Haplotype divergence supports long-term asexuality in the oribatid mite

Significance Putatively ancient asexual species pose a challenge to theory because they appear to escape the predicted negative long-term consequences of asexuality. Although long-term asexuality is difficult to demonstrate, specific signatures of haplotype divergence, called the “Meselson effect,” are regarded as strong support for long-term asexuality. Here, we provide evidence for the Meselson effect in an asexual oribatid mite species, Oppiella nova, and we show that the effect is not caused by hybridization or polyploidization. Our findings provide conclusive evidence for the long-term absence of sex in O. nova and suggest that asexual oribatid mites can escape the dead-end fate usually associated with asexual reproduction.
Sex strongly impacts genome evolution via recombination and segregation. In the absence of these processes, haplotypes within lineages of diploid organisms are predicted to accumulate mutations independently of each other and diverge over time. This so-called “Meselson effect” is regarded as a strong indicator of the long-term evolution under obligate asexuality. Here, we present genomic and transcriptomic data of three populations of the asexual oribatid mite species Oppiella nova and its sexual relative Oppiella subpectinata. We document strikingly different patterns of haplotype divergence between the two species, strongly supporting Meselson effect–like evolution and long-term asexuality in O. nova: I) variation within individuals exceeds variation between populations in O. nova but vice versa in O. subpectinata; II) two O. nova sublineages feature a high proportion of lineage-specific heterozygous single-nucleotide polymorphisms (SNPs), indicating that haplotypes continued to diverge after lineage separation; III) the deepest split in gene trees generally separates the two haplotypes in O. nova, but populations in O. subpectinata; and IV) the topologies of the two haplotype trees match each other. Our findings provide positive evidence for the absence of canonical sex over evolutionary time in O. nova and suggest that asexual oribatid mites can escape the dead-end fate usually associated with asexual lineages.