Low levels of relatedness on black grouse leks despite male philopatry

In lekking species, males cluster on specific areas for display (the leks) and females generally prefer to copulate with males on large aggregations. The maintenance of leks in which only a few males reproduce might be explained if subordinate males gain indirect fitness benefits. By joining a lek on which relatives are displaying, subordinates might attract more females to the lek thereby increasing the mating opportunities of their kin. In black grouse, a genetic structure among leks has previously been found suggesting that relatives could display together. Using 11 microsatellite loci, we extended this result by testing for the presence of kin structures in nine black grouse leks (101 males). The genetic differentiation among flocks was higher in males than in females, suggesting female-biased dispersal and male philopatry. Because of this genetic structure, males were more related within than among leks. However, the mean relatedness within each lek hardly differed from zero. The lekking males were not more related than random assortments of males from the winter flocks and there were no kin clusters within leks. Thus, black grouse males do not choose to display with and close to relatives. Male philopatry alone was not sufficient to induce elevated levels of relatedness on the leks either because of male partial dispersal or a rapid turnover of the successful males. The indirect fitness benefits associated with males' settlement decision are probably limited compared to the direct benefits of joining large aggregations such as increased current and future mating opportunities.     

Assortative mating for relatedness in a large naturally occurring population of Drosophila melanogaster

New theoretical work on kin selection and inclusive fitness benefits predicts that individuals will sometimes choose close or intermediate relatives as mates to maximize their fitness. However, empirical examples supporting such predictions are rare. In this study, we look for such evidence in a natural population of Drosophila melanogaster. We compared mating and nonmating individuals to test whether mating was nonrandom with respect to relatedness. Consistent with optimal inbreeding, males were more closely related to their mate than to randomly sampled females. However, all individuals collected mating showed higher relatedness and males were not significantly more related to their mate than to other mating females. We also found a negative relationship between relatedness and fecundity. Our results are consistent with the hypothesis that inclusive fitness benefits may drive inbreeding tolerance despite direct costs to fitness; however, an experimental approach is needed to investigate the link between mate preference and relatedness.     

Microsatellite markers reveal the potential for kin selection on black grouse leks

The evolution of social behaviour has puzzled biologists since Darwin. Since Hamilton''s theoretical work in the 1960s it has been realized that social behaviour may evolve through the effects of kinship. By helping relatives, an individual may pass on its genes despite negative effects on its own reproduction. Leks are groups of males that females visit primarily to mate. The selective advantage for males to join such social groups has been given much recent attention, but no clear picture has yet emerged. Here we show, using microsatellite analysis, that males but not females of a lekking bird (the black grouse, Tetrao tetrix) are genetically structured at the lek level. We interpret this structuring to be the effects of strong natal philopatry in males. This has the consequence that males on any specific lek should be more related than expected by chance as indicated by our genetic data. Our results thus suggest that kin selection is a factor that needs to be considered in the evolution and maintenance of the lek mating system in black grouse and sheds new light on models of lek evolution.     

Polyandrous females acquire indirect benefits in a nuptial feeding species

The relative force of direct and indirect selection underlying the evolution of polyandry is contentious. When females acquire direct benefits during mating, indirect benefits are often considered negligible. Although direct benefits are likely to play a prominent role in the evolution of polyandry, post‐mating selection for indirect benefits may subsequently evolve. We examined whether polyandrous females acquire indirect benefits and quantified direct and indirect effects of multiple mating on female fitness in a nuptial gift‐giving spider (Pisaura mirabilis). In this system, the food item donated by males during mating predicts direct benefits of polyandry. We compared fecundity, fertility and survival of singly mated females to that of females mated three times with the same (monogamy) or different (polyandry) males in a two‐factorial design where females were kept under high and low feeding conditions. Greater access to nutrients and sperm had surprisingly little positive effect on fitness, apart from shortening the time until oviposition. In contrast, polyandry increased female reproductive success by increasing the probability of oviposition, and egg hatching success indicating that indirect benefits arise from mating with several different mating partners rather than resources transferred by males. The evolution of polyandry in a male‐resource‐based mating system may result from exploitation of the female foraging motivation and that indirect genetic benefits are subsequently derived resulting from co‐evolutionary post‐mating processes to gain a reproductive advantage or to counter costs of mating. Importantly, indirect benefits may represent an additional explanation for the maintenance of polyandry.     

