The evolution of endemism within a major legume lineage of the campos rupestres

The campos rupestres (CR) are a grassy vegetation mosaic found on ancient mountains in Brazil. CR areas accumulate a high plant endemism that has been primarily explained by two contrasting processes, the Plio-Pleistocene climatic oscillations and long-term specialization and persistence in climatically stable areas. To investigate these alternative processes, we adopted the mountain-geobiodiversity (MG) hypothesis and studied the genus Chamaecrista, an emblematic plant lineage in CR areas. We hypothesized that species would have evolved towards environmental specialization upon colonizing CR areas due to selective pressures imposed by environmental heterogeneity. Moreover, species would have undergone faster diversification in CR areas during the Plio-Pleistocene, when climatic oscillations would have promoted speciation over extinction. Throughout, species would have originated primarily through geographic speciation in CR areas, where topographic complexity would have imposed physical barriers to plant dispersal.

We used geographical and phylogenetic data on the genus Chamaecrista, including CR-endemic and non-endemic species. We applied biogeographic reconstruction to infer when species became endemic to CR areas. We applied environmental niche modeling to estimate specialization, fitting evolutionary models to infer how specialization evolved. We fitted state-dependent models to infer species diversification dynamic. We estimated the degree of geographic isolation during speciation.

CR-endemic species evolved environmental niches twice more specialized than non-endemic species, likely under selective pressures. CR-endemic species experienced a faster diversification than non-endemic species at deeper evolutionary times, before the Plio-Pleistocene periods. CR-endemic species originated under greater geographic isolation than non-endemic species.

Colonization of CR areas accelerated species diversification, enhancing the pool of species to later become endemic. Environmental specialization has enforced plant endemism in CR areas by constraining the potential for persistence in habitats outside CR areas. Topographic complexity has enhanced plant endemism in CR areas by hindering plant dispersal and promoting geographic speciation.