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. 2008 Aug 22:8:240.
doi: 10.1186/1471-2148-8-240.

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

Eva Bellemain  1 , Eldredge Bermingham, Robert E Ricklefs
Affiliations

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

Eva Bellemain et al. BMC Evol Biol. .

Abstract

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.

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Figures

Figure 1
Figure 1
Geographic representation of the sample localities of the Coereba flaveola specimens analyzed. Locality codes are the same as in additional file 1.
Figure 2
Figure 2
Coereba flaveola phylogenetic relationships based on the combined mitochondrial dataset (ATPase 8/6, cyt b, BCO1, ND2 and ND6 genes) inferred from a Bayesian analysis and rooted using three outgroup species (Tiaris olivacea, Loxigilla portoricensis and Melanospiza richardsoni). Values above the major branches represent the number of substitutions per site, estimated as the mean value of the branch in all samples of the Markov chain where the branch appears. Values below each major branch represent posterior probability values. Sample names are composed of a locality code (same as in additional file 1) and a sample number.
Figure 3
Figure 3
Coereba flaveola phylogenetic relationships based on the combined nuclear Bfib5, Rag1 and CHDZ genes, inferred from a Bayesian analysis and rooted using three outgroup species (Tiaris olivacea, Loxigilla portoricensis and Melanospiza richardosoni). Letters following each sample name (a or b) represent the two haplotypes for each sample.
Figure 4
Figure 4
Haplotype networks for the three nuclear genes (Bfib5, Rag1 and CHDZ) and the combined genes for Coereba flaveola. Branch lengths are proportional to the number of mutations and the size of each node is proportional to haplotype frequency. Each of the clades defined from the mitochondrial or nuclear consensus trees (Figures 2 and 3) is given a specific color.
Figure 5
Figure 5
Phylogeny of Coereba flaveola surimposed on the geography of the Caribbean region. The geographic patterns of the different mitochondrial and nuclear lineages allow resolving the complex phylogenetic history of the species.
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References

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    1. Lack D. Island Biology Illustrated by the Land Birds of Jamaica. Berkeley, CA: University of California Press; 1976.

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