Abstract
While the tempo of diversification in biodiversity hotspots has received much attention, the spatial scale of diversification has often been overlooked. Addressing this deficiency requires understanding the drivers of population divergence and the spatial scales at which they operate in species-rich clades and ecosystems. South Africa's Succulent Karoo (SK) hotspot provides an excellent system for such research, being both compact (ca. 110,000km2 ) and home to spectacular in-situ radiations, such as the ruschioid Aizoaceae. Here we use GBS to document genetic structure in two co-occurring ruschioid species, at both coarse (>10km) and fine (<500m) spatial scales. Where Ruschia burtoniae shows strong between-population genetic differentiation and no gene flow, Conophytum calculus shows weak differentiation, with high levels of admixture suggesting recent or ongoing gene flow. Community analysis and transplant experiments reveal that R.burtoniae occupies a narrow, low-pH edaphic niche, and at scales of a few hundred metres, areas of elevated genetic turnover correspond to patches of edaphically unsuitable habitat. In contrast, C.calculus occupies a broader niche and exhibits isolation-by-distance without a habitat effect. We suggest that edaphic specialisation, coupled with highly restricted seed and pollen dispersal in heterogeneous landscapes, has played a major role in driving rapid diversification at small spatial scales in this system. However, the contrasting patterns in our study species show that these factors do not influence all organisms uniformly, being strongly modulated by lineage-specific traits that influence both the spatial scale of gene flow and habitat specificity.
Highlights
Biodiversity hotspots are areas characterized by high concentrations of species richness and taxonomic endemism (Guilhaumon et al, 2008; Mazel et al, 2014; Mittermeier et al, 2011; Myers et al, 2000; but see Orme et al, 2005)
The latter process can operate at fine spatial scales, underpinning the “budding” speciation pattern observed in small, sympatric or parapatric populations of monkeyflower (Grossenbacher et al, 2014) and in twelve plant families in the California Floristic Province (Anacker & Strauss, 2014).Importantly, regardless of the mechanism involved, heterogeneity-driven divergence is not expected to yield a pattern of isolation by distance, the latter being more consistent with intrinsically limited short-range dispersal in a continuously-distributed population (Wright, 1943)
Consistent with our expectation of fine-scale differentiation in Succulent Karoo (SK) plants, population-level genetic differentiation in R. burtoniae was strong given the proximity of our sampling localities (17–42 km apart). This pattern is comparable with that observed in another Knersvlakte-endemic succulent, Argyroderma pearsonii (Aizoaceae), which showed a global FST = 0.07 across six populations located
Summary
Biodiversity hotspots are areas characterized by high concentrations (per unit area) of species richness and taxonomic endemism (Guilhaumon et al, 2008; Mazel et al, 2014; Mittermeier et al, 2011; Myers et al, 2000; but see Orme et al, 2005). In the absence of rugged topography, some authors have identified fine-scale edaphic heterogeneity as an alternative driver of localized speciation in the SK (Ellis & Weis, 2006; Ellis et al, 2006), while others have invoked organismal traits, the evolution (in Ruschioideae) of rain-triggered, hygrochastic seed capsules whose sophisticated seed retention structures restrict primary dispersal distances to
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