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Natal dispersal is an important life-history stage influencing individual fitness, social dynamics of groups and population structure. Understanding factors influencing dispersal is essential for evaluating explanations for the evolution and maintenance of social organization, including parental care and mating systems. The social and mating systems of Azara's owl monkeys (Aotus azarae) are infrequent among mammals; these primates are pair-living, serially and genetically monogamous and both sexes directly care for offspring. To evaluate the role that competition and inbreeding avoidance play in shaping dispersal patterns, we used 25 years of demographic and genetic data to examine how variation in timing of natal dispersal is related to social (adult replacements, step-parents, births and group size) and ecological factors (seasonal abundance of resources) in a wild population of A. azarae in Formosa, Argentina. We found that all males and females dispersed from their natal groups, but subadults delayed dispersal when a step-parent of the opposite sex joined the group, indicating that they may perceive these step-parents as potential mates. Dispersal was more probable when resource conditions were better, regardless of age. Overall, agonistic conflict over food and potential mates with adults in the natal group, as well as inbreeding avoidance, contribute to regulating dispersal.

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AbstractInbreeding results from matings between relatives and often leads to a reduction in the fitness of inbred offspring, known as inbreeding depression. There is substantial variation in the magnitude of inbreeding depression among and within species, driven by differences in the biotic and abiotic environment. Recent studies in three species found that parental care has the potential to buffer against inbreeding depression in the offspring, but the generality of this pattern is still unknown. Here, we performed a meta-analysis to test whether variation in the magnitude of inbreeding depression is related to among-species differences in parental care in fishes. We synthesized 536 effect sizes across 56 studies and 18 species, spanning 47 years of research. We found that inbred offspring suffer a smaller reduction in fitness in species that provide biparental care than in species with uniparental or no care. By using a comparative approach, this study provides novel insights into the capacity of parental care to moderate inbreeding depression and suggests that these effects may currently be underappreciated. Considering the potential effects of parental care on inbreeding depression can help us understand why some species avoid inbreeding, whereas others tolerate or even prefer inbreeding, which has important implications for the maintenance of genetic variation within populations.

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Inbreeding (reproduction between relatives) often decreases the fitness of offspring and is thus expected to lead to the evolution of inbreeding avoidance strategies. Chimpanzees (Pan troglodytes) are expected to avoid inbreeding as they are long-lived, invest heavily in offspring and may encounter adult, opposite sex kin frequently, especially in populations where both males and females commonly remain in the group in which they were born (bisexual philopatry). However, it is unclear whether substantial bisexual philopatry has been a feature of chimpanzees' evolutionary history or whether it is a result of recent anthropogenic interference, as the only groups for which it has been documented are significantly impacted by human encroachment and experience notable rates of potentially unsustainable inbreeding. Here we use 14 years of observational data and a large genomic dataset of 256 481 loci sequenced from 459 individuals to document dispersal and inbreeding dynamics in an eastern chimpanzee (P. t. schweinfurthii) community with low levels of anthropogenic disturbance. We document the first case of substantial bisexual philopatry in a relatively undisturbed chimpanzee community and show that, despite an increased inbreeding risk incurred by females who do not disperse before reaching reproductive age, natal females were still able to avoid producing inbred offspring.

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The negative consequences of inbreeding have led animal biologists to assume that mate choice is generally biased against relatives. However, inbreeding avoidance is highly variable and by no means the rule across animal taxa. Even when inbreeding is costly, there are numerous examples of animals failing to avoid inbreeding or even preferring to mate with close kin. We argue that selective and mechanistic constraints interact to limit the evolution of inbreeding avoidance, notably when there is a risk of mating with heterospecifics and losing fitness through hybridization. Further, balancing inbreeding avoidance with conspecific mate preference may drive the evolution of multivariate sexual communication. Studying different social and sexual decisions within the same species can illuminate trade-offs among mate-choice mechanisms.

