ASEXEVOL

Sexual reproduction allows elimination of deleterious mutations and genomic plasticity in animals through meiotic recombination and exchange of alleles. Hence, absence of meiosis and sexual reproduction is viewed as an evolutionary dead end in animals. Challenging these views, a few animals are considered as ancient strict asexuals. Their genomes may hold the secrets of survival and adaptation in the absence of sexual reproduction. The genome sequence of the root-knot nematode Meloidogyne incognita is the only one currently available for an animal that reproduces exclusively asexually. This notorious pest, causing billions of € damage to agriculture annually reproduces without meiosis via parthenogenesis. Annotation and analysis of its genome, coordinated by our laboratory, revealed a singular architecture, mainly constituted of pairs of similar yet divergent and re-arranged regions that might represent former allelic haplotypes or result from past hybridization. In Bdelloid rotifers, another animal with strict asexual reproduction, a similar genome structure in multiple re-arranged and divergent copies has been observed. Such a structure in multiple copies could favor functional divergence between corresponding gene copies through neo- or sub-functionalization, exactly as for paralogous genes. This kind of phenomenon could represent a mechanism of genomic plasticity despite absence of sex. However, it has never been tested at the whole genome scale in an animal. Surprisingly, root-knot nematodes with obligate asexual reproduction have a wider host range and geographical distribution than their “sexual” cousins. Whether these features, contradictory with the supposed benefits of sexual reproduction, are correlated to the observed peculiar genomic structure is unknown. In this project, we propose to combine whole genome and transcriptome data in Meloidogyne to assess whether the observed sequence divergence between pairs has functional consequences on corresponding gene copies and provides adaptability in an asexually-reproducing animal. We will first establish an inventory of genes present in multiple copies due to the peculiar genomic structure of M. incognita. We will then assess whether some of these diverged copies potentially present divergent functions, by analyzing their rate of non-synonymous versus synonymous mutations. Using RNA-seq expression data obtained from different developmental stages of M. incognita, we will assess whether divergent copies at the nucleotide level present different expression patterns. Identification of gene copies with different expression patterns will provide the first evidence at a whole genome scale for a functional consequence of the peculiar genome structures observed in asexually-reproducing animals. To determine whether the genome architecture of M. incognita can be linked to its wider host plant range compared to its sexual cousin, M. hapla, we will infest different host plants with M. incognita and generate the corresponding parasitic transcriptomes using RNA-seq technique. The selected host plants are either hosts compatible both with M. hapla and M. incognita (Tomato, Pepper) or hosts compatible only with M. incognita (Watermelon, Rice). If, through comparison of RNA-seq transcriptomes, we identify structure-specific M. incognita gene copies expressed differentially on host plants incompatible with M. hapla, our analysis will show that the genome structure in pairs, observed in M. incognita, can provide adaptability to a strictly parthenogenetic animal. With the unique genomics and transcriptomics resources we have generated, our project represents an unparalleled opportunity to provide the first models and highlight the possible mechanisms that would allow asexually-reproducing species to evolve and adapt in the absence of meiotic recombination, an important evolutionary question unresolved so far.