Madagascar as an evolutionary source for the Paleotropical flora: New insights from the biogeography of Grewia (Malvaceae)

Abstract

Oceanic islands are natural laboratories for investigating the processes that generate, maintain, and redistribute biodiversity through time. An ideal flowering plant system to investigate these processes is Grewia L. (Malvaceae, Grewioideae), comprising ca. 283 species, of which nearly 30% are endemic to Madagascar, where they display considerable morphological diversity. Using Angiosperms353 target-capture sequencing for 171 accessions (119 Grewia spp.), we reconstructed the first densely sampled phylogeny of Grewia and performed divergence-time estimation, diversification analyses, and ancestral-range reconstruction. Our results support a Malagasy origin of the crown group around 27 million years ago, followed by extensive in situ diversification of Grewia. Repeated dispersal events from Madagascar to continental Africa subsequently contributed to the establishment of new African lineages, whereas colonization of the western Indian Ocean islands was more recent and resulted in anagenetic dispersals. Africa acted as the principal source of dispersal toward Arabia and into tropical Asia, suggesting the presence of a Miocene Afro-Arabian migration corridor under warm and humid conditions. Subsequent eastward dispersal from Asia to Australia is consistent with the stepping stone pathway provided by the Sunda and Sahul regions during the Miocene. This complex dispersal history was likely aided by fleshy fruits adapted for endozoochory. Our new evolutionary framework provides a robust basis for future taxonomic revision of this morphologically and ecologically diverse genus, and for identifying which characters have contributed to its exceptional diversification. Highlights This is the first phylogenomic analysis of Grewia, one of the largest genera in Malvaceae. We reconstruct dispersal events for Grewia across the Paleotropics. Miocene corridors and fleshy fruits aided dispersal out of Africa and eastward. Grewia originated in Madagascar at 27 Ma and colonised Africa at least 5 times. Madagascar is the center of Grewia diversity with more than 80 endemic species.