival or fecundity of the progeny of such matings. Here we derive a model to correct this deficiency and extend the model to haplodiploids where differential effects of inbreeding in males and females is a crucial consideration. Our analyses indicate that sibmating can readily evolve in both diploids and haplodiploids in which male mating costs and inbreeding depression are reasonably low, provided there is some mechanism to permit sibmating such as siblings being reared in nests or other forms of aggregation. Our analyses also indicate that once sibmating invades, it typically will go to fixation, although sib-/randommating polymorphisms can persist in both diploids and haplodiploids if male mating costs are close to zero and inbreeding depression reduces survival by around one-third. The conditions favouring sibmating are slightly more restrictive in haplodiploids than in diploids. In light of this we may ask why we see intense sibmating in many haplodiploids such as parasitic wasps, fig wasps, ants, bark beetles and mites, and only rarely in diploid animals. The common factor could be certain kinds of aggregation behaviour that are a prerequisite for sibmating in the absence of kin recognition. Another possibility is that inbreeding depression is likely to be more severe in diploids than in haplodiploids because deleterious recessives are purged from haplodiploid populations when expressed by haploid males. Thus, lower levels of inbreeding depression might be one important reason why sibmating appears to arise more frequently in haplodiploids than diploids. Phylogenetic analysis of groups, such as bark beetles and mites, exhibiting both diploid and haplodiploid populations may be useful in elucidating the relative importance of gregarious behaviour and haplodiploidy in facilitating sibmating systems.     

Benefits of foundress associations in the paper wasp Polistes dominulus: increased productivity and survival, but no assurance of fitness returns

Successful Polistes dominulus nests can be started by one ormore nest founding queens (foundresses). Consequently, thereis much interest in the specific benefits that induce cooperationamong foundresses. Here, we experimentally demonstrate one majorbenefit of cooperation, namely that multiple foundresses increasecolony productivity. This increase is close to the value predictedby subtracting the productivity of undisturbed single-foundresscolonies from the productivity of undisturbed multiple-foundresscolonies. However, we found no evidence that an associatingfoundress' contribution to colony growth is preserved if shedisappears (assured fitness returns). Our correlational datasuggest that cooperation provides survival benefits, multiple-foundresscolonies are more likely to survive to produce offspring thanare single-foundress colonies, and individual foundresses inmultiple-foundress groups are less likely to disappear beforeworker emergence than foundresses nesting alone. Therefore,association provides substantial productivity and survival benefitsfor cooperating foundresses.     

The validity and value of inclusive fitness theory

Social evolution is a central topic in evolutionary biology, with the evolution of eusociality (societies with altruistic, non-reproductive helpers) representing a long-standing evolutionary conundrum. Recent critiques have questioned the validity of the leading theory for explaining social evolution and eusociality, namely inclusive fitness (kin selection) theory. I review recent and past literature to argue that these critiques do not succeed. Inclusive fitness theory has added fundamental insights to natural selection theory. These are the realization that selection on a gene for social behaviour depends on its effects on co-bearers, the explanation of social behaviours as unalike as altruism and selfishness using the same underlying parameters, and the explanation of within-group conflict in terms of non-coinciding inclusive fitness optima. A proposed alternative theory for eusocial evolution assumes mistakenly that workers' interests are subordinate to the queen's, contains no new elements and fails to make novel predictions. The haplodiploidy hypothesis has yet to be rigorously tested and positive relatedness within diploid eusocial societies supports inclusive fitness theory. The theory has made unique, falsifiable predictions that have been confirmed, and its evidence base is extensive and robust. Hence, inclusive fitness theory deserves to keep its position as the leading theory for social evolution.     

