MHC odours are not required or sufficient for recognition of individual scent owners

To provide information about specific depositors, scent marks need to encode a stable signal of individual ownership. The highly polymorphic major histocompatibility complex (MHC) influences scents and contributes to the recognition of close kin and avoidance of inbreeding when MHC haplotypes are shared. MHC diversity between individuals has also been proposed as a primary source of scents used in individual recognition. We tested this in the context of scent owner recognition among male mice, which scent mark their territories and countermark scents from other males. We examined responses towards urine scent according to the scent owner's genetic difference to the territory owner (MHC, genetic background, both and neither) or genetic match to a familiar neighbour. While urine of a different genetic background from the subject always stimulated greater scent marking than own, regardless of familiarity, MHC-associated odours were neither necessary nor sufficient for scent owner recognition and failed to stimulate countermarking. Urine of a different MHC type to the subject stimulated increased investigation only when this matched both the MHC and genetic background of a familiar neighbour. We propose an associative model of scent owner recognition in which volatile scent profiles, contributed by both fixed genetic and varying non-genetic factors, are learnt in association with a stable involatile ownership signal provided by other highly polymorphic urine components.     

The direct assessment of genetic heterozygosity through scent in the mouse

The role of individual genetic heterozygosity in mate choice is the subject of much current debate. Several recent studies have reported female preference for more heterozygous males, but the mechanisms underlying heterozygote preference remain largely unknown. Females could favor males that are more successful in intrasexual competition, but they could also assess male heterozygosity directly at specific polymorphic genetic markers. Here, we use a breeding program to remove the intrinsic correlation between genome-wide heterozygosity and two highly polymorphic gene clusters that could allow direct assessment of heterozygosity through scent in mice: the major histocompatibility complex (MHC) and the major urinary proteins (MUPs). When other sources of variation are controlled and intrasexual competition is minimized, female mice prefer to associate with MUP heterozygous over MUP homozygous males. MHC heterozygosity does not influence preference, and neither does heterozygosity across the rest of the genome when intrasexual competition between males is restricted. Female mice thus assess male heterozygosity directly through multiple MUP isoforms expressed in scent signals, independently of the effects of genome-wide heterozygosity on male competitiveness. This is the first evidence that animals may use signals of genetic heterozygosity that have no direct association with individual vigour.     

The major histocompatibility complex and mating preferences in wild house mice (mus domesticus)

This study examined the relationship between the major histocompatibilitycomplex (MHC) genes and mate choice by wild house mice in acontrolled laboratory setting in an attempt to understand themechanisms maintaining natural MHC diversity. Three rearinggroups of wild test mice were produced: nonfostered controlmice, mice fostered into families of an inbred laboratory mousestrain, and mice fostered into families of a second mouse straindiffering genetically from the first only within the MHC region.At maturity, test mice were given a choice of two opposite-sexstimulus mice of the two MHC-congenic strains used for fostering.Test mice were scored for several measures of preference includingamount of time spent with either stimulus mouse, and ejaculationwith a stimulus mouse. Females in two of three rearing groupsspent more time with one MHC type regardless of rearing environment,suggesting that females did not prefer mates dissimilar fromfamily MHC type. Time preferences tended to be stronger in femalesthan in males. Male test mice ejaculated indiscriminantly. Femalewild mice mated to ejaculation more often in longer trials,but these matings were still too infrequent to assess preferences.Fostering had little or no effect on MHC-based mate preferencesof wild house mice, and no evidence suggested that MHC was usedto avoid inbreeding. Wild female mice may still choose matesbased on MHC haplotypes (but do not necessarily prefer MHC-dissimilarmates); other cues are probably also used. Based on these results,inbreeding avoidance does not seem a strong mechanism for maintainingnatural MHC diversity     

Kin discrimination and female mate choice in the naked mole-rat Heterocephalus glaber

