David P. L. Toews

Plumage Genes and Little Else Distinguish the Genomes of Hybridizing Warblers

When related taxa hybridize extensively, their genomes may become increasingly homogenized over time. This mixing via hybridization creates conservation challenges when it reduces genetic or phenotypic diversity and when it endangers previously distinct species via genetic swamping [1]. However, hybridization also facilitates admixture mapping of traits that distinguish each species and the associated genes that maintain distinctiveness despite ongoing gene flow [2]. We address these dual aspects of hybridization in the golden-winged/blue-winged warbler complex, two phenotypically divergent warblers that are indistinguishable using traditional molecular markers and that draw substantial conservation attention [3-5]. Whole-genome comparisons show that differentiation is extremely low: only six small genomic regions exhibit strong differences. Four of these divergence peaks occur in proximity to genes known to be involved in feather development or pigmentation: agouti signaling protein (ASIP), follistatin (FST), ecodysplasin (EDA), wingless-related integration site (Wnt), and beta-carotene oxygenase 2 (BCO2). Throat coloration-the most striking plumage difference between these warblers-is perfectly associated with the promoter region of agouti, and genotypes at this locus obey simple Mendelian recessive inheritance of the black-throated phenotype characteristic of golden-winged warblers. The more general pattern of genomic similarity between these warblers likely results from a protracted period of hybridization, contradicting the broadly accepted hypothesis that admixture results from solely anthropogenic habitat change in the past two centuries [4]. Considered in concert, these results are relevant to both the genetic architecture of avian feather pigmentation and the evolutionary history and conservation challenges associated with these declining songbirds.

Genomic approaches to understanding population divergence and speciation in birds

ABSTRACT The widespread application of high-throughput sequencing in studying evolutionary processes and patterns of diversification has led to many important discoveries. However, the barriers to utilizing these technologies and interpreting the resulting data can be daunting for first-time users. We provide an overview and a brief primer of relevant methods (e.g., whole-genome sequencing, reduced-representation sequencing, sequence-capture methods, and RNA sequencing), as well as important steps in the analysis pipelines (e.g., loci clustering, variant calling, whole-genome and transcriptome assembly). We also review a number of applications in which researchers have used these technologies to address questions related to avian systems. We highlight how genomic tools are advancing research by discussing their contributions to 3 important facets of avian evolutionary history. We focus on (1) general inferences about biogeography and biogeographic history, (2) patterns of gene flow and isolation upon secondary contact and hybridization, and (3) quantifying levels of genomic divergence between closely related taxa. We find that in many cases, high-throughput sequencing data confirms previous work from traditional molecular markers, although there are examples in which genome-wide genetic markers provide a different biological interpretation. We also discuss how these new data allow researchers to address entirely novel questions, and conclude by outlining a number of intellectual and methodological challenges as the genomics era moves forward.

The Evolution and Genetics of Carotenoid Processing in Animals

Coloration is one of the most conspicuous traits that varies among organisms. Carotenoid pigments are responsible for many of the red, orange, and yellow colors in the natural world and, at least for most animals, these molecules must be acquired from their environment. Identifying genes important for carotenoid transport, deposition, and processing has been difficult, in contrast to the well-characterized genes involved in the melanogenesis pathways. We review recent progress in the genetics of carotenoid processing, advances owing in part to the application of high-throughput sequencing data. We focus on examples from several classes of genes coding for scavenger receptors, β-carotene oxygenases, and ketolases. We also review comparative studies that have revealed several important findings in the evolution of these genes. Namely, that they are conserved across deep phylogenetic timescales, are associated with gene/genome duplications, and introgression has contributed to their movement between several taxa.