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Investigating whether mating patterns are biased in relation to kinship in isolated populations can provide a better understanding of the occurrence of inbreeding avoidance mechanisms in wild populations. Here, we report on the genetic relatedness (r) among breeding pairs in a relict population of Thorn-tailed Rayadito (Aphrastura spinicauda) in north-central Chile that has experienced a long-term history of isolation. We used simulations based on 8 years of data to assess whether mating is random with respect to relatedness. We found that mean and median population values of pair relatedness tended to be lower than randomly generated values, suggesting that mating is not random with respect to kinship. We hypothesize that female-biased dispersal is the main mechanism reducing the likelihood of mating among kin, and that the proportion of related pairs (i.e., r > 0.125) in the study population (25%) would presumably be higher in the absence of sex-biased dispersal. The occurrence of other mechanisms such as extra-pair copulations, delayed breeding, and active inbreeding avoidance through kin discrimination cannot be dismissed and require further study.

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Inbreeding often imposes net fitness costs,1-5 leading to the expectation that animals will engage in inbreeding avoidance when the costs of doing so are not prohibitive.4-9 However, one recent meta-analysis indicates that animals of many species do not avoid mating with kin in experimental settings,6 and another reports that behavioral inbreeding avoidance generally evolves only when kin regularly encounter each other and inbreeding costs are high.9 These results raise questions about the processes that separate kin, how these processes depend on kin class and context, and whether kin classes differ in how effectively they avoid inbreeding via mate choice-in turn, demanding detailed demographic and behavioral data within individual populations. Here, we address these questions in a wild mammal population, the baboons of the Amboseli ecosystem in Kenya. We find that death and dispersal are very effective at separating opposite-sex pairs of close adult kin. Nonetheless, adult kin pairs do sometimes co-reside, and we find strong evidence for inbreeding avoidance via mate choice in kin classes with relatedness ≥0.25. Notably, maternal kin avoid inbreeding more effectively than paternal kin despite having identical coefficients of relatedness, pointing to kin discrimination as a potential constraint on effective inbreeding avoidance. Overall, demographic and behavioral processes ensure that inbred offspring are rare in undisturbed social groups (1% of offspring). However, in an anthropogenically disturbed social group with reduced male dispersal, we find inbreeding rates 10× higher. Our study reinforces the importance of demographic and behavioral contexts for understanding the evolution of inbreeding avoidance.9.

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Mate preferences and mating-related behaviours are hypothesised to change over the menstrual cycle to increase reproductive fitness. Recent large-scale studies suggest that previously reported hormone-linked behavioural changes are not robust. The proposal that women's preference for associating with male kin is down-regulated during the ovulatory (high-fertility) phase of the menstrual cycle to reduce inbreeding has not been tested in large samples. Consequently, we investigated the relationship between longitudinal changes in women's steroid hormone levels and their perceptions of faces experimentally manipulated to possess kinship cues (Study 1). Women viewed faces displaying kinship cues as more attractive and trustworthy, but this effect was not related to hormonal proxies of conception risk. Study 2 employed a daily diary approach and found no evidence that women spent less time with kin generally or with male kin specifically during the fertile phase of the menstrual cycle. Thus, neither study found evidence that inbreeding avoidance is up-regulated during the ovulatory phase of the menstrual cycle.