Naked mole-rats are fossorial, eusocial rodents that naturally exhibit high levels of inbreeding. Persistent inbreeding in animals often results in a substantial decline in fitness and, thus, dispersal and avoidance of kin as mates are two common inbreeding avoidance mechanisms. In the naked mole-rat evidence for the former has recently been found. Here we address the latter mechanism by investigating kin recognition and female mate choice using a series of choice tests in which the odour, social and mate preferences of females were determined. Discrimination by females appears to be dependent on their reproductive status. Reproductively active females prefer to associate with unfamiliar males, whereas reproductively inactive females do not discriminate. Females do not discriminate between kin and non-kin suggesting that the criterion for recognition is familiarity, not detection of genetic similarity per se. In the wild, naked mole-rats occupy discrete burrow systems and dispersal and mixing with non-kin is thought to be comparatively rare. Thus, recognition by familiarity may function as a highly efficient kin recognition mechanism in the naked mole-rat. A preference by reproductively active females for unfamiliar males is interpreted as inbreeding avoidance. These findings suggest that, despite an evolutionary history of close inbreeding, naked mole-rats may not be exempt from the effects of inbreeding depression and will attempt to outbreed should the opportunity arise.     

Inbreeding avoidance mechanisms: dispersal dynamics in cooperatively breeding southern pied babblers

1.?Breeding with kin can reduce individual fitness through the deleterious effects of inbreeding depression. Inbreeding avoidance mechanisms are expected to have developed in most species, and especially in cooperatively breeding species where individuals may delay dispersal until long after sexual maturity. Such potential mechanisms include sex-biased dispersal and avoidance of kin known through associative learning. 2.?The investigation of inbreeding avoidance through dispersal dynamics can be enhanced by combining fine-scale population genetic structure data with detailed behavioural observations of wild populations. 3.?We investigate possible inbreeding avoidance in a wild population of cooperatively breeding southern pied babblers (Turdoides bicolor). A combination of genetic, geographic and observational data is used to examine fine-scale genetic structure, dispersal (including sex-biased dispersal) and inheritance of dominance in cooperatively breeding groups. 4.?Unusually, sex-bias in dispersal distance does not occur. Rather, individuals appear to avoid inbreeding through two routes. First, through dispersal itself: although both males and females disperse locally, they move outside the range within which genetically similar individuals are usually found, going twice as far from natal groups as from non-natal groups. Second, through avoidance of familiar group members as mates: individuals inherit a dominant position in the natal group only when an unrelated breeding partner is present. 5.?This study uses spatial genetic analyses to investigate inbreeding avoidance mechanisms in a cooperative breeder and shows that individuals of both sexes can avoid inbreeding through a dispersal distance mechanism. While it appears that dispersal allows most individuals to move beyond the range of closely related kin, matings may still occur between distant kin. Nevertheless, any costs of breeding with a distant relative may be outweighed by the benefits of local dispersal and the immense fitness gains available from attaining a breeding position.     

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.     

The Scent of Genetic Compatibility: Sexual Selection and the Major Histocompatibility Complex

Individuals in some species prefer mates carrying dissimilar genes at the major histocompatibility complex (MHC), which may function to increase the MHC or overall heterozygosity of progeny. Here I review the evidence for MHC-dependent mating preferences from recent studies, including studies on the underlying olfactory mechanisms and evolutionary functions. Many studies indicate that MHC genes influence odour, and some work is beginning to examine the potential role of MHC-linked olfactory receptor genes in mating preferences. MHC-dependent mating preference increases the MHC-heterozygosity of progeny, which is suspected to confer resistance to infectious diseases. In humans, heterozygosity at MHC loci is associated with increased resistance to hepatitis and HIV infections, but experimental evidence for the heterozygote advantage hypothesis has been lacking. Here I re-analyse data from previously published experimental infection studies with mice. I show that although overdominance is rare, resistance is often dominant, suggesting that heterozygotes are often protected. A second (nonmutually exclusive) possibility is that MHC-disassortative mating preferences promotes inbreeding avoidance. This hypothesis is supported by recent evidence that MHC genes play a role in kin recognition, and that mating with close kin has rather deleterious fitness consequences. In conclusion, I discuss other ways that MHC genes might influence sexual selection. The research on MHC-mediated mating preferences is integrating the study of animal behaviour with other seemingly disparate fields, including sensory biology and immunogenetics.     

