Asymmetric introgression reveals the genetic architecture of a plumage trait

Genome-wide variation in introgression rates across hybrid zones offers a powerful opportunity for studying population differentiation. One poorly understood pattern of introgression is the geographic displacement of a trait implicated in lineage divergence from genome-wide population boundaries. While difficult to interpret, this pattern can facilitate the dissection of trait genetic architecture because traits become uncoupled from their ancestral genomic background. We studied an example of trait displacement generated by the introgression of head plumage coloration from personata to alba subspecies of the white wagtail. A previous study of their hybrid zone in Siberia revealed that the geographic transition in this sexual signal that mediates assortative mating was offset from other traits and genetic markers. Here we show that head plumage is associated with two small genetic regions. Despite having a simple genetic architecture, head plumage inheritance is consistent with partial dominance and epistasis, which could contribute to its asymmetric introgression. Hybrid zones are windows into the evolutionary process. Semenov et al. find that the head plumage differences between white wagtail subspecies have a simple genetic basis involving two small genetic regions, in which partially dominant and epistatic interactions help to explain how this sexual signal has become decoupled from other plumage traits

Rapid adaptive radiation of Darwin's finches depends on ancestral genetic modules

Recent adaptive radiations are models for investigating mechanisms contributing to the evolution of biodiversity. An unresolved question is the relative importance of new mutations, ancestral variants, and introgressive hybridization for phenotypic evolution and speciation. Here, we address this issue using Darwin's finches and investigate the genomic architecture underlying their phenotypic diversity. Admixture mapping for beak and body size in the small, medium, and large ground finches revealed 28 loci showing strong genetic differentiation. These loci represent ancestral haplotype blocks with origins predating speciation events during the Darwin's finch radiation. Genes expressed in the developing beak are overrepresented in these genomic regions. Ancestral haplotypes constitute genetic modules for selection and act as key determinants of the unusual phenotypic diversity of Darwin's finches. Such ancestral haplotype blocks can be critical for how species adapt to environmental variability and change

Sex role similarity and sexual selection predict male and female song elaboration and dimorphism in fairy-wrens

Historically, bird song complexity was thought to evolve primarily through sexual selection on males; yet, in many species, both sexes sing and selection pressure on both sexes may be broader. Previous research suggests competition for mates and resources during short, synchronous breeding seasons leads to more elaborate male songs at high, temperate latitudes. Furthermore, we expect male–female song structure and elaboration to be more similar at lower, tropical latitudes, where longer breeding seasons and year-round territoriality yield similar social selection pressures in both sexes. However, studies seldom take both types of selective pressures and sexes into account. We examined song in both sexes in 15 populations of nine-fairy- wren species (Maluridae), a Southern Hemisphere clade with female song. We compared song elaboration (in both sexes) and sexual song dimorphism to latitude and life-history variables tied to sexual and social selection pressures and sex roles. Our results suggest that song elaboration evolved in part due to sexual competition in males: male songs were longer than female songs in populations with low male survival and less male provisioning. Also, female songs evolved independently of male songs: female songs were slower paced than male songs, although only in less synchronously breeding populations. We also found male and female songs were more similar when parental care was more equal and when male survival was high, which provides strong evidence that sex role similarity correlates with male–female song similarity. Contrary to Northern Hemisphere latitudinal patterns, male and female songs were more similar at higher, temperate latitudes. These results suggest that selection on song can be sex specific, with male song elaboration favored in contexts with stronger sexual selection. At the same time, selection pressures associated with sex role similarity appear to favor sex role similarity in song structure

