Kin Selection Models Research Articles

Why Skew Selection, a Model of Parental Exploitation, Should Replace Kin Selection

In his 1964 paper, William Hamilton wrote that inclusive fitness trumps direct fitness if, and only if, the effect of interactions among siblings on their parent’s fitness is ‘zero’. Kin selection models have succeeded only because they have ignored the fact that, if an altruist dies saving two siblings, the ‘zero impact on their parent’s fitness’ constraint is violated. Imagine a parent with three offspring. If two offspring drown, parental fitness is 1. On the other hand, if one altruistic offspring dies saving its two drowning siblings, parental fitness doubles to 2. Thus, direct fitness trumps inclusive fitness as an explanation for the evolution of altruism. In other words, parents that produce some portion of altruistic offspring willing to die to save some of their siblings (who would die without the intervention of the altruist) will realize greater fitness than parents producing no altruists. Skew selection, a bioeconomic extension of Michael Ghiselin’s (1974) parental exploitation model, is presented to explain the evolution of altruism from a direct fitness point of view.

Why kin and group selection models may not be enough to explain human other-regarding behaviour

Models of kin or group selection usually feature only one possible fitness transfer. The phenotypes are either to make this transfer or not to make it and for any given fitness transfer, Hamilton's rule predicts which of the two phenotypes will spread. In this article we allow for the possibility that different individuals or different generations face similar, but not necessarily identical possibilities for fitness transfers. In this setting, phenotypes are preference relations, which concisely specify behaviour for a range of possible fitness transfers (rather than being a specification for only one particular situation an animal or human can be in). For this more general set-up, we find that only preference relations that are linear in fitnesses can be explained using models of kin selection and that the same applies to a large class of group selection models. This provides a new implication of hierarchical selection models that could in principle falsify them, even if relatedness—or a parameter for assortativeness—is unknown. The empirical evidence for humans suggests that hierarchical selection models alone are not enough to explain their other-regarding or altruistic behaviour.

Strong Reciprocity and the Comparative Method

Abstract Ernst Fehr and his collaborators have argued that traditional explanations of human cooperation cannot account for strong reciprocity. They provide substantial empirical evidence that strong reciprocity is an important phenomenon that cannot be explained by the traditional models of kin selection or reciprocal altruism. In this note, however, I argue that it will be difficult to test specific adaptive explanations of strong reciprocity because it is apparently unique to humans. Consequently, it is difficult to employ the comparative method, which is one of biology’s best tools for testing adaptationist claims.

Helping effort in a dominance hierarchy

In many cooperatively breeding species, group members form a dominance hierarchy or queue to inherit the position of breeder. Models aimed at understanding individual variation in helping behavior, however, rarely take into account the effect of dominance rank on expected future reproductive success and thus the potential direct fitness costs of helping. Here we develop a kin-selection model of helping behavior in multimember groups in which only the highest ranking individual breeds. Each group member can invest in the dominant's offspring at a cost to its own survivorship. The model predicts that lower ranked subordinates, who have a smaller probability of inheriting the group, should work harder than higher ranked subordinates. This prediction holds regardless of whether the intrinsic mortality rate of subordinates increases or decreases with rank. The prediction does not necessarily hold, however, where the costs of helping are higher for lower ranked individuals: a situation that may be common in vertebrates. The model makes two further testable predictions: that the helping effort of an individual of given rank should be lower in larger groups, and the reproductive success of dominants should be greater where group members are more closely related. Empirical evidence for these predictions is discussed. We argue that the effects of rank on stable helping effort may explain why attempts to correlate individual helping effort with relatedness in cooperatively breeding species have met with limited success.

A kin-selection approach to the resolution of sex-ratio conflict between mates

We investigate an instance of conflict between mates over the sex ratio of their brood. We construct a kin-selection model for the evolution of the sex ratio assuming local resource competition (LRC) among females. We explore two basic scenarios: (a) the case where parents make simultaneous sex-ratio decisions (the simultaneous allocation model); and (b) the case where parental sex-ratio decisions occur one after the other (the sequential allocation model). In the simultaneous investment model, resolution of the conflict between mates depends on the extent to which relative paternal contribution influences the brood sex ratio. In the sequential allocation model, fathers determine primary sex-ratio through fertilization bias; then mothers modify the paternal sex-ratio decision by adjusting the level of investment of some resource that contributes to offspring survival. Under the sequential model, a compromise is always achieved; however this compromise favours one perspective or the other, depending on the extent to which maternal investment influences offspring survival.