Quantitative genetic versions of Hamilton's rule with empirical applications

Hamilton''s theory of inclusive fitness revolutionized our understanding of the evolution of social interactions. Surprisingly, an incorporation of Hamilton''s perspective into the quantitative genetic theory of phenotypic evolution has been slow, despite the popularity of quantitative genetics in evolutionary studies. Here, we discuss several versions of Hamilton''s rule for social evolution from a quantitative genetic perspective, emphasizing its utility in empirical applications. Although evolutionary quantitative genetics offers methods to measure each of the critical parameters of Hamilton''s rule, empirical work has lagged behind theory. In particular, we lack studies of selection on altruistic traits in the wild. Fitness costs and benefits of altruism can be estimated using a simple extension of phenotypic selection analysis that incorporates the traits of social interactants. We also discuss the importance of considering the genetic influence of the social environment, or indirect genetic effects (IGEs), in the context of Hamilton''s rule. Research in social evolution has generated an extensive body of empirical work focusing—with good reason—almost solely on relatedness. We argue that quantifying the roles of social and non-social components of selection and IGEs, in addition to relatedness, is now timely and should provide unique additional insights into social evolution.     

Investment in the public good through conditional phenotypes of large effect

We investigate the evolution of an individual's willingness to invest in a public good (what we call, helping) in a patch‐structured population with limited natal dispersal. We assume that an individual's decision to invest is informed by its dispersal status: an individual makes one decision given it is native to the patch on which it breeds, and is free to make a different decision given that it is not native to the patch on which it breeds. Unlike previous work, we assume that investment in the public good, and the public good, itself, both have a large effect on individual fecundity. Kin selection analysis reveals that only extreme investment decisions (i.e. ‘always invest’ or ‘never invest’) can be evolutionarily stable. Numerical results suggest that the evolutionary instability of the ‘never invest’ phenotype (what we call, complete nonhelping) implies the evolutionary stability of ‘always invest’ (what we call, complete helping). In addition, numerical results show that bistability of extreme phenotypes is possible, indicating that the adaptive significance of altruism, in this context, is greater than has been previously recognized. Numerical results are supported by computer simulation, and results, themselves, are briefly discussed in a concluding section.     

The genetic structure of swarms and the timing of their production in the queen cycles of neotropical wasps

Kin selection theory has received some of its strongest support from analyses of within-colony conflicts between workers and queens in social insects. One of these conflicts involves the timing of queen production. In neotropical wasps, new queens are only produced by colonies with just one queen while males are produced by colonies with more queens, a pattern favoured by worker interests. We now show that new colonies, or swarms, have few queens and variable within-colony relatednesses which means that their production is not tied to new queen production. The queens in these swarms are seldom the mothers of the workers in the swarm. Therefore, either colonies producing swarms have very many queens, or queens joining daughter swarms are reproductive losers on the original colonies. As new colony production is not linked to queen production, it can occur at the ecologically optimum time, i.e. the rainy season. This disassociation between queen production and new colony production allows worker interests in sex ratios to prevail without hampering new colony production at the most favourable season, an uncoupling that may contribute to the ecological success of the Epiponini.     

The role of maternal and paternal effects in the evolution of parental quality by sexual selection

Genetic models of maternal effects and models of mate choice have focused on the evolutionary effects of variation in parental quality. There have been, however, few attempts to combine these into a single model for the evolution of sexually selected traits. We present a quantitative genetic model that considers how male and female parental quality (together or separately) affect the expression of a sexually selected offspring trait. We allow female choice of males based on this parentally affected trait and examine the evolution of mate choice, parental quality and the indicator trait. Our model reveals a number of consequences of maternal and paternal effects. (1) The force of sexual selection owing to adaptive mate choice can displace parental quality from its natural selection optimum. (2) The force of sexual selection can displace female parental quality from its natural selection optimum even when nonadaptive mate choice occurs (e.g. runaway sexual selection), because females of higher parental quality produce more attractive sons and these sons counterbalance the loss in fitness owing to over-investment in each offspring. (3) Maternal and paternal effects can provide a source of genetic variation for offspring traits, allowing evolution by sexual selection even when those traits do not show direct genetic variation (i.e. are not heritable). (4) The correlation between paternal investment and the offspring trait influenced by the parental effects can result in adaptive mate choice and lead to the elaboration of both female preference and the male sexually selected trait. When parental effects exist, sexual selection can drive the evolution of parental quality when investment increases the attractiveness of offspring, leading to the elaboration of indicator traits and higher than expected levels of parental investment.     

