Selection and geographic isolation influence hummingbird speciation: genetic, acoustic and morphological divergence in the wedge-tailed sabrewing (Campylopterus curvipennis)

Abstract

BackgroundMesoamerica is one of the most threatened biodiversity hotspots in the world, yet we are far from understanding the geologic history and the processes driving population divergence and speciation for most endemic taxa. In species with highly differentiated populations selective and/or neutral factors can induce rapid changes to traits involved in mate choice, promoting reproductive isolation between allopatric populations that can eventually lead to speciation. We present the results of genetic differentiation, and explore drift and selection effects in promoting acoustic and morphological divergence among populations of Campylopterus curvipennis, a lekking hummingbird with an extraordinary vocal variability across Mesoamerica.ResultsAnalyses of two mitochondrial genes and ten microsatellite loci genotyped for 160 individuals revealed the presence of three lineages with no contemporary gene flow: C. c. curvipennis, C. c. excellens, and C. c. pampa disjunctly distributed in the Sierra Madre Oriental, the Tuxtlas region and the Yucatan Peninsula, respectively. Sequence mtDNA and microsatellite data were congruent with two diversification events: an old vicariance event at the Isthmus of Tehuantepec (c. 1.4 Ma), and a more recent Pleistocene split, isolating populations in the Tuxtlas region. Hummingbirds of the excellens group were larger, and those of the pampa group had shorter bills, and lineages that have been isolated the longest shared fewer syllables and differed in spectral and temporal traits of a shared syllable. Coalescent simulations showed that fixation of song types has occurred faster than expected under neutrality but the null hypothesis that morphological divergence resulted from drift was not rejected.ConclusionsOur phylogeographic analyses uncovered the presence of three Mesoamerican wedge-tailed sabrewing lineages, which diverged at different time scales. These results highlight the importance of the Isthmus of Tehuantepec and more recent Pleistocene climatic events in driving isolation and population divergence. Coalescent analyses of the evolution of phenotypic traits suggest that selection is driving song evolution in wedge-tailed sabrewings but drift could not be rejected as a possibility for morphological divergence.

Comparative Phylogeographic Analyses Illustrate the Complex Evolutionary History of Threatened Cloud Forests of Northern Mesoamerica

“…A broad-reaching vicariant event during the Pliocene has been suggested as being responsible for the divergence of numerous lineages across the isthmus [15], [18], [19], [45], [51]. Two discrete diversification events across the Isthmus of Tehuantepec were detected for populations of eight bird species occurring in pine-oak forests on either side of the Isthmus and currently isolated from one another by the intervening valley [18].…”

“…DNA data sets were obtained as part of ongoing projects investigating the evolutionary history of cloud forests in eastern Mexico. For the bird species, sequence data from the mitochondrial NADH dehydrogenase subunit 2 gene (ND2) and subunit 5 gene (ND5), cytochrome b (CYTB), control region (CR), and ATPase 6 and 8 (ATP6, ATP8) were obtained from DNA extracted from tail feathers or tissue samples using standard molecular laboratory protocols, which are fully described elsewhere [17], [19], [20]. For the plant taxa, sequence data from the nuclear ribosomal DNA (nrDNA) internal transcribed spacer (ITS) and plastid rpl 32- trn L, psb A- trn H, trn S- trn G, and trn L- trn F intergeneric spacers were obtained from silica-dried leaf material also using standard protocols (e.g., [14], [15]).…”

“…The DNA sequences from published sources were obtained from GenBank with the accession numbers also specified in Table S1. Methods for DNA preparation, PCR amplification, and sequence generation are given elsewhere [14], [15], [17], [19], [20], [23]–[27].…”

“…The 15 taxa were also chosen because they are thought to be cloud forest endemics whose distributions span northern Mesoamerica and closely follow the highly fragmented forest; all of the birds are considered to be cloud forest residents. Some of the targeted species ecologically interact with one another; P. padifolia and M. deppeana are mainly pollinated by the hummingbird species ( C. curvipennis , A. cyanocephala , and L. amethystinus , respectively) and seeds of R. baccifera are dispersed by C. ophthalmicus [15], [19], [20]. Our a priori expectation was that such ecologically linked species might share a common biogeographic history.…”

Geographic Variation in the Acoustic Traits of Greater Horseshoe Bats: Testing the Importance of Drift and Ecological Selection in Evolutionary Processes

“…The pattern of geographic variation in phenotypic characters can provide insights into the historical roles of drift and selection [2], [3], [4] including potential microevolutionary processes that drive population diversification and speciation [5], [6]. Acoustic signals in communication systems are one of the few diverse phenotypes that present opportunities for this kind of research.…”