Kin selection and coefficients of relatedness in family-structured populations with inbreeding

We consider family specific fitnesses that depend on mixed strategies of two basic phenotypes or behaviours. Pairwise interactions are assumed, but they are restricted to occur between sibs. To study the change in frequency of a rare mutant allele, we consider two different forms of weak selection, one applied through small differences in genotypic values determining individual mixed strategies, the other through small differences in viabilities according to the behaviours chosen by interacting sibs. Under these two specific forms of weak selection, we deduce conditions for initial increase in frequency of a rare mutant allele for autosomal genes in the partial selfing model as well as autosomal and sex-linked genes in the partial sib-mating model with selection before mating or selection after mating. With small differences in mixed strategies, we show that conditions for protection of a mutant allele are tantamount to conditions for initial increase in frequency obtained in additive kin selection models. With particular reference to altruism versus selfishness, we provide explicit ranges of values for the selfing or sib-mating rate based on a fixed cost–benefit ratio and the dominance scheme that allow the spreading of a rare mutant allele into the population. This study confirms that more inbreeding does not necessarily promote the evolution of altruism. Under the hypothesis of small differences in viabilities, the situation is much more intricate unless an additive model is assumed. In general however, conditions for initial increase in frequency of a mutant allele can be obtained in terms of fitness effects that depend on the genotypes of interacting individuals or their mates and generalized conditional coefficients of relatedness according to the inbreeding condition of the interacting individuals.

The details of food-sharing interactions – their cost in social prestige

I agree with Gurven that costly signaling can explain food-sharing phenomena. However, costly signaling may also explain the role of food sharing in deterring rivals. Details of food-sharing interactions may reveal gains and losses in the social prestige of the interacting parties. The evolutionary models of kin selection and of reciprocal altruism are unstable and should be avoided.

The robustness of Hamilton's rule with inbreeding and dominance: kin selection and fixation probabilities under partial sib mating.

Assessing the validity of Hamilton's rule when there is both inbreeding and dominance remains difficult. In this article, we provide a general method based on the direct fitness formalism to address this question. We then apply it to the question of the evolution of altruism among diploid full sibs and among haplodiploid sisters under inbreeding resulting from partial sib mating. In both cases, we find that the allele coding for altruism always increases in frequency if a condition of the form rb>c holds, where r depends on the rate of sib mating alpha but not on the frequency of the allele, its phenotypic effects, or the dominance of these effects. In both examples, we derive expressions for the probability of fixation of an allele coding for altruism; comparing these expressions with simulation results allows us to test various approximations often made in kin selection models (weak selection, large population size, large fecundity). Increasing alpha increases the probability of fixation of recessive altruistic alleles (h<1/2), while it can increase or decrease the probability of fixation of dominant altruistic alleles (h>1/2).

Seed provisioning within holly fruits: test of the hierarchical model

Seed provisioning within holly Ilex aquifolium fruits was examined after a controlled pollination experiment to obtain full-sibs. The distribution of dry mass in stony endocarp and endosperm was determined according to the rank in the size hierarchy of the sibs within fruit. Resources were more equally distributed among sibs in the endocarps than in the endosperms, which might suggest sibling competition among endosperms and no evidences of competition in the tissue controlled by the maternal sporophyte. When the sibs are ranked by size, seed provisioning fit reasonably with the hierarchical model. Differences among consecutive sibs increased down the hierarchy, the second sib in the size hierarchy was less variable in resource acquisition than the others, and the disparity in the distribution of resources among sibs decreased with fruit size increases. These results seems to be in accordance with both kin selection model and hierarchical model, which indicates at the same time control of resource provisioning by the maternal plant and differences in vigour among sibs.

The Robustness of Hamilton's Rule with Inbreeding and Dominance: Kin Selection and Fixation Probabilities under Partial Sib Mating

Assessing the validity of Hamilton’s rule when there is both inbreeding and dominance remains difficult. In this article, we provide a general method based on the direct fitness formalism to address this question. We then apply it to the question of the evolution of altruism among diploid full sibs and among haplodiploid sisters under inbreeding resulting from partial sib mating. In both cases, we find that the allele coding for altruism always increases in frequency if a condition of the form $$rb> c$$ holds, where r depends on the rate of sib mating α but not on the frequency of the allele, its phenotypic effects, or the dominance of these effects. In both examples, we derive expressions for the probability of fixation of an allele coding for altruism; comparing these expressions with simulation results allows us to test various approximations often made in kin selection models (weak selection, large population size, large fecundity). Increasing α increases the probability of fixation of recessive altruistic alleles ($$h< 1/ 2$$), while it can increase or decrease the probability of fixation of dominant altruistic alleles ($$h> 1/ 2$$).

