Genetic tests of ancient asexuality in Root Knot Nematodes reveal recent hybrid origins

Background: The existence of "ancient asexuals", taxa that have persisted for long periods of evolutionary history without sexual recombination, is both controversial and important for our understanding of the evolution and maintenance of sexual reproduction. A lack of sex has consequences not only for the ecology of the asexual organism but also for its genome. Several genetic signatures are predicted from long-term asexual (apomictic) reproduction including (i) large "allelic" sequence divergence (ii) lack of phylogenetic clustering of "alleles" within morphological species and (iii) decay and loss of genes specific to meiosis and sexual reproduction. These genetic signatures can be hard to assess since it is difficult to demonstrate the allelic nature of very divergent sequences, divergence levels may be complicated by processes such as inter-specific hybridization, and genes may have secondary roles unrelated to sexual reproduction. Apomictic species of Meloidogyne root knot nematodes have been suggested previously to be ancient asexuals. Their relatives reproduce by meiotic parthenogenesis or facultative sexuality, which in combination with the abundance of nematode genomic sequence data, makes them a powerful system in which to study the consequences of reproductive mode on genomic divergence. Results: Here, sequences from nuclear protein-coding genes are used to demonstrate that the first two predictions of ancient asexuality are found within the apomictic root knot nematodes. Alleles are more divergent in the apomictic taxa than in those species exhibiting recombination and do not group phylogenetically according to recognized species. In contrast some nuclear alleles, and mtDNA, are almost identical across species. Sequencing of Major Sperm Protein, a gamete-specific gene, from both meiotic and ameiotic species reveals no increase in evolutionary rate nor change in substitution pattern in the apomictic taxa, indicating that the locus has been maintained by selection. Conclusion: The data strongly suggests the tropical root knot nematode apomicts have a recent origin and are not anciently asexual. The results support that interspecific hybridization has been involved in the origin of this asexual group and has played a role in shaping the patterns of genetic diversity observed. This study suggests that genetic signatures of ancient asexuality must be taken with caution due to the confounding effect of interspecific hybridization, which has long been implicated in the origins of apomictic species.