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Equine reproductive behavior is affected by many factors, some remaining poorly understood. This study tested the hypothesis that a period of captivity during the juvenile period and human-controlled reproduction may potentially be involved in the disruption of the development of incestuous mating avoidance behavior in sanctuary-reintroduced male Konik polski horses. Between 1986 and 2000, cases of incestuous behavior in harem stallions born and reared until weaning in the sanctuary were studied. Eight males lived in the sanctuary's feral herd for the rest of their lives (the non-captive group; nC). They gained their own harem of mares without human intervention (no human-controlled reproductive activity, nHC). Another five stallions were removed as weanlings, reared in captivity and then reintroduced as adults (captive, C). Three of these C stallions were used as in-hand breeding stallions, one as a "teaser" (human-controlled reproductive activity, HC) and one was not used for reproduction in captivity (nHC). Reproductive records for 46 mares, daughters of all 13 harem stallions, were scrutinized and cases of incestuous breeding were recorded by interrogation of foal parentage records. C stallions failed to expel more daughters than nC stallions (33% vs. 18%, P = 0.045), and mated with significantly more of them (28% vs. 11%, P = 0.025). Interestingly, HC stallions expelled fewer (60%) and successfully mated with more (33%) daughters that nHC stallions (84% expelled, P = 0.013, and 10% successful mating with daughters, P = 0.010). All HC stallions bred incestuously at least once. We propose that human intervention during a critical period of development of social and reproductive behavior in young stallions, by enforced separation from their natal herd and in-hand breeding, may contribute to their later aberrant behavior and disruption of inbreeding avoidance mechanisms in these stallions. The previous occurrence of human-controlled breeding may be one of the factors promoting incestuous behavior of stallions in natural conditions. The uninterrupted presence of stallions in their harems and herd member recognition may also play important roles in inbreeding avoidance in horses.

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BACKGROUND: Wolbachia are intracellular α-proteobacteria that have a wide distribution among various arthropods and nematodes. They affect the host reproduction favoring their maternal transmission, which sets up a potential conflict in inbreeding situations when the host avoids sexual reproduction preventing inbreeding depression, while Wolbachia pushes it. We used the wasp Habrobracon hebetor to test the hypothesis that Wolbachia modulates inbreeding avoidance behavior and promotes sib mating. RESULTS: Our results showed no obvious pre-copulatory inbreeding avoidance in this wasp. However, H. hebetor showed a strong post-copulatory inbreeding avoidance behavior that resulted in a low fertilization rate of uninfected siblings and therefore high rate of production of male progeny was obtained. We observed higher rates of fertilization success in the Wolbachia-infected lines that resulted in significantly higher female progeny production compared to the uninfected sib mates. Since diploid females are the result of successful fertilization due to haplodiploidy sex determination system in this insect, our results indicate that Wolbachia promoted fertile sib mating in H. hebetor. Interestingly, the rate of adult emergence in the progeny of Wolbachia-infected sib mates were almost similar to the non-sib mate crosses and significantly more than those observed in the uninfected sib mate crosses. CONCLUSION: Our results support the idea that Wolbachia modulates inbreeding avoidance and promotes sib mating and also mitigates inbreeding depression. By promoting successful sex with siblings and increasing the probability of female progeny, Wolbachia enhances its transmission to the next generation. This is an undescribed effect of Wolbachia on the host reproduction. © 2021 Society of Chemical Industry.

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Conservation breeding management aims to reduce inbreeding and maximize the retention of genetic diversity in endangered populations. However, breeding management of wild populations is still rare, and there is a need for approaches that provide data-driven evidence of the likelihood of success of alternative in situ strategies. Here, we provide an analytical framework that uses in silico simulations to evaluate, for real wild populations, (i) the degree of population-level inbreeding avoidance, (ii) the genetic quality of mating pairs, and (iii) the potential genetic benefits of implementing two breeding management strategies. The proposed strategies aim to improve the genetic quality of breeding pairs by splitting detrimental pairs and allowing the members to re-pair in different ways. We apply the framework to the wild population of the Critically Endangered helmeted honeyeater by combining genomic data and field observations to estimate the inbreeding (i.e., pair-kinship) and genetic quality (i.e., Mate Suitability Index) of all mating pairs for seven consecutive breeding seasons. We found no evidence of population-level inbreeding avoidance and that ~91.6% of breeding pairs were detrimental to the genetic health of the population. Furthermore, the framework revealed that neither proposed management strategy would significantly improve the genetic quality or reduce inbreeding of the mating pairs in this population. Our results demonstrate the usefulness of our analytical framework for testing the efficacy of different in situ breeding management strategies and for making evidence-based management decisions.

