Scott A. Taylor

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.

Population genetic structure in Atlantic and Pacific Ocean common murres (Uria aalge): Natural replicate tests of post-Pleistocene evolution

Understanding the factors that influence population differentiation in temperate taxa can be difficult because the signatures of both historic and contemporary demographics are often reflected in population genetic patterns. Fortunately, analyses based on coalescent theory can help untangle the relative influence of these historic and contemporary factors. Common murres (Uria aalge) are vagile seabirds that breed in the boreal and low arctic waters of the Northern Hemisphere. Previous analyses revealed that Atlantic and Pacific populations are genetically distinct; however, less is known about population genetic structure within ocean basins. We employed the mitochondrial control region, four microsatellite loci and four intron loci to investigate population genetic structure throughout the range of common murres. As in previous studies, we found that Atlantic and Pacific populations diverged during the Pleistocene and do not currently exchange migrants. Therefore, Atlantic and Pacific murre populations can be used as natural replicates to test mechanisms of population differentiation. While we found little population genetic structure within the Pacific, we detected significant east–west structuring among Atlantic colonies. The degree that population genetic structure reflected contemporary population demographics also differed between ocean basins. Specifically, while the low levels of population differentiation in the Pacific are at least partially due to high levels of contemporary gene flow, the east–west structuring of populations within the Atlantic appears to be the result of historic fragmentation of populations rather than restricted contemporary gene flow. The contrasting results in the Atlantic and Pacific Oceans highlight the necessity of carefully considering multilocus nonequilibrium population genetic approaches when reconstructing the demographic history of temperate Northern Hemisphere taxa.

Differentially expressed genes match bill morphology and plumage despite largely undifferentiated genomes in a Holarctic songbird

Understanding the patterns and processes that contribute to phenotypic diversity and speciation is a central goal of evolutionary biology. Recently, high‐throughput sequencing has provided unprecedented phylogenetic resolution in many lineages that have experienced rapid diversification. The Holarctic redpoll finches (Genus: Acanthis) provide an intriguing example of a recent, phenotypically diverse lineage; traditional sequencing and genotyping methods have failed to detect any genetic differences between currently recognized species, despite marked variation in plumage and morphology within the genus. We examined variation among 20 712 anonymous single nucleotide polymorphisms (SNPs) distributed throughout the redpoll genome in combination with 215 825 SNPs within the redpoll transcriptome, gene expression data and ecological niche modelling to evaluate genetic and ecological differentiation among currently recognized species. Expanding upon previous findings, we present evidence of (i) largely undifferentiated genomes among currently recognized species; (ii) substantial niche overlap across the North American Acanthis range; and (iii) a strong relationship between polygenic patterns of gene expression and continuous phenotypic variation within a sample of redpolls from North America. The patterns we report may be caused by high levels of ongoing gene flow between polymorphic populations, incomplete lineage sorting accompanying very recent or ongoing divergence, variation in cis‐regulatory elements, or phenotypic plasticity, but do not support a scenario of prolonged isolation and subsequent secondary contact. Together, these findings highlight ongoing theoretical and computational challenges presented by recent, rapid bouts of phenotypic diversification and provide new insight into the evolutionary dynamics of an intriguing, understudied non‐model system.

Spatiotemporally consistent genomic signatures of reproductive isolation in a moving hybrid zone

Studies of hybrid zone dynamics often investigate a single sampling period and draw conclusions from that temporal snapshot. Stochasticity can, however, result in loci with spurious outlier patterns, which is exacerbated by limited temporal or geographic sampling. Comparing admixed populations from different geographic regions is one way to detect repeatedly divergent genomic regions potentially involved in reproductive isolation. Temporal comparisons also allow us to control partially for the role of stochasticity, but the power of temporal sampling has not yet been adequately explored. In North America, black‐capped (Poecile atricapillus) and Carolina (P. carolinensis) chickadees hybridize in a contact zone extending from New Jersey to Kansas. The hybrid zone is likely maintained by strong intrinsic selection against hybrids, and it is moving north. We used a reduced representation genomic approach and temporally spaced sampling—two samples of ∼80 individuals separated by a decade—to determine the pattern and consistency of selection and genomic introgression in the chickadee hybrid zone. We report consistently low introgression for highly divergent loci between P. atricapillus and P. carolinensis in this moving hybrid zone. This is strong evidence that these loci may be linked to genomic regions involved in reproductive isolation between chickadees.

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.

