Rapid chromosomal rearrangements and sex chromosome turnover underlie the evolution of parapatric Pacific Scomber mackerels

Teleost display remarkable species diversity despite relatively conserved karyotypes, suggesting an important role for chromosomal rearrangements in speciation. Yet this hypothesis remains poorly tested in pelagic marine fishes, as genomic studies have predominantly focused on freshwater and coastal taxa. In this study, we investigated the genomic basis of hybrid incompatibility between two parapatric Pacific mackerels, Scomber japonicus and S. australasicus, hypothesizing chromosomal rearrangements as the major driving forces. We generated haplotype-resolved de novo genome assemblies for both Pacific species and assessed genomic rearrangements along with the genome of the Atlantic species, S. scombrus, reconstructed from publicly available data. Comparative genomic analyses revealed extensive chromosomal rearrangements across the genomes. Notably, the rate of chromosomal inversions was approximately sevenfold higher between the two Pacific species than between allopatric lineages. These rearrangements included complex structural changes involving megabase-scale inversions and associated translocations. Our analyses also showed that the sex chromosomes of the three species evolved independently. In the two Pacific species, large recombination-suppression regions (>10 Mb) arose convergently but through distinct mechanisms: tandem chromosomal inversions in S. japonicus and, most likely, transposable element-mediated sequence divergence in S. australasicus. By contrast, recombination suppression in S. scombrus is restricted to a [~]14 kb hemizygous region containing amhr2Y, generated by duplication and translocation. Population-level analyses further revealed ongoing evolution of recombination-suppressed regions in the Pacific species and uncovered multiple Y chromosome lineages in S. australasicus that differ markedly in the extent of recombination suppression. Together, these results demonstrate rapid structural genome evolution in Scomber and provide a genomic framework for understanding how chromosomal rearrangements contribute to reproductive isolation, sex chromosome turnover, and the diversification of pelagic marine fishes.