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Inbreeding and inbreeding depression are processes in small populations of particular interest for a range of human activities such as animal breeding, species conservation or pest management. In particular, biological control programs should benefit from a thorough understanding of the causes and consequences of inbreeding because natural enemies experience repetitive bottlenecks during importation, laboratory rearing, and introduction. Predicting the effect of inbreeding in Hymenopteran parasitoid wasps, frequently used in biological control programs, is nonetheless a difficult endeavor. In haplodiploid parasitoids, the purge of deleterious alleles via haploid males should reduce genetic load, but if these species also have complementary sex determination (CSD) abnormal diploid males will be produced, which may jeopardize the success of biological control introductions. Mastrus ridens is such a parasitoid wasp with CSD, introduced to control the codling moth, Cydia pomonella (L.). We studied its life history traits in the laboratory under two conditions: inbred (full sib) and outbred (non-sib) crosses, across five generations, in order to examine the consequences of inbreeding in this species. We found that in inbred lines non reproducing females live less, the number of daughters produced was lower, and that sex ratio (proportion of males) and proportion of diploid males were higher. Diploid males were able to produce fertile daughters, but fewer than haploid males. Lineage survival was similar for inbred and outbred lines across the five generations. The most significant decrease in fitness was thus a consequence of the production of diploid males, but this effect was not as extreme as in most other species with CSD, due to the fertility of diploid males. This study highlights the importance of determining the type of sex determination in parasitoid wasps used for biological control, and the importance of maintaining genetic diversity in species with CSD when importation or augmentation is the goal. This article is protected by copyright. All rights reserved.

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100047) 1. Sib-mating avoidance is a pervasive behaviour that likely evolves in species subject to inbreeding depression. Laboratory studies have provided elegant demonstrations of sib-mating avoidance, but small-scale bioassays often minimize the costs associated with mate finding and choice, which could lead to spurious findings. 2. We used the hymenopteran parasitoid wasp Venturia canescens as a model organism, because previous laboratory studies revealed that sib-mating led to a 25% decrease in fertile offspring, and that sib-mating was partially avoided. 3. Our study consisted of a mate choice experiment in laboratory cages to determine if kin discrimination occurs in this species. We further performed a field study in which 86 wild-caught males, 155 wild-caught females and their 226 daughters were genotyped at eighteen microsatellite loci. With these data, we reconstructed the genotype of each female ′s mate and estimated the relatedness of each mating pair. 4. Mate choice experiments confirmed that females are capable of discriminating kin. Time to mating depended on the frequency of female encounters with related and unrelated males. Contrary to previously published results, however, no sib-mating avoidance was detected. In the field, the effective rate of sib-mating did not differ from the probability that sibs encounter one other at random, which corroborates the absence of sib-mating avoidance. We also detected a weak but significant male bias in dispersal, which could reduce encounters between sibs. 5. Our results suggest that, despite kin discrimination, V. canescens tolerates sib-mating in the field. The weak male-biased dispersal cannot explain entirely this pattern. This raises the question as to why kin discrimination is maintained in this species. It further calls into question the idea that inbreeding depression occurs in most species with single-locus complementary sex determination.

Inbreeding depression is a major concern in almost all human activities relating to plant and animal breeding. The biological control of pests with natural enemies is no exception, because populations of biocontrol agents experience a series of bottlenecks during importation, rearing, and introduction. A classical biological control program for the Comstock mealybug Pseudococcus comstocki (Hemiptera: Pseudococcidae) was initiated in France in 2008, based on the introduction of an exotic parasitoid, Allotropa burrelli Mues. (Hymenoptera: Platygastridae), a haplodiploid parasitoid imported from Japan. We evaluated the sensitivity of A. burrelli to inbreeding, to optimize rearing and release strategies. We compared several morphological and life‐history traits between the offspring of siblings and the offspring of unrelated parents. We took into account the low level of genetic variability due to the relatively small size of laboratory‐reared populations by contrasting two types of pedigree: one for individuals from a strain founded from a single field population, and the other generated by hybridizing individuals from two strains founded from two highly differentiated populations. Despite this careful design, we obtained no evidence for a negative impact of inbreeding on laboratory‐reared A. burrelli. We discussed the results in light of haplodiploid sex determination and parasitoid mating systems, and classical biological control practices.