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Immune defence is a key component of fitness, and individuals are expected to have evolved preferences for mates that ensure immunocompetent offspring. Potential preferences include those for mates with specific heritable immune gene profiles ("good genes") or for immunogenetically dissimilar mates to increase offspring immune gene diversity. The major histocompatibility complex (MHC) is by far the most investigated immune gene in mate choice studies, but we still know very little about its role in sexual selection for genetic benefits. In this issue of Molecular Ecology, Huang et al. capitalize on the extraordinary wealth of behavioural, life history and genetic/genomic data from the free-living Soay sheep population on the Island of Hirta to address this problem. While the authors find evidence of both pre- and postcopulatory MHC-based sexual selection, postcopulatory MHC-dissimilar mate choice is indistinguishable from genome-wide effects, suggesting it is a byproduct of inbreeding avoidance in Soay sheep. The study's comprehensive sampling ensures that inferences are generalizable to the entire population and provides a gold standard for studies investigating immune gene-based sexual selection.

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Kin recognition, the ability to detect relatives, is important for cooperation, altruism and also inbreeding avoidance. A large body of research on kin recognition mechanisms exists for vertebrates and insects, while little is known for other arthropod taxa. In spiders, nepotism has been reported in social and solitary species. However, there are very few examples of kin discrimination in a mating context, one coming from the orb-weaver Argiope bruennichi. Owing to effective mating plugs and high rates of sexual cannibalism, both sexes of A. bruennichi are limited to a maximum of two copulations. Males surviving their first copulation can either re-mate with the current female (monopolizing paternity) or leave and search for another. Mating experiments have shown that males readily mate with sisters but are more likely to leave after one short copulation as compared with unrelated females, allowing them to search for another mate. Here, we ask whether the observed behaviour is based on chemical cues. We detected family-specific cuticular profiles that qualify as kin recognition cues. Moreover, correlations in the relative amounts of some of the detected substances between sexes within families indicate that kin recognition is likely based on subsets of cuticular substances, rather than entire profiles.

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Individuals are expected to avoid mating with relatives as inbreeding can reduce offspring fitness, a phenomenon known as inbreeding depression. This has led to the widespread assumption that selection will favour individuals that avoid mating with relatives. However, the strength of inbreeding avoidance is variable across species and there are numerous cases where related mates are not avoided. Here we test if the frequency that related males and females encounter each other explains variation in inbreeding avoidance using phylogenetic meta-analysis of 41 different species from six classes across the animal kingdom. In species reported to mate randomly with respect to relatedness, individuals were either unlikely to encounter relatives, or inbreeding had negligible effects on offspring fitness. Mechanisms for avoiding inbreeding, including active mate choice, post-copulatory processes and sex-biased dispersal, were only found in species with inbreeding depression. These results help explain why some species seem to care more about inbreeding than others: inbreeding avoidance through mate choice only evolves when there is both a risk of inbreeding depression and related sexual partners frequently encounter each other.

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The MHC is one of the most polymorphic gene clusters in vertebrates and play an essential role in adaptive immunity. Apart from pathogen-mediated selection, sexual selection can also contribute to the maintenance of MHC diversity. MHC-dependent sexual selection could occur via several mechanisms but at present there is no consensus as to which of these mechanisms are involved and their importance. Previous studies have often suffered from limited genetic and behavioural data and small sample size, and were rarely able to examine all the mechanisms together, determine whether signatures of MHC-based non-random mating are independent of genomic effects or differentiate whether MHC-dependent sexual selection takes place at the pre- or post-copulatory stage. In this study, we use Monte Carlo simulation to investigate evidence for non-random MHC-dependent mating patterns by all three mechanisms in a free-living population of Soay sheep. Using 1710 sheep diplotyped at the MHC class IIa region and genome-wide SNPs, together with field observations of consorts, we found sexual selection against a particular haplotype in males at the pre-copulatory stage and sexual selection against female MHC heterozygosity during the rut. We also found MHC-dependent disassortative mating at the post-copulatory stage, along with strong evidence of inbreeding avoidance at both stages. However, results from generalized linear mixed models suggest that the pattern of MHC-dependent disassortative mating could be a by-product of inbreeding avoidance. Our results therefore suggest that while multiple apparent mechanisms of non-random mating with respect to the MHC may occur, some of them have alternative explanations.