The inbreeding strategy of a solitary primate,Microcebus murinus

Inbreeding depression may be common in nature, reflecting either the failure of inbreeding avoidance strategies or inbreeding tolerance when avoidance is costly. The combined assessment of inbreeding risk, avoidance and depression is therefore fundamental to evaluate the inbreeding strategy of a population, that is how individuals respond to the risk of inbreeding. Here, we use the demographic and genetic monitoring of 10 generations of wild grey mouse lemurs (Microcebus murinus), small primates from Madagascar with overlapping generations, to examine their inbreeding strategy. Grey mouse lemurs have retained ancestral mammalian traits, including solitary lifestyle, polygynandry and male‐biased dispersal, and may therefore offer a representative example of the inbreeding strategy of solitary mammals. The occurrence of close kin among candidate mates was frequent in young females (~37%, most often the father) and uncommon in young males (~6%) due to male‐biased dispersal. However, close kin consistently represented a tiny fraction of candidate mates (< 1%) across age and sex categories. Mating biases favouring partners with intermediate relatedness were detectable in yearling females and adult males, possibly partly caused by avoidance of daughter–father matings. Finally, inbreeding depression, assessed as the effect of heterozygosity on survival, was undetectable using a capture–mark–recapture study. Overall, these results indicate that sex‐biased dispersal is a primary inbreeding avoidance mechanism at the population level, and mating biases represent an additional strategy that may mitigate residual inbreeding costs at the individual level. Combined, these mechanisms explain the rarity of inbreeding and the lack of detectable inbreeding depression in this large, genetically diverse population.     

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.     

MHC-disassortative mating preferences reversed by cross-fostering.

House mice (Mus musculus domesticus) avoid mating with individuals that are genetically similar at the major histocompatibility complex (MHC). Mice are able recognize MHC-similar individuals through specific odour cues. However, to mate disassortatively for MHC genes, individuals must have a referent, either themselves (self-inspection) or close kin (familial imprinting), with which to compare the MHC identity of potential mates. Although studies on MHC-dependent mating preferences often assume that individuals use self-inspection, laboratory experiments with male mice indicate that they use familial imprinting, i.e. males learn the MHC identity of their family and then avoid mating with females carrying ''familial'' MHC alleles. To determine if female mice use familial imprinting, we cross-fostered wild-derived female mouse pups into MHC-dissimilar families, and then tested if this procedure reversed their mating preferences compared with in-fostered controls. Our observations of the female''s mating behaviour in seminatural social conditions and the genetic typing of their progeny both indicated that females avoided mating with males carrying MHC genes of their foster family, supporting the familial imprinting hypothesis. We show that MHC-dependent familial imprinting potentially provides a more effective mechanism for avoiding kin matings and reducing inbreeding than self-inspection.     

Inbreeding avoidance through non-random mating in sticklebacks

Negative effects of inbreeding are well documented in a wide range of animal taxa. Hatching success and survival of inbred offspring is reduced in many species and inbred progeny are often less attractive to potential mates. Thus, individuals should avoid mating with close kin. However, experimental evidence for inbreeding avoidance through non-random mating in vertebrates is scarce. Here, we show that gravid female three-spined sticklebacks (Gasterosteus aculeatus) when given the choice between a courting familiar brother and a courting unfamiliar non-sib prefer to mate with the non-sib and thus avoid the disadvantages of incest. We controlled for differences in males' body size and red intensity of nuptial coloration. Thus, females adjust their courting behaviour to the risk of inbreeding.     

