Mate choice for major histocompatibility complex genetic divergence as a bet-hedging strategy in the Atlantic salmon (Salmo salar)

Major histocompatibility complex (MHC)-dependent mating preferences have been observed across vertebrate taxa and these preferences are expected to promote offspring disease resistance and ultimately, viability. However, little empirical evidence linking MHC-dependent mate choice and fitness is available, particularly in wild populations. Here, we explore the adaptive potential of previously observed patterns of MHC-dependent mate choice in a wild population of Atlantic salmon (Salmo salar) in Québec, Canada, by examining the relationship between MHC genetic variation and adult reproductive success and offspring survival over 3 years of study. While Atlantic salmon choose their mates in order to increase MHC diversity in offspring, adult reproductive success was in fact maximized between pairs exhibiting an intermediate level of MHC dissimilarity. Moreover, patterns of offspring survival between years 0+ and 1+, and 1+ and 2+ and population genetic structure at the MHC locus relative to microsatellite loci indicate that strong temporal variation in selection is likely to be operating on the MHC. We interpret MHC-dependent mate choice for diversity as a likely bet-hedging strategy that maximizes parental fitness in the face of temporally variable and unpredictable natural selection pressures.     

MHC class II DRB diversity, selection pattern and population structure in a neotropical bat species, Noctilio albiventris

Genes of the major histocompatibility complex (MHC) have a crucial role in the immune response of vertebrates, alter the individual odour and are involved in shaping mating preferences. Pathogen-mediated selection, sexual selection and maternal-fetal interactions have been proposed as the main drivers of frequently observed high levels of polymorphism in functionally important parts of the MHC. Bats constitute the second largest mammalian order and have recently emerged as important vectors of infectious diseases. In addition, Chiroptera are interesting study subjects in evolutionary ecology in the context of olfactory communication, mate choice and associated fitness benefits. Thus, it is surprising that they belong to the least studied mammalian taxa in terms of their MHC diversity. In this study, we investigated the variability in the functionally important MHC class II gene DRB, evidence for selection and population structure in the group-living lesser bulldog bat, Noctilio albiventris, in Panama. We found a single expressed, polymorphic Noal-DRB gene. The substitution pattern of the nucleotide sequences of the 18 detected alleles provided evidence for positive selection acting above the evolutionary history of the species in shaping MHC diversity. Roosting colonies were not genetically differentiated but females showed lower levels of heterozygosity than males, which might be a sign that the sexes differ in the selection pressures acting on the MHC. This study provides the prerequisites for further investigations of the role of the individual MHC constitution in parasite resistance, olfactory communication and mate choice in N. albiventris and other bats.     

Males with high genetic similarity to females sire more offspring in sperm competition in Peron's tree frog Litoria peronii

Recent work has confirmed that genetic compatibility among mates can be an important determinant of siring success in sperm competition experiments and in free-ranging populations. Most of this work points towards mate choice of less related mates. However, there may also be the potential for mate choice for intermediate or even genetically similar mates to prevent outbreeding depression or hybridization with closely related taxa. We studied relatedness effects on post-copulatory gametic choice and/or sperm competition in an external fertilizer, Peron's tree frog (Litoria peronii), since external fertilizers offer exceptional control in order to test gametic interaction effects on probability of paternity and zygote viability. Sperm competition experiments were done blindly with respect to genetic relatedness among males and females. Thereafter, paternity of offspring was assigned using eight microsatellite loci. Three hybridization trials between L. peronii and a closely related sympatric species Litoria tyleri were also carried out. In the sperm competition trials, males that are more genetically similar to the female achieved higher siring success compared with less genetically similar males. The hybridization trials confirmed that the two species can interbreed and we suggest that the risk of hybridization may contribute to selection benefits for genetically more similar males at fertilization. To our knowledge, this study is the first to show evidence for post-copulatory selection of sperm from genetically more similar individuals within a natural population.     

