MHC class II‐assortative mate choice in European badgers (Meles meles)

The major histocompatibility complex (MHC) plays a crucial role in the immune system, and in some species, it is a target by which individuals choose mates to optimize the fitness of their offspring, potentially mediated by olfactory cues. Under the genetic compatibility hypothesis, individuals are predicted to choose mates with compatible MHC alleles, to increase the fitness of their offspring. Studies of MHC‐based mate choice in wild mammals are under‐represented currently, and few investigate more than one class of MHC genes. We investigated mate choice based on the compatibility of MHC class I and II genes in a wild population of European badgers (Meles meles). We also investigated mate choice based on microsatellite‐derived pairwise relatedness, to attempt to distinguish MHC‐specific effects from genomewide effects. We found MHC‐assortative mating, based on MHC class II, but not class I genes. Parent pairs had smaller MHC class II DRB amino acid distances and smaller functional distances than expected from random pairings. When we separated the analyses into within‐group and neighbouring‐group parent pairs, only neighbouring‐group pairs showed MHC‐assortative mating, due to similarity at MHC class II loci. Our randomizations showed no evidence of genomewide‐based inbreeding, based on 35 microsatellite loci; MHC class II similarity was therefore the apparent target of mate choice. We propose that MHC‐assortative mate choice may be a local adaptation to endemic pathogens, and this assortative mate choice may have contributed to the low MHC genetic diversity in this population.     

No evidence for MHC class I‐based disassortative mating in a wild population of great tits

Genes of the major histocompatibility complex (MHC) are regarded as a potentially important target of mate choice due to the fitness benefits that may be conferred to the offspring. According to the complementary genes hypothesis, females mate with MHC dissimilar males to enhance the immunocompetence of their offspring or to avoid inbreeding depression. Here, we investigate whether selection favours a preference for maximally dissimilar or optimally dissimilar MHC class I types, based on MHC genotypes, average amino acid distances and the functional properties of the antigen‐binding sites (MHC supertypes); and whether MHC type dissimilarity predicts relatedness between mates in a wild great tit population. In particular, we explore the role that MHC class I plays in female mate choice decisions while controlling for relatedness and spatial population structure, and examine the reproductive fitness consequences of MHC compatibility between mates. We find no evidence for the hypotheses that females select mates on the basis of either maximal or optimal MHC class I dissimilarity. A weak correlation between MHC supertype sharing and relatedness suggests that MHC dissimilarity at functional variants may not provide an effective index of relatedness. Moreover, the reproductive success of pairs did not vary with MHC dissimilarity. Our results provide no support for the suggestion that selection favours, or that mate choice realizes, a preference for complimentary MHC types.     

MHC,mate choice and heterozygote advantage in a wild social primate

Preferences for mates carrying dissimilar genes at the major histocompatibility complex (MHC) may help animals increase offspring pathogen resistance or avoid inbreeding. Such preferences have been reported across a range of vertebrates, but have rarely been investigated in social species other than humans. We investigated mate choice and MHC dynamics in wild baboons (Papio ursinus). MHC Class II DRB genes and 16 microsatellite loci were genotyped across six groups (199 individuals). Based on the survey of a key segment of the gene‐rich MHC, we found no evidence of mate choice for MHC dissimilarity, diversity or rare MHC genotypes. First, MHC dissimilarity did not differ from random expectation either between parents of the same offspring or between immigrant males and females from the same troop. Second, female reproductive success was not influenced by MHC diversity or genotype frequency. Third, population genetic structure analysis revealed equally high genotypic differentiation among troops, and comparable excess heterozygosity within troops for juveniles, at both Mhc‐DRB and neutral loci. Nevertheless, the age structure of Mhc‐DRB heterozygosity suggested higher longevity for heterozygotes, which should favour preferences for MHC dissimilarity. We propose that high levels of within‐group outbreeding, resulting from group‐living and sex‐biased dispersal, might weaken selection for MHC‐disassortative mate choice.     

'Good genes as heterozygosity': the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar).