The fitness consequences of kin-biased dispersal in a cooperatively breeding bird

Cooperative alliances among kin may not only lead to indirect fitness benefits for group-living species, but can also provide direct benefits through access to mates or higher social rank. However, the immigrant sex in most species loses any potential benefits of living with kin unless immigrants disperse together or recruit relatives into the group in subsequent years. To look for evidence of small subgroups of related immigrants within social groups (kin substructure), we used microsatellites to assess relatedness between immigrant females of the cooperatively breeding superb starling, Lamprotornis superbus. We determined how timing of immigration led to kin subgroup formation and if being part of one influenced female fitness. Although mean relatedness in groups was higher for males than females, 26% of immigrant females were part of a kin subgroup with a sister. These immigrant sibships formed through kin recruitment across years more often than through coalitions immigrating together in the same year. Furthermore, females were more likely to breed when part of a kin subgroup than when alone, suggesting that female siblings form alliances that may positively influence their fitness. Ultimately, kin substructure should be considered when determining the role of relatedness in the evolution of animal societies.     

Age-dependent inbreeding risk and offspring fitness costs in female black grouse

Dispersal is an important mechanism used to avoid inbreeding. However, dispersal may only be effective for part of an individual's lifespan since, post-dispersal individuals that breed over multiple reproductive events may risk mating with kin of the philopatric sex as they age. We tested this hypothesis in black grouse Tetrao tetrix, and show that yearling females never mated with close relatives whereas older females did. However, matings were not with direct kin suggesting that short-distance dispersal to sites containing kin and subsequent overlap of reproductive lifespans between males and females were causing this pattern. Chick mass was lower when kinship was high, suggesting important fitness costs associated with inbred matings. This study shows that increased inbreeding risk might be a widespread yet rarely considered cost of ageing.     

Females benefit from multiple mating but not multiple mates in the burying beetle Nicrophorus vespilloides

Male reproductive success generally increases with number of mates but this need not be true for females. If females are the limiting sex, as few as one mate can be optimal. Despite the theoretical differences driving multiple mating in the sexes, multiple mating is the norm rather than the exception. Empirical investigations are therefore required to determine why females mate with multiple males. Both nonadaptive (correlated responses to selection on males, given the mean mating rates have to be the same) and adaptive (direct or indirect fitness benefits) can drive the evolution of multiple mating in females. Females of the burying beetle Nicorphorus vespilloides often mate repeatedly with the same male, but this appears to be a correlated response to selection on males rather than reflecting direct benefits to females for multiple mating. However, an unexamined alternative to this nonadaptive explanation is that females benefit by mating with multiple different males and therefore are selected for general promiscuity. Here we examine if mating polyandrously provides fitness benefits by examing the effects of number of mates (1, 2 or 3), mating system (monogamous, polyandrous) and their interaction. The only significant influence was mating more than once. This did not depend on type of mating. We suggest that unlike most other species examined, in N. vespilloides mating with the same male repeatedly or with several different males reflects an indiscriminate willingness to mate as a result of correlated selection on males for high rates of mating.     

Direct and indirect fitness consequences of female choice in a crustacean

Understanding the evolution and maintenance of female mate choice requires information on both the benefits (the sum of direct and indirect benefits) and costs of selective mating. In this study, I assessed the fitness consequences of female mate choice in a freshwater crustacean. In Hyalella amphipods, males attempt to form precopulatory pairs with females. Large males, bearing large posterior gnathopods, tend to be over-represented in precopulatory pairs. I show that females receive both direct (reduced risk of predation while paired) and indirect (sexy sons) benefits from mating with these males. Furthermore, the behavioral mechanisms used to filter male phenotypes carry no detectable energetic cost for females. Thus, females that choose males with successful phenotypes are expected to have higher Darwinian fitness than females that mate at random. This study shows that direct and indirect selection act together to favor large male size, which explains the sexual size dimorphism and size-based mating biases observed in this species.     

