Temporal sampling helps unravel the genetic structure of naturally occurring populations of a phytoparasitic nematode. 1. Insights from the estimation of effective population sizes

Abstract

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.

Temporal sampling helps unravel the genetic structure of naturally occurring populations of a phytoparasitic nematode. 2. Separating the relative effects of gene flow and genetic drift

“…Our results suggest that passive dispersal through cysts movement is actually limited in the wild. This is consistent with the small effective population sizes ( N e ranging from 50 to 400) observed in wild H. schachtii populations (Jan et al., ). Small effective sizes are one consequence of limited gene flow among populations and support the hypothesis that H. schachtii is a species constituted of genetically disconnected populations in the wild, even at very small spatial scale.…”

“…In this beach, the observed slope of IBD pattern and mean F ST in 2013 laid out the 95% confidence interval for N e > 500 individuals (data not shown). Overall, simulations of the evolution of allelic frequencies under pure drift are consistent with observed patterns of population genetic structure, at least for effective population sizes that are in the range of what has been estimated for these populations (Jan et al., ).…”

“…This may even be more pronounced in populations that are founded by seeds (plants) or cysts (nematodes), which are forms that can survive belowground until local conditions allow their development. Once a potential host plant grows in a place where cysts are present, the local multiplication of nematodes may generate a patchy distribution of populations and heterogeneity in infestation levels among hosts, as observed in several nematode species (Gavassoni, Tylka, & Munkvold, ; Jan et al., ; Villate et al., ). Most nematode movements in coastal populations may be thus related to exceptional events such as high tides during storms.…”

“…maritima plants on four different beaches in Normandy, France. Distances separating the four beaches (Montfarville, Granville Nord, Granville Sud, and Saint Léonard) ranged from 300 m to 150 km (for more details, see Jan et al., ) to mimic the geographical sampling scheme that was performed in a previous investigation on H. schachtii conducted in sugar beet fields (Plantard & Porte, ). Populations of the host plant, the sea beet, are often composed of individuals clustered in geographically and genetically distinct patches (De Cauwer et al., ).…”

“…However, because drift effects accumulate with time and because our sampling period covered between four and ten nematode generations only (see Jan et al., ), these variations may not be detectable. To prevent this problem, we simulated the evolution of allele frequencies observed in 2012 under four to ten generations under a model of pure genetic drift.…”