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Geographic Variability in Mitochondrial Introgression Among Hybridizing Populations of Golden-Winged (Vermivora Chrysoptera) and Blue-Winged (V

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Geographic Variability in Mitochondrial Introgression Among Hybridizing Populations of Golden-Winged (Vermivora Chrysoptera) and Blue-Winged (V Conservation Genetics (2005) 6:843–853 Ó Springer 2005 DOI 10.1007/s10592-005-9028-2 Geographic variability in mitochondrial introgression among hybridizing populations of Golden-winged (Vermivora chrysoptera) and Blue-winged (V. pinus) Warblers A. Dabrowski1, R. Fraser1,2, J. L. Confer3 & I. J. Lovette1,* 1Evolutionary Biology Program, Laboratory of Ornithology, Cornell University, 159 Sapsucker Woods Road, Ithaca, NY, 14850, USA; 2Department of Biology, Queen’s University, 116 Barrie St., Kingston Ontario, K7L 3N6, Canada; 3Biology Department, Ithaca College, Ithaca, NY, 14850, USA (*Corresponding author: Phone: +607-254-2140; E-mail: [email protected]) Received 9 September 2004; accepted 22 December 2005 Key words: conservation, hybridization, introgression, mitochondrial DNA, Vermivora chrysoptera, Vermivora pinus Abstract The rapidly declining Golden-winged Warbler (Vermivora chrysoptera) is of conservation concern owing in part to hybridization with the closely related Blue-winged Warbler (V. pinus). These species hybridize extensively in eastern North America and over the past century the Blue-winged Warbler has displaced the Golden-winged Warbler from substantial regions of its historic breeding range. A previous study suggested that these genetic interactions result in rapid and asymmetric introgression of Blue-winged Warbler mitochondrial DNA (mtDNA) into Golden-winged phenotype populations within the zones of contact, but more recent and extensive surveys have documented a more complex pattern of genetic interchange between these taxa. We surveyed mtDNA/phenotype associations in 104 individuals of known phenotype drawn from two locations with different histories of contact and found substantial variation between sites in the extent of introgression. Where both species have co-existed for more than a century, we found evidence of bi-directional introgression and the long-term persistence of Golden-winged mtDNA haplotypes. At the leading edge of the northward expansion of Blue-winged Warblers, we found predominantly Golden-winged Warbler mtDNA haplotypes in both Golden-winged and hybrid-pheno- type individuals. Across both sites, genetic swamping does not appear to be occurring via the early immigration of Blue-winged Warbler females into populations dominated by Golden-winged Warbler phenotypes. Instead, the differing patterns of mitochondrial introgression may be driven by the relative local population sizes of the parental species coupled with subtle between-species differences in mate choice and habitat preferences. Introduction prevalent as species’ distributions are modified by anthropogenic changes that bring formerly allo- Natural hybridization can result in conservation patric taxa into contact (Rhymer and Simberloff problems when a declining species is genetically 1996). Hybridization can also pose legal dilemmas swamped by introgression from closely related taxa. related to the definition of species or other taxo- Such genetic mixing has resulted in the extinction of nomic units of conservation (Allendorf et al. 2001; some species and is likely to become increasingly Avise 2004). Understanding the frequency and 844 pattern of hybrid introgression is therefore impor- stage population, the RFLP haplotype diagnostic tant for the effective conservation of taxa threatened of Blue-winged mtDNA was almost fixed (40 of 41 by interspecific genetic interactions. individuals) regardless of phenotype: all six of The Golden-winged Warbler (Vermivora chry- the Golden-winged phenotype individuals had soptera) has declined throughout much of its Blue-winged mtDNA, as did six of the seven breeding range in northeastern North America, Brewster’s hybrid individuals and all 28 Blue- and the species is currently being considered for winged phenotype individuals. Blue-winged phe- listing within the USA Endangered Species Act. notype individuals were rare at the early stage site, Causes of this decline include the reduction of but nonetheless the frequency of Blue-winged shrub habitat as abandoned farmlands enter later mtDNA in Golden-winged phenotype individuals stages of succession (Confer and Pascoe 2003) as increased from 27% to 70% over the 1988–1992 well as behavioral (Confer et al. 2003) and genetic sampling interval. In the pooled sample from both (Gill 1997) interactions with the closely related years at this site, nearly half (10 of 21) of the Blue-winged Warbler (V. pinus) (Gill 2004). The Golden-winged phenotype individuals had Blue- geographic range displacement of the Golden- winged mtDNA, as did the single Brewster’s winged Warbler has been