Repeated Resource-Driven Speciation with Gene Flow in Isolated Island Finches

The endemic Nesospiza finches constitute a small avian radiation on the isolated Tristan da Cunha archipelago in the South Atlantic Ocean, and offer unique insights to the balance between selection and gene flow during speciation. They display pronounced adaptation to food sources by divergent natural selection on bill size, a trait that also serves as a cue for assortative mating. On Inaccessible and Nightingale Islands, similar pairs of small-billed feeding generalists and large-billed feeding specialists occur, fully reproductively isolated on Nightingale and partially hybridizing on Inaccessible. Using a multitude of sequencing and analytical approaches, we:

(1) identified one genomic region regulating differences in body size on both islands, homologous to a region associated with growth rates in chicken
(2) identified a region on a sex chromosome, containing the homeobox protein ISL1—which acts as a transcription factor within the neural crest differentiation pathway—independently regulating bill size on Inaccessible but not on Nightingale
(3) found indications of epistatic interactions between the two genomic regions on Inaccessible
(4) confirmed that Nesospiza colonized the Tristan archipelago from the mainland rather than from other oceanic islands
(5) established that the founding population was small-billed
(6) recovered the two non-hybridizing species on Nightingale as sisters

The colonization occurred already 4 Mya and the selection pressure for large bills was introduced with the colonisation of Phylica trees ~1 Mya. Nevertheless, the current taxa only radiated within the last 3 Kya, and available evidence strongly supports independent ecological speciation in parallel on the two islands.