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Abstract Background Four 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? Results Total 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. Conclusions Genetic 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.

Abstract Background Inter-population distance and differences in breeding times are barriers to reproduction that can contribute to genotypic differentiation between populations. Temporal changes in environmental conditions and local selective processes can further contribute to the establishment of reproductive barriers. Telopea speciosissima (Proteaceae) is an excellent subject for studying the effect of geographic, edaphic and phenological heterogeneity on genotypic differentiation because previous studies show that these factors are correlated with morphological variation. Molecular, morphological and environmental datasets were combined to characterise the relative influence of these factors on inter-population differentiation, and Bayesian analyses were used to investigate current levels of admixture between differentiated genomes. Results A landscape genetic approach involving molecular and morphological analyses identified three endpoints of differentiated population groups: coastal, upland and southern. The southern populations, isolated from the other populations by an edaphic barrier, show low migration and no evidence of admixture with other populations. Amongst the northern populations, coastal and upland populations are connected along a skewed altitudinal gradient by genetically intermediate populations. The strong association between temperature and flowering time in Telopea speciosissima was shown to maintain a temporally unstable reproductive barrier between coastal and upland populations. Conclusions Substrate-mediated allopatry appears to be responsible for long-term genetic isolation of the southern populations. However, the temperature-dependent reproductive barrier between upland and coastal populations bears the genetic signature of temporal adjustments. The extreme climatic events of the last glacial maximum are likely to have caused more complete allochronic isolation between upland and coastal populations, as well as exerting increased selective pressure upon local genomes. However, at intermediate altitudes, current climatic conditions allow for the incorporation of alleles from previously distinct genomes, generating new, intermediate genomic assemblages and possibly increasing overall adaptive potential.