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Male introductions into captive primate breeding groups can be risky and unsuccessful. However, they are necessary to prevent inbreeding in naturalistic breeding groups. The procedure used to introduce new individuals may affect the success and influence the risks associated with group introductions. At the Biomedical Primate Research Centre (BPRC) in Rijswijk, the Netherlands, male rhesus macaque (Macaca mulatta) introductions into naturalistic social groups with a matrilineal structure and without a breeding male achieve relatively high success rates. This paper describes the male introduction procedure used at the BPRC. Males are stepwise familiarized with and introduced to their new group, while all interactions between the new male and the resident females are closely monitored. Monitoring the behaviour of the resident females and their new male during all stages of the introduction provides crucial information as to whether or not it is safe to proceed. The BPRC introduction procedure is widely applicable and may improve the management of captive primate groups in any housing facility worldwide. Thus, the careful introduction management can minimize the risk associated with male introductions and enhance the welfare of captive primates.

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AbstractKin recognition plays an important role in social behavior and evolution, but the proximate mechanisms by which individuals recognize kin remain poorly understood. In many species, individuals form a "kin template" that they compare with conspecifics' phenotypes to assess phenotypic similarity-and, by association, relatedness. Individuals may form a kin template through self-inspection (i.e., self-referencing) and/or by observing their rearing associates (i.e., family referencing). However, despite much interest, few empirical studies have successfully disentangled self-referencing and family referencing. Here, we employ a novel set of breeding crosses using the Trinidadian guppy (Poecilia reticulata) to disentangle referencing systems by manipulating exposure to kin from conception onward. We show that guppies discriminate among their full and maternal half siblings, which can be explained only by self-referencing. Additional behavioral experiments revealed no evidence that guppies incorporate the phenotypes of their broodmates or mother into the kin template. Finally, by manipulating the format of our behavioral tests, we show that olfactory communication is both necessary and sufficient for kin discrimination. These results provide robust evidence that individuals recognize kin by comparing the olfactory phenotypes of conspecifics with their own. This study resolves key questions about the proximate mechanisms underpinning kin recognition, with implications for the ontogeny and evolution of social behavior.

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Inbreeding costs can be high in haplodiploid hymenopterans due to their particular mechanism of sex determination (i.e., single-locus complementary sex-determination system, sl-CSD), as it can lead to the production of sterile males. Therefore, mechanisms contributing to reduced inbred matings can be beneficial. In this sense, asynchronous nest departure of sibling drones and gynes could reduce kin encounters in social hymenopterans. Using six observation colonies, we determined under field conditions the nest departure behaviour of sibling reproductives of the social wasp Vespula germanica (Hymenoptera: Vespidae). We determined that sexuals leave the nests definitively and detected asynchronous departure not fixed to a particular caste at a seasonal scale in some colonies, as gynes or drones delayed their departure as a function of the departure of the opposite sex, depending on the colony. At a higher temporal resolution (i.e., within a day), we discovered that drones consistently began to leave nests 1 h before gynes and this difference was driven by those individuals that left on the same day as did the opposite-sex kin. Even though other mechanisms such as polyandry and differential dispersal could also be important at reducing inbred matings in the species, the observed departure patterns (i.e., in some colonies actually leave together with the opposite caste, while in others temporal segregation seems to occur) from nests could be complementary to the former and be important at reducing the negative effects of inbreeding in this invasive species.

