Heterozygote deficits in cyst plant‐parasitic nematodes: possible causes and consequences

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.

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

“…The life cycle of H. schachtii and the low dispersal ability of larvae result in inbreeding and/or substructuring (Wahlund effect), which leads to an increase of heterozygote deficiencies over time (Plantard and Porte ; Montarry et al. ). However, this increase in heterozygote deficiencies is possible only in populations that produce new generations.…”

“…A recent study conducted both on field and wild populations suggested that HW departures also may be explained by genetic substructuring due to Wahlund effects at the scale of the host plant (Montarry et al. ).…”

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

“…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. Interestingly, a recent study documented a Wahlund effect in some wild H. schachtii populations sampled at the host scale, suggesting that active dispersal of this species can also be extremely limited even between subpopulations that occupy the same host plant (Montarry et al., ). These subpopulations may thus correspond to the smallest genetic unit at which individuals interbreed, that is the actual boundaries of populations in H. schachtii (Waples & Gaggiotti, ).…”

“…Field populations of H. schachtii have a similar substructuring patterns than wild populations, suggesting that active dispersal capabilities of nematodes are equivalent in wild and field conditions (Montarry et al., ). By contrast, in agrosystems, low genetic differentiation suggests that nematode populations are connected through gene flow among fields separated by distances that reach 150 km.…”

“…In all, 1,754 H. schachtii individuals were identified and successfully genotyped at eight microsatellite loci, named Hs33, Hs36, Hs55, Hs56, Hs68, Hs84, Hs111, and Hs114 and described in Montarry et al. (). Microsatellites PCR products were analyzed on an ABI Prism ® 3130xl sequencer (Applied Biosystems, Foster City, CA, USA).…”