Transposable elements as drivers of reproductive isolation: A framework for testing hybridization-induced escalation of genetic conflicts

Fritjof Lammers, Valentina Peona, Reto Burri

Contrary to long-held views, the exchange of genetic diversity between species by hybridization is now recognized as an important process contributing to the evolution of biodiversity. However, hybridization has molecular consequences beyond the exchange of genetic variation. The clash of divergent genomes upon hybridization can escalate genetic conflicts previously resolved in parental species – notably between transposable elements (TEs) and their repressors – and unleash a cascade of molecular events inducing the evolution of chromosomal rearrangements (structural variants, SVs). Novel TE insertions and other SVs are often associated with cancer, reduced longevity, and genomic disorders, and usually inflict high fitness costs, thus they likely incur major constraints to gene flow among species and may constitute an integral component of reproductive isolation. Furthermore, in the presence of gene flow, certain SVs (e.g., inversions) may help protect beneficial combinations of alleles across genes from breaking up. By mediating an increased input of SVs, TE reactivation may therefore act as an architect of SVs underlying reproductive isolation. While the hypothesis of such TE-related reproductive barriers is not new, tests of its predictions – especially in the wild – remain scarce. With this perspective we aim at synthesizing ideas and providing a roadmap to stimulate research targeted towards an increased understanding of hybridization-induced TE reactivation and its potential knock-on effects for the evolution of structural variation and reproductive isolation. We argue that technological advances now provide unprecedented opportunities to identify genomic, transcriptomic and epigenomic signatures of such re-escalating genetic conflict upon hybridization and present a practical roadmap to guide researcher to investigate such genetic conflict in wild populations. While our perspective is centred predominantly on vertebrates, with adaptations to the taxon-specific TE biology, our roadmap represents a generalizable framework for the study of hybridization-induced escalations of TE-related genomic conflicts.