Phylogeography of the Vermilion Flycatcher species complex: Multiple speciation events, shifts in migratory behavior, and an apparent extinction of a Galapagos-endemic bird species

摘要

The Vermilion Flycatcher (Pyrocephalus rubinus) is a widespread species found in North and South America and the Galapagos. Its 12 recognized subspecies vary in degree of geographic isolation, phenotypic distinctness, and migratory status. Some authors suggest that Galapagos subspecies nanus and dubius constitute one or more separate species. Observational reports of distinct differences in song also suggest separate species status for the austral migrant subspecies rubinus. To evaluate geographical patterns of diversification and taxonomic limits within this species complex, we carried out a molecular phylogenetic analysis encompassing 10 subspecies and three outgroup taxa using mitochondrial (ND2, Cyt b) and nuclear loci (ODC introns 6 through 7, FGB intron 5). We used samples of preserved tissues from museum collections as well as toe pad samples from museum skins. Galapagos and continental clades were recovered as sister groups, with initial divergence at similar to 1 mya. Within the continental Glade, North and South American populations were sister groups. Three geographically distinct clades were recovered within South America. We detected no genetic differences between two broadly intergrading North American subspecies, mexicanus and flammeus, suggesting they should not be recognized as separate taxa. Four western South American subspecies were also indistinguishable on the basis of loci that we sampled, but occur in a region with patchy habitat, and may represent recently isolated populations. The austral migrant subspecies, rubinus, comprised a monophyletic mitochondrial Glade and had many unique nuclear DNA alleles. In combination with its distinct song, exclusive song recognition behavior, different phenology, and an isolated breeding range, our data suggests that this taxon represents a separate species from other continental populations. Mitochondrial and nuclear genetic data, morphology, and behavior suggest that Galapagos forms should be elevated to two full species corresponding to the two currently recognized subspecies, nanus and dubius. The population of dubius is presumed to be extinct, and thus would represent the first documented extinction of a Galapagos-endemic bird species. Two strongly supported mitochondrial clades divide Galapagos subspecies nanus in a geographic pattern that conflicts with previous hypotheses that were based on plumage color. Several populations of nanus have recently become extinct or are in serious decline. Urgent conservation measures should seek to preserve the deep mitochondrial DNA diversity within nanus, and further work should explore whether additional forms should be recognized within nanus. Ancestral states analysis based on our phylogeny revealed that the most recent common ancestor of extant Vermilion Flycatcher populations was migratory, and that migratory behavior was lost more often than gained within Pyrocephalus and close relatives, as has been shown to be the case within Tyrannidae as a whole. (C) 2016 Elsevier Inc. All rights reserved.