On the evolutionary dynamics of Adineta vaga (Bdelloidea)

Abstract

Bdelloid rotifers are notorious for their long-term evolution in the absence of meiosis, which led John Maynard Smith to dub them “evolutionary scandals” as it seemed to contravene the general prevalence of sexual reproduction in the animal kingdom. Although bdelloids do not exchange genes via conventional sex, evidence is mounting for their ongoing accumulation of non-metazoan genes through horizontal gene transfers. These transfers have been linked to the capacity of bdelloid rotifers to withstand desiccation at any stage in their life cycle, as desiccation creates multiple DNA double-strand breaks that are repaired upon rehydration. Furthermore, desiccated individuals group together and are easily dispersed by wind over extended geographical ranges. To understand the consequences of asexuality and desiccation on the evolution of bdelloid rotifers, my PhD thesis addressed several questions investigating the evolutionary and ecological dynamics of the widespread bdelloid lineage Adineta vaga, for which a draft reference genome was already available.First, by designing new genetic markers I detected, for the first time, apparent genetic exchanges among Adineta individuals sampled in the wild. I observed allele sharing that could be explained by inter-individual recombination among conspecific bdelloid individuals, as delimited using a tree-based approach as well as an allele sharing-based approach (haplowebs and a conspecificity matrix). Moreover, I detected incongruence in species boundaries inferred from distinct genetic markers, suggesting the occurrence of DNA transfers between species. These results were published in Current Biology and are presented in Chapter 1. A research group from Imperial College London challenged those results, and therefore I devoted Chapter 2 to discuss these criticisms and performed additional experiments to validate my observations, as presented in Chapter 3.Second, I further investigated the possible mechanisms underlying the observed patterns of genetic exchanges by conducting genomic analyses of the regions (<10 kb) surrounding the genetic markers I had previously studied. This revealed intermixed signatures of DNA transfers, gene conversion and asexual evolution, highlighting the highly dynamic nature of the genome of bdelloid rotifers as presented in Chapter 1.Third, the impact of various ecological parameters (dispersal, reproduction, survival, species interactions and environmental conditions) on the community structure of Adineta lineages was studied and presented in Chapter 4. A simple ecological model, combined with quantitative field data, was usedto highlight the spatio-temporal dynamics of Adineta spp. natural communities. Overall, the model fitted empirical data well, showing that dispersal is the most important factor shaping bdelloid communities. Individuals disperse passively over long ranges, but the frequency of dispersal is correlated with geographical distance, i.e. there ismore dispersal among close-by communities. In addition, I found that habitat preference varies among Adineta species and seems to have an effect on community dynamics. I also found that community dynamics vary with seasons: colonization and population expansion increase from spring to autumn, whereas strong bottlenecks happen in winter. Finally, very local sampling in the town of Namur revealed the dominance of one Adineta species in this area that is also present, albeit less abundantly, in other places around Belgium. The distribution of Adineta within Belgium is briefly presented in annex Chapter 5.In this PhD thesis, I developed and applied new methods to study the evolutionary and ecological dynamics of bdelloid rotifer individuals from the genus Adineta, from genomes to natural communities. Overall, my results and published data suggest that despite their asexuality, the evolution of bdelloid rotifers reveals apparent genome diversification through chromosomal re-arrangements and DNA transfers; genome homogenization through gene conversion; community diversification through passive dispersal; and habitat specialization. Desiccation may play an important role in all these processes, reinforcing its potential impact on the evolution of bdelloid rotifers. Yet, additional studies quantifying the exact consequences of desiccation at different levels (from genes to communities) will be necessary to resolve the mystery of these “evolutionary scandals”.

Date of Award	4 May 2018
Original language	English
Awarding Institution	University of Namur
Sponsors	Fund for Research Training in Industry and Agriculture (FRIA) & ARC (Actions de recherche concentrées)
Supervisor	Karine Van Doninck (Supervisor), Jean-Francois Flot (Co-Supervisor), Frederik De Laender (President), Diego FONTANETO (Jury) & Yannis Michalakis (Jury)