Abstract
BackgroundFour of the five species of Telopea (Proteaceae) are distributed in a latitudinal replacement pattern on the south-eastern Australian mainland. In similar circumstances, a simple allopatric speciation model that identifies the origins of genetic isolation within temporal geographic separation is considered as the default model. However, secondary contact between differentiated lineages can result in similar distributional patterns to those arising from a process of parapatric speciation (where gene flow between lineages remains uninterrupted during differentiation). Our aim was to use the characteristic distributional patterns in Telopea to test whether it reflected the evolutionary models of allopatric or parapatric speciation. Using a combination of genetic evidence and environmental niche modelling, we focused on three main questions: do currently described geographic borders coincide with genetic and environmental boundaries; are there hybrid zones in areas of secondary contact between closely related species; did species distributions contract during the last glacial maximum resulting in distributional gaps even where overlap and hybridisation currently occur?ResultsTotal genomic DNA was extracted from 619 individuals sampled from 36 populations representing the four species. Seven nuclear microsatellites (nSSR) and six chloroplast microsatellites (cpSSR) were amplified across all populations. Genetic structure and the signature of admixture in overlap zones was described using the Bayesian clustering methods implemented in STUCTURE and NewHybrids respectively. Relationships between chlorotypes were reconstructed as a median-joining network. Environmental niche models were produced for all species using environmental parameters from both the present day and the last glacial maximum (LGM).The nSSR loci amplified a total of 154 alleles, while data for the cpSSR loci produced a network of six chlorotypes. STRUCTURE revealed an optimum number of five clusters corresponding to the four recognised species with the additional division of T. speciosissima into populations north and south of the Shoalhaven River valley. Unexpectedly, the northern disjunct population of T. oreades grouped with T. mongaensis and was identified as a hybrid swarm by the Bayesian assignment test implemented in NewHybrids. Present day and LGM environmental niche models differed dramatically, suggesting that distributions of all species had repeatedly expanded and contracted in response to Pleistocene climatic oscillations and confirming strongly marked historical distributional gaps among taxes.ConclusionsGenetic structure and bio-climatic modeling results are more consistent with a history of allopatric speciation followed by repeated episodes of secondary contact and localised hybridisation, rather than with parapatric speciation. This study on Telopea shows that the evidence for temporal exclusion of gene flow can be found even outside obvious geographical contexts, and that it is possible to make significant progress towards excluding parapatric speciation as a contributing evolutionary process.
Highlights
Four of the five species of Telopea (Proteaceae) are distributed in a latitudinal replacement pattern on the south-eastern Australian mainland
Conclusions the traditional separation of speciation processes into allopatric and parapatric categories might not capture the full complexity of spatial relationships among taxa [65], our study shows that the evidence for temporal exclusion of gene flow can be found even outside obvious geographical contexts
We show that it is possible to make significant progress towards excluding parapatric speciation as a contributing evolutionary process in a selected study system
Summary
Four of the five species of Telopea (Proteaceae) are distributed in a latitudinal replacement pattern on the south-eastern Australian mainland. A simple allopatric speciation model that identifies the origins of genetic isolation within temporal geographic separation is considered as the default model. Secondary contact between differentiated lineages can result in similar distributional patterns to those arising from a process of parapatric speciation (where gene flow between lineages remains uninterrupted during differentiation). The parapatric and sympatric speciation models involve the differentiation of lineages despite the possibility for ongoing exchange of genetic material. In these models, selective barriers must have a strong impact in order to preserve between-lineage divergence [4,5]
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