Patterns of MHC-dependent mate selection in humans and nonhuman primates: a meta-analysis.

Genes of the major histocompatibility complex (MHC) in vertebrates are integral for effective adaptive immune response and are associated with sexual selection. Evidence from a range of vertebrates supports MHC-based preference for diverse and dissimilar mating partners, but evidence from human mate choice studies has been disparate and controversial. Methodologies and sampling peculiarities specific to human studies make it difficult to know whether wide discrepancies in results among human populations are real or artefact. To better understand what processes may affect MHC-mediated mate choice across humans and nonhuman primates, we performed phylogenetically controlled meta-analyses using 58 effect sizes from 30 studies across seven primate species. Primates showed a general trend favouring more MHC-diverse mates, which was statistically significant for humans. In contrast, there was no tendency for MHC-dissimilar mate choice, and for humans, we observed effect sizes indicating selection of both MHC-dissimilar and MHC-similar mates. Focusing on MHC-similar effect sizes only, we found evidence that preference for MHC similarity was an artefact of population ethnic heterogeneity in observational studies but not among experimental studies with more control over sociocultural biases. This suggests that human assortative mating biases may be responsible for some patterns of MHC-based mate choice. Additionally, the overall effect sizes of primate MHC-based mating preferences are relatively weak (Fisher's Z correlation coefficient for dissimilarity Zr = 0.044, diversity Zr = 0.153), calling for careful sampling design in future studies. Overall, our results indicate that preference for more MHC-diverse mates is significant for humans and likely conserved across primates.

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.

Parasite-mediated evolution of the functional part of the MHC in primates.

The major histocompatibility complex (MHC) is a key model of genetic polymorphism, but the mechanisms underlying its extreme variability are debated. Most hypotheses for MHC diversity focus on pathogen-driven selection and predict that MHC polymorphism evolves under the pressure of a diverse parasite fauna. Several studies reported that certain alleles offer protection against certain parasites, yet it remains unclear whether variation in parasite pressure more generally covaries with allelic diversity and rates of molecular evolution of MHC across species. We tested this prediction in a comparative study of 41 primate species. We characterized polymorphism of the exon 2 of DRB region of the MHC class II. Our phylogenetic analyses controlled for the potential effects of neutral mutation rate, population size, geographic origin and body mass and revealed that nematode species richness associates positively with nonsynonymous nucleotide substitution rate at the functional part of the molecule. We failed to find evidence for allelic diversity being strongly related to parasite species richness. Continental distribution was a strong predictor of both allelic diversity and substitution rate, with higher values in Malagasy and Neotropical primates. These results indicate that parasite pressure can influence the different estimates of MHC polymorphism, whereas geography plays an independent role in the natural history of MHC.

Migratory divides and their consequences for dispersal, population size and parasite-host interactions.

Populations of migratory birds differ in their direction of migration with neighbouring populations often migrating in divergent directions separated by migratory divides. A total of 26% of 103 passerine bird species in Europe had migratory divides that were located disproportionately often along a longitudinal gradient in Central Europe, consistent with the assumption of a Quaternary glacial origin of such divides in the Iberian and Balkan peninsulas followed by recolonization. Given that studies have shown significant genetic differentiation and reduced gene flow across migratory divides, we hypothesized that an absence of migratory divides would result in elevated rates of gene flow and hence a reduced level of local adaptation. In a comparative study, species with migratory divides had larger population sizes and population densities and longer dispersal distances than species without migratory divides. Species with migratory divides tended to be habitat generalists. Bird species with migratory divides had higher richness of blood parasites and higher growth rates of Staphylococcus on their eggs during the incubation period. There was weaker cell-mediated immunity in adults and stronger cell lysis in species with migratory divides. These findings may suggest that migratory divides constitute barriers to dispersal with consequences for ecology and evolution of distributions, population sizes, habitats and parasite-host interactions. They also suggest that migratory divides may play a role in local adaptation in host-parasite interactions.

Determinants of distribution and prevalence of avian malaria in blue tit populations across Europe: separating host and parasite effects.

