Where and when does a ring start and end? Testing the ring-species hypothesis in a species complex of Australian parrots

Abstract

Speciation, despite ongoing gene flow can be studied directly in nature in ring species that comprise two reproductively isolated populations connected by a chain or ring of intergrading populations. We applied three tiers of spatio-temporal analysis (phylogeny/historical biogeography, phylogeography and landscape/population genetics) to the data from mitochondrial and nuclear genomes of eastern Australian parrots of the Crimson Rosella Platycercus elegans complex to understand the history and present genetic structure of the ring they have long been considered to form. A ring speciation hypothesis does not explain the patterns we have observed in our data (e.g. multiple genetic discontinuities, discordance in genotypic and phenotypic assignments where terminal differentiates meet). However, we cannot reject that a continuous circular distribution has been involved in the group's history or indeed that one was formed through secondary contact at the 'ring's' east and west; however, we reject a simple ring-species hypothesis as traditionally applied, with secondary contact only at its east. We discuss alternative models involving historical allopatry of populations. We suggest that population expansion shown by population genetics parameters in one of these isolates was accompanied by geographical range expansion, secondary contact and hybridization on the eastern and western sides of the ring. Pleistocene landscape and sea-level and habitat changes then established the birds' current distributions and range disjunctions. Populations now show idiosyncratic patterns of selection and drift. We suggest that selection and drift now drive evolution in different populations within what has been considered the ring.

Figure 1

(a) Distribution and plumage phenotype variation in parrots of the Crimson Rosella complex in eastern Australia (from Forshaw & Cooper (2002) in this and subsequent figures). Note the narrow zone of unsuitable habitat currently separating Adelaide and Yellow (see the electronic supplementary material). (b,c) Sampling scheme of vouchered museum specimens for mtDNA analyses of the full mainland distribution of the complex.

Figure 2

Unrooted network of mtDNA diversity in southeastern Australian populations of the Crimson Rosella complex, showing groups (a) 1, (b) 2 and (c) 3 as referred to in the text. Open circles indicate unsampled haplotypes. Colours in circles indicate the plumage phenotype of samples as in figure 1. The sample size for each haplotype is 1, unless otherwise indicated with a number. KI refers to haplotypes found in eight Kangaroo Island Crimson individuals. A solid line with open circles shows where the North Queensland populations join the network. A unimodal mismatch plot for (c) is shown in (d). (d) Dotted line, observation; solid line, expected.

Figure 3

(a) Summary of microsatellite analyses of southeastern Australian populations of the Crimson Rosella complex. Coloured squares are microsatellite-based Geneland classifications of individuals as described in the text (Eastern^GL, Central^GL and Western^GL). Bicoloured symbols show the three individuals that were classified as ‘hybrid’ assignments of 0.61 Eastern^GL/0.38 Central^GL, 0.05 Eastern^GL/0.95 Central^GL and 0.16 Eastern^GL/0.84 Western^GL. (b) The map details sampling for microsatellites in the upper and middle reaches of the Murray River system and shows discordance between microsatellite-based assignments (squares) and plumage phenotypes (circles).