Genomes of ancient asexual mites appear streamlined in their architecture

Abstract

The long-term persistence of obligate asexual lineages represents one of the most enduring and critical paradoxes in evolutionary biology. Sexual reproduction, through meiotic recombination and segregation, enables the efficient removal of deleterious mutations and facilitates rapid adaptation to shifting environmental pressures. Lineages that lose sex are therefore classically predicted to experience genomic decay and face rapid extinction. Oribatid mites (Acari, Sarcoptiformes) represent a unique system for testing these predictions, as they feature multiple, ancient, and independent transitions to asexuality, providing a natural experiment on the evolutionary fate of asexual genomes. We compared four sets of sister sexual and asexual species using high-quality nuclear genome assemblies to investigate the genomic consequences of long-term asexuality. Our study revealed a profound, reproductive-mode-dependent dichotomy in the evolution of genome architecture. Contrary to their expected genomic decay, asexual species have mostly streamlined genomes with less novel genes than their sexual sister species. In contrast, sexual species have acquired genetic innovations, encompassing both gene and transposable element content. These results challenge classical expectations of genomic deterioration in asexual species and might explain the long-term evolutionary persistence of oribatid mites.