Odour signals major histocompatibility complex genotype in an Old World monkey

The major histocompatibility complex (MHC) is an extraordinarily diverse cluster of genes that play a key role in the immune system. MHC gene products are also found in various body secretions, leading to the suggestion that MHC genotypes are linked to unique individual odourtypes that animals use to assess the suitability of other individuals as potential mates or social partners. We investigated the relationship between chemical odour profiles and genotype in a large, naturally reproducing population of mandrills, using gas chromatography–mass spectrometry and MHC genotyping. Odour profiles were not linked to the possession of particular MHC supertypes. Sex influenced some measures of odour diversity and dominance rank influenced some measures of odour diversity in males, but not in females. Odour similarity was strongly related to similarity at the MHC, and, in some cases, to pedigree relatedness. Our results suggest that odour provides both a cue of individual genetic quality and information against which the receiver can compare its own genotype to assess genetic similarity. These findings provide a potential mechanism underlying mate choice for genetic diversity and MHC similarity as well as kin selection.     

MHC-mediated mate choice increases parasite resistance in salmon

Natural (parasite-driven) and sexual selection are thought to maintain high polymorphism in the genes of the major histocompatibility complex (MHC), but support for a link between mate choice, MHC variation and increased parasite resistance is circumstantial. We compared MHC diversity and Anisakis loads among anadromous Atlantic salmon (Salmo salar L.) returning to four rivers to spawn, which had originated from natural spawning (parents allowed to mate freely) or artificial crosses (parents deprived from the potential benefits of mate choice). We found that the offspring of artificially bred salmon had higher parasite loads and were almost four times more likely to be infected than free-mating salmon, despite having similar levels of MHC diversity. Moreover, the offspring of wild salmon were more MHC dissimilar than the offspring of artificially crossed salmon, and uninfected fish were more dissimilar for MHC than infected fish. Thus, our results suggest a link between disassortative mating and offspring benefits and indicate that MHC-mediated mate choice and natural (parasite-driven) selection act in combination to maintain MHC diversity, and hence fitness. Therefore, artificial breeding programmes that negate the potential genetic benefits of mate choice may result in inherently inferior offspring, regardless of population size, rearing conditions or genetic diversity.     

MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler

The existence and nature of indirect genetic benefits to mate choice remain contentious. Major histocompatibility complex (MHC) genes, which play a vital role in determining pathogen resistance in vertebrates, may be the link between mate choice and the genetic inheritance of vigour in offspring. Studies have shown that MHC-dependent mate choice can occur in mammal and fish species, but little work has focused on the role of the MHC in birds. We tested for MHC-dependent mating patterns in the Seychelles warbler (Acrocephalus sechellensis). There was no influence of MHC class I exon 3 variation on the choice of social mate. However, females were more likely to obtain extra-pair paternity (EPP) when their social mate had low MHC diversity, and the MHC diversity of the extra-pair male was significantly higher than that of the cuckolded male. There was no evidence that females were mating disassortatively, or that they preferred males with an intermediate number of MHC bands. Overall, the results are consistent with the 'good genes' rather than the 'genetic compatibility' hypothesis. As female choice will result in offspring of higher MHC diversity, MHC-dependent EPP may provide indirect benefits in the Seychelles warbler if survival is positively linked to MHC diversity.     

Extra‐pair mating in a passerine bird with highly duplicated major histocompatibility complex class II: Preference for the golden mean

Genes of the major histocompatibility complex (MHC) are essential in vertebrate adaptive immunity, and they are highly diverse and duplicated in many lineages. While it is widely established that pathogen‐mediated selection maintains MHC diversity through balancing selection, the role of mate choice in shaping MHC diversity is debated. Here, we investigate female mating preferences for MHC class II (MHCII) in the bluethroat (Luscinia svecica), a passerine bird with high levels of extra‐pair paternity and extremely duplicated MHCII. We genotyped family samples with mixed brood paternity and categorized their MHCII alleles according to their functional properties in peptide binding. Our results strongly indicate that females select extra‐pair males in a nonrandom, self‐matching manner that provides offspring with an allelic repertoire size closer to the population mean, as compared to offspring sired by the social male. This is consistent with a compatible genes model for extra‐pair mate choice where the optimal allelic diversity is intermediate, not maximal. This golden mean presumably reflects a trade‐off between maximizing pathogen recognition benefits and minimizing autoimmunity costs. Our study exemplifies how mate choice can reduce the population variance in individual MHC diversity and exert strong stabilizing selection on the trait. It also supports the hypothesis that extra‐pair mating is adaptive through altered genetic constitution in offspring.     

