Population genomics supports clonal reproduction and multiple independent gains and losses of parasitic abilities in the most devastating nematode pest.

Georgios D Koutsovoulos,Marc Bailly‐Bechet,Djampa K Kozlowski,Regina M D G Carneiro,Marie‐Jeanne Arguel,Erika V S Albuquerque,Eder Marques,Andressa C Z Machado,Etienne G J Danchin,Laurent Duret,Philippe Castagnone‐Sereno

doi:10.1111/eva.12881

Abstract

The root‐knot nematodes are the most devastating worms to worldwide agriculture with Meloidogyne incognita being the most widely distributed and damaging species. This parasitic and ecological success seems surprising given its supposed obligatory clonal reproduction. Clonal reproduction has been suspected based on cytological observations but, so far, never confirmed by population genomics data. As a species, M. incognita is highly polyphagous with thousands of host plants. However, different M. incognita isolates present distinct and overlapping patterns of host compatibilities. Historically, four “host races” had been defined as a function of ranges of compatible and incompatible plants. In this study, we used population genomics to assess whether (a) reproduction is actually clonal in this species, (b) the host races follow an underlying phylogenetic signal or, rather represent multiple independent transitions, and (c) how genome variations associate with other important biological traits such as the affected crops and geographical distribution. We sequenced the genomes of 11 M. incognita isolates across Brazil that covered the four host races in replicates. By aligning the genomic reads of these isolates to the M. incognita reference genome assembly, we identified point variations. Analysis of linkage disequilibrium and 4‐gametes test showed no evidence for recombination, corroborating the clonal reproduction of M. incognita. The few point variations between the isolates showed no significant association with the host races, the geographical origin of the samples, or the crop on which they have been collected. Addition of isolates from other locations around the world confirmed this lack of underlying phylogenetic signal. This suggests multiple gains and losses of parasitic abilities and adaptations to different environments account for the broad host spectrum and wide geographical distribution of M. incognita and thus to its high economic impact. This surprising adaptability without sex poses both evolutionary and agro‐economic challenges.

Highlights

Nematodes annually cause severe damages to the world agricultural production, and the root‐knot nematodes (RKN, genus Meloidogyne) are the most economically harmful species in all temperate and tropical producing areas (Moens et al, 2009; Jones et al, 2013)
The dif‐ ferent analyses we performed at the population genomics level con‐ verge in supporting the lack of recombination and genetic exchanges in M. incognita
In sexual “recombining” species, the mitochondrial ge‐ nome accumulates mutations much faster than the nuclear genome. This is true in the model nematode C. elegans where the mito‐ chondrial mutation rate is at least two orders of magnitude higher than the nuclear mutation rate (Denver et al, 2009; Denver, Morris, Lynch, & Thomas, 2004)

Summary

| INTRODUCTION

Nematodes annually cause severe damages to the world agricultural production, and the root‐knot nematodes (RKN, genus Meloidogyne) are the most economically harmful species in all temperate and tropical producing areas (Moens et al, 2009; Jones et al, 2013). We used population genomics analyses to investigate (a) whether the supposed absence of meiosis is sup‐ ported by the properties of genomewide single‐nucleotide variant (SNV) markers between isolates, (b) the level of variation between isolates at the whole‐genome level and (c) whether these varia‐ tions follow a phylogenetic signal underlying life‐history traits such as the host compatibility patterns, the geographical distribu‐ tion or the current host crop plant To address these questions, we have sequenced the genomes of 11 isolates covering the four M. incognita host races in replicates from populations parasitizing six crops across different locations in Brazil (Figure 1). While associ‐ ation between phylogenetic signal and patterns of host compatibili‐ ties would tend to show stable inheritance from ancestral states, the nonassociation would support multiple gains and losses of parasitic abilities and substantial adaptability

| MATERIALS AND METHODS

| DISCUSSION

Findings

CONFLICT OF INTEREST