Evolutionary stability, landscape heterogeneity, and human land-usage shape population genetic connectivity in the Cape Floristic Region biodiversity hotspot

Abstract

As human-induced change eliminates natural habitats, it impacts genetic diversity and population connectivity for local biodiversity. The South African Cape Floristic Region (CFR) is the most diverse extratropical area for plant biodiversity, and much of its habitat is protected as a UNESCO World Heritage site. There has long been great interest in explaining the underlying factors driving this unique diversity, especially as much of the CFR is endangered by urbanization and other anthropogenic activity. Here, we use a population and landscape genetic analysis of SNP data from the CFR endemic plant Leucadendron salignum or "common sunshine conebush" as a model to address the evolutionary and environmental factors shaping the vast CFR diversity. We found that high population structure, along with relatively deeper and older genealogies, is characteristic of the southwestern CFR, whereas low population structure and more recent lineage coalescence depict the eastern CFR. Population network analyses show genetic connectivity is facilitated in areas of lower elevation and higher seasonal precipitation. These population genetic signatures corroborate CFR species-level patterns consistent with high Pleistocene biome stability and landscape heterogeneity in the southwest, but with coincident instability in the east. Finally, we also find evidence of human land-usage as a significant gene flow barrier, especially in severely threatened lowlands where genetic connectivity has been historically the highest. These results help identify areas where conservation plans can prioritize protecting high genetic diversity threatened by contemporary human activities within this unique cultural UNESCO site.

Keywords: Cape Floristic Region; gene flow; land use; social network; urbanization.

FIGURE 1

Map of southern South Africa with 51 sampled locales of 306 Leucadendron salignum (Table S1 for locale information). Pie charts provide geographic reference to color coding in phylogenetic (Figure 2), population structure (Figures 3 and 4), and population connectivity (Figure 5) analyses. Shaded area denotes recognized Cape Floristic Region (after Cowling et al., 2017)

FIGURE 2

Consensus BEAST phylogenetic tree topology of 306 Leucadendron salignum chloroplast DNA SNP haplotypes, rooted by outgroup, with estimates of genetic divergence times (see Materials and Methods). Black dots on nodes represent major branches with support >75%

FIGURE 3

Bi‐plots of the first four principal components of Leucadendron salignum datasets using (a) chloroplast DNA SNPs from 306 sequences, and (b) nuclear DNA SNPs from 408 sequences. Color‐coding reflects the five major phylogenetic tree clusters (Figure 2)

FIGURE 4

fastSTRUCTURE analysis of 306 Leucadendron salignum chloroplast DNA SNP haplotypes from 51 sampled locales (see Figure 1 for geographic sampling, Table S1 for locale information)

FIGURE 5

Popgraph of genetic connectivity among 51 sampled locales of Leucadendron salignum chloroplast DNA (see Figure 1 for geographic sampling, Table S1 for locale information). Color‐coding reflects the five major phylogenetic tree clusters (Figure 2)