No abstract

Deviations of genotypic frequencies from Hardy-Weinberg equilibrium (HWE) expectations could reveal important aspects of the biology of populations. Deviations from HWE due to heterozygote deficits have been recorded for three plant-parasitic nematode species. However, it has never been determined whether the observed deficits were due (i) to the presence of null alleles, (ii) to a high level of consanguinity and/or (iii) to a Wahlund effect. The aim of the present work was, while taking into the possible confounding effect of null alleles, to disentangle consanguinity and Wahlund effect in natural populations of those three economically important cyst nematodes using microsatellite markers: Globodera pallida, G. tabacum and Heterodera schachtii, pests of potato, tobacco and sugar beet, respectively. The results show a consistent pattern of heterozygote deficiency in the three nematode species sampled at the spatial scale of the host plant. We demonstrate that the prevalence of null alleles is weak and that heterozygote deficits do not have a single origin. Our results suggested that it is restricted dispersal that leads to heterozygote deficits through both consanguinity and substructure, which effects can be linked to soil movement, cyst density, and the number of generations per year. We discuss potential implications for the durability of plant resistances that are used to protect crops against parasites in which mating between relatives occur. While consanguineous mating leads to homozygosity at all loci, including loci governing avirulence/virulence, which favours the expression of virulence when recessive, the Wahlund effect is expected to have no particular effect on the adaptation of nematodes to resistances.

The sustainability of modern agriculture relies on strategies that can control the ability of pathogens to overcome chemicals or genetic resistances through natural selection. This evolutionary potential, which depends partly on effective population size (N e), is greatly influenced by human activities. In this context, wild pathogen populations can provide valuable information for assessing the long‐term risk associated with crop pests. In this study, we estimated the effective population size of the beet cyst nematode, Heterodera schachtii, by sampling 34 populations infecting the sea beet Beta vulgaris spp. maritima twice within a one‐year period. Only 20 populations produced enough generations to analyze the variation in allele frequencies, with the remaining populations showing a high mortality rate of the host plant after only 1 year. The 20 analyzed populations showed surprisingly low effective population sizes, with most having N e close to 85 individuals. We attribute these low values to the variation in population size through time, systematic inbreeding, and unbalanced sex‐ratios. Our results suggest that H. schachtii has low evolutionary potential in natural environments. Pest control strategies in which populations on crops mimic wild populations may help prevent parasite adaptation to host resistance.

The effective size of a population is the size of an ideal population which would undergo genetic drift at the same rate as the real population. The balance between selection and genetic drift depends on the effective population size (N e ), rather than the real numbers of individuals in the population (N). The objectives of the present study were to estimate N e in the potato cyst nematode Globodera pallida and to explore the causes of a low N e /N ratio in cyst nematodes using artificial populations. Using a temporal analysis of 24 independent populations, the median N e was 58 individuals (min N e ¼ 25 and max N e ¼ 228). N e is commonly lower than N but in the case of cyst nematodes, the N e /N ratio was extremely low. Using artificial populations showed that this low ratio did not result from migration, selection and overlapping generations, but could be explain by the fact that G. pallida populations deviate in structure from the assumptions of the ideal population by having unequal sex ratios, high levels of inbreeding and a high variance in family sizes. The consequences of a low N e , resulting in a strong intensity of genetic drift, could be important for their control because G. pallida populations will have a low capacity to adapt to changing environments.

Studying wild pathogen populations in natural ecosystems offers the opportunity to better understand the evolutionary dynamics of biotic diseases in crops and to enhance pest control strategies. We used simulations and genetic markers to investigate the spatial and temporal population genetic structure of wild populations of the beet cyst nematode Heterodera schachtii on a wild host plant species, the sea beet (Beta vulgaris spp. maritima), the wild ancestor of cultivated beets. Our analysis of the variation of eight microsatellite loci across four study sites showed that (i) wild H. schachtii populations displayed fine‐scaled genetic structure with no evidence of substantial levels of gene flow beyond the scale of the host plant, and comparisons with simulations indicated that (ii) genetic drift substantially affected the residual signals of isolation‐by‐distance processes, leading to departures from migration–drift equilibrium. In contrast to what can be suspected for (crop) field populations, this showed that wild cyst nematodes have very low dispersal capabilities and are strongly disconnected from each other. Our results provide some key elements for designing pest control strategies, such as decreasing passive dispersal events to limit the spread of virulence among field nematode populations.