Phylogenomic analysis reveals dispersal-driven speciation and divergence with gene flow in Lesser Sunda Flying Lizards (Genus Draco)

The Lesser Sunda Archipelago offers exceptional potential as a model system for studying the dynamics of dispersal-driven diversification. The geographic proximity of the islands suggests the possibility for successful dispersal, but this is countered by the permanence of the marine barriers and extreme intervening currents that are expected to hinder gene flow. Phylogenetic and species delimitation analyses of flying lizards (genus Draco) using single mitochondrial genes, complete mitochondrial genomes, and exome-capture data sets identified 9–11 deeply divergent lineages both within and between islands, with the largest islands each containing parapatrically-distributed non-sister lineages. Population clustering and demographic analyses confirmed these genetic boundaries and suggest the occurrence of 9–10 cryptic and non-cryptic species rather than the two species currently recognized. These analyses indicate initial entry of Draco into the archipelago at 5.5–7.5 Ma, with most inter-island colonization events having occurred between 1–3 Ma. Biogeographical model testing favors scenarios integrating geographic distance and historical island connectivity, including an initial stepping-stone dispersal process from the Greater Sunda Shelf through the Sunda Arc as far eastward as Lembata Island. However, rather than reaching the adjacent island of Pantar by dispersing over the 15-km wide Alor Strait, Draco ultimately reached Pantar (and much of the rest of the archipelago) by way of a circuitous route involving dispersal from either Sumbawa or Flores south to Sumba, east to Timor (across a 300-km marine barrier), north to Wetar, and then westward back to Pantar. These findings suggest that historical geological and oceanographic conditions heavily influenced dispersal pathways and gene flow, which in turn drove species formation and shaped species boundaries.