Transposons accelerate chromosomal speciation by centromere expansion and chromosome fission

Abstract

Chromosomal speciation poses a paradox: if rearrangements cause postmating isolation, how do they persist and spread? We propose that centromere remodeling, driven by transposable element accumulation, provides a mechanistic solution. In Opsariichthys, a hyper-diverse lineage of Asian river chub with 2N = 76-78 chromosomes, we identify [~]15 fission events coinciding with TE-fueled centromeric DNA expansion, potentially linked to a mutation in the PIWI1 protein. These expansions enable neokinetochore formation, allowing fissioned chromosomes to segregate faithfully, while subsequent rearrangements disrupt pairing and reduce gene flow. Comparative genomics reveals that fissioned chromosomes exhibit lower migration and greater divergence, acting as reproductive barriers. Our findings show that TE-mediated kinetochore duplication can facilitate extensive chromosome fission without meiotic disruption, providing a viable and previously underappreciated path to rapid speciation.