Sylvain Fournet

Intra- and interspecific host discrimination by host-seeking larvae of coleopteran parasitoids

Abstract Intraspecific host discrimination is widespread in solitary parasitoids whose adult females forage for and evaluate host suitability, whereas interspecific discrimination is less common. In some parasitoid species, mostly Diptera and Coleoptera, the larva performs the last step of host searching. It has been suggested that host discrimination will rarely occur in such host-seeking larvae because their low mobility results in a low host encounter rate. We determined the extent to which the larvae of Aleochara bilineata Gyllenhal (Coleoptera: Staphylinidae), a solitary parasitoid of aggregated Diptera pupae: (1) discriminated between unparasitized hosts and hosts parasitized by conspecifics; (2) used semiochemical cues to discriminate; (3) were influenced by life expectancy, presence of conspecifics and host availability in their host acceptance decision; and the extent to which (4) A. bilineata and A. bipustulata L., a species exploiting the same hosts and occurring sympatrically, showed interspecific host discrimination. A. bilineata larvae were able to discriminate between unparasitized hosts and hosts parasitized by conspecifics in a choice experiment. Such behavior has never previously been described for a coleopteran parasitoid or for a parasitoid species whose larvae perform host searching. Host discrimination in this species was not based on the presence of visual or tactile cues (e.g., entrance holes) but rather on chemical cues. The life expectancy of A. bilineata larvae was significantly shorter in the presence than in absence of hosts, and older larvae had lower parasitism success than young larvae in a 24-h experiment. However, the host acceptance decision of A. bilineata larvae was not influenced by larval age or the presence of conspecifics when the ratio of hosts per larva was greater than or equal to 1. When hosts were scarce, the degree of superparasitism increased significantly with the number of foraging conspecifics and the age of the larvae. Both species of Aleochara showed intra- and interspecific host discrimination in a choice experiment. In contrast to A. bipustulata, A. bilineata larvae more frequently parasitized hosts parasitized by A. bipustulata than those parasitized by conspecifics. We suggest that host discrimination will be frequent in solitary parasitoids with host-seeking larvae when hosts are aggregated.

A cyst nematode 'species factory' called the Andes.

The cyst nematode, Globodera pallida , is a major pest of potato, a plant native to South America. To investigate its phylogeography, an extensive sampling survey was conducted in 2002 in Peru and has laid the foundations of the ancient evolutionary history of this nematode species. We argue that the uplift of the Andes Mountains has triggered a variety of adaptive biotic radiations for Solanaceous plant-parasitic nematodes and has represented a key factor for the evolution and specialisation of Globodera species. We discuss the consequences of the wide genetic diversity observed in South American populations on the efficiency and durability of potato resistance and also the reliability of current molecular identification tools for quarantine purposes. Finally, we emphasise the need to get a more in-depth taxonomic characterisation of some of these nematode populations, and to conduct more extensive sampling in South America, especially south of Lake Titicaca, in order to understand fully potato cyst nematode evolution and their adaptation to their host plants.

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

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.

Quantitative Resistance to Plant Pathogens in Pyramiding Strategies for Durable Crop Protection

Quantitative resistance has gained interest in plant breeding for pathogen control in low-input cropping systems. Although quantitative resistance frequently has only a partial effect and is difficult to select, it is considered more durable than major resistance (R) genes. With the exponential development of molecular markers over the past 20 years, resistance QTL have been more accurately detected and better integrated into breeding strategies for resistant varieties with increased potential for durability. This review summarizes current knowledge on the genetic inheritance, molecular basis, and durability of quantitative resistance. Based on this knowledge, we discuss how strategies that combine major R genes and QTL in crops can maintain the effectiveness of plant resistance to pathogens. Combining resistance QTL with complementary modes of action appears to be an interesting strategy for breeding effective and potentially durable resistance. Combining quantitative resistance with major R genes has proven to be a valuable approach for extending the effectiveness of major genes. In the plant genomics era, improved tools and methods are becoming available to better integrate quantitative resistance into breeding strategies. Nevertheless, optimal combinations of resistance loci will still have to be identified to preserve resistance effectiveness over time for durable crop protection.