According to the theory of mate choice based on heterozygosity, mates should choose each other in order to increase the heterozygosity of their offspring. In this study, we tested the 'good genes as heterozygosity' hypothesis of mate choice by documenting the mating patterns of wild Atlantic salmon (Salmo salar) using both major histocompatibility complex (MHC) and microsatellite loci. Specifically, we tested the null hypotheses that mate choice in Atlantic salmon is not dependent on the relatedness between potential partners or on the MHC similarity between mates. Three parameters were assessed: (i) the number of shared alleles between partners (x and y) at the MHC (M(xy)), (ii) the MHC amino-acid genotypic distance between mates' genotypes (AA(xy)), and (iii) genetic relatedness between mates (r(xy)). We found that Atlantic salmon choose their mates in order to increase the heterozygosity of their offspring at the MHC and, more specifically, at the peptide-binding region, presumably in order to provide them with better defence against parasites and pathogens. This was supported by a significant difference between the observed and expected AA(xy) (p = 0.0486). Furthermore, mate choice was not a mechanism of overall inbreeding avoidance as genetic relatedness supported a random mating scheme (p = 0.445). This study provides the first evidence that MHC genes influence mate choice in fish.     

Female mating preferences and offspring survival: testing hypotheses on the genetic basis of mate choice in a wild lekking bird

Indirect benefits of mate choice result from increased offspring genetic quality and may be important drivers of female behaviour. ‘Good‐genes‐for‐viability’ models predict that females prefer mates of high additive genetic value, such that offspring survival should correlate with male attractiveness. Mate choice may also vary with genetic diversity (e.g. heterozygosity) or compatibility (e.g. relatedness), where the female's genotype influences choice. The relative importance of these nonexclusive hypotheses remains unclear. Leks offer an excellent opportunity to test their predictions, because lekking males provide no material benefits and choice is relatively unconstrained by social limitations. Using 12 years of data on lekking lance‐tailed manakins, Chiroxiphia lanceolata, we tested whether offspring survival correlated with patterns of mate choice. Offspring recruitment weakly increased with father attractiveness (measured as reproductive success, RS), suggesting attractive males provide, if anything, only minor benefits via offspring viability. Both male RS and offspring survival until fledging increased with male heterozygosity. However, despite parent–offspring correlation in heterozygosity, offspring survival was unrelated to its own or maternal heterozygosity or to parental relatedness, suggesting survival was not enhanced by heterozygosity per se. Instead, offspring survival benefits may reflect inheritance of specific alleles or nongenetic effects. Although inbreeding depression in male RS should select for inbreeding avoidance, mates were not less related than expected under random mating. Although mate heterozygosity and relatedness were correlated, selection on mate choice for heterozygosity appeared stronger than that for relatedness and may be the primary mechanism maintaining genetic variation in this system despite directional sexual selection.     

Can MHC‐assortative partner choice promote offspring diversity? A new combination of MHC‐dependent behaviours among sexes in a highly successful invasive mammal

Sexual selection involving genetically disassortative mate choice is one of several evolutionary processes that can maintain or enhance population genetic variability. Examples of reproductive systems in which choosers (generally females) select mates depending on their major histocompatibility complex (MHC) genes have been reported for several vertebrate species. Notably, the role of MHC‐dependent choice not in mating contexts, but in other kinds of social interactions such as in the establishment of complex social systems, has not yet drawn significant scientific interest and is virtually absent from the literature. We have investigated male and female MHC‐dependent choice in an invasive population of North American raccoons (Procyon lotor) in Germany. Both male and female raccoons rely on olfaction for individual recognition. Males have an unusually complex social system in which older individuals choose unrelated younger ones to form stable male coalitions that defend territories and a monopoly over females. We have confirmed that females perform MHC‐disassortative mate choice and that this behaviour fosters genetic diversity of offspring. We have also observed that males build coalitions by choosing male partners depending on their MHC, but in an assortative manner. This is the first observation of antagonistic MHC‐dependent behaviours among sexes. We show that this is the only combination of MHC‐dependent partner choice that leads to outbreeding. In the case of introduced raccoons, such behaviours can act together to promote the invasive potential of the species by increasing its adaptive genetic divergence.     

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.     

A Test of Inbreeding Avoidance in the Zebra Finch

Optimal-outbreeding theory suggests that the genetic relatedness of individuals may be an important factor in mate choice. Several studies have demonstrated that matings between individuals of intermediate genetic relatedness tend to produce more offspring than those between more closely or distantly related mates. Inbreeding avoidance has been studied in captive zebra finches, Poephila guttata. Slater & Clements (1981) found a preference for closely related individuals, while Evans-Layng (1987), in a different design, found a preference for less related mates. Our study examines patterns of mate choice in small flocks of zebra finches of known genetic relatedness. 13 flocks of 9 birds (3 females and 6 males) were released into separate aviaries and left until pairs had formed. 6 of these flocks consisted of siblings and nonrelatives and 7 consisted of cousins and nonrelatives. The degree of genetic relatedness of the individuals used did not affect mate choice, while factors such as male age and experience were correlated with mating success. There was a marginally significant trend for sibling pairs to take longer to lay eggs, although no overall difference in clutch size among sibling pairs, cousin pairs and genetically unrelated pairs was detected. We conclude, then, that there is no evidence of inbreeding avoidance in captive zebra finches.     

