Different ornaments signal male health and MHC variation in two populations of a warbler

Male traits that signal health and vigour are used by females to choose better quality mates, but in some cases the male trait selected by females differs among populations. Multiple male traits can be maintained through female mate choice if both traits are equally honest indicators of male quality, but tests of this prediction are rare. By choosing males based on such traits, females could gain direct benefits from males (assistance with parental care), but when females choose extra‐pair mates based on these traits, females gain only male sperm, and potentially indirect genetic benefits for their offspring. In common yellowthroats (Geothylpis trichas), female choice of extra‐pair mates targets two different plumage ornaments: the black mask in a Wisconsin population and the yellow bib in a New York population. Previously, we found that the black mask in Wisconsin is related to greater major histocompatibility complex (MHC) class II variation, which in turn signals better survival and disease resistance. In this study, we examined the signalling function of the yellow bib in New York to test whether it signals the same aspects of male quality as the black mask in Wisconsin. As predicted, we found that the yellow bib in New York is most closely associated with MHC variation, which also signals survival and resistance to blood parasites. Thus, the ornament preferred by females differs between the two populations, but the different ornaments signal similar aspects of male health and genetic quality, specifically information regarding MHC variation and potential indirect genetic benefits to females.     

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.     

Female rose bitterling prefer MHC-dissimilar males: experimental evidence

The role of genetic benefits in female mate choice remains a controversial aspect of sexual selection theory. In contrast to "good allele" models of sexual selection, "compatible allele" models of mate choice predict that females prefer mates with alleles complementary to their own rather than conferring additive effects. While correlative results suggest complementary genetic effects to be plausible, direct experimental evidence is scarce. A previous study on the Chinese rose bitterling (Rhodeus ocellatus) demonstrated a positive correlation between female mate choice, offspring growth and survival, and the functional dissimilarity between the Major Histocompatibility Complex (MHC) alleles of males and females. Here we directly tested whether females used cues associated with MHC genes to select genetically compatible males in an experimental framework. By sequentially pairing females with MHC similar and dissimilar males, based on a priori known MHC profiles, we showed that females discriminated between similar and dissimilar males and deposited significantly more eggs with MHC dissimilar males. Notably, the degree of dissimilarity was an important factor for female decision to mate, possibly indicating a potential threshold value of dissimilarity for decision making, or of an indirect effect of the MHC.     

Are large wattles related to particular MHC genotypes in the male pheasant?

In sexually dimorphic species, partners can assess heritable mate quality by analyzing costly sexual ornaments in terms of their dimension and possibly of their symmetry. In vertebrates an important aspect of genetic quality is the efficiency of the immune system, and in particular the Major Histocompatibility Complex (MHC). If ornaments are honest advertisements of pathogen resistance (good genes), in line with the Hamilton-Zuk hypothesis, a correlation between ornament expression and MHC profiles should exist. We tested this hypothesis in the common pheasant Phasianus colchicus by comparing male ornament characteristics (wattle and spur size, and wattle fluctuating asymmetry) with a portion of exon 2 of the class IIB MHC genes containing 19 putative antigen recognition sites. A total of 8 new alleles was observed in the MHCPhco exon IIB. We found significant differences in the occurrence of MHC genotypes between males carrying large or small wattles. Homozygous genotypes predicted large wattle males more correctly than small wattle males. The association between the dimension of the spur and the occurrence of MHC genotypes was marginally significant, however, we did not find any significant association between MHC genotypes and asymmetry. Our results suggest that female pheasants may use the ornament size as a cue to evaluate male quality and thus choose males carrying particular MHC profiles.     