MHC-associated mating strategies and the importance of overall genetic diversity in an obligate pair-living primate

Mate choice is one of the most important evolutionary mechanisms. Females can improve their fitness by selectively mating with certain males. We studied possible genetic benefits in the obligate pair-living fat-tailed dwarf lemur (Cheirogaleus medius) which maintains life-long pair bonds but has an extremely high rate of extra-pair paternity. Possible mechanisms of female mate choice were investigated by analyzing overall genetic variability (neutral microsatellite marker) as well as a marker of adaptive significance (major histocompatibility complex, MHC-DRB exon 2). As in human medical studies, MHC-alleles were grouped to MHC-supertypes based on similarities in their functional important antigen binding sites. The study indicated that females preferred males both as social and as genetic fathers for their offspring having a higher number of MHC-alleles and MHC-supertypes, a lower overlap with female’s MHC-supertypes as well as a higher genome wide heterozygosity than randomly assigned males. Mutual relatedness had no influence on mate choice. Females engaged in extra-pair mating shared a significant higher number of MHC-supertypes with their social partner than faithful females. As no genetic differences between extra-pair young (EPY) and intra-pair young (IPY) were found, females might engage in extra-pair mating to ‘correct’ for genetic incompatibility. Thus, we found evidence that mate choice is predicted in the first place by the ‘good-genes-as-heterozygosity hypothesis’ whereas the occurrence of extra-pair matings supports the ‘dissassortative mating hypothesis’. To the best of our knowledge this study represents the first investigation of the potential roles of MHC-genes and overall genetic diversity in mate choice and extra-pair partner selection in a natural, free-living population of non-human primates.     

Genetic dissimilarity,genetic diversity,and mate preferences in humans

It is clear that genes at the major histocompatibility complex (MHC) are involved in mate preferences in a range of species, including humans. However, many questions remain regarding the MHC's exact influence on mate preference in humans. Some research suggests that genetic dissimilarity and individual genetic diversity (heterozygosity) at the MHC influence mate preferences, but the evidence is often inconsistent across studies. In addition, it is not known whether apparent preferences for MHC dissimilarity are specific to the MHC or reflect a more general preference for genome-wide dissimilarity, and whether MHC-related preferences are dependent on the context of mate choice (e.g., when choosing a short-term and long-term partner). Here, we investigated whether preferences for genetic dissimilarity are specific to the MHC and also whether preferences for genetic dissimilarity and diversity are context dependent. Genetic dissimilarity (number of alleles shared) influenced male, but not female, partner preferences, with males showing a preference for the faces of MHC-dissimilar females in both mating contexts. Genetic diversity [heterozygosity (H) and standardized mean (d²)] influenced both male and female preferences, regardless of mating context. Females preferred males with greater diversity at MHC loci (H) and males preferred females with greater diversity at non-MHC loci (d²) in both contexts. Importantly, these findings provide further support for a special role of the MHC in human sexual selection and suggest that male and female mate preferences may work together to potentially enhance both male and female reproductive success by increasing genetic diversity in offspring.     

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.     