Inbreeding avoidance influences the viability of reintroduced populations of African wild dogs (Lycaon pictus)

The conservation of many fragmented and small populations of endangered African wild dogs (Lycaon pictus) relies on understanding the natural processes affecting genetic diversity, demographics, and future viability. We used extensive behavioural, life-history, and genetic data from reintroduced African wild dogs in South Africa to (1) test for inbreeding avoidance via mate selection and (2) model the potential consequences of avoidance on population persistence. Results suggested that wild dogs avoided mating with kin. Inbreeding was rare in natal packs, after reproductive vacancies, and between sibling cohorts (observed on 0.8%, 12.5%, and 3.8% of occasions, respectively). Only one of the six (16.7%) breeding pairs confirmed as third-order (or closer) kin consisted of animals that were familiar with each other, while no other paired individuals had any prior association. Computer-simulated populations allowed to experience inbreeding had only a 1.6% probability of extinction within 100 years, whereas all populations avoiding incestuous matings became extinct due to the absence of unrelated mates. Populations that avoided mating with first-order relatives became extinct after 63 years compared with persistence of 37 and 19 years for those also prevented from second-order and third-order matings, respectively. Although stronger inbreeding avoidance maintains significantly more genetic variation, our results demonstrate the potentially severe demographic impacts of reduced numbers of suitable mates on the future viability of small, isolated wild dog populations. The rapid rate of population decline suggests that extinction may occur before inbreeding depression is observed.     

GENETIC SIMILARITY BETWEEN PARENTS PREDICTS HATCHING FAILURE: NONINCESTUOUS INBREEDING IN THE GREAT REED WARBLER?

The DNA-fingerprinting technique was used to find the true pedigrees and to detect the overall genetic similarity between mates of great reed warblers (Acrocephalus arundinaceus) at an isolated breeding site in Sweden. The study covered 4 yr preceded by 3 yr when almost all adults and nestlings in the study area had been banded. DNA fingerprinting revealed that the putative father had sired 97% of the young (N = 455). The mate's genetic similarity, revealed as the proportion of bands shared in restriction fragment length polymorphism (RFLP) patterns, was high compared with other species of wild birds. Also, band sharing was higher between mates native to the area than between pairs in which the female was experimentally introduced from a distant breeding site. Hatching success of eggs was negatively correlated with the degree of genetic similarity between the mates, whereas pedigree data, up to the level of great-grandparents, clearly demonstrated an absence of close inbreeding. These are the first data showing a significant fitness cost associated with the choice of a mate that has high genetic similarity, even if it is not a close kin. This cost might be caused by generalized negative consequences of genomewide inbreeding in the present study, possibly accentuated by recent population bottlenecks.     

MHC‐disassortative mate choice and inbreeding avoidance in a solitary primate

Sexual selection theory suggests that choice for partners carrying dissimilar genes at the major histocompatibility complex (MHC) may play a role in maintaining genetic variation in animal populations by limiting inbreeding or improving the immunity of future offspring. However, it is often difficult to establish whether the observed MHC dissimilarity among mates drives mate choice or represents a by‐product of inbreeding avoidance based on MHC‐independent cues. Here, we used 454‐sequencing and a 10‐year study of wild grey mouse lemurs (Microcebus murinus), small, solitary primates from western Madagascar, to compare the relative importance on the mate choice of two MHC class II genes, DRB and DQB, that are equally variable but display contrasting patterns of selection at the molecular level, with DRB under stronger diversifying selection. We further assessed the effect of the genetic relatedness and of the spatial distance among candidate mates on the detection of MHC‐dependent mate choice. Our results reveal inbreeding avoidance, along with disassortative mate choice at DRB, but not at DQB. DRB‐disassortative mate choice remains detectable after excluding all related dyads (characterized by a relatedness coefficient r > 0), but varies slightly with the spatial distance among candidate mates. These findings suggest that the observed deviations from random mate choice at MHC are driven by functionally important MHC genes (like DRB) rather than passively resulting from inbreeding avoidance and further emphasize the need for taking into account the spatial and genetic structure of the population in correlative tests of MHC‐dependent mate choice.     