Parasitism, host immune function, and sexual selection

Parasite-mediated sexual selection may arise as a consequence of 1) females avoiding mates with directly transmitted parasites, 2) females choosing less-parasitized males that provide parental care of superior quality, or 3) females choosing males with few parasites in order to obtain genes for parasite resistance in their offspring. Studies of specific host-parasite systems and comparative analyses have revealed both supportive and conflicting evidence for these hypotheses. A meta-analysis of the available evidence revealed a negative relationship between parasite load and the expression of male secondary sexual characters. Experimental studies yielded more strongly negative relationships than observations did, and the relationships were more strongly negative for ectoparasites than for endoparasites. There was no significant difference in the magnitude of the negative effect for species with and without male parental care, or between behavioral and morphological secondary sexual characters. There was a significant difference between studies based on host immune function and those based on parasite loads, with stronger effects for measures of immune function, suggesting that the many negative results from previous analyses of parasite-mediated sexual selection may be explained because relatively benign parasites were studied. The multivariate analyses demonstrating strong effect sizes of immune function in relation to the expression of secondary sexual characters, and for species with male parental care as compared to those without, suggest that parasite resistance may be a general determinant of parasite-mediated sexual selection.     

No Evidence for the Effect of MHC on Male Mating Success in the Brown Bear

Mate choice is thought to contribute to the maintenance of the spectacularly high polymorphism of the Major Histocompatibility Complex (MHC) genes, along with balancing selection from parasites, but the relative contribution of the former mechanism is debated. Here, we investigated the association between male MHC genotype and mating success in the brown bear. We analysed fragments of sequences coding for the peptide-binding region of the highly polymorphic MHC class I and class II DRB genes, while controlling for genome-wide effects using a panel of 18 microsatellite markers. Male mating success did not depend on the number of alleles shared with the female or amino-acid distance between potential mates at either locus. Furthermore, we found no indication of female mating preferences for MHC similarity being contingent on the number of alleles the females carried. Finally, we found no significant association between the number of MHC alleles a male carried and his mating success. Thus, our results provided no support for the role of mate choice in shaping MHC polymorphism in the brown bear.     

Gene duplication,allelic diversity,selection processes and adaptive value of MHC class II <Emphasis Type="Italic">DRB</Emphasis> genes of the bank vole, <Emphasis Type="Italic">Clethrionomys glareolus</Emphasis>

The generation and maintenance of allelic polymorphism in genes of the major histocompatibility complex (MHC) is a central issue in evolutionary genetics. Recently, the focus has changed from ex situ to in situ populations to understand the mechanisms that determine adaptive MHC polymorphism under natural selection. Birth-and-death evolution and gene conversion events are considered to generate sequence diversity in MHC genes, which subsequently is maintained by balancing selection through parasites. The ongoing arms race between the host and parasites leads to an adaptive selection pressure upon the MHC, evident in high rates of non-synonymous vs synonymous substitution rates. We characterised the MHC class II DRB exon 2 of free living bank voles, Clethrionomys glareolus by single-strand conformation polymorphism and direct sequencing. Unlike other arvicolid species, the DRB locus of the bank vole is at least quadruplicated. No evidence for gene conversion events in the Clgl-DRB sequences was observed. We found not only high allelic polymorphism with 26 alleles in 36 individuals but also high rates of silent polymorphism. Exceptional for MHC class II genes is a purifying selection pressure upon the majority of MHC-DRB sequences. Further, we analysed the association between certain DRB alleles and the parasite burden with gastrointestinal trichostrongyle nematodes Heligmosomum mixtum and Heligmosomoides glareoli and found significant quality differences between specific alleles with respect to infection intensity. Our findings suggest a snapshot in an evolutionary process of ongoing birth-and-death evolution. One allele cluster has lost its function and is already silenced, another is loosing its adaptive value in terms of gastrointestinal nematode resistance, while a third group of alleles indicates all signs of classical functional MHC alleles.     

The use of extrapair copulations for mate appraisal by razorbills, Alca torda

Razorbills (Alca Undo) engaged in extrapair copulations (EPCs)during two phases of their breeding cycle when fertilizationof eggs was not possible, suggesting that EPCs provide nongeneticbenefits. Females actively pursued extrapair mountings afterthey completed egg laying, the first monogamous species reportedto do so. Mountings were performed in mating arenas outsideof the breeding colony, where attendance by postlaying femalesindicated that they sought encounters with extrapair males whiletheir mates were incubating. Postlaying females always successfullyresisted insemination yet positioned themselves to receive mountings.These findings support the hypothesis that resistance to inseminationis a ploy used by females to appraise males. At the end of thebreeding cycle, when males escorted the fledgling to sea, femalesremained at the colony where they consorted and sometimes copulatedwith other males. Nonfertilizable extrapair copulations mayserve two social functions for razorbills: female appraisalof males for future fertilizable EPCs and the appraisal andacquisition of new mates by both sexes.     

