Homologous chromosomes in asexual rotiferAdineta vagasuggest automixis

Abstract

The several hundreds of species of bdelloid rotifers are notorious because they represent an ancient clade comprising only asexual lineages 1 . 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 2 . 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 3, 4 . 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.Bdelloid rotifers are a notorious clade of ancient asexual animals. However, both its longevity (>60 My) and diversity 1 contradicts the expectation that obligatory parthenogenetic animal lineages are evolutionary dead-ends. Historical observations 2 (or lack thereof) have produced a consensus that bdelloid rotifers are strictly parthenogenetic without any meiosis (e.g. no 3 males or hermaphrodites 1 , ameiotic genome structure in the model species Adineta vaga 3 , apomictic oogenesis 5, 6 ). However, 4 recent studies brought doubt regarding the supposed absence of meiotic recombination in these microscopic animals. These 5 include a drop of linkage disequilibrium with increasing distance between loci in A. vaga 7 , signatures of gene conversion 3, 8 , 6 heterozygosity levels falling within the range observed for sexual metazoans 3, 4, 9 and reports of allele sharing between bdelloid 7 individuals 7, 10-12 . 8In addition to its asexual evolution, the bdelloid rotifer A. vaga also became a model species for its extreme resistance to 9 desiccation and radiation, with implications for space research. Both prolonged desiccation and radiation induce oxidative 10 1 stress and massive genome breakage that A. vaga seem to handle well, maintaining high survival and fecundity rates while 11 efficiently repairing its DNA double strand breaks (DSBs) 2 . The exact nature of their DSB repair mechanism remains unknown, 12 but homologous recombination (HR) should ...

Evolutionary dynamics of transposable elements in bdelloid rotifers

“…Broken down by class and superfamily, the mean values are class I total = 2.09% ± 0.75 (PLEs = 0.59% ± 0.14; LTRs = 0.68% ± 0.26; and LINEs = 0.82% ± 0.47); class II total = 2.79 ± 0.8 (DNA transposons = 2.49% ± 0.77; rolling circles = 0.30 ± 0.11). These results are in broad agreement with previous estimates of TE content in bdelloids (Arkhipova et al, 2017;Flot et al, 2013;Nowell et al, 2018;Simion et al, 2020).…”

Evolutionary dynamics of transposable elements in bdelloid rotifers

“…Broken down by class and superfamily, the mean values are: class I total = 2.09% ± 0.75 (PLEs = 0.59% ± 0.14; LTRs = 0.68% ± 0.26; and LINEs = 0.82% ± 0.47); class II total = 2.79 ± 0.8 (DNA transposons = 2.49% ± 0.77; rolling circles = 0.30 ± 0.11). These results are in broad agreement with previous estimates of TE content in bdelloids [44,46,47,59].…”

“…Genetic and genomic evidence for their proposed ancient and obligate asexuality remains uncertain, however. Initial evidence of long-term asexuality [43,44] has been refuted by later studies or confounded by alternative explanations [45–47]. Some recent studies have proposed alternative modes of inter-individual genetic exchange, but these suggestions would require exotic mechanisms unknown in other animals [44,48], or rates of sex that are difficult to reconcile with the lack of observed males [49].…”

Genomic Signature of Sexual Reproduction in the Bdelloid RotiferMacrotrachella quadricornifera

“…Recently, phased sequencing of A. vaga and hybridization in situ revealed that its 12 chromosomes constitute 6 homologous pairs, a finding interpreted by the authors as evidence of automixis (50). Other recent sequencing found Hardy-Weinberg equilibrium and a fall-off of linkage with distance within a group of 11 isolates of A. vaga, suggested by the authors to be a result of horizontal gene transfer (56).…”