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.

地理隔离是众多脊椎动物演化支物种形成的主要驱动力。这一趋势以北美洲镖鲈（darters）为例得到充分印证——这类淡水鱼类演化支中，几乎所有姊妹物种对均为异域分布（allopatric），且彼此间的分化时长可达数百万年。其中为数不多的例外之一，便是沃卡莫湖（Lake Waccamaw）特有种长体镖鲈（Etheostoma perlongum）及其淡水姊妹物种斑头镖鲈（E. maculaticeps），二者之间不存在阻碍基因流（gene flow）的物理屏障。本研究表明，长体镖鲈的湖栖物种形成过程以形态学与生态学分化为典型特征，该分化过程或得益于一段大型染色体倒位（chromosomal inversion）。尽管长体镖鲈在系统发育上嵌套于地理分布广泛的斑头镖鲈支系之内，但在沃卡莫河水系的湖-河交界地带，存在着显著的遗传与形态学分界。尽管二者分化时间较近、存在活跃的杂交带（hybrid zone）且存在持续的基因流，基于从头组装参考基因组（de novo reference genome）的分析显示，一段长度为9 Mb的染色体倒位区域在长体镖鲈与斑头镖鲈之间呈现出升高的分化水平。该区域与两个远缘鱼类支系中已报道的倒位超基因（inversion supergene）具有显著的同线性（synteny），暗示基因组架构存在深层的进化趋同。本研究结果表明，即便在以地理隔离为主要物种形成机制的类群中，伴随基因流的快速生态物种形成仍是可行的。