Major histocompatibility complex variation and mate choice in a lekking bird, the great snipe (Gallinago media)

Genes of the major histocompatibility complex (MHC) play a major part in the activation of the vertebrate immune system. In addition, they also appear to function as cues for mate choice. In mammals especially, several kinds of MHC-dependent mate choice have been hypothesized and observed. These include choice of mates that share no or few alleles with the choosing individual, choice of mates with alleles that differ as much as possible from the choosing individual, choice of heterozygous mates, choice of certain genotypes and choice of rare alleles. We investigated these different aspects of mate choice in relation to MHC in a lekking bird species, the great snipe (Gallinago media). We found no evidence for MHC disassortative mating, no preference for males with many MHC alleles and no preference for rare alleles. However, we did find that some allelic lineages were more often found in males with mating success than in males without mating success. Females do not seem to use themselves as references for the MHC-dependent mate choice, rather they seem to prefer males with certain allele types. We speculate that these alleles may be linked to resistance to common parasites.     

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.     

Social and extra-pair mating in relation to major histocompatibility complex variation in common yellowthroats

Females are thought to gain better-quality genes for their offspring by mating with particular males. Genes of the major histocompatibility complex (MHC) play a critical role in adaptive immunity, and several studies have examined female mate choice in relation to MHC variation. In common yellowthroats, females prefer males that have larger black facial masks, an ornament associated with MHC variation, immune function and condition. Here we also tested whether mating patterns are directly correlated with MHC diversity or similarity. Using pyrosequencing, we found that the presence of extra-pair young in the brood was not related to male MHC diversity or similarity between the female and her within-pair mate. Furthermore, extra-pair sires did not differ in overall diversity from males they cuckolded, or in their similarity to the female. MHC diversity is extremely high in this species, and it may limit the ability of females to assess MHC variation in males. Thus, mating may be based on ornaments, such as mask size, which are better indicators of overall male health and genetic quality.     

No evidence of an MHC-based female mating preference in great reed warblers

Female mate-choice based on genetic compatibility is an area of growing interest. The major histocompatibility complex (MHC) genes are likely candidates for such mate-choice since these highly polymorphic genes may both increase offspring viability and also provide direct cues for mate-choice. In great reed warblers, females actively choose a breeding partner out of a handful of males that they visit and evaluate; thus, female preference for compatible or heterozygous MHC genes could have evolved. Here, I investigate whether great reed warbler females preferentially mate with males with dissimilar MHC class I alleles or with males that are heterozygous at MHC class I. Despite favourable conditions, a thorough screening method and a large sample size, there was no evidence of an MHC-based female mating preference based on either genetic compatibility or heterozygosity in this population. Power analyses of the data sets revealed that relatively small differences (15% and 8%, respectively) between true and random pairs should have been detected.     

MATE CHOICE FOR NONADDITIVE GENETIC BENEFITS CORRELATE WITH MHC DISSIMILARITY IN THE ROSE BITTERLING (RHODEUS OCELLATUS)

Good genes models of mate choice predict additive genetic benefits of choice whereas the compatibility hypothesis predicts nonadditive fitness benefits. Here the Chinese rose bitterling, Rhodeus ocellatus, a freshwater fish with a resource‐based mating system, was used to separate additive and nonadditive genetic benefits of female mate choice. A sequential blocked mating design was used to test female mate preferences, and a cross‐classified breeding design coupled with in vitro fertilizations for fitness benefits of mate choice. In addition, the offspring produced by the pairing of preferred and nonpreferred males were reared to maturity and their fitness traits were compared. Finally, the MHC DAB1 gene was typed and male MHC genotypes were correlated with female mate choice. Females showed significant mate preferences but preferences were not congruent among females. There was a significant interaction of male and female genotype on offspring survival, rate of development, growth rate, and body size. No significant male additive effects on offspring fitness were observed. Female mate preferences corresponded with male genetic compatibility, which correlated with MHC dissimilarity. It is proposed that in the rose bitterling genetic compatibility is the mechanism by which females obtain a fitness benefit through mate choice and that male MHC dissimilarity, likely mediated by odor cues, indicates genetic compatibility.     