Although avian malarial parasites are globally distributed, the factors that affect the geographical distribution and local prevalence of different parasite lineages across host populations or species are still poorly understood. Based on the intense screening of avian malarial parasites in nine European blue tit populations, we studied whether distribution ranges as well as local adaptation, host specialization and phylogenetic relationships can determine the observed prevalences within populations. We found that prevalence differed consistently between parasite lineages and host populations, indicating that the transmission success of parasites is lineage specific but is partly shaped by locality-specific effects. We also found that the lineage-specific estimate of prevalence was related to the distribution range of parasites: lineages found in more host populations were generally more prevalent within these populations. Additionally, parasites with high prevalence that were also widely distributed among blue tit populations were also found to infect more host species. These findings suggest that parasites reaching high local prevalence can also realize wide distribution at a global scale that can have further consequences for host specialization. Although phylogenetic relationships among parasites did not predict prevalence, we detected a close match between a tree based on the geographic distance of the host populations and the parasite phylogenetic tree, implying that neighbouring host populations shared a related parasite fauna.

Latitudinal distribution, migration, and testosterone levels in birds.

Tropical bird species usually have lower testosterone (T) levels during breeding than temperate species. However, the potential mechanisms behind the positive interspecific correlation between T and latitude remain unexplored. In a comparative study of more than 100 bird species, we examined whether social constraints during male-male competition arising from migration and breeding synchrony are responsible for the latitude effects. Species that breed at higher latitudes are more likely to migrate and experience more intense intrasexual competition upon spring arrival than nonmigrant species from lower latitudes. Additionally, species from higher latitudes cope with shorter breeding seasons and thus with more synchronous breeding, which selects for high T titers via increased male-male conflicts. Accordingly, peak T levels were associated with migration and the duration of the egg laying period that reflects breeding synchrony. Because migration and breeding synchrony were related to latitudinal distribution, they appear to be important components of the latitude effects on T. A multivariate model controlling for covariation of predictor variables revealed that latitude remained the strongest predictor of peak T. Therefore, selection due to migration and breeding synchrony may partially cause the latitude effect, but other geographically varying factors may also play a role in mediating peak T levels at different latitudes.

Genetic similarity, breeding distribution range and sexual selection.

Large populations with extensive breeding distributions may sustain greater genetic variability, thus producing a positive relationship between genetic variation and population size. Levels of genetic variability may also be affected by sexual selection, which could either reduce levels because a small fraction of males contribute to the following generation, or augment them by generating genetic variability through elevated rates of mutations. We investigated to what extent genetic variability, as estimated from band sharing coefficients for minisatellite markers, could be predicted by breeding distribution range, population size and intensity of sexual selection (as reflected by degree of polygyny and extra-pair paternity). Across a sample of 62 species of birds in the Western Palearctic, we found extensive interspecific variation in band sharing coefficients. High band sharing coefficients (implying low local genetic variability among individuals) were associated with restricted breeding distributions, a conclusion confirmed by analysis of statistically independent linear contrasts. Independently, species with large population sizes had small band sharing coefficients. Furthermore, bird species with a high richness of subspecies for their breeding distribution range had higher band sharing coefficients. Finally, bird species with high levels of polygyny and extra-pair paternity had small band sharing coefficients. These results suggest that breeding distribution range, population size and intensity of sexual selection are important predictors of levels of genetic variability in extant populations.

Maternal effects and the evolution of brain size in birds: overlooked developmental constraints.

A central dogma for the evolution of brain size posits that the maintenance of large brains incurs developmental costs, because they need prolonged periods to grow during the early ontogeny. Such constraints are supported by the interspecific relationship between ontological differences and relative brain size in birds and mammals. Given that mothers can strongly influence the development of the offspring via maternal effects that potentially involve substances essential for growing brains, we argue that such effects may represent an important but overlooked component of developmental constraints on brain size. To demonstrate the importance of maternal effect on the evolution of brains, we investigated the interspecific relationship between relative brain size and maternal effects, as reflected by yolk testosterone, carotenoids, and vitamins A and E in a phylogenetic study of birds. Females of species with relatively large brains invested more in eggs in terms of testosterone and vitamin E than females of species with small brains. The effects of carotenoid and vitamin A levels on the evolution of relative brain size were weaker and non-significant. The association between relative brain size and yolk testosterone was curvilinear, suggesting that very high testosterone levels can be suppressive. However, at least in moderate physiological ranges, the positive relationship between components of maternal effects and relative brain size may imply one aspect of developmental costs of large brains. The relationship between vitamin E and relative brain size was weakened when we controlled for developmental mode, and thus the effect of this antioxidant may be indirect. Testosterone-enhanced neurogenesis and vitamin E-mediated defence against oxidative stress may have key functions when the brain of the embryo develops, with evolutionary consequences for relative brain size.

