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.     

Behavioural inbreeding avoidance in wild African elephants

The costs of inbreeding depression, as well as the opportunity costs of inbreeding avoidance, determine whether and which mechanisms of inbreeding avoidance evolve. In African elephants, sex-biased dispersal does not lead to the complete separation of male and female relatives, and so individuals may experience selection to recognize kin and avoid inbreeding. However, because estrous females are rare and male-male competition for mates is intense, the opportunity costs of inbreeding avoidance may be high, particularly for males. Here we combine 28 years of behavioural and demographic data on wild elephants with genotypes from 545 adult females, adult males, and calves in Amboseli National Park, Kenya, to test the hypothesis that elephants engage in sexual behaviour and reproduction with relatives less often than expected by chance. We found support for this hypothesis: males engaged in proportionally fewer sexual behaviours and sired proportionally fewer offspring with females that were natal family members or close genetic relatives (both maternal and paternal) than they did with nonkin. We discuss the relevance of these results for understanding the evolution of inbreeding avoidance and for elephant conservation.     

Kin recognition and incest avoidance in a group-living insect

Mate choice theories predict that animals evolved strategiesto mate with optimally genetically dissimilar partners, providingfitness benefits. In group-living species, when adults do notdisperse, assessment of relatedness between conspecifics canbe a key factor for choosing mates. Here, we report for thefirst time, kin recognition abilities and their implicationin mate choice in the gregarious cockroach, Blattella germanica(L.). Binary choice tests showed that females mated preferentiallywith nonsibling rather than with sibling males, thus avoidingincest. In addition, inbreeding induced an important decreaseof their reproductive success. Contrary to what could be expectedwhen females had the choice between a nonsibling strain memberand a nonstrain member, they did not avoid mating with distantlyrelated nonstrain members, and extreme outbreeding induced anincrease of their reproductive success. Furthermore, our matechoice experiments disentangled the influences of familiarityfrom those of relatedness and evidenced that kin discriminationwas based on genetic cues independently of familiarity. Phenotypematching was a plausible mechanism for kin recognition. Contraryto many insect species, body size was not a salient criterionfor mate choice and had no consequences on reproductive success.     

Precision in sex allocation is influenced by mate choice in Drosophila melanogaster

Theory predicts that a 1 : 1 sex ratio is favoured in the absence of countervailing selection pressures. In an experiment with Drosophila melanogaster, we found significantly greater variation in the offspring sex ratios of freely mated flies than would be expected by the binomial distribution. In a surprise result, control flies given no mate choice exhibited significant under-dispersal in their sex ratio variation, possibly from sperm limitation. Both treatments, however, produced populations with a 1 : 1 sex ratio. This supports the hypothesis that sexually antagonistic selection for reproductive success in sons, and fecundity in daughters, may overcome selection for an equal sex ratio. Such precision in sex allocation may allow for the maintenance of genetic variation underlying trade-offs between male and female reproductive success.     

Evolution of precopulatory and post‐copulatory strategies of inbreeding avoidance and associated polyandry

Inbreeding depression is widely hypothesized to drive adaptive evolution of precopulatory and post‐copulatory mechanisms of inbreeding avoidance, which in turn are hypothesized to affect evolution of polyandry (i.e. female multiple mating). However, surprisingly little theory or modelling critically examines selection for precopulatory or post‐copulatory inbreeding avoidance, or both strategies, given evolutionary constraints and direct costs, or examines how evolution of inbreeding avoidance strategies might feed back to affect evolution of polyandry. Selection for post‐copulatory inbreeding avoidance, but not for precopulatory inbreeding avoidance, requires polyandry, whereas interactions between precopulatory and post‐copulatory inbreeding avoidance might cause functional redundancy (i.e. ‘degeneracy’) potentially generating complex evolutionary dynamics among inbreeding strategies and polyandry. We used individual‐based modelling to quantify evolution of interacting precopulatory and post‐copulatory inbreeding avoidance and associated polyandry given strong inbreeding depression and different evolutionary constraints and direct costs. We found that evolution of post‐copulatory inbreeding avoidance increased selection for initially rare polyandry and that evolution of a costly inbreeding avoidance strategy became negligible over time given a lower‐cost alternative strategy. Further, fixed precopulatory inbreeding avoidance often completely precluded evolution of polyandry and hence post‐copulatory inbreeding avoidance, but fixed post‐copulatory inbreeding avoidance did not preclude evolution of precopulatory inbreeding avoidance. Evolution of inbreeding avoidance phenotypes and associated polyandry is therefore affected by evolutionary feedbacks and degeneracy. All else being equal, evolution of precopulatory inbreeding avoidance and resulting low polyandry is more likely when post‐copulatory inbreeding avoidance is precluded or costly, and evolution of post‐copulatory inbreeding avoidance greatly facilitates evolution of costly polyandry.     

