Rethinking asexuality: the enigmatic case of functional sexual genes inLepraria(Stereocaulaceae)

AbstractBackgroundThe ubiquity of sex across eukaryotes, given its high costs, strongly suggests it is evolutionarily advantageous. Asexual lineages can avoid, for example, the risks and energetic costs of recombination, but suffer short-term reductions in adaptive potential and long-term damage to genome integrity. Despite these costs, lichenized fungi have frequently evolved asexual reproduction, likely because it allows the retention of symbiotic algae across generations. The relatively speciose lichenized fungal genusLeprariais thought to be exclusively asexual, while its sister genusStereocauloncompletes a sexual reproductive cycle. A comparison of sister sexual and asexual clades should shed light on the evolution of asexuality in lichens in general, as well as the apparent long-term maintenance of asexuality inLepraria, specifically.ResultsIn this study, we assembled and annotated representative long-read genomes from the putatively asexualLeprariagenus and its sexual sister genusStereocaulon, and added short-read assemblies from an additional 22 individuals across both genera. Comparative genomic analyses revealed that both genera were heterothallic, with intact mating-type loci of both idiomorphs present across each genus. Additionally, we identified and assessed 29 genes involved in meiosis and mitosis and 45 genes that contribute to formation of fungal sexual reproductive structures (ascomata). All genes were present and appeared functional in nearly allLepraria, and we failed to identify a general pattern of relaxation of selection on these genes across theLeprarialineage. Together, these results suggest thatLeprariamay be capable of sexual reproduction, including mate recognition, meiosis, and production of ascomata.ConclusionsDespite apparent maintenance of machinery essential for fungal sex, over 200 years of careful observations by lichenologists have produced no evidence of canonical sexual reproduction inLepraria. We suggest thatLeprariamay have instead evolved a form of parasexual reproduction, perhaps by repurposingMATand meiosis-specific genes. This may, in turn, allow these lichenized fungi to avoid long-term consequences of asexuality, while maintaining the benefit of an unbroken bond with their algal symbionts.