Zombie Gene Flow: Asexual Hybrids Mediate Extensive Genomic Introgression from Extinct Species Into Their Sexual Parent

Abstract

Interspecific gene flow may profoundly impact genome integrity and adaptive evolution in hybridizing species, leading to novelties such as transgressive traits, supergenes, or, sometimes, the emergence of asexually reproducing lineages. Conventionally, introgression is thought to proceed between reproductively interacting species, mediated by recombining interspecific hybrids, while asexual lineages are considered evolutionary deadlock for genomes trapped in them. Our study on Cobitis loaches in the western Balkan watersheds demonstrates an alternative mechanism where a mix of asexuality and polyploidy facilitates significant introgression from a long-extinct species. Through extensive sampling and cytogenetic and phylogenomic analyses, we identified a sexual species, C. ohridana (OO) coexisting with its asexual hybrid form (OX) originating from hybridization with an extinct species (XX). The diploid OX hybrids pass both parental subgenomes mostly clonally with occasional gene conversions, while triploid OOX hybrids reproduce through meiotic hybridogenesis, producing O-like gametes with localized gene conversions by X alleles. Their mating with the locally dominant sexual species consequently leads to over 4% admixture in both nuclear and mitochondrial genomes. Our findings challenge the view of hybrid asexual lineages as evolutionary dead ends, revealing their significant role as reservoirs of genetic diversity and agents of interspecific gene exchange, even after the extinction of one parental taxon.