The complex hybrid origins of the root knot nematodes revealed through comparative genomics

Abstract

Meloidogyne root knot nematodes (RKN) can infect most of the world's agricultural crop species and are among the most important of all plant pathogens. As yet however we have little understanding of their origins or the genomic basis of their extreme polyphagy. The most damaging pathogens reproduce by mitotic parthenogenesis and are suggested to originate by interspecific hybridizations between unknown parental taxa. We sequenced the genome of the diploid meiotic parthenogen Meloidogyne floridensis, and use a comparative genomic approach to test the hypothesis that it was involved in the hybrid origin of the tropical mitotic parthenogen M. incognita. Phylogenomic analysis of gene families from M. floridensis, M. incognita and an outgroup species M. hapla was used to trace the evolutionary history of these species' genomes, demonstrating that M. floridensis was one of the parental species in the hybrid origins of M. incognita. Analysis of the M. floridensis genome revealed many gene loci present in divergent copies, as they are in M. incognita, indicating that it too had a hybrid origin. The triploid M. incognita is shown to be a complex double-hybrid between M. floridensis and a third, unidentified parent. The agriculturally important RKN have very complex origins involving the mixing of several parental genomes by hybridization and their extreme polyphagy and agricultural success may be related to this hybridization, producing transgressive variation on which natural selection acts. Studying RKN variation via individual marker loci may fail due to the species' convoluted origins, and multi-species population genomics is essential to understand the hybrid diversity and adaptive variation of this important species complex. This comparative genomic analysis provides a compelling example of the importance and complexity of hybridization in generating animal species diversity more generally