Haplotype divergence supports long-term 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 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.

New records of oribatid mites from Michoacán state, Mexico

“…nova are cosmopolitan. Only females of the latter species were collected, in agreement with its reported asexual reproduction (Brandt et al 2021). Belbodamaeus (Lanibelba) palaciosi and S. (S.) elegans have been collected in cave soils, agricultural and natural areas, showing great capacity for adaptation to adverse conditions.…”

Parthenogenesis doubles the rate of amino acid substitution in whiptail mitochondria

“…First, in the absence of recombination, haplotypes can diverge in what is known as the Meselson effect in ancient asexuals (Birky 1996;Welch et al 2000). Recent genomic data have demonstrated the Meselson effect and the long-term evolution in oribatid mites (Brandt et al 2021). Second, hybridization between divergent sexual progenitors instantaneously produces asexual lineages with high heterozygosity; this is the mechanism seen in nearly all parthenogenetic lizards (Fujita et al 2020).…”

“…On the other hand, recent studies using whole genomic-and transcriptomic-wide data have found evidence that is contrary to the expectation of mutation accumulation in asexual populations. Transcriptome-wide data from orib-atid mites revealed that purifying selection was more effective in the extremely old asexual lineages (∼10 million years old) than in sexual lineages (Brandt et al 2017(Brandt et al , 2021. Nonrecombining portions of the genome are expected to accumulate transposable elements (TE) and other repetitive content that leads to genomic degradation such as in the Y-chromosomes (Junakovic et al 1998;Bachtrog 2013).…”

Evolution of an Apomixis-Specific Allele Class in Supernumerary Chromatin of Apomictic Boechera

“…In addition, apomictic genomes exhibit significant levels of hemizygosity [ sensu Meselson effect; refer to (Brandt et al, 2021 ), also reviewed in (Hand and Koltunow, 2014 )], and repetitive element accumulation (Calderini et al, 2006 ). Whether these structural genomic features are the cause or a consequence of apomixis is still a subject of debate (Hand and Koltunow, 2014 ).…”