Heritable variation in the timing of spermatophore removal, a mechanism of post-copulatory female choice in crickets

Female crickets can exert post-copulatory mating preferences by prematurely removing a male's spermatophore after copulation, which terminates sperm transfer. Although most models of sexual selection assume that female mating preferences are heritable, there has been little work addressing genetic variation underlying post-copulatory mate choice. We used a paternal half-sib design, in which different males were randomly assigned as mates to several females to create half-sib families, to determine the heritability of spermatophore retention time in female house crickets, Acheta domesticus. There was significant additive genetic variance in the timing of spermatophore removal by females [h(2) = 0.50 +/- 0.19 (+/- SE)], suggesting that the timing of spermatophore removal is determined, in part, by the female's own genotype independent of the quality of her mate. The relatively high heritability of spermatophore retention time may be reflective of the absence of strong selection on this trait, consistent with previous work showing no difference in the fitness of females permitted to freely remove the spermatophore of their mates and those forced to accept complete ejaculates.     

Opposites attract: MHC‐associated mate choice in a polygynous primate

We investigated reproduction in a semi‐free‐ranging population of a polygynous primate, the mandrill, in relation to genetic relatedness and male genetic characteristics, using neutral microsatellite and major histocompatibility complex (MHC) genotyping. We compared genetic dissimilarity to the mother and genetic characteristics of the sire with all other potential sires present at the conception of each offspring (193 offspring for microsatellite genetics, 180 for MHC). The probability that a given male sired increased as pedigree relatedness with the mother decreased, and overall genetic dissimilarity and MHC dissimilarity with the mother increased. Reproductive success also increased with male microsatellite heterozygosity and MHC diversity. These effects were apparent despite the strong influence of dominance rank on male reproductive success. The closed nature of our study population is comparable to human populations for which MHC‐associated mate choice has been reported, suggesting that such mate choice may be especially important in relatively isolated populations with little migration to introduce genetic variation.     

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.     

The Opportunity for Post-Copulatory Sexual Selection in the Ectoparasitic Pea Crab,Dissodactylus primitivus (Brachyura: Pinnotheridae)

Pea crabs, Dissodactylus primitivus, inhabit multiple echinoid (heart urchin) hosts. Male and female crabs move among hosts in search for mates, and both sexes mate multiple times, creating opportunities for post-copulatory sexual selection. For such selection to occur, only a fraction of the males who succeed in mating can also succeed in siring progeny. Jossart et al. 2014 used 4 microsatellite loci to document parentage and mating frequencies of both sexes in D. primitivus. From these data we identified the mean and variance in female offspring numbers, as well as the proportions of the female population that were gravid and not bearing offspring. We next identified the proportions of the male population who had (1) mated and sired offspring, (2) mated but failed to sire offspring, and (3) failed to mate altogether. We used these results to estimate the opportunity for selection on males and females in terms of mate numbers and offspring numbers, and estimated the sex difference in the opportunity for selection (i.e., the opportunity for sexual selection) using both forms of data. We then partitioned the total variance in male fitness into pre- and post-copulatory components and identified the fraction of the total opportunity for selection occurring in each context. Our results show that the opportunity for selection on each sex was of similar magnitude (0.69–0.98), consistent with this polyandrogynous mating system. We also found that 37% of the total opportunity for sexual selection on males occurred within the context of post-copulatory sexual selection. However, the fraction of the total opportunity for selection that was due to sexual selection, estimated using both mate numbers and offspring numbers, was 9% and 23% respectively. Thus, we further reduced our estimate of the opportunity for post-copulatory sexual selection in D. primitivus to less than 10% of the total opportunity for selection (0.37 of 0.09 and 0.23 = 0.03 and 0.09). Our results provide the first estimate of the maximum possible strength of post-copulatory sexual selection in crustaceans using this approach.     

