Plumage Genes and Little Else Distinguish the Genomes of Hybridizing Warblers

Abstract

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 [1Seehausen O. Conservation: losing biodiversity by reverse speciation.Curr. Biol. 2006; 16: R334-R337Abstract Full Text Full Text PDF PubMed Scopus (200) Google Scholar]. However, hybridization also facilitates admixture mapping of traits that distinguish each species and the associated genes that maintain distinctiveness despite ongoing gene flow [2Poelstra J.W. Vijay N. Bossu C.M. Lantz H. Ryll B. Müller I. Baglione V. Unneberg P. Wikelski M. Grabherr M.G. Wolf J.B. The genomic landscape underlying phenotypic integrity in the face of gene flow in crows.Science. 2014; 344: 1410-1414Crossref PubMed Scopus (340) Google Scholar]. 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 [3Vallender R. Robertson R.J. Friesen V.L. Lovette I.J. Complex hybridization dynamics between golden-winged and blue-winged warblers (Vermivora chrysoptera and Vermivora pinus) revealed by AFLP, microsatellite, intron and mtDNA markers.Mol. Ecol. 2007; 16: 2017-2029Crossref PubMed Scopus (82) Google Scholar, 4Buehler D.A. Roth A.M. Vallender R. Will T.C. Confer J.L. Canterbury R.A. Swarthout S.B. Rosenberg K.V. Bulluck L.P. Status and conservation priorities of golden-winged warbler (Vermivora chrysoptera) in North America.Auk. 2007; 124: 1439-1445Crossref Scopus (53) Google Scholar, 5Gill F.B. Blue-winged warblers (Vermivora pinus) versus golden-winged warblers (V. chrysoptera).Auk. 2004; 121: 1014-1018Crossref Google Scholar]. 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 [4Buehler D.A. Roth A.M. Vallender R. Will T.C. Confer J.L. Canterbury R.A. Swarthout S.B. Rosenberg K.V. Bulluck L.P. Status and conservation priorities of golden-winged warbler (Vermivora chrysoptera) in North America.Auk. 2007; 124: 1439-1445Crossref Scopus (53) Google Scholar]. 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.