Neighbouring male spotted bowerbirds are not related, but do maraud each other

Males with elaborate secondary sexual traits can enhance their mating success both by choosing to display at a site that increases the efficacy of their signal and by displaying at a site where the population is structured to provide inclusive fitness benefits via kin selection. Theoretical models and field studies reveal that, across a range of species and especially those with nonresource-based mating systems, males do display with kin. Bowerbirds use a nonresource-based mating system where males show spatial site fidelity and females visit the sites for the purpose of mate choice. However, neighbours can interfere with bower display by marauding (destroying and decoration stealing). Models suggest that local nonaggression pacts provide the best conditional strategy for males, a situation that may be facilitated by kin-mediated inclusive fitness benefits if males displayed together. We used a novel method of calculating relatedness, based on amplified fragment length polymorphism (AFLP), in a population of spotted bowerbirds, Chlamydera maculata, and found no evidence of fine-scale genetic structuring of display sites. Furthermore, males did not display next to kin, but instead an owner's neighbours were those most likely to maraud his bower. Marauders did not discriminate between kin and nonkin as their victims. Such theft and destruction may affect the mating success of the targeted bower owner.     

Kin selection may contribute to lek evolution and trait introgression across an avian hybrid zone

Understanding the mechanism(s) that favour cooperation among individuals competing for the same resources provides direct insights into the evolution of grouping behaviour. In a hybrid zone between golden-/yellow-collared (Manacus vitellinus) and white-collared (Manacus candei) manakins, males form aggregations composed of white and yellow males solely to attract females ('mixed leks'). Previous work shows that yellow males in these mixed leks experience a clear mating advantage over white males, resulting in the preferential introgression of yellow plumage allele(s) into the white species. However, the yellow male mating advantage only occurs in mixed leks with high frequencies of yellow males, and only a few of these males probably mate. Hence, it remains unclear why unsuccessful males join leks. Here, we used microsatellite markers to estimate pairwise relatedness among males within and between leks to test whether indirect genetic benefits of helping kin ('kin selection') can promote grouping. We found that yellow males are significantly more related to each other within than between leks, while relatedness among white males did not differ within and between leks. This suggests that yellow males may indirectly enhance their own reproductive success by preferentially lekking with relatives because yellow plumage is under positive frequency-dependent selection (positive FDS). Our results are consistent with the hypothesis that kin selection may promote grouping and facilitate positive FDS for yellow males, mediating the movement of yellow plumage across this hybrid zone.     

The evolution of repeated mating in the burying beetle, Nicrophorus vespilloides

Animals of many species accept or solicit recurring copulations with the same partner; i.e., show repeated mating. An evolutionary explanation for this excess requires that the advantages of repeated mating outweigh the costs, and that behavioral components of repeated mating are genetically influenced. There can be benefits of repeated mating for males when there is competition for fertilizations or where the opportunities for inseminating additional mates are rare or unpredictable. The benefits to females are less obvious and, depending on underlying genetic architecture, repeated mating may have evolved as a correlated response to selection on males. We investigated the evolution of repeated mating with the same partner in the burying beetle Nicrophorus vespilloides by estimating the direct and indirect fitness benefits for females and the genetics of behavior underlying repeated mating. The number of times a female mated had minimal direct and no indirect fitness benefits for females. The behavioral components of repeated mating (mating frequency and mating speed) were moderately negatively genetically correlated in males and uncorrelated in females. However, mating frequency and mating speed were strongly positively genetically correlated between males and females. Our data suggest that repeated mating by female N. vespilloides may have evolved as a correlated response to selection on male behavior rather than in response to benefits of repeated mating for females.     

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.     

Fighting in fig wasps: do males avoid killing brothers or do they never meet them?