A comparative assessment of SNP and microsatellite markers for assigning parentage in a socially monogamous bird

Single‐nucleotide polymorphisms (SNPs) are preferred over microsatellite markers in many evolutionary studies, but have only recently been applied to studies of parentage. Evaluations of SNPs and microsatellites for assigning parentage have mostly focused on special cases that require a relatively large number of heterozygous loci, such as species with low genetic diversity or with complex social structures. We developed 120 SNP markers from a transcriptome assembled using RNA‐sequencing of a songbird with the most common avian mating system—social monogamy. We compared the effectiveness of 97 novel SNPs and six previously described microsatellites for assigning paternity in the black‐throated blue warbler, Setophaga caerulescens. We show that the full panel of 97 SNPs (mean Ho = 0.19) was as powerful for assigning paternity as the panel of multiallelic microsatellites (mean Ho = 0.86). Paternity assignments using the two marker types were in agreement for 92% of the offspring. Filtering individual samples by a 50% call rate and SNPs by a 75% call rate maximized the number of offspring assigned with 95% confidence using SNPs. We also found that the 40 most heterozygous SNPs (mean Ho = 0.37) had similar power to assign paternity as the full panel of 97 SNPs. These findings demonstrate that a relatively small number of variable SNPs can be effective for parentage analyses in a socially monogamous species. We suggest that the development of SNP markers is advantageous for studies that require high‐throughput genotyping or that plan to address a range of ecological and evolutionary questions.

Male/Female Classification of the Peruvian Booby

Abstract We studied adult Peruvian Boobies (Sula variegata) on two islands in northern Peru to classify males and females using DNA-based techniques. We used this information to (1) assess the extent of size dimorphism in this species, (2) identify males and females using discriminant functions of external characters, and (3) validate use of voice as a reliable method for identifying male and female Peruvian Boobies in the field. Female Peruvian Boobies were 19% heavier and their culmens and wings were 3 and 4% larger than males, respectively. A discriminant function that included body weight and wing chord correctly classified 90% of the birds. Alternatively, 88% of correct identification of males and females was obtained with a function that incorporated only wing chord. Whistles were performed exclusively by males (25/25 of cases), whereas grunts or goose-like honk vocalizations were performed only by females (24/24 of cases). The female-larger size dimorphism of Peruvian Boobies is intermediate in comparison to other Sula boobies. Calls and biometry provide a fast, reliable, and inexpensive method for classifying most adult Peruvian Boobies as males or females in the field. We recommend a hierarchical system for classification of male and female Peruvian Boobies: (1) use of vocalizations, (2) use of body weight and wing chord when the bird did not vocalize and was weighed immediately after daybreak or before the first feeding trip of the day, and (3) use of wing chord only when there is uncertainty in temporal variations of body weight.

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.

Cryptic introgression between murre sister species (Uria spp.) in the Pacific low Arctic: frequency, cause, and implications

As southern species undergo northward range expansions, reports of hybridization between temperate and arctic taxa are increasing, which may have important implications for the evolution, conservation, and management of arctic species. The extent of hybridization between temperate common murres (Uria aalge) and arctic thick-billed murres (U. lomvia), seabirds in the family Alcidae, has been the subject of debate. In a previous survey of variation in mitochondrial DNA (mtDNA) in common and thick-billed murres sampled from throughout the North Pacific and low Arctic, 12 of 327 common murres (~4%) were found to possess DNA sequences characteristic of thick-billed murres. In the present study, we surveyed variation in three nuclear introns in 230 common murres and 56 thick-billed murres and report that these putative hybrids carry various combinations of intron alleles from common and thick-billed murres. Analysis using the program STRUCTURE indicated that nine of these individuals possessed high proportions of thick-billed murre intron alleles, two possessed alleles in F1 and F2 proportions, and one individual possessed predominantly common murre intron alleles. We propose that the asymmetric mtDNA introgression we observed is most likely the result of mate choice at mixed colonies based on differences in male mating behaviours. Our results highlight that hybridization between thick-billed and common murres is more prevalent than previously thought, which may have important implications for the conservation and management of arctic-dwelling thick-billed murres as common murres expand northward.

Isolation and characterization of ten microsatellite loci in Blue-footed (Sula nebouxii) and Peruvian Boobies (Sula variegata)

Ten microsatellite loci were isolated and characterized from Blue-footed (Sula nebouxii) and Peruvian Boobies (S. variegata). The loci were screened in 24 Blue-footed Boobies and 27 Peruvian Boobies: 8 were polymorphic in Blue-footed Boobies with between 2 and 10 alleles per locus and 9 were polymorphic in Peruvian Boobies with between 2 and 12 alleles per locus. Observed heterozygosity ranged from 0.29 to 0.84. These loci were also tested in Brown Boobies (S. leucogaster) and were variably polymorphic. These new loci are currently being used to assess population genetic structure in Blue-footed and Peruvian Boobies and will also be used to examine hybridization between the species.