Ecological adaptation in European eels is based on phenotypic plasticity

The relative role of genetic adaptation and phenotypic plasticity is of fundamental importance in evolutionary ecology [M. J. West-Eberhard, Proc. Natl. Acad. Sci. U.S.A. 102 (suppl. 1), 6543-6549 (2005)]. European eels have a complex life cycle, including transitions between life stages across ecological conditions in the Sargasso Sea, where spawning occurs, and those in brackish and freshwater bodies from northern Europe to northern Africa. Whether continental eel populations consist of locally adapted and genetically distinct populations or comprise a single panmictic population has received conflicting support. Here we use whole-genome sequencing and show that European eels belong to one panmictic population. A complete lack of geographical genetic differentiation is demonstrated. We postulate that this is possible because the most critical life stages-spawning and embryonic development-take place under near-identical conditions in the Sargasso Sea. We further show that within-generation selection, which has recently been proposed as a mechanism for genetic adaptation in eels, can only marginally change allele frequencies between cohorts of eels from different geographic regions. Our results strongly indicate plasticity as the predominant mechanism for how eels respond to diverse environmental conditions during postlarval stages, ultimately solving a long-standing question for a classically enigmatic species

Data from: Female ornamentation is associated with elevated aggression and testosterone in a tropical songbird

In males, testosterone plays a key role in ornament production and linking ornamentation with reproductive behaviors and other traits to produce an integrated phenotype. Less is known about whether females couple testosterone, ornamentation, and aggressive behaviors to achieve female-specific combinations of traits. Ornamentation in females may be the result of correlated expression with male ornamentation, or female traits could arise as the result of sex specific selection pressures. Resolving between these alternatives is necessary to understand the degree to which selection acts on female traits. The White-shouldered Fairywren (Malurus alboscapulatus) provides a useful context to address these questions because populations vary in degree of female ornamentation, a derived trait, whereas male ornamentation is constant across both populations. We found that ornamented females have higher levels of circulating testosterone and respond more aggressively to experimental territorial intrusions than do unornamented females. These findings are consistent with the idea that, among female White-shouldered Fairywrens, testosterone may mechanistically link plumage and behavioral traits to produce an integrated competitive phenotype, as has been reported for males of closely related species. In contrast, circulating testosterone in males did not differ significantly between populations. More broadly, our findings are consistent with ongoing selection on the mechanisms underlying female ornaments, likely via social selection

Structure and Characterization of Phosphoglucomutase 5 from Atlantic and Baltic Herring-An Inactive Enzyme with Intact Substrate Binding

Phosphoglucomutase 5 (PGM5) in humans is known as a structural muscle protein without enzymatic activity, but detailed understanding of its function is lacking. PGM5 belongs to the alpha-D-phosphohexomutase family and is closely related to the enzymatically active metabolic enzyme PGM1. In the Atlantic herring, Clupea harengus, PGM5 is one of the genes strongly associated with ecological adaptation to the brackish Baltic Sea. We here present the first crystal structures of PGM5, from the Atlantic and Baltic herring, differing by a single substitution Ala330Val. The structure of PGM5 is overall highly similar to structures of PGM1. The structure of the Baltic herring PGM5 in complex with the substrate glucose-1-phosphate shows conserved substrate binding and active site compared to human PGM1, but both PGM5 variants lack phosphoglucomutase activity under the tested conditions. Structure comparison and sequence analysis of PGM5 and PGM1 from fish and mammals suggest that the lacking enzymatic activity of PGM5 is related to differences in active-site loops that are important for flipping of the reaction intermediate. The Ala330Val substitution does not alter structure or biophysical properties of PGM5 but, due to its surface-exposed location, could affect interactions with protein-binding partners

Drought disrupts year-round breeding readiness in a tropical songbird

Climate change is expected to increase the prevalence and severity of extreme weather events like drought. For many opportunistically breeding tropical bird species, precipitation serves as a primary cue for onset of breeding, and sustained drought can have major impacts on reproductive fitness. The physiological effects of drought are poorly understood, but understanding physiological responses can help resolve the mechanisms underlying effects of drought on population demography. We used physiological data collected on a year-round breeding New Guinea endemic passerine, the White-shouldered Fairywren (Malurus alboscapulatus), during years with persistent rainfall and during the 2015–2016 El Niño drought event to assess patterns of breeding readiness, body condition, and molt. Many males lost their cloacal protuberances, a sperm storage organ they typically maintain year-round, during the drought period. Body molt, which also occurs year-round in this species, was higher in males during the drought period. Using a sliding-window statistical model approach, we identified a critical precipitation window of 0–40 days prior to capture for cloacal protuberance volume and a window of 8–53 days for molt, with lower precipitation associated with smaller cloacal protuberances and greater molt. Plasma androgens were predictive of variation in male cloacal protuberance volume and molt, thus potentially mediating transitions between life-history stages in response to environmental conditions. Female molt, androgens, and male mass varied with photoperiod, with longer but decreasing day lengths characteristic of the austral summer associated with increasing molt and decreasing androgens. Collectively, our results indicate the potential for photoperiod to cue some life-history stages, whereas reduced rainfall impacts male but apparently not female reproductive physiology and readiness to breed. Improving our understanding of environmental regulation of life-history transitions in tropical taxa is essential for identifying which taxa are most at risk under a changing climate

