Genomic tests of the species-pump hypothesis: Recent island connectivity cycles drive population divergence but not speciation in Caribbean crickets across the Virgin Islands

Abstract

Harnessing the power of genomic scans, we test the debated "species pump" hypothesis that implicates repeated cycles of island connectivity and isolation as drivers of divergence. This question has gone understudied given the limited resolution of past molecular markers for studying such dynamic phenomena. With an average of 32,000 SNPs from the genome of 136 individuals from 10 populations of a Caribbean flightless ground cricket species (Amphiacusta sanctaecrucis) and a complementary set of statistical approaches, we infer a stepping-stone colonization model and high levels of genetic differentiation across the Virgin Islands, which have been periodically interconnected until 8 ka. Estimates of divergence times from models based on the site frequency spectrum coincide with a period of repeated connection and fragmentation of the islands at 75-130 ka. These results are consistent with a role of island connectivity cycles in promoting genomic divergence and indicate that the genetic distinctiveness of island populations has persisted despite subsequent and extended interisland connections identified from bathymetric data. We discuss these findings in the broader context of Caribbean biogeography, and more specifically why high levels of genomic divergence across the Virgin Islands associated with repeated connectivity cycles do not actually translate into species diversification.

Keywords: Biogeography; Pleistocene Aggregate Island Complex; Rad-seq; sea-level change.