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

Geographic isolation is the primary driver of speciation in many
vertebrate lineages. 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, which have 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. Despite recent
divergence, an active hybrid zone, and ongoing gene flow, analyses using a
de novo reference genome reveal a 9 Mb chromosomal inversion with elevated
divergence between E. perlongum and E. maculaticeps. This region exhibits
striking synteny with known inversion supergenes in two distantly related
fish lineages, suggesting deep evolutionary convergence of genomic
architecture. Our results illustrate that rapid, ecological speciation
with gene flow is possible even in lineages where geographic isolation is
the dominant mechanism of speciation.