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.

Phylogenetic analysis of beak and feather disease virus across a host ring-species complex

“…3 contains all BFDV sequences from P. e. elegans but also BFDV samples from the WS hybrids. This finding was surprising, as we might expect that BFDV in a host hybrid zone would be intermediate between P. e. elegans and P. e. flaveolus, particularly as the host mitochondrial data suggest that WS hybrids cluster with both parental species (21). However, this finding is consistent with the host microsatellite data, which show phenotypic WS hybrids clustering with P. e. elegans (21).…”

“…The P. elegans complex is a long-postulated example of a "circular overlap" or "ring species," of which only about 25 have been proposed worldwide (2,(18)(19)(20), because it features clinally diverging populations with ongoing gene flow (21,22) in an approximate horse shoe-shaped distribution, which culminate in a zone of overlap between the most divergent taxa (terminal forms). Such species complexes offer powerful and unique insights into coevolution of traits, population divergence, and speciation (e.g., refs.…”

Phylogeography: its development and impact in Australo-Papuan ornithology with special reference to paraphyly in Australian birds

“…Figure 5 shows much potential for molecular tests of hypotheses in earlier literature about diversity within and across putative refugia, barriers and hybrid zones (see Ford 1987;Schodde and Mason 1999;Schodde 2006). Nonetheless, as noted earlier, new and interesting biological questions do arise from phylogeographic data gathered to date (Driskell et al 2002;Joseph et al , 2008Kearns et al 2008;Lee and Edwards 2008). Examples are the biological dynamics within hybrid zones (Australian Ringnecks and Splendid Fairy-wrens) and how reproductive biology and ecology impacts the movement of genetic markers across and through these zones (Crimson Rosella group).…”

“…With respect to subspecies especially, we are sceptical, however, of what external morphology can convey about evolutionary history for reasons outlined long ago by Wilson and Brown (1953). Phylogeography of Australian birds clearly show that molecules and morphology are often discordant in determining where putative historical breaks should be considered to occur, at least in widespread species (Driskell et al 2002;Toon et al 2007;Joseph et al 2008;Lee and Edwards 2008). Sometimes molecular data show that the question itself is inappropriate: Johnson et al (2005) argue from molecular data that the Cape Verde Kite, sometimes considered the rarest raptor in the world, does not even exist!…”

Towards modelling persistence of woodland birds: the role of genetics

“…Genetic approaches give new insights into some longstanding questions of taxonomy and evolution. For example, the Crimson Rosella (Platycercus elegans) ring species appears to be driven by geographically differentiated selection and drift, and is not the simple ring as traditionally thought (Joseph et al 2008).…”