Low mating frequency of queens in the stingless bee Scaptotrigona postica 1 and worker maternity of males

Kin selection models of intracolonial conflict over the maternity of males predict that social hymenopteran workers should favour the production of sons and nephews over brothers when the effective mating frequency (me) of the queen is low (me 2. Stingless bees have been used to support these models in that me within the group is considered low and workers are thought often to monopolise the parentage of males. We genetically analysed 20 worker and 20 male pupae from each of 10 colonies of the stingless bee Scaptotrigona postica (= Scaptotrigona aff. depilis) using six microsatellite loci and demonstrate queen monandry in eight nests and apparent low me in the other two. However, four colonies contained an additional matriline, possibly due to queen supersedure (serial polygyny), which complicated their genetic structure. Across colonies, workers were responsible for the maternity of 13% of all males. These data are broadly in agreement with predictions from kin selection theory, though the question remains open as to why workers do not secure a greater share of male maternity in this and other stingless bee species in which workers are more closely related to nephews than brothers.

Helping effort and future fitness in cooperation animal societies.

Little attention has been paid to a conspicuous and universal feature of animal societies: the variation between individuals in helping effort. Here, we develop a multiplayer kin-selection model that assumes that subordinates face a trade-off because current investment in help reduces their own future reproductive success. The model makes two predictions: (i) subordinates will work less hard the closer they are to inheriting breeding status; and (ii) for a given dominance rank, subordinates will work less hard in larger groups. The second prediction reflects the larger pay-off from inheriting a larger group. Both predictions were tested through a field experiment on the paper wasp Polistes dominulus. First, we measured an index of helping effort among subordinates, then we removed successive dominants to reveal the inheritance ranks of the subordinates: their positions in the queue to inherit dominance. We found that both inheritance rank and group size had significant effects on helping effort, in the manner predicted by our model. The close match between our theoretical and empirical results suggests that individuals adjust their helping effort according to their expected future reproductive success. This relationship has probably remained hidden in previous studies that have focused on variation in genetic relatedness.

Sex Ratio Conflict and Worker Production in Eusocial Hymenoptera

The best known of the conflicts occurring in eusocial Hymenoptera is queen-worker conflict over sex ratio. So far, sex ratio theory has mostly focused on optimal investment in the production of male versus female sexuals, neglecting the investment in workers. Increased investment in workers decreases immediate sexual productivity but increases expected future colony productivity. Thus, an important issue is to determine the queen's and workers' optimal investment in each of the three castes (workers, female sexuals, and male sexuals), taking into account a possible trade-off between production of female sexuals and workers (both castes developing from diploid female eggs). Here, we construct a simple and general kin selection model that allows us to calculate the evolutionarily stable investments in the three castes, while varying the identity of the party controlling resource allocation (relative investment in workers, female sexuals, and male sexuals). Our model shows that queens and workers favor the investment in workers that maximizes lifetime colony productivity of sexual males and females, whatever the colony kin structure. However, worker production is predicted to be at this optimum only if one of the two parties has complete control over resource allocation, a situation that is evolutionarily unstable because it strongly selects the other party to manipulate sex allocation in its favor. Queens are selected to force workers to raise all the males by limiting the number of eggs they lay, whereas workers should respond to egg limitation by raising a greater proportion of the female eggs into sexual females rather than workers as a means to attain a more female-biased sex allocation. This tug-of-war between queens and workers leads to a stable equilibrium where sex allocation is between the queen and worker optima and the investment in workers is below both parties' optimum. Our model further shows that, under most conditions, female larvae are in strong conflict with queens and workers over their developmental fate because they value their own reproduction more than that of siblings. With the help of our model, we also investigate how variation in queen number and number of matings per queen affect the level of conflict between queens, workers, and larvae and ultimately the allocation of resource in the three castes. Finally, we make predictions that allow us to test which party is in control of sex allocation and caste determination.

Sex Ratio Conflict and Worker Production in Eusocial Hymenoptera

The best known of the conflicts occurring in eusocial Hymenoptera is queen‐worker conflict over sex ratio. So far, sex ratio theory has mostly focused on optimal investment in the production of male versus female sexuals, neglecting the investment in workers. Increased investment in workers decreases immediate sexual productivity but increases expected future colony productivity. Thus, an important issue is to determine the queen’s and workers’ optimal investment in each of the three castes (workers, female sexuals, and male sexuals), taking into account a possible trade‐off between production of female sexuals and workers (both castes developing from diploid female eggs). Here, we construct a simple and general kin selection model that allows us to calculate the evolutionarily stable investments in the three castes, while varying the identity of the party controlling resource allocation (relative investment in workers, female sexuals, and male sexuals). Our model shows that queens and workers favor the investment in workers that maximizes lifetime colony productivity of sexual males and females, whatever the colony kin structure. However, worker production is predicted to be at this optimum only if one of the two parties has complete control over resource allocation, a situation that is evolutionarily unstable because it strongly selects the other party to manipulate sex allocation in its favor. Queens are selected to force workers to raise all the males by limiting the number of eggs they lay, whereas workers should respond to egg limitation by raising a greater proportion of the female eggs into sexual females rather than workers as a means to attain a more female‐biased sex allocation. This tug‐of‐war between queens and workers leads to a stable equilibrium where sex allocation is between the queen and worker optima and the investment in workers is below both parties’ optimum. Our model further shows that, under most conditions, female larvae are in strong conflict with queens and workers over their developmental fate because they value their own reproduction more than that of siblings. With the help of our model, we also investigate how variation in queen number and number of matings per queen affect the level of conflict between queens, workers, and larvae and ultimately the allocation of resource in the three castes. Finally, we make predictions that allow us to test which party is in control of sex allocation and caste determination.

