Understanding and quantifying consanguineous mating in phytoparasitic nematodes for an improved plant resistances management

In theory, low active dispersal capabilities of cyst nematodes could lead to a high frequency of mating between siblings (consanguinity) and/or to a spatial sub-structuration of the population (Walhund effect). Previous studies have documented strong heterozygote deficits in natural populations of Globodera pallida, G. tabacum and Heterodera schachtii which attack potato, tobacco and sugar beet, respectively.

The objective of this project was to determine if the deficit was due to:

• the presence of null alleles,
• a high rate of consanguineous mating and/or
• a sub-structuration of the genetic variability at a finer scale than the scale of the rhizosphere.

Nineteen G. pallida populations (including 4 Peruvian populations), 13 G. tabacum and 34 H. schachtii were sampled at the scale of the host plant and 30 individuals per population were genotyped using new sets of microsatellite markers. Those data were used to show that the heterozygote deficits were not due to the presence of null alleles and to disentangle consanguinity and Wahlund effect.

We show that low dispersal leads to heterozygote deficits caused either by mating between siblings (consanguinity) or by sub-structuration at the scale of the host plant, depending on the number of generations realized by the species. While G. pallida performs one generation per year (monovoltine species), G. tabacum and H. schachtii perform several generations per year (polyvoltine species).

Likelihood surfaces for (A) a French Globodera pallida population, (B) a Peruvian G. pallida population, (C) a Globodera tabacum population and (D) an Heterodera schachtii population. The darkest spot indicates the joint maximum likelihood.

Our results indicate that consanguinity is prevalent in the monovoltine species (A) whereas it is sub-structuration that is detected in polyvoltine species (C and D). The case of the Peruvian G. pallida populations suggests that limited or superficial soil movements (fields in Peru are located in a hilly region where only hand-ploughing occurs) also favors to sub-structuration (B). The observed sub-structuration for the polyvoltine species could hide undetectable high rates of consanguinity. Theoretical and experimental approaches will be used to test this hypothesis.

The presence of a high frequency of mating between siblings in phytoparasitic nematodes has consequences in terms of breakdown of plant resistances. Consanguineous mating lead all loci to homozygozity, including those involved in virulence, which is often recessive and thus favored at the homozygous state

Montarry J., Jan P.L., Gracianne C., Overall A.D.J., Bardou-Valette S., Olivier E., Fournet S., Grenier E. and Petit E.J. (2015) Heterozygote deficits in cyst plant-parasitic nematodes: possible causes and consequences. Molecular Ecology24: 1654-1667. DOI

SPE Project 2012-2013 ‘Les faibles capacités actives de dispersion des nématodes entrainent-elles une sous-structuration des populations ?’ managed by Josselin Montarry (UMR IGEPP) and Eric Petit (UMR ESE).

This article is a part of the thesis manuscript of Cécile Gracianne, untitled ‘De la génétique des populations à la gestion durable des résistances : intérêt de l’étude des populations sauvages des pathogènes des cultures. Cas de deux nématodes à kystes et de leur hôte sauvage commun.’ and defended the 10^th april 2015.