Gene duplication and divergence produce divergent MHC genotypes without disassortative mating

Genes of the major histocompatibility complex (MHC) exhibit heterozygote advantage in immune defence, which in turn can select for MHC‐disassortative mate choice. However, many species lack this expected pattern of MHC‐disassortative mating. A possible explanation lies in evolutionary processes following gene duplication: if two duplicated MHC genes become functionally diverged from each other, offspring will inherit diverse multilocus genotypes even under random mating. We used locus‐specific primers for high‐throughput sequencing of two expressed MHC Class II B genes in Leach's storm‐petrels, Oceanodroma leucorhoa, and found that exon 2 alleles fall into two gene‐specific monophyletic clades. We tested for disassortative vs. random mating at these two functionally diverged Class II B genes, using multiple metrics and different subsets of exon 2 sequence data. With good statistical power, we consistently found random assortment of mates at MHC. Despite random mating, birds had MHC genotypes with functionally diverged alleles, averaging 13 amino acid differences in pairwise comparisons of exon 2 alleles within individuals. To test whether this high MHC diversity in individuals is driven by evolutionary divergence of the two duplicated genes, we built a phylogenetic permutation model. The model showed that genotypic diversity was strongly impacted by sequence divergence between the most common allele of each gene, with a smaller additional impact of monophyly of the two genes. Divergence of allele sequences between genes may have reduced the benefits of actively seeking MHC‐dissimilar mates, in which case the evolutionary history of duplicated genes is shaping the adaptive landscape of sexual selection.     

Major histocompatibility complex similarity and sexual selection: different does not always mean attractive

Females that mate multiply have the possibility to exert postcopulatory choice and select more compatible sperm to fertilize eggs. Prior work suggests that dissimilarity in major histocompatibility complex (MHC) plays an important role in determining genetic compatibility between partners. Favouring a partner with dissimilar MHC alleles would result in offspring with high MHC diversity and therefore with enhanced survival thanks to increased resistance to pathogens and parasites. The high variability of MHC genes may further allow discrimination against the sperm from related males, reducing offspring homozygosity and inbreeding risk. Despite the large body of work conducted at precopulatory level, the role of MHC similarity between partners at postcopulatory level has been rarely investigated. We used an internal fertilizing fish with high level of multiple matings (Poecilia reticulata) to study whether MHC similarity plays a role in determining the outcome of fertilization when sperm from two males compete for the same set of eggs. We also controlled for genomewide similarity by determining similarity at 10 microsatellite loci. Contrary to prediction, we found that the more MHC‐similar male sired more offspring while similarity at the microsatellite loci did not predict the outcome of sperm competition. Our results suggest that MHC discrimination may be involved in avoidance of hybridization or outbreeding rather than inbreeding avoidance. This, coupled with similar findings in salmon, suggests that the preference for MHC‐dissimilar mates is far from being unanimous and that pre‐ and postcopulatory episodes of sexual selection can indeed act in opposite directions.     

No evidence of inbreeding avoidance in a polygynous ungulate: the reindeer (Rangifer tarandus)

In polygynous species, mate choice is an integrated part of sexual selection. However, whether mate choice occurs independently of the genetic relatedness among mating pairs has received little attention, although inbreeding may have fitness consequences. We studied whether genetic relatedness influenced females' choice of partner in a highly polygynous ungulate--the reindeer (Rangifer tarandus)--in an experimental herd during two consecutive rutting seasons; the herd consisting of 75 females in 1999 and 74 females in 2000 was exposed to three 4.5-year-old adults and three 1.5-year-old young males, respectively. The females' distribution during peak rut was not influenced by their genetic relatedness with the dominant males of the mating groups. Further, genetic relatedness did not influence the actual choice of mating partner. We conclude that inbreeding avoidance through mating group choice as well as choice of mating partner, two interconnected processes of female mate choice operating at two different scales in space and time, in such a highly female-biased reindeer populations with low level of inbreeding may not occur.     