EFFECTS OF A HAEMATOPHAGOUS MITE ON THE BARN SWALLOW (HIRUNDO RUSTICA): A TEST OF THE HAMILTON AND ZUK HYPOTHESIS

I tested three assumptions of the Hamilton and Zuk hypothesis (1982), which suggests that the extravagant male plumage of many bird species allows females to choose mates that are resistant to the parasites exploiting the host population at a given time. By choosing such males as mates, females will rear offspring carrying the genes for resistance. I tested three necessary conditions for the Hamilton and Zuk model: (1) whether parasites affect the fitness of their hosts; (2) whether there is heritable variation in parasite resistance, and (3) whether the expression of the sexual ornament varies with parasite burden. The haematophagous mite Ornithonyssus bursa (Macronyssidae, Gamasida) sucks blood from their Barn Swallow (Hirundo rustica) hosts. Experimental manipulation of mite loads and partial cross-fostering experiments on Barn Swallows, where half of the nestlings in the brood were exchanged with nestlings from another nest, shows that parasite burdens and origin, but not rearing conditions, of Bam Swallow nestlings, affected their adult tarsus length and maximum body weight shortly before fledging. Mite loads of adult Barn Swallows at spring arrival were more similar to mite loads of their own offspring, whether reared in their own or in foster nests inoculated with mites, than to loads of foster offspring. Parent Barn Swallows with long tail ornaments had offspring with smaller mite loads in the partial cross-fostering experiments. The amount of increase in male tail ornaments from one year to another was negatively related to experimentally manipulated mite loads of Barn Swallow nests during the preceding breeding season. In conclusion, the three assumptions of the hypothesis were supported by the experimental tests.     

Neutral versus adaptive genetic variation in parasite resistance: importance of major histocompatibility complex supertypes in a free-ranging primate

Current discussions in evolutionary ecology and conservation genetics focus on the relative importance of using selective neutral markers or markers of coding genes to identify adaptive and evolutionary relevant processes. Genetic diversity might be particularly important in immune genes (e.g., in genes of the major histocompatibility complex, MHC), which are influencing pathogen and parasite resistance. We investigated the effects of neutral versus adaptive genetic variation in parasite resistance in a natural population of fat-tailed dwarf lemurs (Cheirogaleus medius). No association between neutral overall individual genetic diversity and parasite load could be detected. In 149 individuals, we identified 50 MHC class II alleles of the functionally important duplicated DRB locus. The investigation of the functional importance of immune gene (MHC) diversity and parasite selection in natural populations is often problematic due to extensive polymorphism in the MHC genes and restrictions in available sample sizes. Here, for the first time we applied an approach that has been developed in human medical studies. Eleven MHC class II supertypes were identified based on shared antigen-binding similarities. The number of individual MHC supertypes had no influence on the nematode burden. However, we found evidence for a specific MHC supertype (supertype 1) that was linked to infected individuals, a higher number of different nematode infections and high intensity of infection per individual. Moreover, one rare MHC supertype (supertype 7) was revealed to be advantageous with respect to parasite burden. Thus, our results add evidence to the small body of studies that show significant associations between specific MHC constitutions and naturally occurring parasites in the complexity of natural populations.     

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.     

MHC diversity, malaria and lifetime reproductive success in collared flycatchers

Major histocompatibility complex (MHC) genes encode proteins involved in the recognition of parasite-derived antigens. Their extreme polymorphism is presumed to be driven by co-evolution with parasites. Host-parasite co-evolution was also hypothesized to optimize within-individual MHC diversity at the intermediate level. Here, we use unique data on lifetime reproductive success (LRS) of female collared flycatchers to test whether LRS is associated with within-individual MHC class II diversity. We also examined the association between MHC and infection with avian malaria. Using 454 sequencing, we found that individual flycatchers carry between 3 and 23 functional MHC class II B alleles. Predictions of the optimality hypothesis were not confirmed by our data as the prevalence of blood parasites decreased with functional MHC diversity. Furthermore, we did not find evidence for an association between MHC diversity and LRS.     

