Homoploid Hybrid Speciation in a Marine Pelagic Fish Megalaspis cordyla (Carangidae)

Homoploid hybrid speciation (HHS) is an enigmatic evolutionary process where new species arise through hybridization of divergent lineages without changes in chromosome number. Although increasingly documented in various taxa and ecosystems, convincing cases of HHS in marine fishes have been lacking. This study presents evidence of HHS in Torpedo scad Megalaspis cordyla based on comprehensive genomic, morphological, and ecological analyses. A Principal Component Analysis using thousands of SNPs identified three sympatric clusters in the western Pacific. Genome-wide differentiation between the clusters and the admixed nature of a cluster between the others were evident from population genomic analyses, species tree estimation, mitochondrial DNA divergence, and tests of introgression. Multiple statistical methods for hybrid detection also supported the admixed ancestry of this cluster. Moreover, model-based demographic inference favored a hybrid speciation scenario over introgression. Examination of occurrence data and ecologically relevant morphological characters suggested ecological differences between the clusters, potentially contributing to reproductive isolation and niche partitioning in sympatry. The clusters are morphologically distinguishable and thus can be taxonomically recognized as separate species. The hybrid cluster is restricted to the coasts of Taiwan and Japan, where all three clusters coexist. The parental clusters are additionally found in lower latitudes such as the coasts of the Philippines, Vietnam, Thailand, and Malaysia, where they display non-overlapping distributions. Given the geographical distributions, estimated times of the species formation, and patterns of historical demographic changes, we propose that the Pleistocene glacial cycles were the primary driver of HHS in this system. Based on this argument, we develop an ecogeographic model of HHS in marine coastal ecosystems, including a novel hypothesis to explain the initial stages of HHS.