ddRADLacustrine speciation associated with chromosomal inversion in a lineage of riverine fishes

Geographic isolation is the driver of speciation in most vertebrate lineages. Physical barriers that reduce or eliminate flow between populations allow genetic drift and natural selection to contribute to the evolution of reproductive isolation. This trend is exemplified by North American darters, a clade of freshwater fishes where nearly all sister species pairs are allopatric and separated by millions of years of divergence. One of the only exceptions is the Lake Waccamaw endemic Etheostoma perlongum and its riverine sister species E. maculaticeps with no physical barriers to gene flow. Here we show that lacustrine speciation of E. perlongum is characterized by morphological and ecological divergence likely facilitated by a large chromosomal inversion. While Etheostoma perlongum is phylogenetically nested within the geographically widespread E. maculaticeps, there is a sharp genetic and morphological break coinciding with the lake-river boundary in the Waccamaw River system. Demographic analyses reveal that E. perlongum and E. maculaticeps diverged 11,000-45,000 years ago, consistent with the young age of Lake Waccamaw. Despite an active hybrid zone and ongoing gene flow, analyses using a de novo reference genome reveal a 10 Mb genomic region with elevated divergence between E. perlongum and E. maculaticeps that is likely a chromosomal inversion. Our results illustrate that rapid, ecological speciation with gene flow is possible in lineages where geographic isolation is the dominant mechanism of speciation.