1. In many fig wasp species, armoured wingless males regularly engage in lethal fights for access to females inside figs, which act as discrete mating patches. 2. Kin selection generally opposes killing brothers, because their reproductive success provides indirect genetic benefits (inclusive fitness). However, siblicide may be avoided if (i) brothers do not occur in the same figs, or (ii) males avoid fighting brothers in the same fig. Alternatively, (iii) siblicide may occur because intense mate competition between brothers at the local scale overcomes kin selection effects, or (iv) males do not recognise kin. 3. A fig may also contain wasps from other closely related species and it is not known if males also fight with these individuals. 4. Nine microsatellite loci were used in the first genetic analysis of fighting in fig wasps. We assigned species and sibling identities to males and tested alternative fighting scenarios for three Sycoscapter wasp species in figs of Ficus rubiginosa. 5. Approximately 60% of figs contained males from more than one Sycoscapter species and approximately 80% of fights were between conspecifics, but a surprising 20% were between heterospecific males. 6. Within species, few figs contained brothers, suggesting that females typically lay one son per fig. Overall, most males do not compete with brothers and all fights observed were between unrelated males.     

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.     

Promiscuous mating produces offspring with higher lifetime fitness

In many species, each female pairs with a single male for the purpose of rearing offspring, but may also engage in extra-pair copulations. Despite the prevalence of such promiscuity, whether and how multiple mating benefits females remains an open question. Multiple mating is typically thought to be favoured primarily through indirect benefits (i.e. heritable effects on the fitness of offspring). This prediction has been repeatedly tested in a variety of species, but the evidence has been equivocal, perhaps because such studies have focused on pre-reproductive survival rather than lifetime fitness of offspring. Here, we show that in a songbird, the dark-eyed junco (Junco hyemalis), both male and female offspring produced by extra-pair fertilizations have higher lifetime reproductive success than do offspring sired within the social pair. Furthermore, adult male offspring sired via extra-pair matings are more likely to sire extra-pair offspring (EPO) themselves, suggesting that fitness benefits to males accrue primarily through enhanced mating success. By contrast, female EPO benefited primarily through enhanced fecundity. Our results provide strong support for the hypothesis that the evolution of extra-pair mating by females is favoured by indirect benefits and shows that such benefits accrue much later in the offspring's life than previously documented.     

Secondary sexual ornamentation and non-additive genetic benefits of female mate choice

Ornamental secondary sexual traits are hypothesized to evolve in response to directional mating preferences for more ornamented mates. Such mating preferences may themselves evolve partly because ornamentation indicates an individual's additive genetic quality (good genes). While mate choice can also confer non-additive genetic benefits (compatible genes), the identity of the most 'compatible' mate is assumed to depend on the choosy individual's own genotype. It is therefore unclear how choice for non-additive genetic benefits could contribute to directional mating preferences and consequently the evolution of ornamentation. In free-living song sparrows (Melospiza melodia), individual males varied in their kinship with the female population. Furthermore, a male's song repertoire size, a secondary sexual trait, was negatively correlated with kinship such that males with larger repertoires were less closely related to the female population. After excluding close relatives as potential mates, individual females were on average less closely related to males with larger repertoires. Therefore, female song sparrows expressing directional preferences for males with larger repertoires would on average acquire relatively unrelated mates and produce relatively outbred offspring. Such non-additive genetic fitness benefits of directional mating preferences, which may reflect genetic dominance variance expressed in structured populations, should be incorporated into genetic models of sexual selection.     

Context-dependent effects of tail-ornament damage on mating success in black grouse

Male black grouse (Tetrao tetrix) may receive damage to theirtail ornaments, the lyre, during goshawk predation attemptsand during fights with other males. In this study we confirma previous observation that black grouse males with damagedtail ornaments suffer reduced mating success. In males thatheld territories on the edge of the leks, tail damage was unrelatedto mating success, whereas in central males damage was negativelycorrelated with mating success. We tested experimentally whetherabsence of damage is used by females in mate choice. In maleswith edge territories, intact, control males had higher matingsuccess than males with cut tails, but in males with centralterritories, lyre cutting had no effect on mating success. Theseresults suggest two interpretations. First, female choice alsodepends on factors other than tail damage such as position onthe lek and dominance. Second, the effect of tail damage iscontext dependent; in males that otherwise meet females standards(e.g., dominant males), the effect of tail damage is negligible,but in less dominant males, tail damage could be used by femalesin mate selection. The second interpretation provides an explanationfor why the data on unmanipulated and manipulated birds differ.In experimental central birds, factors other than tail damageprobably determine male mating success, whereas in experimentaledge birds such factors are probably absent and therefore taildamage is relatively more important. In central unmanipulatedbirds, however, males with natural damage are probably not chosenbecause tail damage and absence of other attractive traits arecorrelated. The absence of an effect on peripheral unmanipulatedbirds may be explained by their overall low mating success     

What is driving male mate preference evolution in Jamaican field crickets?