Competition for access to mates predicts female-specific ornamentation and male investment in relative testis size

Sexually selected ornaments are highly variable and the factors that drive variation in ornament expression are not always clear. Rare instances of female-specific ornament evolution (such as in some dance fly species) are particularly puzzling. While some evidence suggests that such rare instances represent straightforward reversals of sexual selection intensity, the distinct nature of trade-offs between ornaments and offspring pose special constraints in females. To examine whether competition for access to mates generally favors heightened ornament expression, we built a phylogeny and conducted a comparative analysis of Empidinae dance fly taxa that display female-specific ornaments. We show that species with more female-biased operational sex ratios in lek-like mating swarms have greater female ornamentation, and in taxa with more ornate females, male relative testis investment is increased. These findings support the hypothesis that ornament diversity in dance flies depends on female receptivity to mates, which is associated with contests for nutritious nuptial gifts provided by males. Moreover, our results suggest that increases in female receptivity lead to higher levels of sperm competition among males. The incidence of both heightened premating sexual selection on females and postmating selection on males contradicts assertions that sex roles are straightforwardly reversed in dance flies.     

Do pheromones reveal male immunocompetence?

Pheromones function not only as mate attractors, but they may also relay important information to prospective mates. It has been shown that vertebrates can distinguish, via olfactory mechanisms, major histocompatibility complex types in their prospective mates. However, whether pheromones can transmit information about immunocompetence is unknown. Here, we show that female mealworm beetles (Tenebrio molitor) prefer pheromones from males with better immunocompetence, indicated by a faster encapsulation rate against a novel antigen, and higher levels of phenoloxidase in haemolymph. Thus, the present study indicates that pheromones could transmit information about males' parasite resistance ability and may work as a reliable sexual ornament for female choice.     

Effect of parasitic infection on male color pattern and female choice in guppies

We infected male guppies Poecilia reticulata with a naturallyoccurring monogenean parasite, Gyrodactylus turnbulli, in orderto examine effects of parasitism on the expression of colorpatterns and on attractiveness to females. The color of carotenoidspots and ability to attract females were compared between experimentallyinfected fish and a control group of their fullsib brothers,which had identical color patterns and were treated identicallyexcept for actual exposure to parasites. The orange spots ofmales that had been infected for 9 days followed by treatmentwith medication to remove parasites became significandy palerand less saturated. Control males (also treated widi medication)showed no significant changes in their orange spots. Femalesin a divided aquarium choice-apparatus showed no preferencebetween control and infection-treatment males initially, butshowed significant discrimination after the infectiondisinfectiontreatment. Females spent less time near males that had beeninfected and responded to a smaller fraction of their courtshipdisplays relative to control males. There were slight differencesin courting rates of males between treatments. Parasitic infectionappears to reduce the degree of expression of carotenoid colorsin guppies, and females are able to discriminate against recentlyinfected males, probably on the basis of the color change. Byavoiding infected males, females may be able to avoid becominginfected themselves, or they may be able to identify mates basedon "good genes" for parasite resistance diat can be passed onto their offspring.     

Female barn owls (Tyto alba) advertise good genes

The good genes hypothesis of sexual selection postulates that ornamentation signals superior genetic quality to potential mates. Support for this hypothesis comes from studies on male ornamentation only, while it remains to be shown that female ornamentation may signal genetic quality as well. Female barn owls (Tyto alba) display more black spots on their plumage than males. The expression of this plumage trait has a genetic basis and it has been suggested that males prefer to mate with females displaying more black spots. Given the role of parasites in the evolution of sexually selected traits and of the immune system in parasite resistance, we hypothesize that the extent of female plumage 'spottiness' reflects immunological defence. We assessed the genetic variation in specific antibody production against a non-pathogenic antigen among cross-fostered nestlings and studied its covariation with the plumage spottiness of genetic parents. The magnitude of the antibody response was positively correlated with the plumage spottiness of the genetic mother but not of the genetic father. Our study thereby provides the first experimental support, to our knowledge, for the hypothesis that female ornamentation signals genetic quality.     

