Female choice and male humoral immune response in the lekking great snipe (Gallinago media)

Parasites and diseases constitute major evolutionary forcesin many natural populations, and thus having an efficient immunedefense to resist infections is crucial for many organisms.Properties of the immune response may also influence mate choicedecisions in many animals. Theory predicts several advantagesfor females when choosing males with superior immune systems.These benefits can be both direct (e.g. increased paternal careand reduced disease transmission) and indirect (good genes).We have investigated female choice with respect to antibodyresponse to two novel antigens in males of a lekking bird, thegreat snipe (Gallinago media). Because of the lek mating system,female choice probably mainly incurs indirect (genetic) ratherthan direct benefits. Males responded to vaccination with diphtheriaand tetanus toxoids by producing specific antibodies to bothantigens. Triggering the immune system had no negative impacton display activities or survival. Males that were chosen byfemales as mates had on average higher antibody response tothe tetanus antigen than their neighbors. We did not, however,find any covariance between the strength of the antibody responseand male mating success.     

Correlates of male mating success in the lekking great snipe (Gallinago media): results from a four-year study

To investigate behavioral or morphological traits importantas mate choice cues, we measured selection differentials (s)as the covariances between each trait and male mating success,and directional selection gradients (J3) from multiple linearregression of the standardized traits on male mating success.Data from two leks in four consecutive years were included,and the annual data were analyzed separately. The main findingsare: (1) the distribution of male mating success proved to beless skewed than those found in many other lekking species,(2) only a few traits yielded significant selection gradients,(3) the importance of age on male mating success changed acrossyears, (4) females may use traits with a high variance as matechoice cues, and (5) individual males achieved similar matingsuccesses between years. Attendance and age were the traitsmost consistently correlated with male mating success, but notraits showed significant selection gradients in all years.Our results indicate that variable sexual selection pressuresexisted between years, but the high correlation found betweenthe mating success of individual males in successive seasonsalso indicates that permanent differences in male traits areimportant. Key words: lek, mate choice, sexual selection.     

Major histocompatibility complex class II compatibility,but not class I,predicts mate choice in a bird with highly developed olfaction

Mate choice for major histocompatibility complex (MHC) compatibility has been found in several taxa, although rarely in birds. MHC is a crucial component in adaptive immunity and by choosing an MHC-dissimilar partner, heterozygosity and potentially broad pathogen resistance is maximized in the offspring. The MHC genotype influences odour cues and preferences in mammals and fish and hence olfactory-based mate choice can occur. We tested whether blue petrels, Halobaena caerulea, choose partners based on MHC compatibility. This bird is long-lived, monogamous and can discriminate between individual odours using olfaction, which makes it exceptionally well suited for this analysis. We screened MHC class I and II B alleles in blue petrels using 454-pyrosequencing and quantified the phylogenetic, functional and allele-sharing similarity between individuals. Partners were functionally more dissimilar at the MHC class II B loci than expected from random mating (p = 0.033), whereas there was no such difference at the MHC class I loci. Phylogenetic and non-sequence-based MHC allele-sharing measures detected no MHC dissimilarity between partners for either MHC class I or II B. Our study provides evidence of mate choice for MHC compatibility in a bird with a high dependency on odour cues, suggesting that MHC odour-mediated mate choice occurs in birds.     

Food supply and breeding occurrences: the West European population of the lekking great snipe Gallinago media (Latham, 1787) (Aves)

