The impact of distance and a shifting temperature gradient on genetic connectivity across a heterogeneous landscape

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.

Figure 1

Distribution of populations and genotypic groups for T. speciosissima. Distribution map of T. speciosissima (from herbarium records), with sampled population represented by a pie representing Q values for the three main groups identified by STRUCTURE at K = 3 (red: coastal group; green: upland group; blue: southern group). The map includes average maximum temperatures in degree intervals for the month of September (darkest orange: 21-22°C; yellow: 19-20°C; deepest blue: 11-12°C). Population numbers correspond to those listed in Table 1.

Figure 2

Environmental maps for T. speciosissima. a) Map including average maximum temperatures in degree intervals for the month of October. b) Map including average maximum temperatures in degree intervals for the month of November. c) Map including average annual rainfall in mm (darkest red: 600-700 mm; darkest blue: 1900-2000 mm). d) Map showing the distribution of all sandstone-derived geology types (in green) on which herbarium specimens of T. speciosissima are found.

Figure 3

PCoA of genetic and morphological data. Plots of the first two principal coordinates obtained for T. speciosissima from the principal coordinate analysis of: a) pairwise genetic distances (by population) and b) morphometric distances (by individual).

Figure 4

Proportions of admixture among selected populations. New Hybrids results showing the relative proportion of admixture among genotypes representative of coastal, intermediate and upland populations. White represents pure coastal source, black pure upland source, and grey admixed origin.