Scheben, A.; McKeown, A.; Walsh, T.; Westcott, D. A.; Metcalfe, S. S.; Vanderduys, E. P.; Webber, B. L.

Speciation results from shifts between genetic connectivity and isolation of populations. Flying-foxes (Pteropus) are a compelling model to study the interplay of these evolutionary processes due to 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, we examined the extent to which panmixia, isolation-by-distance, and hybridization shaped these populations. Phylogenetic and demographic modeling approaches indicate that isolation-by-distance, despite ongoing gene flow, is prevalent in P. alecto and P. conspicillatus populations while P. poliocephalus and P. scapulatus are panmictic across Australia. We further find that hybridization and asymmetric gene flow from P. conspicillatus to P. alecto plays a role in shaping the historic and contemporary populations of these recently diverged species, which exhibit gene flow along a geographic ring connecting Indonesia to Australia and New Guinea. We also uncover cryptic speciation within P. alecto, highlighting its complex evolutionary history. Together, our findings indicate that long-range population connectivity and limited restrictions on gene flow have shaped the evolution and diversification of flying-foxes.