Out of Amazonia: Biogeography of a Neotropical fern radiation

The Neotropics are Earth’s most species-rich region, so understanding how this diversity has emerged is of great interest. Here we address this question by assessing how species richness, speciation and dispersal are connected to geological and climatic history using the Neotropical fern genus Danaea (Marattiaceae) as a model. We evaluated alternative time calibrations to account for uncertain fossil affinities and integrated a dated phylogenetic tree of 78 Danaea species with 2,289 verified occurrence records, ancestral range and niche reconstructions, and biogeographic stochastic mapping. Our results suggest that Danaea diverged from the rest of the extant Marattiaceae ~128 million years ago (Ma), and the deepest divergence within the genus occurred ~53 Ma, likely separating eastern and western Amazonian lineages. The eastern lineage, corresponding to the subgenus Arthrodanaea , remains more restricted to Amazonia and low elevations than the more species-rich western lineage, which gave rise to the subgenera Danaea and Holodanaea . Speciation occurred mainly within regions rather than between adjacent regions. Amazonia has been the most species-rich region throughout the history of the genus, while the Andes have been the most important source of dispersals to other regions. Most Amazonian diversity arose within the last 6 Ma, coinciding with edaphic and climatic changes that occurred in western Amazonia in connection with Andean orogeny. Elsewhere, much of the diversification coincided with uplift of the Northern Andes and the emergence of terrestrial ecosystems in Southern Central America and the Pacific coast. Overall, all three subgenera seem to show parallel evolutionary responses to similar environmental changes. Although neotropical ferns in general show an Andean-centred diversity pattern, we found diversity in the genus Danaea (Marattiaceae) to be Amazon-centred. This may be related to the lack of epiphytes (which are most speciose in tropical mountain forests) in this genus. Even though Marattiaceae is an ancient family, most of the speciation leading to the extant species of Danaea has taken place in the last 6 million years and can be associated with geological processes such as Andean uplift and the draining of Amazonian megawetlands. Several lineages colonised montane areas before expanding further away from the equator, suggesting that physiological adaptation to high elevations may preadapt tropical plants for dispersal into more seasonal climates. In a comparison of different methods to calibrate a phylogenetic tree, the timing based on a molecular clock approach using well-known fossils and evolutionary rates from sister groups gave results more compatible with external biological and geological evidence than timings using fossils representing the target order but with uncertain phylogenetic placement within it.