Admixture mapping in a hybrid zone reveals loci associated with avian feather coloration

Identifying the genetic bases for colour patterns has provided important insights into the control and expression of pigmentation and how these characteristics influence fitness. However, much more is known about the genetic bases for traits based on melanin pigments than for traits based on another major class of pigments, carotenoids. Here, we use natural admixture in a hybrid zone between Audubons and myrtle warblers (Setophaga coronata auduboni/S. c. coronata) to identify genomic regions associated with both types of pigmentation. Warblers are known for rapid speciation and dramatic differences in plumage. For each of five plumage coloration traits, we found highly significant associations with multiple single-nucleotide polymorphisms (SNPs) across the genome and these were clustered in discrete regions. Regions near significantly associated SNPs were enriched for genes associated with keratin filaments, fibrils that make up feathers. A carotenoid-based trait that differs between the taxa—throat colour—had more than a dozen genomic regions of association. One cluster of SNPs for this trait overlaps the Scavenger Receptor Class F Member 2 (SCARF2) gene. Other scavenger receptors are presumed to be expressed at target tissues and involved in the selective movement of carotenoids into the target cells, making SCARF2 a plausible new candidate for carotenoid processing. In addition, two melanin-based plumage traits—colours of the eye line and eye spot—show very strong associations with a single genomic region mapping to chromosome 20 in the zebra finch. These findings indicate that only a subset of the genomic regions differentiated between these two warblers are associated with the plumage differences between them and demonstrate the utility of reduced-representation genomic scans in hybrid zones.

Evolution: A Genomic Guide to Bird Population History

How species responded to the climatic oscillations during the past few million years is debated. A new study analyzing the genomes of 38 bird species finds variable patterns of population growth and declines that broadly correlate with global environmental change.

Black or red: A sex-linked colour polymorphism in a songbird is maintained by balancing selection

Colour polymorphisms play a key role in sexual selection and speciation, yet the mechanisms that generate and maintain them are not fully understood. Here, we use genomic and transcriptomic tools to identify the precise genetic architecture and evolutionary history of a sex-linked colour polymorphism in the Gouldian finch Erythrura gouldiae that is also accompanied by remarkable differences in behaviour and physiology. We find that differences in colour are associated with an ~72-kbp region of the Z chromosome in a putative regulatory region for follistatin, an antagonist of the TGF-β superfamily genes. The region is highly differentiated between morphs, unlike the rest of the genome, yet we find no evidence that an inversion is involved in maintaining the distinct haplotypes. Coalescent simulations confirm that there is elevated nucleotide diversity and an excess of intermediate frequency alleles at this locus. We conclude that this pleiotropic colour polymorphism is most probably maintained by balancing selection.Colour polymorphisms play a key role in sexual selection and speciation, yet the mechanisms that generate and maintain them are not fully understood. We therefore used genomic and transcriptomic tools to identify the precise genetic architecture and evolutionary history of a sex-linked colour polymorphism in the Gouldian finch Erythrura gouldiae that is also accompanied by remarkable differences in behaviour and physiology. We found that differences in colour are associated with an ~72-kbp region of the Z chromosome in a putative regulatory region for follistatin , an antagonist of the TGF-β superfamily genes. The region is highly differentiated between morphs, unlike the rest of the genome, yet we found no evidence that an inversion is involved in maintaining the distinct haplotypes. Coalescent simulations confirm that that there is elevated nucleotide diversity and an excess of intermediate frequency alleles at this locus. We conclude that this pleiotropic colour polymorphism is most probably maintained by balancing selection.

Similar hybrid composition among different age and sex classes in the Myrtle–Audubon's warbler hybrid zone

ABSTRACT Hybrid zones provide a key natural context within which to study the barriers between incipient species. In some avian hybrid zones, there is indirect evidence of selection against hybrid offspring, yet the source of that selection is often unclear. We examined the frequency distribution of hybrids between Myrtle Warblers (Setophaga coronata coronata) and Audubons Warblers (S. c. auduboni), using data to quantify—for the first time at a genomic scale—the composition of hybrids in this hybrid zone. We sampled birds during the breeding season and during fall migration and compared the frequencies of hybrids of different sex and age classes. Specifically, we tested for evidence of early-generation hybrids being significantly under- or over-represented in any of these classes, as would be expected if hybrids have lower or higher fitness than non-hybrids. We found that the genomic composition of birds in the hybrid zone spans the full ancestry spectrum. Across all our sampling periods, we found an excess of birds that had more Audubons ancestry, with a stronger bias toward Audubons ancestry in fall migrants than in breeding birds, consistent with asymmetric introgression. Notably, we did not find any differences in hybrid frequencies between juvenile and adult age classes or between males and females. Therefore, our results do not support large differences in viability between male and female hybrids or between different age classes of hybrids.