Indirect genetics effects and evolutionary constraint: an analysis of social dominance in red deer, Cervus elaphus

By determining access to limited resources, social dominance is often an important determinant of fitness. Thus, if heritable, standard theory predicts mean dominance should evolve. However, dominance is usually inferred from the tendency to win contests, and given one winner and one loser in any dyadic contest, the mean proportion won will always equal 0.5. Here, we argue that the apparent conflict between quantitative genetic theory and common sense is resolved by recognition of indirect genetic effects (IGEs). We estimate selection on, and genetic (co)variance structures for, social dominance, in a wild population of red deer Cervus elaphus, on the Scottish island of Rum. While dominance is heritable and positively correlated with lifetime fitness, contest outcomes depend as much on the genes carried by an opponent as on the genotype of a focal individual. We show how this dependency imposes an absolute evolutionary constraint on the phenotypic mean, thus reconciling theoretical predictions with common sense. More generally, we argue that IGEs likely provide a widespread but poorly recognized source of evolutionary constraint for traits influenced by competition.     

MHC,mate choice and heterozygote advantage in a wild social primate

Preferences for mates carrying dissimilar genes at the major histocompatibility complex (MHC) may help animals increase offspring pathogen resistance or avoid inbreeding. Such preferences have been reported across a range of vertebrates, but have rarely been investigated in social species other than humans. We investigated mate choice and MHC dynamics in wild baboons (Papio ursinus). MHC Class II DRB genes and 16 microsatellite loci were genotyped across six groups (199 individuals). Based on the survey of a key segment of the gene‐rich MHC, we found no evidence of mate choice for MHC dissimilarity, diversity or rare MHC genotypes. First, MHC dissimilarity did not differ from random expectation either between parents of the same offspring or between immigrant males and females from the same troop. Second, female reproductive success was not influenced by MHC diversity or genotype frequency. Third, population genetic structure analysis revealed equally high genotypic differentiation among troops, and comparable excess heterozygosity within troops for juveniles, at both Mhc‐DRB and neutral loci. Nevertheless, the age structure of Mhc‐DRB heterozygosity suggested higher longevity for heterozygotes, which should favour preferences for MHC dissimilarity. We propose that high levels of within‐group outbreeding, resulting from group‐living and sex‐biased dispersal, might weaken selection for MHC‐disassortative mate choice.     

Evolution of eusociality and the soldier caste in termites: a validation of the intrinsic benefit hypothesis

In termites the evolution of reproductive altruism is not based on a particularly high relatedness between nestmates. For the evolution and maintenance of the ancestral sterile soldier caste, the benefits generated by the soldiers' presence must compensate the loss of the soldiers' reproductive potential. To study the impact of soldiers on colony's fitness, we manipulated the proportion of soldiers to nonsoldiers in colonies of the dry-wood termite Cryptotermes secundus.'Soldier-less' colonies were obtained by removing soldiers and inhibiting their development with an extract of soldier heads. The colonies were set up for 1 year in experimental nests in the field. 'Soldier-less' colonies produced fewer soldiers. The reduction of soldiers neither affected colony survival nor helper growth, but fewer dispersing sexuals were produced in 'soldier-less' than in control colonies. This confirms what was only supposed so far, that in termites soldiers are maintained for their intrinsic benefit to cost ratio.     

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.     

The joint effects of kin, multilevel selection and indirect genetic effects on response to genetic selection

Kin and levels-of-selection models are common approaches for modelling social evolution. Indirect genetic effect (IGE) models represent a different approach, specifying social effects on trait values rather than fitness. We investigate the joint effect of relatedness, multilevel selection and IGEs on response to selection. We present a measure for the degree of multilevel selection, which is the natural partner of relatedness in expressions for response. Response depends on both relatedness and the degree of multilevel selection, rather than only one or the other factor. Moreover, response is symmetric in relatedness and the degree of multilevel selection, indicating that both factors have exactly the same effect. Without IGEs, the key parameter is the product of relatedness and the degree of multilevel selection. With IGEs, however, multilevel selection without relatedness can explain evolution of social traits. Thus, next to relatedness and multilevel selection, IGEs are a key element in the genetical theory of social evolution.     

