African phylogeography; expansion-contraction paradigm; forest refugia; fruit bats; island evolution; Last Glacial Maximum; pluvial-drought cycles; Rousettus; species distribution modelling; stepping-stone dispersal

Aim: The impact of Pleistocene climatic oscillations on tropical biomes is associated with changes in the extent of forest cover. Fruit bats have played a role in woodland dynamics via pollination and seed dispersal. We hypothesized that phylogeographic patterns of Rousettus on continental Africa and adjacent islands should show a signature of pluvial‐drought cycles, involving demographic expansions and contractions. Main Conclusion: Palaeodistributional modelling ascertained that the Indian Ocean islands provided more extensive areas of suitable habitat in the past relative to conditions today, suggesting stepping stone connectivity between Asia and Africa during Pleistocene interpluvial sea‐level lowstands. Inverse pluvial‐drought demography was detected in lineages ancestral to recent haplogroups, providing evidence of past forest refugia and complex ecogeographic scenarios of haplogroup origins involving allopatry and parapatry connected with the eastern Afromontane biodiversity hotspot, and subsequent admixture of nuclear gene pools. The Middle Eastern lineage probably originated during pluvial green Sahara periods, possibly in co‐evolution with ancestors of tree crop species domesticated later during the Neolithic revolution. The keystone role of rousettine bats for forest regeneration and their ability to pioneer dry and distant habitats emphasize their role in conservation biology and restoration ecology.