For species with very high energetic costs during reproduction we expect occurence during the reproduction season to be dramatically affected by the availability of energy. Recent studies have shown very high energetic costs of lekking for great snipe males, Gallinago media (Latham, 1787) and that breeding great snipes prefer to feed in soft soil with a high abundance of earthworms. We here evaluate the hypothesis that the breeding occurrence of great snipe is restricted to areas with very high availability of food. All the 125 registered great snipe leks in Scandinavia were situated in open habitats along the tree line. The occurrence of leks were analysed in relation to bedrock quality, soil chemistry and earthworm biomass. There was a strong positive relationship between soil pH and earthworm biomass. High pH values were found on or in the close vicinity of base-rich bedrocks. No great snipe leks were documented in areas with acid soil, even if the extent of acid bedrocks along the tree line predicts that 31% of the leks should be situated on acid soils. Hypotheses, including both natural and sexual selection, for why breeding occurrence of great snipe is restricted to areas with high abundance of high quality food are evaluated, and we find indications for this to be a consequence of the very high energetic costs for the lekking males. These costs have probably evolved through female mate choice and indicate that sexual selection may have important consequences for a species distribution. Population-level effects of sexual selection have previously received little attention. The stringent habitat demands here documented may also make great snipes vulnerable to environmental changes and can contribute to explain the dramatic reduction in breeding range of this species in western Europe during the past 150 years (Løfaldli et al ., 1989).     

Male mate choice relies on major histocompatibility complex class I in a sex‐role‐reversed pipefish

Mate choice for compatible genes is often based on genes of the major histocompatibility complex (MHC). Although MHC‐based mate choice is commonly observed in female choice, male mate choice remains elusive. In particular, if males have intense paternal care and are thus the choosing sex, male choice for females with dissimilar MHC can be expected. Here, we investigated whether male mate choice relies on MHC class I genes in the sex‐role reversed pipefish Syngnathus typhle. In a mate choice experiment, we determined the relative importance of visual and olfactory cues by manipulating visibility and olfaction. We found that pipefish males chose females that maximize sequence‐based amino acid distance between MHC class I genotypes in the offspring when olfactory cues were present. Under visual cues, large females were chosen, but in the absence of visual cues, the choice pattern was reversed. The use of sex‐role reversed species thus revealed that sexual selection can lead to the evolution of male mate choice for MHC class I genes.     

MHC genotype predicts mate choice in the ring-necked pheasant Phasianus colchicus

Females of several vertebrate species selectively mate with males on the basis of the major histocompatibility complex (MHC) genes. As androgen-mediated maternal effects have long-lasting consequences for the adult phenotype, both mating and reproductive success may depend on the combined effect of MHC genotype and exposure to androgens during early ontogeny. We studied how MHC-based mate choice in ring-necked pheasants (Phasianus colchicus) was influenced by an experimental in ovo testosterone (T) increase. There was no conclusive evidence of in ovo T treatment differentially affecting mate choice in relation to MHC genotype. However, females avoided mating with males with a wholly different MHC genotype compared with males sharing at least one MHC allele. Females also tended to avoid mating with MHC-identical males, though not significantly so. These findings suggest that female pheasants preferred males with intermediate MHC dissimilarity. Male MHC heterozygosity or diversity did not predict the expression of ornaments or male dominance rank. Thus, MHC-based mating preferences in the ring-necked pheasant do not seem to be mediated by ornaments' expression and may have evolved mainly to reduce the costs of high heterozygosity at MHC loci for the progeny, such as increased risk of autoimmune diseases or disruption of coadapted gene pools.     

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.     

Major histocompatibility complex polymorphism: dynamics and consequences of parasite-mediated local adaptation in fishes

Parasitism is a common form of life and represents a strong selective pressure for host organisms. In response to this evolutionary pressure, vertebrates have developed genetically coded defences such as the major histocompatibility complex (MHC). Mechanisms of parasite-mediated selection not only maintain outstanding polymorphism in these genes but have also been proposed to further promote host population divergence and ultimately speciation because it can drive evolution of local adaptation in which MHC genes play a crucial role. This review first highlights the dynamics and complexity of parasite-mediated selection in natural systems, which not only depends on dominating parasite strategies and on the taxonomic diversity of the parasite community but also includes the differences in parasite communities between habitats and niches, creating divergent selection on locally adapted populations. Then the different ways in which MHC genes potentially allow vertebrates to respond to these dynamics and to adapt locally are outlined. Finally, it is proposed that varying selection strength in time and space may lead to variation in the strength of precopulatory reproductive isolation which has evolved to maintain local adaptation.     

