Extensive Rangewide Mitochondrial Introgression Indicates Substantial Cryptic Hybridization in the Golden-winged Warbler (Vermivora chrysoptera)

Abstract

Widespread population declines of the Golden-winged Warbler (Vermivora chrysoptera) are thought to be due in part to hybridization with the expanding Blue-winged Warbler (V. pinus), which predictably replaces Golden-winged Warblers at breeding sites in which the two species come into contact. However, the mechanism by which this replacement occurs remains unresolved. Recent genetic work has indicated that, even in areas where the two species have been in contact for a short period, introgression of Blue-winged mitochondrial (mtDNA) and nuclear genes into Golden-winged individuals is common. To explore this process on a broader scale, we screened more than 750 individuals from nine U.S. states and three provinces to examine geographic patterns of mtDNA introgression. The only population in which all phenotypic Golden-winged Warblers had Golden-winged mtDNA haplotypes, and in which there are no breeding Blue-winged or hybrid individuals, was in the province of Manitoba, near the northwestern edge of the species' breeding distribution. The near ubiquity of mitochondrial introgression suggests that there are far fewer genetically pure populations of Goldenwinged Warblers than previously believed, a finding with important implications for this threatened species. RÉSUMÉ. On pense que le déclin à grande échelle des populations de Paruline à ailes dorées (Vermivora chrysoptera) est en partie attribuable à son hybridation avec la Paruline à ailes bleues (V. pinus), laquelle est en expansion et remplace, comme on peut s'y attendre, la Paruline à ailes dorées aux sites de nidification où les deux espèces entrent en contact. Toutefois, le processus par lequel survient ce remplacement demeure inconnu. Des études génétiques récentes ont montré que, même aux endroits où les deux espèces n'ont été en contact que sur une courte période, l'introgression des gènes mitochondriaux (ADNmt) et nucléaires de la Paruline à ailes bleues chez les individus de Paruline à ailes dorées est commune. Pour explorer ce processus à plus grande échelle, nous avons procédé au criblage de plus de 750 individus provenant de neufs États des États-Unis et de trois provinces afin d'examiner les variations géographiques de l'introgression mitochondriale. La seule population dans laquelle toutes les Parulines à ailes dorées phénotypiques présentaient des haplotypes d'ADNmt de Paruline à ailes dorées, et dans laquelle il n'y avait pas d'individus nicheurs de Paruline à ailes bleues ni d'hybrides, se trouvait au Manitoba, près de la limite nord-ouest de l'aire de reproduction de l'espèce. La quasiomniprésence de l'introgression mitochondriale permet de croire qu'il y a beaucoup moins de populations génétiquement pures de Paruline à ailes dorées que ce qu'on pensait, une découverte significative pour cette espèce menacée.

Stand and within-stand factors influencing Golden-winged Warbler use of regenerating stands in the central Appalachian Mountains

“…This is likely because of the fact that we focused our surveys in areas that had a combination of extensive forest cover (mean = 84.2% within 1 km) at higher elevation (mean = 570 m, range = 275-946 m). However, we must caution that cryptic hybridization is likely to occur in the Golden-winged Warbler population we studied (Vallender et al 2009). …”

“…Thus, once the point count was complete, each observer used playback of a Golden-winged Warbler song until achieving positive visual confirmation of each individual by plumage characteristics, e.g., black throat, and behavior, e.g., singing. However, it should be noted that even with the confirmation of a phenotypic Golden-winged Warbler, there likely exists cryptic hybridization in the Golden-winged Warbler population we studied (Vallender et al 2009). …”

“…Golden-winged Warbler populations in the Appalachian Mountains have exhibited considerable range contraction (Confer et al 2011) and precipitous annual population declines of 8.5% per year since the initiation of Breeding Bird Surveys in 1966 (Sauer et al 2014). Although loss of breeding habitat is thought to be a key limiting factor for this imperiled species, competition and hybridization with a close relative, the Blue-winged Warbler (Vermivora cyanoptera), which may overlap in breeding habitat, is also a threat (Buehler et al 2007, Vallender et al 2009, Confer et al 2011). As such, the development of management prescriptions that create or maintain Golden-winged Warbler breeding habitat in areas devoid of Blue-winged Warblers is a conservation priority (Buehler et al 2007, Patton et al 2010).…”

Fire created habitat partitioning and isolation between hybridizing warblers

“…Fowlds (2010) studied GWWAs and BWWAs in a variety of habitat types in central Wisconsin and noted densities of 0.12 (1.3) (SE) to 0.31 (1.2) and 0.06 (1.3) to 0.09 (1.3) per ha for GWWAs and BWWAs respectively. Mitochondrial DNA analysis indi- v www.esajournals.org cates bi-directional introgression in our study area and among the highest introgression rates ever reported for both species (Vallender et al 2009; approximately 15% for GWWAs and 25% for BWWAs).…”

“…Vallender et al (2007) reported a high rate of GWWA intraspecies extra pair matings and suggested this might also be common with the BWWA. Hybridization between the two species has received extensive phenotypic (Parkes 1951, Gill 1980, 1987, mitochondrial DNA (mtDNA) (Gill 1997, Shapiro et al 2004, Dabrowski et al 2005, and nuclear DNA ) study indicating genetic introgression is bi-directional (Shapiro et al 2004, Dabrowski et al 2005) and extensive (Vallender et al 2009). Based on the mtDNA studies, the species' genomes overlap by 95.1-97.0% (Gill 1997, Shapiro et al 2004, Dabrowski et al 2005 and split from an ancestral species approximately 1.5 million years before present (Gill 2004).…”