The effects of relatedness on progeny sex ratio in spider mites

Theory predicts that optimal sex allocation in subdivided populations is dependent on the genetic relatedness among competing offspring such that when relatedness is high, progeny sex allocation should be more biased than when relatedness is low. In the laboratory we compared the progeny sex ratio of four groups of five ovipositing females of various presumed degrees of relatedness (sisters of inbred laboratory population, sisters of outbred field population, non-sisters of the same field population and non-sisters each from a different, geographically distant field population). We found a greater female bias in the progeny of inbred sisters than for sisters from the field population; the progeny sex ratio was also more strongly female biased for sisters than for non-sisters from the field population. These differences in sex ratio are in line with theoretical predictions. Our results indicate that spider mites are capable of some method of discrimination between kin and non-kin.     

Evidence of multiple paternity and mate selection for inbreeding avoidance in wild eastern chipmunks

Mate selection for inbreeding avoidance is documented in several taxa. In mammals, most conclusive evidence comes from captive experiments that control for the availability of mates and for the level of genetic relatedness between mating partners. However, the importance of mate selection for inbreeding avoidance as a determinant of siring success in the wild has rarely been addressed. We followed the reproduction of a wild population of eastern chipmunks (Tamias striatus) during five breeding seasons between 2006 and 2009. Using molecular tools and parentage assignment methods, we found that multiple paternity (among polytocous litters) varied from 25% in an early-spring breeding season when less than a quarter of females in the population were reproductively active to 100% across three summer breeding seasons and one spring breeding season when more than 85% of females were reproductively active. Genetically related parents were common in this population and produced less heterozygous offspring. Furthermore, litters with multiple sires showed a higher average relatedness among partners than litters with only a single sire. In multiply sired litters, however, males that were more closely related to their partners sired fewer offspring. Our results corroborate findings from captive experiments and suggest that selection for inbreeding avoidance can be an important determinant of reproductive success in wild mammals.     

Phenotype matching and inbreeding avoidance in African elephants

Perhaps the most important 'decision' made by any animal (or plant) is whether to disperse--leave kith and kin, or remain with the familiar and related. The benefits of staying at home are obvious, so dispersal requires an explanation--and the most popular is that dispersal functions to avoid inbreeding depression. Strong support comes from the observation that dispersal is so often sex biased. Simply put, all else being equal members of both sexes should prefer to remain philopatric, but this would lead to inbreeding depression so members of one sex have to disperse. In principle, this link between inbreeding depression and sex-biased dispersal could be broken if individuals recognize close kin and avoid mating with them. Archie et al. (2007) provide one of the most compelling analyses to date of the interaction among inbreeding avoidance, kin recognition and mating strategies in any mammal, clearly showing that elephants recognize even close paternal kin and avoid mating with them. Their important results illuminate the subtleties of elephant inbreeding avoidance as well as illustrate the difficulty of arriving at definitive answers to questions about the evolution of dispersal behaviour.     

Inbreeding and inbreeding avoidance in wild giant pandas

Inbreeding can have negative consequences on population and individual fitness, which could be counteracted by inbreeding avoidance mechanisms. However, the inbreeding risk and inbreeding avoidance mechanisms in endangered species are less studied. The giant panda, a solitary and threatened species, lives in many small populations and suffers from habitat fragmentation, which may aggravate the risk of inbreeding. Here, we performed long‐term observations of reproductive behaviour, sampling of mother–cub pairs and large‐scale genetic analyses on wild giant pandas. Moderate levels of inbreeding were found in 21.1% of mating pairs, 9.1% of parent pairs and 7.7% of panda cubs, but no high‐level inbreeding occurred. More significant levels of inbreeding may be avoided passively by female‐biased natal dispersal rather than by breeding dispersal or active relatedness‐based mate choice mechanisms. The level of inbreeding in giant pandas is greater than expected for a solitary mammal and thus warrants concern for potential inbreeding depression, particularly in small populations isolated by continuing habitat fragmentation, which will reduce female dispersal and increase the risk of inbreeding.     

