Genomic signatures of recombination in a natural population of the bdelloid rotifer Adineta vaga

Olga A Vakhrusheva,Georgii A Bazykin,Alexey S Kondrashov,Tatiana V Neretina,Svetlana G Ozerova,Evgeny S Gerasimov,Irina R Arkhipova,Sergey A Naumenko,Arthur O Zalevsky,Aleksey A Penin,Fernando Rodriguez,Irina A Yushenova,Maria D Logacheva,Yan R Galimov,Elena A Mnatsakanova

doi:10.1038/s41467-020-19614-y

Abstract

Sexual reproduction is almost ubiquitous among extant eukaryotes. As most asexual lineages are short-lived, abandoning sex is commonly regarded as an evolutionary dead end. Still, putative anciently asexual lineages challenge this view. One of the most striking examples are bdelloid rotifers, microscopic freshwater invertebrates believed to have completely abandoned sexual reproduction tens of Myr ago. Here, we compare whole genomes of 11 wild-caught individuals of the bdelloid rotifer Adineta vaga and present evidence that some patterns in its genetic variation are incompatible with strict clonality and lack of genetic exchange. These patterns include genotype proportions close to Hardy-Weinberg expectations within loci, lack of linkage disequilibrium between distant loci, incongruent haplotype phylogenies across the genome, and evidence for hybridization between divergent lineages. Analysis of triallelic sites independently corroborates these findings. Our results provide evidence for interindividual genetic exchange and recombination in A. vaga, a species previously thought to be anciently asexual.

Highlights

Sexual reproduction is almost ubiquitous among extant eukaryotes
We confirmed species identity of these individuals using mitochondrial marker-based phylogeny; while the samples clustered into distinct clades, they all were genetically most similar to A. vaga (Supplementary Note 1; Supplementary Figs. 1–3)
Contrary to what would be expected if A. vaga were strictly asexual, we found that among the individuals L4-L11, the linkage disequilibrium (LD) within genome segments from the phased dataset 1 rapidly declined with the distance between polymorphic loci (Fig. 2a and Supplementary Fig. 11), reaching the mean level observed for different contigs at ~2600–2700 nucleotides

Summary

Introduction

Sexual reproduction is almost ubiquitous among extant eukaryotes. As most asexual lineages are short-lived, abandoning sex is commonly regarded as an evolutionary dead end. A number of alleged ancient asexual lineages, sometimes referred to as ‘evolutionary scandals’[3,4], challenge the indispensability of sexual reproduction for the long-term evolutionary success. The list of such lineages includes darwinulid ostracods[5,6], oribatid mites[7], timema stick insects[8], and bdelloid rotifers[9,10,11,12], the most prominent of these groups, that underwent an extensive adaptive radiation after presumably losing sex tens of millions of years ago. It remains unclear if bdelloids regularly engage in any form of genetic exchange

Methods

Results

Conclusion