Population Genomics of Birds: Evolutionary History and Conservation

The use of genome-scale data to understand the evolutionary history of birds has provided important progress in the field of evolutionary biology and conservation. Here we review the conceptual advances of avian genomics, along with key examples from the literature. In each section, we contrast studies that utilized only a small number of genetic markers to studies that incorporated many independent loci across the genome. We discuss the important characteristics of avian genome architecture, and we explore the connections between DNA sequence variation and ecologically relevant phenotypes, such as color and morphology. We ask how environmental factors have left their mark on the genomes of birds and how genomic data can be used to reconstruct histories across multiple species. We outline how admixture and reticulate evolutionary histories have been an important source of variation and review cases in which hybridization has possibly led to the formation of new species. Finally, we discuss how genomic data have helped delineate population structure and inform conservation actions in declining avian species. Like in other taxonomic groups, the ever-expanding molecular toolbox for avian biologists is at once becoming more accessible in cost and more powerful in its applications. Therefore, the study of avian genomes will continue to provide important insights into many aspects of ecology, evolutionary history, and conservation biology.

A comparison of genomic islands of differentiation across three young avian species pairs

Detailed evaluations of genomic variation between sister species often reveal distinct chromosomal regions of high relative differentiation (i.e., “islands of differentiation” in FST), but there is much debate regarding the causes of this pattern. We briefly review the prominent models of genomic islands of differentiation and compare patterns of genomic differentiation in three closely related pairs of New World warblers with the goal of evaluating support for the four models. Each pair (MacGillivrays/mourning warblers; Townsends/black‐throated green warblers; and Audubons/myrtle warblers) consists of forms that were likely separated in western and eastern North American refugia during cycles of Pleistocene glaciations and have now come into contact in western Canada, where each forms a narrow hybrid zone. We show strong differences between pairs in their patterns of genomic heterogeneity in FST, suggesting differing selective forces and/or differing genomic responses to similar selective forces among the three pairs. Across most of the genome, levels of within‐group nucleotide diversity (πWithin) are almost as large as levels of between‐group nucleotide distance (πBetween) within each pair, suggesting recent common ancestry and/or gene flow. In two pairs, a pattern of the FST peaks having low πBetween suggests that selective sweeps spread between geographically differentiated groups, followed by local differentiation. This “sweep‐before‐differentiation” model is consistent with signatures of gene flow within the yellow‐rumped warbler species complex. These findings add to our growing understanding of speciation as a complex process that can involve phases of adaptive introgression among partially differentiated populations.

Prevalence and diversity of haemosporidian parasites in the yellow-rumped warbler hybrid zone

Abstract Parasites can play a role in speciation, by exerting different selection pressures on different host lineages, leading to reproductive barriers in regions of possible interbreeding. Hybrid zones therefore offer an ideal system to study the effect of parasites on speciation. Here, we study a hybrid zone in the foothills of the Rocky Mountains where two yellow‐rumped warbler subspecies, Setophaga coronata coronata and S. c. auduboni, interbreed. There is partial reproductive isolation between them, but no evidence of strong assortative mating within the hybrid zone, suggesting the existence of a postzygotic selection against hybrids. Here, we test whether haemosporidian parasites might play a role in selecting against hybrids between S. c. coronata and S. c. auduboni. We screened birds from five transects across the hybrid zone for three phylogenetic groupings of avian haemosporidians Plasmodium, Haemoproteus and Leucocytozoon parasites and quantified intensity of infection. Contrary to our prediction, hybrids did not have higher haemosporidian parasite prevalence. Variation in Haemoproteus prevalence was best explained by an interaction between a birds’ hybrid index and elevation, while the probability of infection with Leucocytozoon parasites was only influenced by elevation. We also found no significant difference in the diversity of haemosporidian lineages between the warbler subspecies and their hybrids. Finally, intensity of infection by Haemoproteus increased significantly with elevation, but was not significantly linked to birds’ hybrid index. In conclusion, our data suggest that haemosporidian parasites do not seem to play a major role in selecting against hybrids in this system.