No evidence for MHC‐based mate choice in wild giant pandas

Major histocompatibility complex genes (MHC), a gene cluster that controls the immune response to parasites, are regarded as an important determinant of mate choice. However, MHC‐based mate choice studies are especially rare for endangered animals. The giant panda (Ailuropoda melanoleuca), a flagship species, has suffered habitat loss and fragmentation. We investigated the genetic variation of three MHC class II loci, including DRB1, DQA1, and DQA2, for 19 mating‐pairs and 11 parent‐pairs of wild giant pandas based on long‐term field behavior observations and genetic samples. We tested four hypotheses of mate choice based on this MHC variation. We found no supporting evidence for the MHC‐based heterosis, genetic diversity, genetic compatibility and “good gene” hypotheses. These results suggest that giant pandas may not use MHC‐based signals to select mating partners, probably because limited mating opportunities or female‐biased natal dispersal restricts selection for MHC‐based mate choice, acknowledging the caveat of the small sample size often encountered in endangered animal studies. Our study provides insight into the mate choice mechanisms of wild giant pandas and highlights the need to increase the connectivity and facilitate dispersal among fragmented populations and habitats.     

Banded mongooses avoid inbreeding when mating with members of the same natal group

Inbreeding and inbreeding avoidance are key factors in the evolution of animal societies, influencing dispersal and reproductive strategies which can affect relatedness structure and helping behaviours. In cooperative breeding systems, individuals typically avoid inbreeding through reproductive restraint and/or dispersing to breed outside their natal group. However, where groups contain multiple potential mates of varying relatedness, strategies of kin recognition and mate choice may be favoured. Here, we investigate male mate choice and female control of paternity in the banded mongoose (Mungos mungo), a cooperatively breeding mammal where both sexes are often philopatric and mating between relatives is known to occur. We find evidence suggestive of inbreeding depression in banded mongooses, indicating a benefit to avoiding breeding with relatives. Successfully breeding pairs were less related than expected under random mating, which appeared to be driven by both male choice and female control of paternity. Male banded mongooses actively guard females to gain access to mating opportunities, and this guarding behaviour is preferentially directed towards less closely related females. Guard–female relatedness did not affect the guard's probability of gaining reproductive success. However, where mate‐guards are unsuccessful, they lose paternity to males that are less related to the females than themselves. Together, our results suggest that both sexes of banded mongoose use kin discrimination to avoid inbreeding. Although this strategy appears to be rare among cooperative breeders, it may be more prominent in species where relatedness to potential mates is variable, and/or where opportunities for dispersal and mating outside of the group are limited.     

No Inbreeding Avoidance by Female Burying Beetles Regardless of Whether They Encounter Males Simultaneously or Sequentially

Inbreeding avoidance reduces the probability that an individual will mate with a related partner, thereby lowering the risk that it produces inbred offspring suffering from inbreeding depression. Inbreeding avoidance can occur through several mechanisms, including active mate choice, polyandry and sex‐biased dispersal. Here, we focus on the role of active mate choice as a mechanism for inbreeding avoidance. Recent evidence suggests that the experimental design used in mate choice experiments (i.e. simultaneous versus sequential choice) can have a strong impact on the strength of the reported mating preferences. In this study, we examine whether similar effects of experimental design also apply in the context of inbreeding avoidance. To this end, we designed two experiments on the burying beetle Nicrophorus vespilloides that matched two different contexts under which females encounter potential mates in the wild; that is, when females encounter males simultaneously and sequentially. We found that females were as likely to mate with related and unrelated males regardless of whether they encountered male partners simultaneously or sequentially. Thus, our study provides no evidence for inbreeding avoidance in this species, and suggests that the number of mates present did not influence the degree of inbreeding avoidance. We discuss potential explanations for the lack of inbreeding avoidance through mate choice, including lack of mechanisms for recognizing close relatives, low costs and/or low risks of inbreeding and the presence of other inbreeding avoidance mechanisms, such as sex‐biased dispersal and polyandry coupled with post‐copulatory mate choice.     

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.     

Mate choice promotes inbreeding avoidance in the two-spotted spider mite

Since inbreeding in Tetranychus urticae can reduce offspring fitness, sexual selection may favour disassortative mate choice with respect to relatedness of the mating partners. We tested whether T. urticae shows this preference for mating with unrelated partners. We chose an experimental set-up with high potential for female choosiness, since females only mate once and are therefore expected to be the choosier gender. An adult virgin female was placed together with two adult males from the same population. One male was unrelated and the other male was related—a brother with whom she had grown up. Significantly more copulations (64%) took place with the unrelated male. Time to mating did not depend on the female-to-male relatedness. The remaining (non-copulating) male tried to interfere with the ongoing mating in the majority of cases, but this interference did not depend on the female-to-male relatedness. These results imply that T. urticae (a) can recognize kin (via genetic and/or environmental similarity) and (b) has the potential to avoid inbreeding through mate choice.     