Red and white Chinook salmon: genetic divergence and mate choice

Chinook salmon (Oncorhynchus tshawytscha) exhibit extreme differences in coloration of skin, eggs and flesh due to genetic polymorphisms affecting carotenoid deposition, where colour can range from white to bright red. A sympatric population of red and white Chinook salmon occurs in the Quesnel River, British Columbia, where frequencies of each phenotype are relatively equal. In our study, we examined evolutionary mechanisms responsible for the maintenance of the morphs, where we first tested whether morphs were reproductively isolated using microsatellite genotyping, and second, using breeding trials in seminatural spawning channels, we tested whether colour assortative mate choice could be operating to maintain the polymorphism in nature. Next, given extreme difference in carotenoid assimilation and the importance of carotenoids to immune function, we examined mate choice and selection between colour morphs at immune genes (major histocompatibility complex genes: MHC I‐A1 and MHC II‐B1). In our study, red and white individuals were found to interbreed, and under seminatural conditions, some degree of colour assortative mate choice (71% of matings) was observed. We found significant genetic differences at both MHC genes between morphs, but no evidence of MHC II‐B1‐based mate choice. White individuals were more heterozygous at MHC II‐B1 compared with red individuals, and morphs showed significant allele frequency differences at MHC I‐A1. Although colour assortative mate choice is likely not a primary mechanism maintaining the polymorphisms in the population, our results suggest that selection is operating differentially at immune genes in red and white Chinook salmon, possibly due to differences in carotenoid utilization.     

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.     

Major histocompatibility complex genes, symmetry, and body scent attractiveness in men and women

Previous research indicates that the scent of developmentalstability (low fluctuating asymmetry, FA) is attractive to womenwho are fertile (at high-conception risk points in their menstrualcycles), but not to other women or men. Prior research alsoindicates that the scent of dissimilarity in major histocompatibilitycomplex (MHC) genes may play a role in human mate choice. Westudied the scent attractiveness to the opposite sex of t-shirtsworn for 2 nights' sleep. Our results indicate that the twoolfactory systems are independent. We repeated previous resultsfrom studies of the scent of symmetry. We repeated previousresults from MHC research in part; men, but not women, showeda preference for t-shirts with the scent of MHC dissimilarity.Women's scent ratings of t-shirts were uncorrelated with thewearer's MHC dissimilarity and allele frequency, but positivelycorrelated with the wearer's MHC heterozygosity. Fertile womendid not exhibit any MHC trait preferences. Women's preferencefor the scent of men who were heterozygous for MHC alleles maybe stronger in women who are at infertile cycle points. Menpreferred the scent of common MHC alleles, which may functionto avoid mates with rare alleles that exhibit gestational drive.Men also preferred the scent of women at fertile cycle points.The scent of facially attractive women, but not men, was preferred.Neither FA nor facial attractiveness in either sex correlatedwith MHC dissimilarity to others, MHC heterozygosity, or MHCallelic rarity.     

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-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.     

Sexual selection explains more functional variation in the mammalian major histocompatibility complex than parasitism

Understanding drivers of genetic diversity at the major histocompatibility complex (MHC) is vitally important for predicting how vertebrate immune defence might respond to future selection pressures and for preserving immunogenetic diversity in declining populations. Parasite-mediated selection is believed to be the major selective force generating MHC polymorphism, and while MHC-based mating preferences also exist for multiple species including humans, the general importance of mate choice is debated. To investigate the contributions of parasitism and sexual selection in explaining among-species variation in MHC diversity, we applied comparative methods and meta-analysis across 112 mammal species, including carnivores, bats, primates, rodents and ungulates. We tested whether MHC diversity increased with parasite richness and relative testes size (as an indicator of the potential for mate choice), while controlling for phylogenetic autocorrelation, neutral mutation rate and confounding ecological variables. We found that MHC nucleotide diversity increased with parasite richness for bats and ungulates but decreased with parasite richness for carnivores. By contrast, nucleotide diversity increased with relative testes size for all taxa. This study provides support for both parasite-mediated and sexual selection in shaping functional MHC polymorphism across mammals, and importantly, suggests that sexual selection could have a more general role than previously thought.     