Kin Selection and Natal Dispersal in an Age-Structured Population

We examine the effect of iteroparity on the evolution of dispersal for a species living in a stable but fragmented habitat. We use a kin selection model that incorporates the effects of demographic stochasticity on the local age structure and age-specific genetic identities. We consider two cases: when the juvenile dispersal rate is allowed to change with maternal age and when it is not. In the latter case, we find that the unconditional evolutionarily stable dispersal rate increases when the adult survival rate increases. Two antagonistic forces act upon the evolution of age-specific dispersal rates. First, when the local age structure varies between patches of habitat, the intensity of competition between adults and juveniles in the natal patch is, on average, lower for offspring born to older senescent mothers. This selects for decreasing dispersal with maternal age. Second, offspring born to older parents are on average more related to other juveniles in the same patch and they experience a higher intensity of kin competition, which selects for increasing dispersal with maternal age. We show that the evolutionary outcome results from a balance between these two opposing forces, which depends on the amount of variance in age structure among sub-populations.

Kin Selection and Parasite Evolution: Higher and Lower Virulence with Hard and Soft Selection

Conventional models predict that low genetic relatedness among parasites that coinfect the same host leads to the evolution of high parasite virulence. Such models assume adaptive responses to hard selection only. We show that if soft selection is allowed to operate, low relatedness leads instead to the evolution of low virulence. With both hard and soft selection, low relatedness increases the conflict among coinfecting parasites. Although parasites can only respond to hard selection by evolving higher virulence and overexploiting their host, they can respond to soft selection by evolving other adaptations, such as interference, that prevent overexploitation. Because interference can entail a cost, the host may actually be underexploited, and virulence will decrease as a result of soft selection. Our analysis also shows that responses to soft selection can have a much stronger effect than responses to hard selection. After hard selection has raised virulence to a level that is an evolutionarily stable strategy, the population, as expected, cannot be invaded by more virulent phenotypes that respond only to hard selection. The population remains susceptible to invasion by a less virulent phenotype that responds to soft selection, however. Thus, hard and soft selection are not just alternatives. Rather, soft selection is expected to prevail and often thwart the evolution of virulence in parasites. We review evidence from several parasite systems and find support for soft selection. Most of the examples involve interference mechanisms that indirectly prevent the evolution of higher virulence. We recognize that hard selection for virulence is more difficult to document, but we take our results to suggest that a kin selection model with soft selection may have general applicability.

Reproductive effort in viscous populations.

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.

Cooperative Reproduction in Ituri Forest Hunter-Gatherers: Who Cares for Efe Infants?

Cooperative Reproduction in Ituri Forest Hunter-Gatherers: Who Cares for Efe Infants?

REPRODUCTIVE EFFORT IN VISCOUS POPULATIONS

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.Corresponding Editor: C. Boggs

Local Competition, Inbreeding, and the Evolution of Sex-Biased Dispersal.

Using game theory, we developed a kin-selection model to investigate the consequences of local competition and inbreeding depression on the evolution of natal dispersal. Mating systems have the potential to favor strong sex biases in dispersal because sex differences in potential reproductive success affect the balance between local resource competition and local mate competition. No bias is expected when local competition equally affects males and females, as happens in monogamous systems and also in polygynous or promiscuous ones as long as female fitness is limited by extrinsic factors (breeding resources). In contrast, a male-biased dispersal is predicted when local mate competition exceeds local resource competition, as happens under polygyny/promiscuity when female fitness is limited by intrinsic factors (maximal rate of processing resources rather than resources themselves). This bias is reinforced by among-sex interactions: female philopatry enhances breeding opportunities for related males, while male dispersal decreases the chances that related females will inbreed. These results meet empirical patterns in mammals: polygynous/promiscuous species usually display a male-biased dispersal, while both sexes disperse in monogamous species. A parallel is drawn with sex-ratio theory, which also predicts biases toward the sex that suffers less from local competition. Optimal sex ratios and optimal sex-specific dispersal show mutual dependence, which argues for the development of coevolution models.