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 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.
Highlights
Sex strongly impacts genome evolution via recombination and segregation
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
Despite the low assembly contiguity, the genomes were of sufficient quality for downstream analyses, which focused on patterns of heterozygosity and polymorphism
Summary
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 socalled “Meselson effect” is regarded as a strong indicator of the long-term evolution under obligate asexuality. Sexual reproduction is considered as a prerequisite for the long-term persistence of eukaryote species, because it reduces selective interference among loci and facilitates adaptation and purifying selection [recently reviewed in Otto [1]] Contrary to this scientific consensus, some exceptional taxa appear to have persisted in the absence of sex over millions of years, the so-called “ancient asexual scandals” [sensu Judson and Normark [2]]. 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
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