Parental relatedness and major histocompatibility effects on early embryo survivorship in Atlantic salmon

Salmon have provided key insights into the relative influence of natural and sexual selection on major histocompatibility complex (MHC) variation. Natural selection on salmon MHC genes has been demonstrated in pathogen studies, and there is evidence of MHC-based mate choice (sexual selection). We tested whether parental MHC genes affect survivorship of juvenile Atlantic salmon (Salmo salar) by quantifying the influence of parental genome-wide relatedness and MHC genotype on survivorship to the swim-up stage. Thirteen microsatellite loci were used to estimate the influence of genome-wide relatedness between parents on offspring survivorship and MHC genotypes were determined by sequencing part of the class IIβ gene. Our results revealed no significant relationship between early offspring survivorship and genome-wide relatedness, predicted MHC heterozygosity, or MHC allelic similarity. Overall, our data are consistent with the contention that excess MHC heterozygosity in Atlantic salmon juveniles is due to sexual selection as well as differential survival of offspring due to MHC genotype.     

Condition-dependent mate choice and a reproductive disadvantage for MHC-divergent male tiger salamanders

Major histocompatibility complex (MHC) alleles likely have adaptive value because of overdominance, in which case MHC heterozygous individuals have increased fitness relative to homozygotes. Because of this potential benefit, the evolution of sexual reproduction between MHC-divergent individuals (i.e. negative assortative mating, NAM) may be favoured. However, the strongest evidence for MHC-based NAM comes from inbred animals, and context-dependent mating preferences have rarely been evaluated although they often occur in nature. We assessed the extent MHC-based mating preferences among wild tiger salamanders ( Ambystoma tigrinum ) using multiple molecular approaches. We genotyped 102 adults and 864 larvae from 36 breeding trials at both microsatellite and MHC loci. Parentage analysis revealed that reproductive success among males was positively associated with increased tail length and that with respect to the focal female, MHC-similar males sired a significantly higher number of offspring than more dissimilar males. This trend was consistent, even under context-dependent scenarios that favour traditional MHC-based NAM. These results suggest that the most MHC-divergent males may be at a reproductive disadvantage in pairwise breeding trials. Our data add to a growing body of evidence that suggests where it exists, MHC-based choice is probably dynamic and mediated by many factors that vary in the wild, notably signals from other indicator traits and by the quality and quantity of potential mates.     

A theory of mate choice based on heterozygosity

In theories of mate choice that rely on genetic benefits, thenature of the"good genes" involved has received little attention.A review of genetic studies of mate choice in a variety of speciesand situations suggests that individual heterozygosity is moreimportant than previously realized. Females are predicted tovalue heterozygosity in their offspring and under some conditionsin their males. The expression of vigor, condition-sensitiveornaments, and symmetry in males may be a direct reflectionnot of "good genes" but of individual heterozygosity at keyloci or at many loci. Like sexuality itself, mate choice basedon heterozygosity and genic diversity may be an adaptation thatfavors the production of diverse and superior competitors. Femalechoice is made meaningful by sexuality, and the adaptive valueof choice probably depends on some of the same factors thatmaintain sexuality     

Occurrence of extra‐pair paternity is connected to social male's MHC‐variability in the scarlet rosefinch Carpodacus erythrinus

Genes of the Major Histocompatibility Complex (MHC) represent an essential component of the vertebrate acquired immune system. In the last decades, the role of MHC genes in mate choice has been subject of particular scientific interest. However, results of studies dealing with this topic in different species are equivocal and mechanisms conducting MHC‐based mate choice are still puzzling. We investigated the impact of MHC class I variability on within‐pair and extra‐pair fertilisation success in a wild population of a socially monogamous passerine bird with considerable rates of extra‐pair paternity, the scarlet rosefinch Carpodacus erythrinus. We found some support for the ‘good‐genes‐as‐heterozygosity model’, as social males of high MHC‐heterozygosity were cheated by their females less frequently than less MHC‐heterozygous males. However, cuckolding males were not more MHC‐heterozygous than the cheated social males, nor were extra‐pair young more MHC‐heterozygous than within‐pair young. We did not find any evidence for mating preferences according to the complementarity model.     

'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 strategy in an enclosed group of Japanese macaques

Female Japanese macaques (Macaca fuscata) are noted for mating with multiple males and for their ability to exert mate choice. In a captive group of Japanese macaques housed at the Primate Research Institute of Kyoto University, Japan, behavioral and endocrine data were combined to examine female mating strategies. During one breeding season, daily behavioral observations were conducted on females who exhibited copulatory behavior. Blood was collected from females twice weekly and their ovulatory periods estimated by analyzing hormone profiles. Females began mating shortly before ovulation, peaked at ovulation, and continued receiving ejaculations for up to ten weeks after conception. Females were more responsible than males for inbreeding avoidance with matrilineal kin. Males sometimes approached females from their own matriline, but females avoided such males and expressed mate choice behavior preferentially toward non-matrilineal males. Over the entire mating season, females did not choose non-matrilineal males on the basis of displays, dominance rank, age, weight, or weight change during the mating season. When females were likely to conceive, however, they expressed mate choice behavior toward males who displayed most frequently. Female mating strategy may include both mate choice at ovulation and other, non-procreative functions.     

