The evolution of ecological specialization underlies plant endemism in the Atlantic Forest

Abstract

Abstract Background and Aims The evolution of ecological specialization is favoured under divergent selection imposed by increased environmental heterogeneity, although specialization can limit the geographical range of organisms, thus promoting endemism. The Atlantic Forest (AF) is an ancient montane domain with high plant endemism, containing different environments for plant specialization. Miconia is the most diverse genus of woody flowering plant within the AF domain, including AF-endemic and non-endemic lineages. We hypothesized that Miconia species have faced increased environmental heterogeneity and consequently have been selected towards increased specialization in the AF domain, and this increased specialization has greatly reduced species geographical ranges, ultimately promoting endemism. Hence, we made the following predictions: (1) AF-endemic species should face greater environmental heterogeneity than non-endemic species; (2) AF-endemic species should be more specialized than non-endemic species; (3) specialization should lead to smaller geographical ranges; (4) specialization and small geographical ranges among AF-endemic species should conform to a selection-driven evolutionary scenario rather than to a neutral evolutionary scenario; and (5) small geographical ranges among AF-endemic species should date back to the occupation of the AF domain rather than to more recent time periods. Methods We used geographical, environmental and phylogenetic data on a major Miconia clade including AF-endemic and non-endemic species. We calculated Rao’s Q to estimate the environmental heterogeneity faced by species. We used georeferenced occurrences to estimate the geographical ranges of species. We applied environmental niche modelling to infer species niche breadth. We inferred the most likely evolutionary scenario for species geographical range and niche breadth via a model-fitting approach. We used ancestral reconstructions to evaluate species geographical range throughout time. Key Results Atlantic Forest-endemic species faced 33–60 % more environmental heterogeneity, with the increase being associated with montane landscapes in the AF. The AF-endemic species were 60 % more specialized overall, specifically over highly variable environmental gradients in AF montane landscapes. Specialization strongly predicted small geographical ranges among AF-endemic species and was a major range-limiting factor among endemic lineages. The AF-endemic species have evolved towards specialization and small geographical ranges under a selection-driven regime, probably imposed by the great environmental heterogeneity in AF montane landscapes. The AF-endemic species underwent a major reduction of geographical range immediately after their evolution, indicating a long-standing effect of selective pressures in the AF domain. Conclusion Environmental heterogeneity imposes selective pressures favouring ecological specialization and small geographical ranges among plant lineages in the AF domain. This selection-driven process has probably promoted plant endemism in the AF domain throughout its history.