Initiation of maternal effects in Lymantria dispar: Genetic and ecological components of egg provisioning

Resources supplied by mothers to offspring through the egg are known to significantly influence offspring life history traits in the gypsy moth, Lymantria dispar. The purpose of this research was to determine the relative contribution of genetics (based on familial contribution) and the nutritional environment of the parents to the mean and variance of resources supplied to the eggs. Vitellogin, the dominant egg storage protein in the gypsy moth, was selected as the focus of the study. The amount of vitellogin in individual eggs from 48 mothers reared on one of four host species, quaking aspen, chestnut oak, red oak, or pitch pine was quantified with an immunoassay. Results of a nested analysis of variance show that both genetics and parental nutritional experience make significant contributions to egg vitellogin levels. When parents were reared on quaking aspen, vitellogin levels were highest and the expression of familial variation was greatest. This study shows that polyphagy can amplify phenotypic variance in reproductive traits through the interaction between genotype and nutritional environment. To the extent that egg resources influence offspring vigor, the fitness of offspring can include a time-lagged component which arises from the interaction between the parental genotype and the parental environment. The time-lagged expression of such a maternal trait is capable of influencing the rate and direction of character evolution and the stability of local population dynamics.     

The probability of genetic parallelism and convergence in natural populations

Genomic and genetic methods allow investigation of how frequently the same genes are used by different populations during adaptive evolution, yielding insights into the predictability of evolution at the genetic level. We estimated the probability of gene reuse in parallel and convergent phenotypic evolution in nature using data from published studies. The estimates are surprisingly high, with mean probabilities of 0.32 for genetic mapping studies and 0.55 for candidate gene studies. The probability declines with increasing age of the common ancestor of compared taxa, from about 0.8 for young nodes to 0.1–0.4 for the oldest nodes in our study. Probability of gene reuse is higher when populations begin from the same ancestor (genetic parallelism) than when they begin from divergent ancestors (genetic convergence). Our estimates are broadly consistent with genomic estimates of gene reuse during repeated adaptation to similar environments, but most genomic studies lack data on phenotypic traits affected. Frequent reuse of the same genes during repeated phenotypic evolution suggests that strong biases and constraints affect adaptive evolution, resulting in changes at a relatively small subset of available genes. Declines in the probability of gene reuse with increasing age suggest that these biases diverge with time.     

A theoretical basis for measures of kin selection in subdivided populations: finite populations and localized dispersal

The analysis of kin selection in subdivided populations has been hampered by the lack of well‐defined measures of genealogical relatedness in the presence of localized dispersal. Furthermore, the usual arguments underlying the definition of game‐theoretical measures of inclusive fitness are not exact under localized dispersal. We define such measures to give the first‐order effects of selection on the probability of fixation of an allele. The derived measures of kin selection and relatedness are valid in finite populations and under localized dispersal. For the infinite island model, the resulting measure of kin selection is equivalent to a previously used measure. In other cases its definition is based on definitions of relatedness which are different from the usual ones. To illustrate the approach, we reanalyse a model with localized dispersal. We consider sex ratio evolution under sex‐specific dispersal behaviour, and the results confirm the earlier conclusion that the sex ratio is biased towards the sex with the dispersal rate closer to the optimal dispersal rate in the absence of sex‐specific dispersal behaviour.     

Estimating variance components and heritabilities in the wild: a case study using the ‘animal model’ approach

Using a genealogy containing over 1800 dams and nearly 400 sires (estimated by genetic paternity techniques), combined with maximum likelihood procedures and an ‘animal model’, we have estimated the heritabilities, genetic correlations and variance components of three morphometric traits in the Soay sheep (Ovis aries) on St Kilda, Scotland. This approach allows heritabilities to be estimated in natural populations that violate the assumptions of offspring–parent regression methods. Maternal (or paternal) effects can also be estimated under natural conditions. We demonstrate that all the traits, body weight, hind leg length and incisor arcade breadth, have low but significant heritabilities. Body weight, the trait that experiences the strongest selection, had the lowest heritability but the highest additive genetic coefficient of variation. An evolutionary response to selection is predicted. When maternal effects were not taken into consideration heritabilities were over‐estimated, although this effect was only significant in female offspring.