Genome-wide differentiation in closely related populations: the roles of selection and geographic isolation.

Population divergence in geographic isolation is due to a combination of factors. Natural and sexual selection may be important in shaping patterns of population differentiation, a pattern referred to as 'isolation by adaptation' (IBA). IBA can be complementary to the well-known pattern of 'isolation by distance' (IBD), in which the divergence of closely related populations (via any evolutionary process) is associated with geographic isolation. The barn swallow Hirundo rustica complex comprises six closely related subspecies, where divergent sexual selection is associated with phenotypic differentiation among allopatric populations. To investigate the relative contributions of selection and geographic distance to genome-wide differentiation, we compared genotypic and phenotypic variation from 350 barn swallows sampled across eight populations (28 pairwise comparisons) from four different subspecies. We report a draft whole-genome sequence for H. rustica, to which we aligned a set of 9493 single nucleotide polymorphisms (SNPs). Using statistical approaches to control for spatial autocorrelation of phenotypic variables and geographic distance, we find that divergence in traits related to migratory behaviour and sexual signalling, as well as geographic distance, together explain over 70% of genome-wide divergence among populations. Controlling for IBD, we find 42% of genomewide divergence is attributable to IBA through pairwise differences in traits related to migratory behaviour and sexual signalling alone. By (i) combining these results with prior studies of how selection shapes morphological differentiation and (ii) accounting for spatial autocorrelation, we infer that morphological adaptation plays a large role in shaping population-level differentiation in this group of closely related populations.

Phenotypic differentiation is associated with divergent sexual selection among closely related barn swallow populations.

Sexual selection plays a key role in the diversification of numerous animal clades and may accelerate trait divergence during speciation. However, much of our understanding of this process comes from phylogenetic comparative studies, which rely on surrogate measures such as dimorphism that may not represent selection in wild populations. In this study, we assess sexual selection pressures for multiple male visual signals across four barn swallow (Hirundo rustica) populations. Our sample encompassed 2400 linear km and two described subspecies: European H. r. rustica (in the Czech Republic and Romania) and eastern Mediterranean H. r. transitiva (in Israel), as well as a potential area of contact (in Turkey). We demonstrate significant phenotypic differentiation in four sexual signalling axes, despite very low-level genomic divergence and no comparable divergence in an ecological trait. Moreover, the direction of phenotypic divergence is consistent with differences in sexual selection pressures among subspecies. Thus, H. r. transitiva, which have the darkest ventral plumage of any population, experience directional selection for darker plumage. Similarly, H. r. rustica, which have the longest tail feathers of any population, experience directional selection for elongated tail feathers and disruptive selection for ventral plumage saturation. These results suggest that sexual selection is the primary driver of phenotypic differentiation in this species. Our findings add to growing evidence of phenotypic divergence with gene flow. However, to our knowledge, this is the first study to relate direct measures of the strength and targets of sexual selection to phenotypic divergence among closely related wild populations.

Feather moult and bird appearance are correlated with global warming over the last 200 years.

Global warming alters various avian phenological processes, including advanced reproduction and migration schedules. In birds, individual appearance is largely determined by plumage, influencing, for example, bird attractiveness, social status and camouflage. Juveniles of most passerine species replace their nest-grown plumage during the first months of life, a process that is called post-juvenile feather moult. Using data from ten natural history collections, we show that the extent of the post-juvenile moult has increased significantly over the last 212 years (1805-2016), a trend that is positively correlated with the temperature of the environment. Therefore, it seems that birds replaced more feathers under warmer conditions, causing juveniles to appear more similar to adult birds. Moreover, in several species, we describe a male-female switch in the extent of moult, with females currently replacing more feathers than males compared to the past. These results demonstrate different biological responses to climate warming by different phenotypes.

Cortisol advantage of neighbouring the opposite sex in utero.

Population sex ratios naturally fluctuate around equality. It is argued that the production of an equal number of male and female offspring by individual parents should be favoured by selection, if all costs and benefits are equal. Theoretically, an even sex ratio should yield the highest probability for a fetus to be adjacent to a fetus of the opposite sex in utero. This may cause developmental costs or benefits that have been overlooked. We examined the physiological and developmental parameters associated with in utero sex ratios in the nutria (Myocastor coypus), an invasive wildlife species with a strong reproductive output. Using hair testing, we found that litters with even sex ratios had the highest average cortisol levels. Fetuses neighbouring the opposite sex exhibited longer trunks than those neighbouring the same sex, which might imply better lung development. Our results are the first, to our knowledge, to link intra-utero sex ratios and fetal cortisol and suggest that fetal cortisol might be a mechanism by which even sex ratios are maintained via developmental advantages.