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The timing of female maturation in wild mammals is often constrained by ecological variables that relate to food acquisition. However, maturational timing in female mammals can also respond to social variables. Specifically, the arrival of novel males can accelerate maturation while the presence of related males can inhibit it. Despite studies on more than two dozen mammalian taxa in captivity, evidence for male-mediated maturation has not been systematically demonstrated in any wild population. Here, we report the first evidence of male-mediated maturation in a wild primate, the gelada (Theropithecus gelada). After the arrival of a new breeding male in the group (a male takeover), young females were three times more likely to mature. We then examined these takeover-associated maturations in more detail: some were earlier than expected (a presumptive "Vandenbergh effect," or male-accelerated maturation), some were at the expected age for the average female gelada, and some were later than expected (a presumptive "inbreeding avoidance delay," or father-induced reproductive suppression). An examination of fecal estrogens, which rise just before visible signs of maturation in this species, revealed that male takeovers induced a surge in estrogens for immature females of all ages-even females that did not mature. These are the first data to demonstrate that specific males are associated with the onset of maturation in a wild primate and to provide a possible mechanism for this change. These results suggest that all male-mediated maturation (whether accelerated, on-time, or delayed) may be governed by similar neuroendocrine processes.

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Protection and restoration of species in the wild may require conservation breeding programs under genetic management to minimize deleterious effects of genetic changes that occur in captivity, while preserving populations' genetic diversity and evolutionary resilience. Here, through interannual pedigree analyses, we first assessed the efficiency of a 21-year genetic management, including minimization of mean kinship, inbreeding avoidance, and regular addition of founders, of a conservation breeding program targeting on Houbara bustard (Chlamydotis undulata undulata) in Morocco. Secondly, we compared pedigree analyses, the classical way of assessing and managing genetic diversity in captivity, to molecular analyses based on seven microsatellites. Pedigree-based results indicated an efficient maintenance of the genetic diversity (99% of the initial genetic diversity retained) while molecular-based results indicated an increase in allelic richness and an increase in unbiased expected heterozygosity across time. The pedigree-based average inbreeding coefficient F remained low (between 0.0004 and 0.003 in 2017) while the proportion of highly inbred individuals (F > .1) decreased over time and reached 0.2% in 2017. Furthermore, pedigree-based F and molecular-based individual multilocus heterozygosity were weakly negatively correlated, (Pearson's r = -.061 when considering all genotyped individuals), suggesting that they cannot be considered as alternatives, but rather as complementary sources of information. These findings suggest that a strict genetic monitoring and management, based on both pedigree and molecular tools can help mitigate genetic changes and allow to preserve genetic diversity and evolutionary resilience in conservation breeding programs.

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Fisheries often combine high mortality with intensive size selectivity and can, thus, be expected to reduce body size and size variability in exploited populations. In many fish species, body size is a sexually selected trait and plays an important role in mate choice and mate competition. Large individuals are often preferred as mates due to the high fecundity and resources they can provide to developing offspring. Large fish are also successful in competition for mates. Fisheries-induced reductions in size and size variability can potentially disrupt mating systems and lower average reproductive success by decreasing opportunities for sexual selection. By reducing population sizes, fisheries can also lead to an increased level of inbreeding. Some fish species avoid reproducing with kin, and a high level of relatedness in a population can further disrupt mating systems. Reduced body size and size variability can force fish to change their mate preferences or reduce their choosiness. If mate preference is genetically determined, the adaptive response to fisheries-induced changes in size and size variability might not occur rapidly. However, much evidence exists for plastic adjustments of mate choice, suggesting that fish might respond flexibly to changes in their social environment. Here, I first discuss how reduced average body size and size variability in exploited populations might affect mate choice and mate competition. I then consider the effects of sex-biased fisheries on mating systems. Finally, I contemplate the possible effects of inbreeding on mate choice and reproductive success and discuss how mate choice might evolve in exploited populations. Currently, little is known about the mating systems of nonmodel species and about the interplay between size-selective fisheries and sexual selection. Future studies should focus on how reduced size and size variability and increased inbreeding affect fish mating systems, how persistent these effects are, and how this might in turn affect population demography.