Male mating preferences are often a neglected aspect of studies on sexual selection. Male mating preferences may evolve if they provide males with direct‐fitness benefits such as increased opportunity to fertilize more eggs or indirect‐fitness benefits such as enhanced offspring survival. We tested these ideas using Jamaican field crickets, Gryllus assimilis, previously shown to exhibit male mating preferences. We randomly mated males to either their preferred or non‐preferred potential mates and then asked whether mating treatment influenced egg oviposition or offspring viability. Preferred females were not significantly more fecund and did not produce more viable eggs or offspring than non‐preferred females. Male mate preferences were therefore inconsistent with both the direct‐ and indirect‐fitness benefits hypotheses under the conditions of our experiment. Our null results leave us with an open question about what is driving the evolution of mating preferences in male crickets. Future research should explore the whether the offspring of preferred females are more attractive, have stronger immune systems, and/or experience higher adult longevity.     

Female‐biased dispersal alone can reduce the occurrence of inbreeding in black grouse (Tetrao tetrix)

Although inbreeding depression and mechanisms for kin recognition have been described in natural bird populations, inbreeding avoidance through mate choice has rarely been reported suggesting that sex‐biased dispersal is the main mechanism reducing the risks of inbreeding. However, a full understanding of the effect of dispersal on the occurrence of inbred matings requires estimating the inbreeding risks prior to dispersal. Combining pairwise relatedness measures and kinship assignments, we investigated in black grouse whether the observed occurrence of inbred matings was explained by active kin discrimination or by female‐biased dispersal. In this large continuous population, copulations between close relatives were rare. As female mate choice was random for relatedness, females with more relatives in the local flock tended to mate with genetically more similar males. To quantify the initial risks of inbreeding, we measured the relatedness to the males of females captured in their parental flock and virtually translocated female hatchlings in their parental and to more distant flocks. These tests indicated that dispersal decreased the likelihood of mating with relatives and that philopatric females had higher inbreeding risks than the actual breeding females. As females do not discriminate against relatives, the few inbred matings were probably due to the variance in female dispersal propensity and dispersal distance. Our results support the view that kin discrimination mate choice is of little value if dispersal effectively reduces the risks of inbreeding.     

Kin selection in Columbian ground squirrels: direct and indirect fitness benefits

Empirical and theoretical studies have supported kin selection by demonstrating nepotism or modelling its conditions and consequences. As an alternative, we previously found that female Columbian ground squirrels had greater direct fitness when more close kin were present. Extending those results, we used population matrix methods to calculate minimum estimates of individual fitness, estimated direct and indirect components of fitness, estimated inclusive fitness by adding the direct fitness (stripped of estimated influences of the social environment) and indirect fitness components together, and finally looked for inclusive fitness benefits of associations with close kin who seem to be 'genial neighbours'. We examined the estimated fitness of a sample of 35 females for which complete lifetimes were known for themselves, their mothers and their littermate sisters. Six of these females had no cosurviving adult close kin, and their direct fitness was significantly lower than 29 females with such kin (λ = 0.66 vs. λ = 1.23). The net fitness benefit of the presence of close kin was thus 0.57. The estimated indirect component of fitness through benefits to the direct fitness of close kin was 0.43. Thus, estimated inclusive fitness for females with cosurviving close kin (λ = 1.09) was significantly greater than that for females without surviving close kin (viz., λ = 0.66). The presence of closely related and philopatric female kin appeared to result in considerable fitness benefits for female ground squirrels, perhaps through the behavioural mechanisms of lowered aggression and other forms of behavioural cooperation.