Interspecific variation in egg testosterone levels: implications for the evolution of bird song.

Although interspecific variation in maternal effects via testosterone levels can be mediated by natural selection, little is known about the evolutionary consequences of egg testosterone for sexual selection. However, two nonexclusive evolutionary hypotheses predict an interspecific relationship between egg testosterone levels and the elaboration of sexual traits. First, maternal investment may be particularly enhanced in sexually selected species, which should generate a positive relationship. Secondly, high prenatal testosterone levels may constrain the development of sexual characters, which should result in a negative relationship. Here we investigated these hypotheses by exploring the relationship between yolk testosterone levels and features of song in a phylogenetic study of 36 passerine species. We found that song duration and syllable repertoire size were significantly negatively related to testosterone levels in the egg, even if potentially confounding factors were held constant. These relationships imply that high testosterone levels during early development of songs may be detrimental, thus supporting the developmental constraints hypothesis. By contrast, we found significant evidence that song-post exposure relative to the height of the vegetation is positively related to egg testosterone levels. These results support the hypothesis that high levels of maternal testosterone have evolved in species with intense sexual selection acting on the location of song-posts. We found nonsignificant effects for intersong interval and song type repertoire size, which may suggest that none of the above hypothesis apply to these traits, or they act simultaneously and have opposing effects.

Rapid temporal change in the expression and age-related information content of a sexually selected trait.

The expression of sexual signals is often phenotypically plastic and also evolves rapidly. Few studies have considered the possibility that proximate determination -- the pathway between genes and trait expression -- may also be subject to both phenotypic plasticity and evolutionary change. We examined long-term patterns in size, condition- and age-dependence, repeatability and heritability of forehead patch size, a sexually selected plumage trait in male collared flycatchers. We also estimated survival and sexual selection on the phenotypic value of the trait. Forehead patch size linearly declined during the 15 years, probably due to the significantly negative survival selection. In addition, the expression of genetic variation for the ornament apparently underwent an age-limited change, which implies a change in the information content of the signal to receivers. The persistent lack of condition-dependence makes phenotypic plasticity an unlikely explanation to our results. This raises the possibility of a microevolutionary change of both expression and proximate determination during the study period.

The design of complex sexual traits in male barn swallows: associations between signal attributes.

Variation in the expression of sexually selected traits among individuals is widely investigated on the premise that these traits evolved to signal male quality. Significant repeatabilities of sexual signals and their associations with condition, mating success, survivorship and age may be the signatures of sexual selection. However, little is known about the relationship between these sexual attributes. Here we studied 28 acoustic and visual traits in the barn swallow, Hirundo rustica, that may potentially function in sexual selection. Based on effect sizes calculated at the between-individual level, we assessed the relationship between repeatability, condition-dependence, attractiveness, age-dependence and viability indicator value of sexual traits using sexual signals as the units of analyses. Those traits that showed high within-year repeatability also showed high between-year repeatability, indicating that between-individual variation is consistent within and among seasons. In addition, age-dependence of traits, probably causing between-year variation, was negatively related to between-year repeatability. Condition-dependence was negatively correlated with effect sizes for the extent to which traits predicted viability. Therefore, traits that are positively related to immediate condition are those that are negatively related to survival, which may be the signature of a trade-off between current and future reproductive success ultimately reflecting signal reliability. No other significant relationship was found between trait attributes. We conclude that multiple sexual signals reflect different aspects of male quality in the barn swallow.

Coevolutionary arms races: increased host immune defense promotes specialization by avian fleas.