paralleled by range hybrid individual; no Blue-winged phenotype expansions by the Blue-winged Warbler, and the individuals were sampled. These patterns sug- two species hybridize frequently within their gested that introgression of Blue-winged Warbler shifting zone of breeding overlap (e.g. Short 1963), mtDNA into Golden-winged Warbler populations with some sympatric populations exhibiting 7– proceeds rapidly and that there is little reciprocal 15% hybrid phenotypes in surveys of singing introgression of Golden-winged mtDNA into males (Confer 1992). Blue-winged lineages. As mtDNA is inherited Two hybrid phenotypes are particularly com- matrilineally, Gill (1997) suggested that pioneering mon and were named by early workers who ini- female Blue-winged Warblers lead the advance tially described them as new species (reviewed in into Golden-winged dominated populations. This Parkes 1951). The F1 phenotype is termed is plausible as female dispersal into new regions is ‘‘Brewster’s Warbler’’ and generally resembles the common in avian species (Greenwood and Harvey Golden-winged Warbler in plumage, but is lacking 1980), although the more inconspicuous behavior that species’ black eye and throat patch, and of females may cause them to be overlooked (Gill exhibits the black eye-stripe of the Blue-winged 1997), leading researchers to attribute initial arri- Warbler. The far less common ‘‘Lawrence’s War- val to conspicuous, singing males. bler’’ phenotype has a combination of the Golden- A more comprehensive recent survey (Shapiro winged face pattern with the yellow plumage et al. 2004) examined phenotype-haplotype asso- characteristic of the Blue-winged Warbler and ciations in a greatly expanded sample of individual probably results from a backcross (Parkes 1951). warblers from additional study populations. In Two previous studies have used mitochondrial contrast to the rapid and unidirectional intro- markers to explore the pattern of female-mediated gression seen at Gill’s sites, Shapiro et al. (2004) introgression between Blue- and Golden-winged found bi-directional introgression at all locations warblers. The first was conducted by Gill (1997), where both species were well represented, with no who documented the rapid and asymmetric tendency for disproportionate introgression as introgression of mitochondrial DNA (mtDNA) indicated by Blue-winged haplotypes in Golden- from Blue-winged Warblers into phenotypic winged phenotype individuals. Birds with the Golden-winged Warblers. Gill surveyed mtDNA/ ‘‘Brewster’s’’ and ‘‘Lawrence’s’’ hybrid pheno- phenotype associations in two contexts: a late- types similarly had pinus and chrysoptera haplo- stage, lowland site (in the Delaware River valley of types in approximate equal proportions. In areas northeastern Pennsylvania and nearby northwest- where only one pure species-level phenotype was ern Pennsylvania) where the two species had been present, all individuals sampled had the corre- hybridizing for a minimum of several decades, and sponding mtDNA haplotype. These results led an early-stage site (in northeastern Pennsylvania) Shapiro et al. (2004) to conclude that the hybrid- where observations suggested that the two species ization dynamics of these taxa are more complex had more recently come into contact. In the late- than indicated by Gill’s earlier study. 845 Here, we expand on these previous surveys of The recent contact site was located at the mitochondrial/phenotype associations to include Queen’s University Biological Station (QUBS) in additional sites with contrasting histories of con- southeastern Ontario, Canada (44°34¢N, 76°19¢W). tact between Blue- and Golden-winged Warblers, The habitat consists of abandoned farmland, including an unusual site where both species swamps, tracts of second growth forest, and rocky have been present for more than a century and a outcrops associated with the Canadian Shield. In site sampled during the first appearance of Blue- this region the arrival and prevalence of the winged phenotype individuals in a large popula- Golden-winged Warbler has been well docu- tion of Golden-winged phenotypes. Our results are mented. The first Golden-winged Warbler reported broadly congruent with those of Shapiro et al. in the Kingston area (approximately 50 km south (2004) in suggesting that there are substantial of QUBS) was a single male in 1954 (Quilliam differences in patterns of introgression across sites 1973). From 1960 onwards the species was reported and that the initial contact between these species every spring, and nesting behavior was confirmed is not invariably followed by rapid mtDNA in 1961 (Quilliam 1973; Weir 1989). This popula- swamping of Golden-winged Warblers. tion consisted solely of Golden-winged phenotype individuals until the mid-1990’s, when the first hybrid individuals were recorded at the study site. Methods The number of hybrid-phenotype adults has increased with successive breeding seasons
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