Spatial distribution and basic ecology of Heterodera schachtii and H. betae wild populations developing on sea beet, Beta vulgaris ssp. maritima

Most populations of crop pathogens have wild relative populations from which they can originate but for which basic knowledge of their ecological requirements in natura is scarce. However, the study of spatial distribution and ecology of wild pathogen populations may help control them in crops through a better understanding of the environmental factors driving population dynamics. Here, we focused on Heterodera schachtii and H. betae, two cyst nematodes that cause severe damage to sugar beet (Beta vulgaris ssp. vulgaris) crops and can develop on a wild beet relative, the sea beet (B. vulgaris ssp. maritima). We investigated the occurrence of both nematode species in the wild and explored some environmental factors that may influence their geographical distribution. To do so, we sampled the wild host B. v. ssp. maritima along the European Atlantic and North Sea coastlines. Results showed that H. schachtii mainly occurred in the colder environments of northern Europe, whereas H. betae was preferentially distributed in the warm environments of southern Europe. It was previously established that H. betae only recently appeared in The Netherlands, which are in the north of Europe. Thus, our results do not support this hypothesis. Overall, this study accurately documents the geographical occurrence of two nematode crop pest species in the wild and helps identify the main environmental factors affecting their distribution range.

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 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 (Ne), 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 Ne 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.

Adaptation to resistant hosts increases fitness on susceptible hosts in the plant parasitic nematode Globodera pallida

Abstract Trade‐offs between virulence (defined as the ability to infect a resistant host) and life‐history traits are of particular interest in plant pathogens for durable management of plant resistances. Adaptation to plant resistances (i.e., virulence acquisition) is indeed expected to be associated with a fitness cost on susceptible hosts. Here, we investigated whether life‐history traits involved in the fitness of the potato cyst nematode Globodera pallida are affected in a virulent lineage compared to an avirulent one. Both lineages were obtained from the same natural population through experimental evolution on resistant and susceptible hosts, respectively. Unexpectedly, we found that virulent lineages were more fit than avirulent lineages on susceptible hosts: they produced bigger cysts, containing more larvae and hatching faster. We thus discuss possible reasons explaining why virulence did not spread into natural G. pallida populations.

Phenotypic and Genomic Modifications Associated with Globodera pallida Adaptation to Potato Resistances

Studying phenotypic and genomic modifications associated with pathogen adaptation to resistance is a crucial step to better understand and anticipate resistance breakdown. This short review summarizes recent results obtained using experimentally evolved populations of the potato cyst nematode Globodera pallida. In a first step, the variability of resistance durability was explored in four different potato genotypes carrying the resistance quantitative trait loci (QTL) GpaVvrn originating from Solanum vernei but differing by their genetic background. The consequences of the adaptation to resistance in terms of local adaptation, cross-virulence and virulence cost were then investigated. Finally, a genome scan approach was performed in order to identify the genomic regions involved in this adaptation. Results showed that nematode populations were able to adapt to the QTL GpaVvrn, and that the plant genetic background has a strong impact on resistance durability. A trade-off between the adaptations to different resistant potato genotypes was detected, and we also showed that adaptation to the resistance QTL GpaVvrn from S. vernei did not allow adaptation to the colinear locus from S. sparsipilum (GpaVspl). Unexpectedly, the adaptation to resistance led to an increase of virulent individual’s fitness on a susceptible host. Moreover, the genome scan approach allowed the highlighting of candidate genomic regions involved in adaptation to host plant resistance. This review shows that experimental evolution is an interesting tool to anticipate the adaptation of pathogen populations and could be very useful for identifying durable strategies for resistance deployment.

Effective population size and durability of plant resistances in the potato cyst nematode Globodera pallida

The effective size of a population is the size of an ideal population which would drift at the same rate as the real population. The balance between selection and genetic drift depends on the population size expressed as the genetically effective population size (Ne), rather than the real numbers of individuals in the population (N). The objectives of the present study were to estimate Ne in the potato cyst nematode Globodera pallida using artificial populations and to explore the link between Ne and the durability of plant resistances. Using a temporal method on 24 independent pairs of initial and final populations, the median Ne was 58 individuals. Ne is commonly lower than N but in our case the Ne/N ratio was extremely low because 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 Ne could be important for the control of phytoparasitic nematodes because G. pallida populations will have a low capacity to adapt to changing environments unless selection intensity is very strong, which could be greatly beneficial for long-term use of plant resistances.