We investigated the relationship between host defense and specialization by parasites in comparative analyses of bird fleas and T-cell mediated immune response of their avian hosts, showing that fleas with few main host species exploited hosts with weak or strong immune defenses, whereas flea species that parasitized a large number of host species only exploited hosts with weak immune responses. Hosts with strong immune responses were exploited by a larger number of flea species than hosts with weak responses. A path analysis model with an effect of T-cell response on the number of host species, or a model with host coloniality directly affecting host T-cell response, which in turn affected the number of host species used by fleas, best explained the data. Therefore, parasite specialization may have evolved in response to strong host defenses.

Covariation between brain size and immunity in birds: implications for brain size evolution.

Parasitism can negatively affect learning and cognition, setting the scene for coevolution between brain and immunity. Greater susceptibility to parasitism by males may impair their cognitive ability, and relatively greater male investment in immunity could compensate for greater susceptibility to parasites, in particular when males have a relatively large brain. We analysed covariation between relative size of immune defence organs and brain in juvenile and adult birds. The relative size of the bursa of Fabricius and the spleen in adults covaried positively with relative brain size across bird species. The relative size of these two immune defence organs covaried with sex differences in relative size of the brain, indicating that the relationship between immune defence and brain size was stronger for males. In contrast, liver and heart size or sexual size dimorphism in size did not covary with immune defence. Thus, species in which males have relatively large brains also have relatively large immune defence organs.

Testosterone, testes size, and mating success in birds: a comparative study.

Reproductive behaviors of vertebrates are often underpinned by temporal patterns of hormone secretion. We investigated interspecific patterns of circulating testosterone in male birds to test the hypothesis that testosterone plays a crucial role in sexual selection as determined by degree of polygyny and extra-pair paternity. We predicted that the evolution of increased levels of polygyny and extra-pair paternity would have resulted in the evolution of increased levels of testosterone to allow males more efficiently to compete for mates. This hypothesis was tested in comparative analyses of 116 species of birds using Generalized Least Squares Models. We assessed the importance of latitudinal distribution, because this can confound the relationship between testosterone and mating success. There were weak positive phylogenetic correlations between measures of testosterone and estimates of mating success at the social level, but this association appeared to be confounded by latitudinal distribution, a significant correlate of testosterone titers. However, we found a significantly positive relationship between peak and residual peak testosterone (which is the peak testosterone level that is controlled for the baseline level) and extra-pair paternity independent of latitude. These results suggest that selection pressures arising from social and sexual mating differently affected testosterone levels with the former being mediated by factors associated with latitudinal distribution. An analysis of residual testes size revealed a positive association between peak and residual testosterone and testes size relative to body size. In a path analysis, we show that relative testis size primarily evolved in association with intense sperm competition and thus high sperm production, and these mechanisms had a secondary impact on blood testosterone levels at a phylogenetic scale. Our results suggest that sperm competition has played an important role in the evolution of reproductive mechanisms in birds.

Flycatcher song in allopatry and sympatry--convergence, divergence and reinforcement.

The theory of reinforcement predicts that natural selection against the production of unfit hybrids favours traits that increase assortative mating. Whether culturally inherited traits, such as bird song, can increase assortative mating by reinforcement is largely unknown. We compared songs of pied (Ficedula hypoleuca) and collared flycatchers (F. albicollis) from two hybrid zones of different ages with songs from allopatric populations. Previously, a character divergence in male plumage traits has been shown to reinforce premating isolation in sympatric flycatchers. In contrast, we find that the song of the pied flycatcher has converged towards that of the collared flycatcher (mixed singing). However, a corresponding divergence in the collared flycatcher shows that the species differences in song characters are maintained in sympatry. Genetic analyses suggest that mixed song is not caused by introgression from the collared flycatcher, but rather due to heterospecific copying. Circumstantial evidence suggests that mixed song may increase the rate of maladaptive hybridization. In the oldest hybrid zone where reinforcement on plumage traits is most pronounced, the frequency of mixed singing and hybridization is also lowest. Thus, we suggest that reinforcement has reduced the frequency of mixed singing in the pied flycatcher and caused a divergence in the song of the collared flycatcher. Whether a culturally inherited trait promotes or opposes speciation in sympatry may depend on its plasticity. The degree of plasticity may be genetically determined and accordingly under selection by reinforcement.