The dynamic evolutionary history of the bananaquit (Coereba flaveola) in the Caribbean revealed by a multigene analysis

Background: The bananaquit (Coereba flaveola) is a small nectivorous and frugivorous emberizine bird (order Passeriformes) that is an abundant resident throughout the Caribbean region. We used multi-gene analyses to investigate the evolutionary history of this species throughout its distribution in the West Indies and in South and Middle America. We sequenced six mitochondrial genes (3744 base pairs) and three nuclear genes (2049 base pairs) for forty-four bananaquits and three outgroup species. We infer the ancestral area of the present-day bananaquit populations, report on the species' phylogenetic, biogeographic and evolutionary history, and propose scenarios for its diversification and range expansion. Results: Phylogenetic concordance between mitochondrial and nuclear genes at the base of the bananaquit phylogeny supported a West Indian origin for continental populations. Multi-gene analysis showing genetic remnants of successive colonization events in the Lesser Antilles reinforced earlier research demonstrating that bananaquits alternate periods of invasiveness and colonization with biogeographic quiescence. Although nuclear genes provided insufficient information at the tips of the tree to further evaluate relationships of closely allied but strongly supported mitochondrial DNA clades, the discrepancy between mitochondrial and nuclear data in the population of Dominican Republic suggested that the mitochondrial genome was recently acquired by introgression from Jamaica. Conclusion: This study represents one of the most complete phylogeographic analyses of its kind and reveals three patterns that are not commonly appreciated in birds: (1) island to mainland colonization, (2) multiple expansion phases, and (3) mitochondrial genome replacement. The detail revealed by this analysis will guide evolutionary analyses of populations in archipelagos such as the West Indies, which include islands varying in size, age, and geological history. Our results suggest that multi-gene phylogenies will permit improved comparative analysis of the evolutionary histories of different lineages in the same geographical setting, which provide replicated "natural experiments" for testing evolutionary hypotheses.