Sex determination is ruled by haplodiploidy in Hymenoptera, with haploid males arising from unfertilized eggs and diploid females from fertilized eggs. However, diploid males with null fitness are produced under Complementary Sex Determination (CSD), whenindividuals are homozygous for this locus. Diploid males are expected to be more frequent in genetically eroded populations (such as islands and captive populations), as genetic diversity at the csd locus should be low. However, only a few studies have focused on the relation between population size, genetic diversity and the proportion of diploid males in the field. Here, we developed new microsatellites markers in order to assess and compare genetic diversity and diploid male proportion in populations from three distinct habitat types (mainland, island or captive), in the parasitoid waspVenturia canescens. Eroded genetic diversity and higher diploid male proportion were found in island and captive populations, and habitat type had large effect on genetic diversity. Therefore, diploid male proportion reflects the decreasing genetic diversity in small and isolated populations. Thus, Hymenopteran populations can be at high extinction risk due to habitat destruction or fragmentation.

International audience; The parasitoid wasp Mastrus ridens (Hymenoptera: Ichneumonidae) is a particularly well-suited biological model to document the history and evolution of populations used in classical biological control, repeatedly moved from laboratory to laboratory worldwide and introduced in various environments. This specialist ectoparasitoid of the codling moth was first imported from Kazakhstan to the USA in the 1990's, and then sent to Argentina, Chile and New Zealand. More recently, it was sent to Australia and France from other laboratory colonies, and imported again from field collections in Kazakhstan to Chile. Here, we used DNA sequencing to confirm the taxonomic identity of several populations used for biological control worldwide, and developed microsatellite markers for population genetics studies. A multiplex PCR amplifying 11 polymorphic markers was designed. These markers were used to compare the genetic diversity of laboratory and field populations and evaluate genetic differentiation between them. Results showed that laboratory populations with the longest rearing history had lower genetic diversity. Moreover, the geno-typing of males with the markers revealed the occurrence of diploid males, which was further confirmed by flow cytometry, suggesting complementary sex determination (CSD) in this species. The percentage of diploid males in the populations ranged from 4% to 25% and were negatively correlated with diversity indices, which is consistent with a single-locus CSD and genetic bottlenecks in laboratory rearings. Molecular tools proved to be suitable and reliable for genetic diversity analyses in M. ridens, and should be implemented more frequently in classical biological control programs.

International audience; Mating failures at low density – a common type of Allee effect – can reduce the per capita reproductive rate and, if severe enough, doom small populations to extinction. Parasitoids frequently undergo low densities triggered by their typically cyclic dynamic and/or the bottlenecks they experience when introduced for the biological control of agricultural pests. However, most parasitoid species belong to the order Hymenoptera and reproduce via arrhenotokous parthenogenesis: unfertilized eggs develop into males. A common belief is therefore that parasitoids are immune to the mate-finding Allee effect because mating failures yields more males, which should in turn restore mating success. Yet, meta-analyses of biological control introductions suggest that hymenopteran parasitoids are as extinctionprone as non-parthenogenetic species. Here we developed a population dynamic model to investigate the advantage of arrhenotokous parthenogenesis for parasitoid species that experience a mate-finding Allee effect. We show that: i) the conditions for which mating failures drive parasitoids to extinction are marginally more restricted for parthenogenetic species than for non-parthenogenetic ones; ii) parthenogenesis increases the resistance of parasitoids to accidental decrease in density and to invasions by a competing species whether or not parthenogenetic; and iii) parthenogenesis favors population establishment in new environments, whether or not already occupied. Hence even if arrhenotokous parthenogenesis is not as effective as expected to limit parasitoid extinctions caused by mating failures, it provides a significant advantage for population establishment and persistence.

