Speciation and radiations track climate transitions since the Miocene Climatic Optimum: a case study of southern African chameleons

Aim The high amount of species diversity concentrated in southern Africa has been attributed to palaeoclimatic factors, and the timing of radiations in some taxa corresponds to global palaeoclimatic trends. Using dwarf chameleons (Bradypodion: Chamaeleonidae) as a model system, we explored the relationship between palaeoclimatic fluctuations and cladogenesis with respect to both temporal and spatial patterns in an effort to understand the process of speciation in southern Africa. Location South Africa, with particular emphasis on the Cape Floristic Region and the Maputaland-Pondoland-Albany hotspot. Methods Mitochondrial sequence data (ND2 and 16S) were used to estimate the timing of major radiations and to examine the number of lineages through time. A dated phylogeny was constructed using Bayesian phylogenetic reconstruction, and a Bayesian relaxed molecular clock was used to estimate divergence times. Spatial data and lineage-through-time plots were used to identify geographic regions that underwent diversification in connection with major climatic events. Both parsimony and likelihood optimizations of habitat type on the phylogeny were used to determine whether major habitat shifts have occurred. On a coarse scale (half-degree grid cells), phylogenetic diversity (sum of the branch lengths linking terminals) was compared with species richness (absolute number of species) to identify areas of conservation importance. Results The complete species phylogeny of dwarf chameleons shows that the timing and mode of diversification exhibit spatio-temporal patterns that link to phases in the evolution of southern Africa's climate over the last 14 Myr. Optimizations of habitat on the phylogenetic tree show a progression from closed to open habitats since the Mid-Miocene, corresponding to the shift front C-3 to C-4 environments, and later with the development of south-western Africa's winter-rainfall regime. These shifts are not simultaneous across the region, with different geographic centres of diversity generated during different time periods. Main conclusions Regions that are prominent centres of chameleon diversification are encompassed by the current biodiversity hotspots as shown by chameleon species richness and phylogenetic diversity. Diversity within the Cape Floristic Region appears to be the result of a Late Pliocene radiation, whereas the diversity encompassed within the Maputaland-Pondoland-Albany hotspot is an aggregate of asynchronous radiation events, probably influenced by lineage losses. Overall, dwarf chameleons have experienced a shift in habitat types, with recent radiations occupying open habitats, and older lineages persisting in relictual forested habitats, corresponding to the continental shift of vegetation types since the Miocene Climatic Optimum.