The genetic basis of individual-recognition signals in the mouse

The major histocompatibility complex (MHC) is widely assumed to be a primary determinant of individual-recognition scents in many vertebrates [1-6], but there has been no functional test of this in animals with normal levels of genetic variation. Mice have evolved another polygenic and highly polymorphic set of proteins for scent communication, the major urinary proteins (MUPs) [7-12], which may provide a more reliable identity signature ([13, 14] and A.L. Sherborne, M.D.T., S. Paterson, F.J., W.E.R.O., P. Stockley, R.J.B., and J.L.H., unpublished data). We used female preference for males that countermark competitor male scents [15-17] to test the ability of wild-derived mice to recognize individual males differing in MHC or MUP type on a variable genetic background. Differences in MHC type were not used for individual recognition. Instead, recognition depended on a difference in MUP type, regardless of other genetic differences between individuals. Recognition also required scent contact, consistent with detection of involatile components through the vomeronasal system [6, 18]. Other differences in individual scent stimulated investigation but did not result in individual recognition. Contrary to untested assumptions of a vertebrate-wide mechanism based largely on MHC variation, mice use a species-specific [12] individual identity signature that can be recognized reliably despite the complex internal and external factors that influence scents [2]. Specific signals for genetic identity recognition in other species now need to be investigated.     

Major histocompatibility complex and kin discrimination in Atlantic salmon and brook trout

Many species of salmonids can discriminate kin from unrelated conspecifics using olfactory cues. In this study, we determined the role of the major histocompatibility complex (MHC) in kin discrimination by juvenile Atlantic salmon (Salmo salar) and brook trout (Salvelinus fontinalis). Genetic variation at the highly polymorphic exon coding for peptide-binding region of an MHC class II gene was studied using polymerase chain reaction and denaturing gradient gel electrophoresis. Experiments compared discrimination ability based on MHC haplotypes both within and among kin and non-kin groups. Juveniles chose kin sharing both alleles over kin sharing no alleles. Juveniles also preferred non-kin sharing both alleles to non-kin sharing no alleles. These data suggest that the MHC class II gene influence kin discrimination in juvenile Atlantic salmon and brook trout. The influence of additional genes was also apparent in trials where juveniles were able to recognize kin sharing no alleles over non-kin sharing no alleles. However, the inability of juveniles to discriminate between kin sharing no alleles and non-kin sharing either one or both alleles indicates that MHC is as potent as the rest of the genome in producing distinguishable odours.     

Sequence-based evidence for major histocompatibility complex-disassortative mating in a colonial seabird

The major histocompatibility complex (MHC) is a polymorphic gene family associated with immune defence, and it can play a role in mate choice. Under the genetic compatibility hypothesis, females choose mates that differ genetically from their own MHC genotypes, avoiding inbreeding and/or enhancing the immunocompetence of their offspring. We tested this hypothesis of disassortative mating based on MHC genotypes in a population of great frigatebirds (Fregata minor) by sequencing the second exon of MHC class II B. Extensive haploid cloning yielded two to four alleles per individual, suggesting the amplification of two genes. MHC similarity between mates was not significantly different between pairs that did (n = 4) or did not (n = 42) exhibit extra-pair paternity. Comparing all 46 mated pairs to a distribution based on randomized re-pairings, we observed the following (i): no evidence for mate choice based on maximal or intermediate levels of MHC allele sharing (ii), significantly disassortative mating based on similarity of MHC amino acid sequences, and (iii) no evidence for mate choice based on microsatellite alleles, as measured by either allele sharing or similarity in allele size. This suggests that females choose mates that differ genetically from themselves at MHC loci, but not as an inbreeding-avoidance mechanism.     

