The genomic consequences of adaptive divergence and reproductive isolation between species of manakins.

The processes of adaptation and speciation are expected to shape genomic variation within and between diverging species. Here we analyze genomic heterogeneity of genetic differentiation and introgression in a hybrid zone between two bird species (Manacus candei and M. vitellinus) using 59 100 SNPs, a whole genome assembly, and Bayesian models. Measures of genetic differentiation (FST) and introgression (genomic cline center [α] and rate [ß]) were highly heterogeneous among loci. We identified thousands of loci with elevated parameter estimates, some of which are likely to be associated with variation in fitness in Manacus populations. To analyze the genomic organization of differentiation and introgression, we mapped SNPs onto a draft assembly of the M. vitellinus genome. Estimates of FST, α, and ß were autocorrelated at very short physical distances (< 100 bp), but much less so beyond this. In addition, average statistical associations (linkage disequilibrium) between SNPs were generally low and were not higher in admixed populations than in populations of the parental species. Although they did not occur with a constant probability across the genome, loci with elevated FST, α, and ß were not strongly co-localized in the genome. Contrary to verbal models that predict clustering of loci involved in adaptation and isolation in discrete genomic regions, these results are consistent with the hypothesis that genetic regions involved in adaptive divergence and reproductive isolation are scattered throughout the genome. We also found that many loci were characterized by both exceptional genetic differentiation and introgression, consistent with the hypothesis that loci involved in isolation are also often characterized by a history of divergent selection. However, the concordance between isolation and differentiation was only partial, indicating a complex architecture and history of loci involved in isolation.

Genomic insights into adaptation to high-altitude environments.

Elucidating the molecular genetic basis of adaptive traits is a central goal of evolutionary genetics. The cold, hypoxic conditions of high-altitude habitats impose severe metabolic demands on endothermic vertebrates, and understanding how high-altitude endotherms cope with the combined effects of hypoxia and cold can provide important insights into the process of adaptive evolution. The physiological responses to high-altitude stress have been the subject of over a century of research, and recent advances in genomic technologies have opened up exciting opportunities to explore the molecular genetic basis of adaptive physiological traits. Here, we review recent literature on the use of genomic approaches to study adaptation to high-altitude hypoxia in terrestrial vertebrates, and explore opportunities provided by newly developed technologies to address unanswered questions in high-altitude adaptation at a genomic scale.

Sexual selection on plumage and behavior in an avian hybrid zone: experimental tests of male-male interactions.

In western Panama, an unusual hybrid zone exists between white-collared manakins, Manacus candei, and golden-collared manakins, M. vitellinus. Unidirectional introgression of plumage traits from vitellinus into candei has created a region in which all definitively plumaged males have a collar that is lemon-colored. These males are nearly indistinguishable from white-collared candei genetically and morphometrically, but strongly resemble golden-collared vitellinus due to the introgression of secondary sexual plumage traits, particularly the lemon-colored collar. The introgression could be explained by sexual selection for golden-collared traits or by a series of mechanisms that do not invoke sexual selection (e.g., neutral diffusion, dominant allele). Sexual selection on male-male interactions implies behavioral differences among the plumage forms--specifically that golden- and lemon-collared males should be more aggressive than white-collared males. In contrast, the nonsexual hypotheses predict behavioral similarity between lemon- and white-collared males, based on their nearly identical genetics. We tested the sexual selection hypothesis experimentally, by presenting males with taxidermic mounts of the three forms. As response variables, we monitored vocalizations and attacks on the mounts by replicate subject males. Both golden-collared and lemon-collared males were more likely to attack than were white-collared males, as predicted under sexual selection but not by the nonsexual hypotheses. Lemon-collared males were more vocally reactive than either parental form, contrary to the prediction of the nonsexual hypotheses. Our study demonstrates that sexual selection on male-male interactions may play an important role in the dynamics of character evolution and hybrid zones.

Evolutionary implications of divergent clines in an avian (Manacus: Aves) hybrid zone.

A previous study of the hybrid zone in western Panama between white-collared (Manacus candei) and golden-collared manakins (M. vitellinus) documented the unidirectional introgression of vitellinus male secondary sexual traits across the zone. Here, we examine the hybrid zone in greater genetic and morphological detail. Statistical comparisons of clines are performed using maximum-likelihood and nonparametric bootstrap methods. Our results demonstrate that an array of six molecular and two morphometric markers agree in cline position and width. Clines for male collar and belly color are similar in width to the first eight clines, but are shifted in position by at least five cline widths. The result is that birds in intervening populations are genetically and morphometrically very like parental candei, but males have the plumage color of parental vitellinus. Neither neutral diffusion nor nonlinearity of color scales appear to be viable explanations for the large cline shifts. Genetic dominance of vitellinus plumage traits is another potential explanation that will require breeding experiments to test. Sexual selection remains a plausible explanation for the observed introgression of vitellinus color traits in these highly dimorphic, polygynous, lek-mating birds. Two other clines, including a nondiagnostic isozyme locus, are similar in position to the main cluster of clines, but are broader in width. Thus, introgression at some loci is greater than that detected with diagnostic markers. Assuming that narrow clines are maintained by selection, variation in cline width indicates that selection is not uniform throughout the genome and that diagnostic markers are under more intense selective pressure. The traditional focus on diagnostic markers in studies of hybrid zones may therefore lead to underestimates of average introgression. This effect may be more pronounced in organisms with low levels of genetic divergence between hybridizing taxa.

Estimating the unbiased estimator theta for population genetic survey data.

We consider a method of approximating Weir and Cockerham's theta, an unbiased estimator of genetic population structure, using values readily available from published studies using biased estimators (Wright's F(ST) or Nei's G(ST)). The estimation algorithm is shown to be useful for both model populations and real-world avian populations. However, the correlation between Wright's F(ST) and Weir and Cockerham's theta is strong when compared among 39 empirical avian datasets. Thus, the advantage of approximating an unbiased estimator is unclear considering the small actual effect of theta's bias-removing power on empirical datasets.