Sexual selection in a lekking bird: the relative opportunity for selection by female choice and male competition

Leks are classic models for studies of sexual selection due to extreme variance in male reproductive success, but the relative influence of intrasexual competition and female mate choice in creating this skew is debatable. In the lekking lance-tailed manakin (Chiroxiphia lanceolata), these selective episodes are temporally separated into intrasexual competition for alpha status and female mate choice among alpha males that rarely interact. Variance in reproductive success between status classes of adult males (alpha versus non-alpha) can therefore be attributed to male-male competition whereas that within status largely reflects female mate choice. This provides an excellent opportunity for quantifying the relative contribution of each of these mechanisms of sexual selection to the overall opportunity for sexual selection on males (I males). To calculate variance in actual reproductive success, we assigned genetic paternity to 92.3% of 447 chicks sampled in seven years. Reproduction by non-alphas was rare and apparently reflected status misclassifications or opportunistic copulations en route to attaining alpha status rather than alternative mating strategies. On average 31% (range 7-44%, n=6 years) of the total I males was due to variance in reproductive success between alphas and non-alphas. Similarly, in a cohort of same-aged males followed for six years, 44-58% of the total I males was attributed to variance between males of different status. Thus, both intrasexual competition for status and female mate choice among lekking alpha males contribute substantially to the potential for sexual selection in this species.     

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     

Spatial pattern of MHC class II variation in the great snipe (Gallinago media)

The genes of the major histocompatibility complex (MHC) code for proteins involved in antigen recognition and triggering of the adaptive immune response, and are therefore likely to be under selection from parasites. These selection regimes may vary in space and time. Here we report a strong geographical structure in MHC class II B genes of a migrating bird, the great snipe (Gallinago media). Genetic differentiation in the MHC between two ecologically distinct distributional regions (Scandinavian mountain populations vs. East European lowland populations) was still present after statistically controlling for the effect of selectively neutral variation (microsatellites) using partial Mantel tests. This suggests a role for selection in generating this spatial structure and that it represents local adaptation to different environments. Differentiation between populations within the two regions was negligible. Overall, we found a high number of MHC alleles (50, from 175 individuals). This, together with a tendency for a higher rate of nonsynonymous than synonymous substitutions in the peptide binding sites, and high Tajima's D in certain regions of the gene, suggests a history of balancing selection. MHC variation is often thought to be maintained by some form of balancing selection, but the nature of this selection remains unclear. Our results support the hypothesis that spatial variation in selection regimes contributes to the high polymorphism.     

Male mate choice in the chameleon grasshopper (Kosciuscola tristis)

In many species, males can increase their fitness by mating with the highest quality females. Female quality can be indicated by cues, such as body size, age and mating status. In the alpine grasshopper Kosciuscola tristis, males can be found riding on subadult females early in the season, and as the season progresses, males engage in fights over ovipositing females. These observations suggest that males may be competing for females that are either unmated (early season) or sperm‐depleted (late season). We thus hypothesised that male K. tristis may be choosy in relation to female mating status, and specifically, we predicted that males prefer females that are unmated. We conducted behavioural experiments in which males were given the choice of two females, one mated and one unmated. Contrary to our prediction, males did not mate preferentially with unmated females. However, copulation duration with unmated females was, on average, 24 times the length of copulation with mated females. While female K. tristis can reject mates, we did not observe any evidence of overt female choice during our trials. Females may gain additional benefits from mating multiply and may therefore not readily reject males. While our experiment cannot definitively disentangle female from male control over copulation duration, we suggest that males choose to invest more time in copula with unmated females, perhaps for paternity assurance, and that male mate assessment occurs during copulation rather than beforehand.     

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

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