Extreme mobility creates contrasting patterns of panmixia, isolation-by-distance and hybridization in four flying-fox species (Pteropus)

Shifts between population connectivity and isolation shape evolutionary divergence, but their effects remain underexplored in highly mobile taxa. Flying-foxes (Pteropus) are a compelling model to study evolutionary divergence because of their rapid radiation in the island-rich region of the Indo-Australian Archipelago. Here, we investigate the population genetics of the highly mobile flying-foxes Pteropus alecto, P. conspicillatus, P. poliocephalus, and P. scapulatus across large parts of their overlapping ranges in Australia, Indonesia, and New Guinea. Using reduced-representation sequencing of 242 individuals, we examined the extent to which panmixia, isolation-by-distance, and hybridization are prevalent in these lineages. Phylogenetic, principal component and demographic analyses indicated isolation-by-distance in P. alecto, including an unexpected east-west genetic split between Australian populations, whereas P. conspicillatus showed weak differentiation between Australia and New Guinea and P. poliocephalus and P. scapulatus were panmictic across Australia. We further found evidence that infrequent hybridization and asymmetric gene flow, predominantly from P. conspicillatus to P. alecto, have shaped these recently diverged species. Although gene flow connected sampled populations along the geographic chain spanning Indonesia, Australia, and New Guinea, our results did not confirm the hypothesis that P. alecto and P. conspicillatus form a ring species. Rather, demographic analyses supported recent secondary contact during the last 14,848 to 35,856 years after a period of isolation between P. alecto and P. conspicillatus. Together, our findings indicate that long-range connectivity and spatially heterogeneous restrictions on gene flow have shaped the evolution and diversification of flying-foxes.