Haplotype divergence supports ancient asexuality in the oribatid miteOppiella nova

Abstract

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 speciesOppiella novaand its sexual relativeOppiella subpectinata. We document strikingly different patterns of haplotype divergence between the two species, strongly supporting Meselson effect like evolution and ancient asexuality inO. nova: (I) Variation within individuals exceeds variation between populations inO. novabutvice versainO. subpectinata. (II) TwoO. novasub-lineages feature a high proportion of heterozygous genotypes and lineage-specific haplotypes, indicating that haplotypes diverged independently within the two lineages after their split. (III) The deepest split in gene trees generally separates haplotypes inO. nova, but populations inO. subpectinata. (IV) Tree topologies of the two haplotypes match each other. Our findings provide positive evidence for the absence of sex over evolutionary time inO. novaand suggest that asexual oribatid mites can escape the dead-end fate usually associated with asexual lineages.