Density-dependent dispersal promotes female-biased sex allocation in viscous populations

A surprising result emerging from the theory of sex allocation is that the optimal sex ratio is predicted to be completely independent of the rate of dispersal. This striking invariance result has stimulated a huge amount of theoretical and empirical attention in the social evolution literature. However, this sex-allocation invariant has been derived under the assumption that an individual''s dispersal behaviour is not modulated by population density. Here, we investigate how density-dependent dispersal shapes patterns of sex allocation in a viscous-population setting. Specifically, we find that if individuals are able to adjust their dispersal behaviour according to local population density, then they are favoured to do so, and this drives the evolution of female-biased sex allocation. This result obtains because, whereas under density-independent dispersal, population viscosity is associated not only with higher relatedness—which promotes female bias—but also with higher kin competition—which inhibits female bias—under density-dependent dispersal, the kin-competition consequences of a female-biased sex ratio are entirely abolished. We derive analytical results for the full range of group sizes and costs of dispersal, under haploid, diploid and haplodiploid modes of inheritance. These results show that population viscosity promotes female-biased sex ratios in the context of density-dependent dispersal.     

Brothers smell similar: variation in the sex pheromone of male European Beewolves Philanthus triangulum F. (Hymenoptera: Crabronidae) and its implications for inbreeding avoidance

Female choice is thought to increase the fitness returns of females. The complementary choice model states that the best mate depends on the particular genotype of a female. Aculeate Hymenoptera represent a special case of complementary female choice because males should be chosen on the basis of their allele at the sex determination locus. The prevalent sex determination mechanism in bees and wasps (single-locus complementary sex determination) requires that, to produce a daughter, diploid offspring are heterozygous at the sex determination locus. Otherwise, infertile diploid males result. Inevitably, the proportion of diploid males increases with the rate of inbreeding. In the European Beewolf, males scent mark territories to attract mates and the composition of the pheromone might provide a basis for female choice. One crucial prerequisite for females to be able to discriminate against brothers and avoid inbreeding is that the male sex pheromone varies with familial affiliation. This hypothesis was tested by analysing the pheromone of male progeny of eight mothers using gas chromatography and mass spectrometry. A significantly higher similarity was found among brothers than among unrelated individuals. Such a genetic component of a male sex pheromone has not yet been described from aculeate Hymenoptera.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 433–442.     

Kin encounter rate and inbreeding avoidance in canids

Mating with close kin can lead to inbreeding depression through the expression of recessive deleterious alleles and loss of heterozygosity. Mate selection may be affected by kin encounter rate, and inbreeding avoidance may not be uniform but associated with age and social system. Specifically, selection for kin recognition and inbreeding avoidance may be more developed in species that live in family groups or breed cooperatively. To test this hypothesis, we compared kin encounter rate and the proportion of related breeding pairs in noninbred and highly inbred canid populations. The chance of randomly encountering a full sib ranged between 1-8% and 20-22% in noninbred and inbred canid populations, respectively. We show that regardless of encounter rate, outside natal groups mates were selected independent of relatedness. Within natal groups, there was a significant avoidance of mating with a relative. Lack of discrimination against mating with close relatives outside packs suggests that the rate of inbreeding in canids is related to the proximity of close relatives, which could explain the high degree of inbreeding depression observed in some populations. The idea that kin encounter rate and social organization can explain the lack of inbreeding avoidance in some species is intriguing and may have implications for the management of populations at risk.     

Facultative adjustment of the offspring sex ratio and male attractiveness: a systematic review and meta‐analysis

Females can benefit from mate choice for male traits (e.g. sexual ornaments or body condition) that reliably signal the effect that mating will have on mean offspring fitness. These male‐derived benefits can be due to material and/or genetic effects. The latter include an increase in the attractiveness, hence likely mating success, of sons. Females can potentially enhance any sex‐biased benefits of mating with certain males by adjusting the offspring sex ratio depending on their mate's phenotype. One hypothesis is that females should produce mainly sons when mating with more attractive or higher quality males. Here we perform a meta‐analysis of the empirical literature that has accumulated to test this hypothesis. The mean effect size was small (r = 0.064–0.095; i.e. explaining <1% of variation in offspring sex ratios) but statistically significant in the predicted direction. It was, however, not robust to correction for an apparent publication bias towards significantly positive results. We also examined the strength of the relationship using different indices of male attractiveness/quality that have been invoked by researchers (ornaments, behavioural displays, female preference scores, body condition, male age, body size, and whether a male is a within‐pair or extra‐pair mate). Only ornamentation and body size significantly predicted the proportion of sons produced. We obtained similar results regardless of whether we ran a standard random‐effects meta‐analysis, or a multi‐level, Bayesian model that included a correction for phylogenetic non‐independence. A moderate proportion of the variance in effect sizes (51.6–56.2%) was due to variation that was not attributable to sampling error (i.e. sample size). Much of this non‐sampling error variance was not attributable to phylogenetic effects or high repeatability of effect sizes among species. It was approximately equally attributable to differences (occurring for unknown reasons) in effect sizes among and within studies (25.3, 22.9% of the total variance). There were no significant effects of year of publication or two aspects of study design (experimental/observational or field/laboratory) on reported effect sizes. We discuss various practical reasons and theoretical arguments as to why small effect sizes should be expected, and why there might be relatively high variation among studies. Currently, there are no species where replicated, experimental studies show that mothers adjust the offspring sex ratio in response to a generally preferred male phenotype. Ultimately, we need more experimental studies that test directly whether females produce more sons when mated to relatively more attractive males, and that provide the requisite evidence that their sons have higher mean fitness than their daughters.     