The MHC and non-random mating in a captive population of Chinook salmon

Detailed analysis of variation in reproductive success can provide an understanding of the selective pressures that drive the evolution of adaptations. Here, we use experimental spawning channels to assess phenotypic and genotypic correlates of reproductive success in Chinook salmon (Oncorhynchus tshawytscha). Groups of 36 fish in three different sex ratios (1:2, 1:1 and 2:1) were allowed to spawn and the offspring were collected after emergence from the gravel. Microsatellite genetic markers were used to assign parentage of each offspring, and the parents were also typed at the major histocompatibility class IIB locus (MHC). We found that large males, and males with brighter coloration and a more green/blue hue on their lateral integument sired more offspring, albeit only body size and brightness had independent effects. There was no similar relationship between these variables and female reproductive success. Furthermore, there was no effect of sex ratio on the strength or significance of any of the correlations. Females mated non-randomly at the MHC, appearing to select mates that produced offspring with greater genetic diversity as measured by amino-acid divergence. Females mated randomly with respect to male genetic relatedness and males mated randomly with respect to both MHC and genetic relatedness. These results indicate that sexual selection favours increased body size and perhaps integument coloration in males as well as increases genetic diversity at the MHC by female mate choice.     

Genetic association between male attractiveness and female differential allocation

Differential allocation of reproductive effort towards offspring of attractive mates is a form of post-copulatory mate choice. Although differential allocation has been demonstrated in many taxa, its evolutionary implications have received little attention. Theory predicts that mate choice will lead to a positive genetic correlation between female preference and male attractiveness. This prediction has been upheld for pre-copulatory mate choice, but whether such a relationship between male attractiveness and female differential allocation exists has never been tested. Here, we show that both female pre-copulatory mate choice and post-copulatory differential allocation are genetically associated with male attractiveness in house crickets, Acheta domesticus. Daughters of attractive males mated sooner and laid more eggs when paired with larger males. These forms of mate choice are strongest in large females, suggesting that costs decrease with increasing female size. The genetic association between attractiveness and differential allocation suggests potential for differential allocation to become exaggerated by coevolutionary runaway processes in an analogous manner to pre-copulatory choice. Sexual selection is thus likely to be stronger than predicted by pre-copulatory choice alone.     

Genetic diversity revealed in human faces

From an evolutionary perspective, human facial attractiveness is proposed to signal mate quality. Using a novel approach to the study of the genetic basis of human preferences for facial features, we investigated whether attractiveness signals mate quality in terms of genetic diversity. Genetic diversity in general has been linked to fitness and reproductive success, and genetic diversity within the major histocompatibility complex (MHC) has been linked to immunocompetence and mate preferences. We asked whether any preference for genetic diversity is specific to MHC diversity or reflects a more general preference for overall genetic diversity. We photographed and genotyped 160 participants using microsatellite markers situated within and outside the MHC, and calculated two measures of genetic diversity: mean heterozygosity and standardized mean d(2). Our results suggest a special role for the MHC in female preferences for male faces. MHC heterozygosity positively predicted male attractiveness, and specifically facial averageness, with averageness mediating the MHC-attractiveness relationship. For females, standardized mean d(2) at non-MHC loci predicted facial symmetry. Thus, attractive facial characteristics appear to provide visual cues to genetic quality in both males and females, supporting the view that face preferences have been shaped by selection pressures to identify high-quality mates.     

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.     

MHC,parasites and antler development in red deer: no support for the Hamilton & Zuk hypothesis

The Hamilton‐Zuk hypothesis proposes that the genetic benefits of preferences for elaborated secondary sexual traits have their origins in the arms race between hosts and parasites, which maintains genetic variance in parasite resistance. Infection, in turn, can be reflected in the expression of costly sexual ornaments. However, the link between immune genes, infection and the expression of secondary sexual traits has rarely been investigated. Here, we explored whether the presence and identity of functional variants (supertypes) of the highly polymorphic major histocompatibility complex (MHC), which is responsible for the recognition of parasites, predict the load of lung and gut parasites and antler development in the red deer (Cervus elaphus). While we found MHC supertypes to be associated with infection by a number of parasite species, including debilitating lung nematodes, we did not find support for the Hamilton‐Zuk hypothesis. On the contrary, we found that lung nematode load was positively associated with antler development. We also found that the supertypes that were associated with resistance to certain parasites at the same time cause susceptibility to others. Such trade‐offs may undermine the potential genetic benefits of mate choice for resistant partners.