Recent postglacial range expansion drives the rapid diversification of a songbird lineage in the genus Junco

Abstract

Pleistocene glacial cycles are thought to have played a major role in the diversification of temperate and boreal species of North American birds. Given that coalescence times between sister taxa typically range from 0.1 to 2.0 Myr, it has been assumed that diversification occurred as populations were isolated in refugia over long periods of time, probably spanning one to several full glacial cycles. In contrast, the rapid postglacial range expansions and recolonization of northern latitudes following glacial maxima have received less attention as potential promoters of speciation. Here we report a case of extremely rapid diversification in the songbird genus Junco as a result of a single continent-wide range expansion within the last 10 000 years. Molecular data from 264 juncos sampled throughout their range reveal that as the yellow-eyed junco (Junco phaeonotus) of Mesoamerica expanded northward following the last glacial maximum, it speciated into the dark-eyed junco (Junco hyemalis), which subsequently diversified itself into at least five markedly distinct and geographically structured morphotypes in the USA and Canada. Patterns of low genetic structure and diversity in mitochondrial DNA and amplified fragment length polymorphism loci found in dark-eyed juncos relative to Mesoamerican yellow-eyed juncos provide support for the hypothesis of an expansion from the south, followed by rapid diversification in the north. These results underscore the role of postglacial expansions in promoting diversification and speciation through a mechanism that represents an alternative to traditional modes of Pleistocene speciation.

Figure 1

Phenotypic and genetic variation in the genus Junco. (a) Breeding ranges and phenotypic variation. The eight different taxa included in the genetic analyses are shown. Colours indicate breeding ranges and dots represent sampling localities. From the south, clockwise, with sampling locality number in parentheses: volcano (1), yellow-eyed (2–11), red-backed (12, 13), grey-headed (14, 15), white-winged (16), pink-sided (17), Oregon (18, 19) and slate-coloured juncos (20–23). Site 23 corresponds to a wintering locality of the slate-coloured junco in Alabama. See §2 for specific locality designations. (b) Posterior assignment probabilities of 139 individuals in different Junco populations to K values of 2, 3 and 4 using 75 AFLP loci in the program Structure. Each colour in each pie diagram represents the per cent posterior probability of assignment to a given cluster, averaged across all individuals in that population. Posterior assignment probabilities per individual are provided in the electronic supplementary material, figure S2. Taxon abbreviations are as follows: WWJU, white-winged; PSJU, pink-sided; ORJU, Oregon; SCJU, slate-coloured; GHJU, grey-headed; RBJU, red-backed; YEJU, yellow-eyed. Numbers under taxon codes correspond to sampling localities in (a). (c) Minimum-spanning network of absolute distances between mtDNA control region haplotypes found in 264 individual juncos. Each circle represents a haplotype, with size proportional to the haplotype's overall frequency. Letters designate haplotypes and numbers correspond to the sampling localities where the haplotype was detected. Network branches represent a single nucleotide change and hatch marks along branches represent additional changes. Circular symbols to the right of the bird schematics represent yellow or dark iris colour and triangles depict beak colouration.

Figure 2

Estimates of NDIs in the yellow-eyed and dark-eyed juncos based on mtDNA CR sequence, using three mutation rates (0.15, 0.10 and 0.05 substitutions per site Myr⁻¹) and three values for the number of diversified taxa (Nt), 2 (filled diamonds), 3 (filled squares) and 5 (filled triangles).