The transition to social inbred mating systems in spiders: role of inbreeding tolerance in a subsocial predecessor

The social spiders are unusual among cooperatively breeding animals in being highly inbred. In contrast, most other social organisms are outbred owing to inbreeding avoidance mechanisms. The social spiders appear to originate from solitary subsocial ancestors, implying a transition from outbreeding to inbreeding mating systems. Such a transition may be constrained by inbreeding avoidance tactics or fitness loss due to inbreeding depression. We examined whether the mating system of a subsocial spider, in a genus with three social congeners, is likely to facilitate or hinder the transition to inbreeding social systems. Populations of subsocial Stegodyphus lineatus are substructured and spiders occur in patches, which may consist of kin groups. We investigated whether male mating dispersal prevents matings within kin groups in natural populations. Approximately half of the marked males that were recovered made short moves (< 5m) and mated within their natal patch. This potential for inbreeding was counterbalanced by a relatively high proportion of immigrant males. In mating experiments, we tested whether inbreeding actually results in lower offspring fitness. Two levels of inbreeding were tested: full sibling versus non-sib matings and matings of individuals within and between naturally occurring patches of spiders. Neither full siblings nor patch mates were discriminated against as mates. Sibling matings had no effect on direct fitness traits such as fecundity, hatching success, time to hatching and survival of the offspring, but negatively affected offspring growth rates and adult body size of both males and females. Neither direct nor indirect fitness measures differed significantly between within patch and between-patch pairs. We tested the relatedness between patch mates and nonpatch mates using DNA fingerprinting (TE-AFLP). Kinship explained 30% of the genetic variation among patches, confirming that patches are often composed of kin. Overall, we found limited male dispersal, lack of kin discrimination, and tolerance to low levels of inbreeding. These results suggest a history of inbreeding which may reduce the frequency of deleterious recessive alleles in the population and promote the evolution of inbreeding tolerance. It is likely that the lack of inbreeding avoidance in subsocial predecessors has facilitated the transition to regular inbreeding social systems.     

Paternal kin discrimination in wild baboons.

Mammals commonly avoid mating with maternal kin, probably as a result of selection for inbreeding avoidance. Mating with paternal kin should be selected against for the same reason. However, identifying paternal kin may be more difficult than identifying maternal kin in species where the mother mates with more than one male. Selection should nonetheless favour a mechanism of paternal kin recognition that allows the same level of discrimination among paternal as among maternal kin, but the hypothesis that paternal kin avoid each other as mates is largely untested in large mammals such as primates. Here I report that among wild baboons, Papio cynocephalus, paternal siblings exhibited lower levels of affiliative and sexual behaviour during sexual consortships than non-kin, although paternal siblings were not significantly less likely to consort than non-kin. I also examined age proximity as a possible social cue of paternal relatedness, because age cohorts are likely to be paternal sibships. Pairs born within two years of each other were less likely to engage in sexual consortships than pairs born at greater intervals, and were less affiliative and sexual when they did consort. Age proximity may thus be an important social cue for paternal relatedness, and phenotype matching based on shared paternal traits may play a role as well.     

Inbreeding and promiscuity in the endangered grand skink

The inbreeding avoidance hypothesis predicts that organisms that often encounter relatives as potential mates should evolve behaviours to avoid incestuous matings. Avoidance behaviours have practical importance for small populations because deleterious genetic processes may be less imminent than otherwise expected from genetic models that assume random mating. I used genetic techniques to investigate the extent of inbreeding and inbreeding avoidance behaviours in rare lizards from southern New Zealand. Grand skinks, Oligosoma grande, live in small patchily distributed groups, and have low rates of inter-group dispersal (ca. 3–20% disperse). I used data from 15 microsatellite loci to test the hypothesis that adults are likely to encounter kin as potential mates and will inbreed. These data showed that adult skinks usually inhabited rock outcrops with adult relatives of the opposite sex – up to 35% of potential mates were of equivalent relatedness as half-sibs and 17% were equivalent to full sibs. However, skinks did not preferentially breed with less related mates, and 18.2% of matings were between individuals of equivalent relatedness as full-sibs. Instead, skinks mated with partners of all levels of relatedness, and were promiscuous – almost half of adult females and nearly three quarters of adult males reproduced with multiple partners. In addition, inbreeding had no effect on survival of offspring in their first year. Two other putative mechanisms of inbreeding avoidance, sex-biased and natal dispersal, were not pronounced in this species. This study adds to a growing list of species that inbreed despite the risks.