Copy number variation and elevated genetic diversity at immune trait loci in Atlantic and Pacific herring

Background Genome-wide comparisons of populations are widely used to explore the patterns of nucleotide diversity and sequence divergence to provide knowledge on how natural selection and genetic drift affect the genome. In this study we have compared whole-genome sequencing data from Atlantic and Pacific herring, two sister species that diverged about 2 million years ago, to explore the pattern of genetic differentiation between the two species. Results The genome comparison of the two species revealed high genome-wide differentiation but with islands of remarkably low genetic differentiation, as measured by an FST analysis. However, the low FST observed in these islands is not caused by low interspecies sequence divergence (dxy) but rather by exceptionally high estimated intraspecies nucleotide diversity (π). These regions of low differentiation and elevated nucleotide diversity, termed high-diversity regions in this study, are not enriched for repeats but are highly enriched for immune-related genes. This enrichment includes genes from both the adaptive immune system, such as immunoglobulin, T-cell receptor and major histocompatibility complex genes, as well as a substantial number of genes with a role in the innate immune system, e.g. novel immune-type receptor, tripartite motif and tumor necrosis factor receptor genes. Analysis of long-read based assemblies from two Atlantic herring individuals revealed extensive copy number variation in these genomic regions, indicating that the elevated intraspecies nucleotide diversities were partially due to the cross-mapping of short reads. Conclusions This study demonstrates that copy number variation is a characteristic feature of immune trait loci in herring. Another important implication is that these loci are blind spots in classical genome-wide screens for genetic differentiation using short-read data, not only in herring, likely also in other species harboring qualitatively similar variation at immune trait loci. These loci stood out in this study because of the relatively high genome-wide baseline for FST values between Atlantic and Pacific herring

A Chromosome-Level Assembly of Blunt Snout Bream (Megalobrama amblycephala) Genome Reveals an Expansion of Olfactory Receptor Genes in Freshwater Fish

The number of olfactory receptor genes (ORs), which are responsible for detecting diverse odor molecules varies extensively among mammals as a result of frequent gene gains and losses that contribute to olfactory specialization. However, how OR expansions/contractions in fish are influenced by habitat and feeding habit and which OR subfamilies are important in each ecological niche is unknown. Here, we report a major OR expansion in a freshwater herbivorous fish, Megalobrama amblycephala, using a highly contiguous, chromosome-level assembly. We evaluate the possible contribution of OR expansion to habitat and feeding specialization by comparing the OR repertoire in 28 phylogenetically and ecologically diverse teleosts. In total, we analyzed > 4,000 ORs including 3,253 intact, 122 truncated, and 913 pseudogenes. The number of intact ORs is highly variable ranging from 20 to 279. We estimate that the most recent common ancestor of Osteichthyes had 62 intact ORs, which declined in most lineages except the freshwater Otophysa clade that has a substantial expansion in subfamily beta and epsilon ORs. Across teleosts, we found a strong association between duplications of beta and epsilon ORs and freshwater habitat. Nearly, all ORs were expressed in the olfactory epithelium (OE) in three tested fish species. Specifically, all the expanded beta and epsilon ORs were highly expressed in OE of M. amblycephala. Together, we provide molecular and functional evidence for how OR repertoires in fish have undergone gain and loss with respect to ecological factors and highlight the role of beta and epsilon OR in freshwater adaptation