No evidence of inbreeding avoidance or inbreeding depression in a social carnivore

Dispersal by young mammals away from their natal site is generallythought to reduce inbreeding, with its attendant negative fitnessconsequences. Genetic data from the dwarf mongoose, a pack-livingcarnivore common in African savannas, indicate that there areexceptions to this generalization. In dwarf mongoose populationsin the Serengeti National Park, Tanzania, breeding pairs arecommonly related, and close inbreeding has no measurable effecton offspring production or adult survival. Inbreeding occursbecause average relatedness among potential mates within a packis high, because mating patterns within the pack are randomwith respect to the relatedness of mates, and because dispersaldoes little to decrease the relatedness among mates. Young femalesare more likely to leave a pack when the dominant male is aclose relative but are relatively infrequent dispersers. Youngmales emigrate at random with respect to the relatedness ofthe dominant female and tend to disperse to packs that containgenetically similar individuals.[Behav Ecol 7: 480–489(1996)]     

Joint evolution of sex ratio and dispersal: conditions for higher dispersal rates from good habitats

We analyze models of evolution of sex ratio conditional on habitat quality and with sex specific dispersal. Previous analysis concluded that the main constraint on sex ratio is habitat choice and leads to overproduction of the most dispersing sex in low quality habitat. Here, we analyze three models with finite local populations and show that constraints on sex ratio can balance constraints on habitat choice. In the first model, dispersal rates are fixed. In the second, sex specific dispersal can evolve independently of the habitat quality. These models suggests that sex ratio evolution can lead to higher global dispersal rates (mean of male and female dispersal rates) from high quality habitats. In the last model dispersal evolves conditionally with both sex and habitat. Our models suggests that conditions for overproduction of the most dispersing sex in high quality habitat are frequent. The predictions of the models with evolving dispersal contrast with patterns generally described in nature. We discuss possible reasons of this difference.     

Sex allocation conflict between queens and workers in Formica pratensis wood ants predicts seasonal sex ratio variation

Sex allocation theory predicts parents should adjust their investment in male and female offspring in a way that increases parental fitness. This has been shown in several species and selective contexts. Yet, seasonal sex ratio variation within species and its underlying causes are poorly understood. Here, we study sex allocation variation in the wood ant Formica pratensis. This species displays conflict over colony sex ratio as workers and queens prefer different investment in male and female offspring, owing to haplodiploidy and relatedness asymmetries. It is unique among Formica ants because it produces two separate sexual offspring cohorts per season. We predict sex ratios to be closer to queen optimum in the early cohort but more female‐biased and closer to worker optimum in the later one. This is because the power of workers to manipulate colony sex ratio varies seasonally with the availability of diploid eggs. Consistently, more female‐biased sex ratios in the later offspring cohort over a three‐year sampling period from 93 colonies clearly support our prediction. The resulting seasonal alternation of sex ratios between queen and worker optima is a novel demonstration how understanding constraints of sex ratio adjustment increases our ability to predict sex ratio variation.     

Sexual selection in an isopod with Wolbachia‐induced sex reversal: males prefer real females

A variety of genetic elements encode traits beneficial to their own transmission. Despite their ‘selfish’ behaviour, most of these elements are often found at relatively low frequencies in host populations. This is the case of intracytoplasmic Wolbachia bacteria hosted by the isopod Armadillidium vulgare that distort the host sex ratio towards females by feminizing the genetic males they infect. Here we tested the hypothesis that sexual selection against Wolbachia‐infected females could maintain a polymorphism of the infection in populations. The infected neo‐females (feminized males) have lower mating rates and received less sperm relative to uninfected females. Males exhibited an active choice: they interacted more with uninfected females and made more mating attempts. A female behavioural difference was also observed in response to male mating attempts: infected neo‐females more often exhibited behaviours that stop the mating sequence. The difference in mating rate was significant only when males could choose between the two female types. This process could maintain a polymorphism of the infection in populations. Genetic females experimentally infected with Wolbachia are not exposed to the same sexual selection pressure, so the infection alone cannot explain these differences.