Homologous chromosomes in asexual rotifer Adineta vaga suggest automixis

The several hundreds of species of bdelloid rotifers are notorious because they represent an ancient clade comprising only asexual lineages. Moreover, most bdelloid species have the ability to withstand complete desiccation and high doses of ionizing radiation, being able to repair their DNA after massive genome breakage. To better understand the impact of long-term asexuality and DNA breakage on genome evolution, a telomere-to-tolemere reference genome assembly of a bdelloid species is critical.

Here we present the first, high quality chromosome-scale genome assembly for the bdelloid A. vaga validated using three complementary assembly procedures combined with chromosome conformation capture (Hi-C) data. The different assemblies reveal the same genome architecture and using fluorescent in situ hybridization (FISH), we demonstrate that the A. vaga genome is composed of six pairs of homologous chromosomes, compatible with meiosis.

Moreover, the synteny between homoeologous (or ohnologous) chromosomes is also preserved, confirming their paleotetraploidy. The diploid genome structure of A. vaga and the presence of very long homozygous tracts show that recombination between homologous chromosomes occurs in this ancient asexual scandal, either during DSB repair or during meiotic pairing.

These homozygosity tracts are mainly observed towards the chromosome ends in the clonal A. vaga suggesting signatures of a parthenogenetic mode of reproduction equivalent to central fusion automixis, in which homologous chromosomes are not segregated during the meiotic division.

Authors: Paul Simion, Jitendra Narayan, Antoine Houtain, Alessandro Derzelle, Lyam Baudry, Emilien Nicolas, Marie Cariou, Nadège Guiglielmoni, Djampa KL Kozlowski, Florence Rodriguez Gaudray, Matthieu Terwagne, Julie Virgo, Benjamin Noel, Patrick Wincker, Etienne GJ Danchin, Martial Marbouty, Bernard Hallet, Romain Koszul, Antoine Limasset, Jean-François Flot, Karine Van Doninck