Spatio‐temporal variation in parasite communities maintains diversity at the major histocompatibility complex class IIβ in the endangered Rio Grande silvery minnow

Climate change will strongly impact aquatic ecosystems particularly in arid and semi‐arid regions. Fish–parasite interactions will also be affected by predicted altered flow and temperature regimes, and other environmental stressors. Hence, identifying environmental and genetic factors associated with maintaining diversity at immune genes is critical for understanding species’ adaptive capacity. Here, we combine genetic (MHC class IIβ and microsatellites), parasitological and ecological data to explore the relationship between these factors in the remnant wild Rio Grande silvery minnow (Hybognathus amarus) population, an endangered species found in the southwestern United States. Infections with multiple parasites on the gills were observed and there was spatio‐temporal variation in parasite communities and patterns of infection among individuals. Despite its highly endangered status and chronically low genetic effective size, Rio Grande silvery minnow had high allelic diversity at MHC class IIβ with more alleles recognized at the presumptive DAB1 locus compared to the DAB3 locus. We identified significant associations between specific parasites and MHC alleles against a backdrop of generalist parasite prevalence. We also found that individuals with higher individual neutral heterozygosity and higher amino acid divergence between MHC alleles had lower parasite abundance and diversity. Taken together, these results suggest a role for fluctuating selection imposed by spatio‐temporal variation in pathogen communities and divergent allele advantage in maintenance of high MHC polymorphism. Understanding the complex interaction of habitat, pathogens and immunity in protected species will require integrated experimental, genetic and field studies.     

Female mate preferences and subsequent resistance to copulation in the mallard

In the majority of socially monogamous bird species, femalessolicit or accept copulations from males other than their partner.Females may gain direct benefits from extrapair males, suchas greater access to resources, or indirect genetic benefitsthat will influence the future success of their offspring. However,one group of birds appears to be the exception to this generalrule; in the wildfowl (Anseriformes), all extrapair copulationsappear to be resisted by females. It has been suggested thatresistance behavior may be a strategy to allow females a greaterchoice of mates, either at the precopulatory level (to promotechoice of copulation partner) and/or the postcopulatory level(to promote multiple mating to increase their choice of sperm).This paper examines the function of female resistance behaviorin one of the dabbling ducks, the mallard (Anas platyrhynchos).Observations on a marked population of wild mallard and experimentswith captive birds found that although females showed a strongpreference for particular males that are the first to molt intotheir breeding plumage, male attractiveness did not influencefemale responses to pair or extrapair copulation attempts. Femaleresistance decreased the likelihood that copulation attemptswould end in successful insemination. The findings did not supportthe hypothesis that females resist copulations to promote femalechoice and the reasons why waterfowl may benefit from avoidingall extrapair copulations are discussed.     

Selection from parasites favours immunogenetic diversity but not divergence among locally adapted host populations

The unprecedented polymorphism in the major histocompatibility complex (MHC) genes is thought to be maintained by balancing selection from parasites. However, do parasites also drive divergence at MHC loci between host populations, or do the effects of balancing selection maintain similarities among populations? We examined MHC variation in populations of the livebearing fish Poecilia mexicana and characterized their parasite communities. Poecilia mexicana populations in the Cueva del Azufre system are locally adapted to darkness and the presence of toxic hydrogen sulphide, representing highly divergent ecotypes or incipient species. Parasite communities differed significantly across populations, and populations with higher parasite loads had higher levels of diversity at class II MHC genes. However, despite different parasite communities, marked divergence in adaptive traits and in neutral genetic markers, we found MHC alleles to be remarkably similar among host populations. Our findings indicate that balancing selection from parasites maintains immunogenetic diversity of hosts, but this process does not promote MHC divergence in this system. On the contrary, we suggest that balancing selection on immunogenetic loci may outweigh divergent selection causing divergence, thereby hindering host divergence and speciation. Our findings support the hypothesis that balancing selection maintains MHC similarities among lineages during and after speciation (trans‐species evolution).     

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.