The nuanced nature of mesic refugia in arid landscapes: a tale of two peas.

BACKGROUND AND AIMS: Understanding how genetic diversity is distributed and maintained within species is a central tenet of evolutionary and conservation biology, yet is understudied in arid regions of the globe. In temperate, glaciated environments, high genetic diversity in plant species is frequently found in refugial areas, which are often associated with southern non-glaciated landscapes. In arid, unglaciated environments, landscape features providing mesic conditions are likely to be refugia, although our understanding needs more refinement in these biomes. We test whether refugia and nuclear diversity hotspots occur in high-elevation, topographically complex areas for co-distributed shrubs (Petalostylis labicheoides and Indigofera monophylla; Fabaceae) in the ancient, arid Pilbara bioregion of north-western Australia. METHODS: We conducted extensive sampling of the Pilbara (>1400 individuals from 62 widespread populations) to detect patterns in nuclear diversity and structure based on 13-16 microsatellite loci. Evidence of historical refugia was investigated based on patterns of diversity in three non-coding chloroplast (cp) sequence regions for approx. 240 individuals per species. Haplotype relationships were defined with median-joining networks and maximum likelihood phylogenetic trees. KEY RESULTS: We found cpDNA evidence for a high-elevation refugium in P. labicheoides but not for I. monophylla that instead exhibited extraordinary haplotype diversity and evidence for persistence across a widespread area. Nuclear diversity hotspots occurred in, but were not exclusive to, high-elevation locations and extended to adjacent, low-elevation riparian areas in both species. CONCLUSIONS: Phylogeographic refugia in arid environments may occur in high-elevation areas for some species but not all, and may be influenced by species-specific traits: a mesic montane refugium in P. labicheoides could be related to its preference for growth in water-gaining areas, while a lack of such evidence in I. monophylla could be related to maintenance of cpDNA diversity in a large soil seed bank and dynamic evolutionary history. Mesic environments created by the intersection of topographically complex landscapes with riparian zones can be contemporary reservoirs of genetic diversity in arid landscapes.

Limited phylogeographic and genetic connectivity in Acacia species of low stature in an arid landscape.

Widespread plant species are expected to maintain genetic diversity and gene flow via pollen and seed dispersal. Stature is a key life history trait that affects seed and potentially pollen dispersal, with limited stature associated with limited dispersal and greater genetic differentiation. We sampled Hill's tabletop wattle (Acacia hilliana) and curry wattle (Acacia spondylophylla), two co-distributed, widespread, Acacia shrubs of low stature, across the arid Pilbara region of north-western Australia. Using chloroplast sequence and nuclear microsatellite data we evaluated patterns of population genetic and phylogeographic diversity and structure, demographic signals, ratios of pollen to seed dispersal, evidence for historical refugia, and association between elevation and diversity. Results showed strong phylogeographic (chloroplast, G ST = 0.831 and 0.898 for A. hilliana and A. spondylophylla, respectively) and contemporary (nuclear, F ST = 0.260 and 0.349 for A. hilliana and A. spondylophylla, respectively) genetic structure in both species. This indicates limited genetic connectivity via seed and pollen dispersal associated with Acacia species of small stature compared to taller tree and shrub acacias across the Pilbara bioregion. This effect of stature on genetic structure is superimposed on moderate levels of genetic diversity that were expected based on widespread ranges (haplotype diversity h = 25 and 12; nuclear diversity He = 0.60 and 0.47 for A. hilliana and A. spondylophylla, respectively). Contemporary genetic structure was congruent at the greater landscape scale, especially in terms of strong genetic differentiation among geographically disjunct populations in less elevated areas. Measures of diversity and connectivity were associated with traits of greater geographic population proximity, population density, population size, and greater individual longevity, and some evidence for range expansion in A. hilliana. Results illustrate that low stature is associated with limited dispersal and greater patterns of genetic differentiation for congenerics in a common landscape and highlight the complex influence of taxon-specific life history and ecological traits to seed and pollen dispersal.

Extensive Genetic Connectivity and Historical Persistence Are Features of Two Widespread Tree Species in the Ancient Pilbara Region of Western Australia.

Phylogeographic studies can be used as a tool to understand the evolutionary history of a landscape, including the major drivers of species distributions and diversity. Extensive research has been conducted on phylogeographic patterns of species found in northern hemisphere landscapes that were affected by glaciations, yet the body of literature for older, unaffected landscapes is still underrepresented. The Pilbara region of north-western Australia is an ancient and vast landscape that is topographically complex, consisting of plateaus, gorges, valleys, and ranges, and experiences extreme meteorological phenomena including seasonal cyclonic activity. These features are expected to influence patterns of genetic structuring throughout the landscape either by promoting or restricting the movement of pollen and seed. Whilst a growing body of literature exists for the fauna endemic to this region, less is known about the forces shaping the evolution of plant taxa. In this study we investigate the phylogeography of two iconic Pilbara tree species, the Hamersley Bloodwood (Corymbia hamersleyana) and Western Gidgee (Acacia pruinocarpa), by assessing patterns of variation and structure in several chloroplast DNA regions and nuclear microsatellite loci developed for each species. Gene flow was found to be extensive in both taxa and there was evidence of long-distance seed dispersal across the region (pollen to seed ratios of 6.67 and 2.96 for C. hamersleyana and A. pruinocarpa, respectively), which may result from flooding and strong wind gusts associated with extreme cyclonic activity. Both species possessed high levels of cpDNA genetic diversity in comparison to those from formerly glaciated landscapes (C. hamersleyana = 14 haplotypes, A. pruinocarpa = 37 haplotypes) and showed evidence of deep lineage diversification occurring from the late Miocene, a time of intensifying aridity in this landscape that appears to be a critical driver of evolution in Pilbara taxa. In contrast to another study, we did not find evidence for topographic features acting as refugia for the widely sampled C. hamersleyana.