Diversification of porcine MHC class II genes: evidence for selective advantage

The major histocompatibility complex (MHC) is an immunological gene-dense region of high diversity in mammalian species. Sus scrofa was domesticated by at least six independent events over Eurasia during the Holocene period. It has been hypothesized that the level and distribution of MHC variation in pig populations reflect genetic selection and environmental influences. In an effort to define the complexity of MHC polymorphisms and the role of selection in the generation of class II gene diversity (DQB, DRB1, and pseudogene ΨDRB3), DNA from globally distributed unrelated domestic pigs of European and Asian origins and a Suidae out-group was analyzed. The number of pseudogene alleles identified (ΨDRB3 33) was greater than those found in the expressed genes (DQB 20 and DRB1 23) but the level of observed heterozygosity (ΨDRB3 0.452, DQB 0.732, and DRB1 0.767) and sequence diversity (ΨDRB3 0.029, DQB 0.062, and DRB1 0.074) were significantly lower in the pseudogene, respectively. The substitution ratios reflected an excess of d _N (DQB 1.476, DRB1 1.724, and ΨDRB3 0.508) and the persistence of expressed gene alleles suggesting the influence of balancing selection, while the pseudogene was undergoing purifying selection. The lack of a clear MHC phylogeographic tree, coupled with close genetic distances observed between the European and Asian populations (DQB 0.047 and DRB1 0.063) suggested that unlike observations using mtDNA, the MHC diversity lacks phylogeographic structure and appears to be globally uniform. Taken together, these results suggest that, despite regional differences in selective breeding and environments, no skewing of MHC diversity has occurred. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

No evidence for inbreeding avoidance in a natural population of song sparrows (Melospiza melodia)

We studied mate choice and inbreeding avoidance a natural population of song sparrows (Melospiza melodia) on Mandarte Island, Canada. Inbreeding occurred regularly: 59% all matings were between known relatives. We tested for inbreeding avoidance by comparing the observed levels of inbreeding to those expected if mate choice had been random with respect to relatedness. Independent of our assumptions about the availability of mates in the random mating model, we found that the expected and observed distributions of inbreeding coefficients were similar, as was the expected and observed frequency of close (f >/= 0.125) inbreeding. Furthermore, there was no difference in relatedness observed pairs and those that would have resulted had birds mated instead with their nearest neighbors. The only evidence to suggest any inbreeding avoidance was a reduced rate of parent-offspring matings as compared to one random mating model but not the other. Hence, despite substantial inbreeding depression in this population, we found little evidence for inbreeding avoidance through mate choice. We present a simple model to suggest that variation in inbreeding avoidance behaviors in birds may arise from differences in survival rates: in species with low survival rates, the costs of forfeiting matings to avoid inbreeding may exceed the costs of inbreeding.     

The hidden benefits of sex: Evidence for MHC‐associated mate choice in primate societies

Major histocompatibility complex (MHC)‐associated mate choice is thought to give offspring a fitness advantage through disease resistance. Primates offer a unique opportunity to understand MHC‐associated mate choice within our own zoological order, while their social diversity provides an exceptional setting to examine the genetic determinants and consequences of mate choice in animal societies. Although mate choice is constrained by social context, increasing evidence shows that MHC‐dependent mate choice occurs across the order in a variety of socio‐sexual systems and favours mates with dissimilar, diverse or specific genotypes non‐exclusively. Recent research has also identified phenotypic indicators of MHC quality. Moreover, novel findings rehabilitate the importance of olfactory cues in signalling MHC genes and influencing primate mating decisions. These findings underline the importance to females of selecting a sexual partner of high genetic quality, as well as the generality of the role of MHC genes in sexual selection.     

Absence of Evidence for MHC–Dependent Mate Selection within HapMap Populations

The major histocompatibility complex (MHC) of immunity genes has been reported to influence mate choice in vertebrates, and a recent study presented genetic evidence for this effect in humans. Specifically, greater dissimilarity at the MHC locus was reported for European-American mates (parents in HapMap Phase 2 trios) than for non-mates. Here we show that the results depend on a few extreme data points, are not robust to conservative changes in the analysis procedure, and cannot be reproduced in an equivalent but independent set of European-American mates. Although some evidence suggests an avoidance of extreme MHC similarity between mates, rather than a preference for dissimilarity, limited sample sizes preclude a rigorous investigation. In summary, fine-scale molecular-genetic data do not conclusively support the hypothesis that mate selection in humans is influenced by the MHC locus.