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.     

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.     

Alternative Female Choice Tactics in the Scorpionfly Hylobittacus apicalis(Mecoptera) and Their Implications

Females of the scorpionfly Hylobittacus apicalis choose mateson the basis of material benefits (nuptial arthropod prey size)and probably on the basis of genetic benefits males deliverat mating. Females feed on the male's prey throughout copulation.They prefer males with large prey as mates and often refusemales who present small prey. That females may value male geneticquality is suggested by differences in ability of males to obtainlarge prey, which if inherited would influence offspring fitness,and by females often terminating mating with males with smallprey before they transfer any sperm or a complete ejaculate.Females hunt only when males with prey are not available becausehunting exposes individuals to predators. Female Hylobittacusapicalis exhibit alternative mate choice tactics, which arecondition-dependent in expression and probably comprise a conditionalstrategy. Body size, recent feeding history, and male availabilitydetermine how discriminating an individual female actually is,and these conditions may determine the value of material andgenetic benefits in mate choice decisions. The results suggestthat female choice controls male behavior. When females becomechoosy, males are forced to obtain rare large prey despite theincreased risks to males associated with this behavior. The implications of the findings on H. apicalis are discussedin relation to condition dependent female choice patterns inother species and the evolutionary maintenance of female choice.     

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.     

Female choice in the field cricket Gryllus bimaculatus (De Geer)

Females of the field cricket G. bimaculatus show multiple mating. Since such a strategy is likely to incur costs such as time and energy spent in orientation to calling males or increased susceptibility to predation, it must have certain selective advantages. This study shows that multiple mating is a potential mechanism of mate choice. Females removed the spermatophores of some males before complete insemination was achieved. Females also remained with large males in order to mate a second or third time. Since spermathecal morphology may limit last-male sperm precedence in this species, a function of multiple mating may be to dilute the sperm stored from previous matings with that of the current male, so increasing his representation in offspring production.     

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     

Female extrapair mate choice in a cooperative breeder: trading sex for help and increasing offspring heterozygosity

Sexual conflict between males and females over mating is common. Females that copulate with extrapair mates outside the pair-bond may gain (i) direct benefits such as resources or increased paternal care, (ii) indirect genetic benefits for their offspring, or (iii) insurance against infertility in their own social mate. Few studies have been able to demonstrate the different contexts in which females receive varying types of benefits from extrapair mates. Here, I examined sexual conflict, female extrapair mate choice, and patterns of extrapair paternity in the cooperatively breeding superb starling Lamprotornis superbus using microsatellite markers. Although extrapair paternity was lower than many other avian cooperative breeders (14% of offspring and 25% of nests), females exhibited two distinct mating patterns: half of the extrapair fertilizations were with males from inside the group, whereas half were with males from outside the group. Females with few potential helpers copulated with extrapair mates from within their group and thereby gained direct benefits in the form of additional helpers at the nest, whereas females paired to mates that were relatively less heterozygous than themselves copulated with extrapair mates from outside the group and thereby gained indirect genetic benefits in the form of increased offspring heterozygosity. Females did not appear to gain fertility insurance from copulating with extrapair mates. This is the first study to show that individuals from the same population mate with extrapair males and gain both direct and indirect benefits, but that they do so in different contexts.     

Phenotypic plasticity in female mate choice behavior is mediated by an interaction of direct and indirect genetic effects in Drosophila melanogaster

Female mate choice is a complex decision‐making process that involves many context‐dependent factors. In Drosophila melanogaster, a model species for the study of sexual selection, indirect genetic effects (IGEs) of general social interactions can influence female mate choice behaviors, but the potential impacts of IGEs associated with mating experiences are poorly understood. Here, we examined whether the IGEs associated with a previous mating experience had an effect on subsequent female mate choice behaviors and quantified the degree of additive genetic variation associated with this effect. Females from 21 different genetic backgrounds were housed with males from one of two distinct genetic backgrounds for either a short (3 hr) or long (48 hr) exposure period and their subsequent mate choice behaviors were scored. We found that the genetic identity of a previous mate significantly influenced a female's subsequent interest in males and preference of males. Additionally, a hemiclonal analysis revealed significant additive genetic variation associated with experience‐dependent mate choice behaviors, indicating a genotype‐by‐environment interaction for both of these parameters. We discuss the significance of these results with regard to the evolution of plasticity in female mate choice behaviors and the maintenance of variation in harmful male traits.     

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.