Comparative genomics of bdelloid rotifers: Insights from desiccating and nondesiccating species

Abstract

Bdelloid rotifers are a class of microscopic invertebrates that have existed for millions of years apparently without sex or meiosis. They inhabit a variety of temporary and permanent freshwater habitats globally, and many species are remarkably tolerant of desiccation. Bdelloids offer an opportunity to better understand the evolution of sex and recombination, but previous work has emphasised desiccation as the cause of several unusual genomic features in this group. Here, we present high-quality whole-genome sequences of 3 bdelloid species: Rotaria macrura and R. magnacalcarata, which are both desiccation intolerant, and Adineta ricciae, which is desiccation tolerant. In combination with the published assembly of A. vaga, which is also desiccation tolerant, we apply a comparative genomics approach to evaluate the potential effects of desiccation tolerance and asexuality on genome evolution in bdelloids. We find that ancestral tetraploidy is conserved among all 4 bdelloid species, but homologous divergence in obligately aquatic Rotaria genomes is unexpectedly low. This finding is contrary to current models regarding the role of desiccation in shaping bdelloid genomes. In addition, we find that homologous regions in A. ricciae are largely collinear and do not form palindromic repeats as observed in the published A. vaga assembly. Consequently, several features interpreted as genomic evidence for long-term ameiotic evolution are not general to all bdelloid species, even within the same genus. Finally, we substantiate previous findings of high levels of horizontally transferred nonmetazoan genes in both desiccating and nondesiccating bdelloid species and show that this unusual feature is not shared by other animal phyla, even those with desiccation-tolerant representatives. These comparisons call into question the proposed role of desiccation in mediating horizontal genetic transfer.

Demographic processes underlying fitness restoration in bdelloid rotifers emerging from dehydration

“…Moreover, even if selective pressures differed between the two treatments, the hydrated lines would have been constrained in the evolution towards a slow life history for at least three reasons. First, bdelloid reproduction (parthenogenesis) does not involve regular meiosis and recombination (Mark Welch, Ricci, & Meselson, ); second, horizontal gene transfer, although common in bdelloid rotifers, appears to be promoted by desiccation and not by the lack thereof (Eyres et al., ; but see Nowell et al., ); and third, mutation rates are probably too low to enable such a fast (adaptive) response (Ricci & Caprioli, ). For these reasons, we believe that the reduced population growth rates of the hydrated lines result from a lower fitness rather than from an adaptive response.…”

All Eukaryotes Are Sexual, unless Proven Otherwise

“…The presence of some (highly divergent) meiotic proteins in the genome of the seemingly asexual bdelloids suggests that the meiotic machinery in this group assumed new functions and might be employed for a very efficient DNA repair of double‐strand breaks on chromosomes after periods of extreme desiccation; they might be deployed for ameiotic egg production as well. Bdelloids have a very efficient DNA repair and can survive intense ionizing radiation and extreme desiccation . The possible acquisition of new functions by meiotic proteins can weaken the current approach, but, considering only metazoans, this phenomenon seems to have occurred only once among a very large amount of lineages.…”

GenomeScope 2.0 and Smudgeplots: Reference-free profiling of polyploid genomes

“…The methods to analyze polyploid genomes typically rely on mapping reads to a haploid reference. However obtaining a complete haploid reference is usually a challenging task (Claros et al 2012) as the assembly often results in mixed ploidy levels among the assembled sequences depending on the parameter settings (see (Nowell et al 2018) for an example). Genome assembly has an extra layer of complexity when the basic genomic features of the species are unknown (e.g.…”