International audience; Extinctions have no simple determinism, but rather result from complex interplays between environmental factors and demographic‐genetic feedback that occur at small population size. Inbreeding depression has been assumed to be a major trigger of extinction vortices, yet very few models have studied its consequences in dynamic populations with realistic population structure. Here we investigate the impact of Complementary Sex Determination (CSD) on extinction in parasitoid wasps and other insects of the order Hymenoptera. CSD is believed to induce enough inbreeding depression to doom simple small populations to extinction, but we suggest that in parasitoids CSD may have the opposite effect. Using a theoretical model combining the genetics of CSD and the population dynamics of host‐parasitoid systems, we show that CSD can reduce the risk of parasitoid extinction by reducing fluctuations in population size. Our result suggests that inbreeding depression is not always a threat to population survival, and that considering trophic interactions may reverse some pervasive hypotheses on its demographic impact.

International audience; Environmental variation is classically expected to affect negatively population growth and to increase extinction risk, and it has been identified as a major determinant of establishment failures in the field. Yet, recent theoretical investigations have shown that the structure of environmental variation and more precisely the presence of positive temporal autocorrelation might alter this prediction. This is particularly likely to affect the establishment dynamics of biological control agents in the field, as host–parasitoid interactions are expected to induce temporal autocorrelation in host abundance. In the case where parasitoid populations display overcompensatory dynamics, the presence of such positive temporal autocorrelation should increase their establishment success in a variable environment. We tested this prediction in laboratory microcosms by introducing parasitoids to hosts whose abundances were manipulated to simulate uncorrelated or positively autocorrelated variations in carrying capacity. We found that environmental variability decreased population size and increased parasitoid population variance, which is classically expected to extinction risk. However, although exposed to significant environmental variation, we found that parasitoid populations experiencing positive temporal autocorrelation in host abundance were more likely to persist than populations exposed to uncorrelated variation. These results confirm that environmental variation is a key determinant of extinction dynamics that can have counterintuitive effects depending on its autocorrelation structure.

5 pages; International audience; Male insects must find and mate females to have some descendants; male fitness therefore depends on the number of females they inseminate. Males are for this reason expected to optimize the behaviors related to mate location, orientation and copulation. Although optimization of the reproductive behavior of males has long been neglected in the literature, recent studies suggest a renewed interest for this idea. Here we discuss the parallel between male mate-finding and mating strategies in insects and optimal foraging theory (OFT), a class of models which formalize the behavior of organisms seeking and exploiting resources, generally food. We highlight the different facets of male mating systems allowing such a parallel, and claim for a unifying approach of foraging behavior. Finally, we discuss novel research perspective emerging from the application of OFT to male reproductive behavior.

International audience; In insects, mating often occurs after natal dispersal, and hence relies on a coevolved combination of sexual communication and movement allowing mate encounter. Volatile sex pheromones are widespread, generally emitted by females and triggering in-flight orientation of conspecific males. In parasitoid wasps, unmated females can start laying unfertilized eggs via parthenogenesis so that host patches could serve as sites of rendezvous for mating. Males could therefore use cues associated with host patches to focus their search on females that have successfully found oviposition sites. We hypothesized that in parasitoids exploiting herbivorous hosts, sex pheromones, and herbivore-induced plant volatiles (HIPV) should act in synergy, triggering male orientation toward ovipositing females. We tested this hypothesis with the aphid parasitoid Lysiphlebus testaceipes. Results from both field and laboratory experiments show that males are strongly attracted to virgin females, but that volatiles from aphid-infested plants have no effect on male orientation, neither has a cue, nor in interaction with the female sex pheromone. The absence of synergy between sex pheromones and HIPV contrasts with results on other species and raises interesting questions on mating systems and sexual selection in parasitoid wasps.

Background Single-locus complementary sex determination (sl-CSD), which occurs in some insects of the order Hymenoptera, imposes a heavy genetic load that can drive small populations to extinction. The core process in these species is the development of individuals homozygous at the sex-determining locus into unfit diploid males. The risk of extinction of populations with sl-CSD is theoretically much higher if diploid males are viable and capable of mating but sterile, because diploid males then decrease the reproductive output of both their parents and the females with which they mate. Results In the parasitoid wasp Venturia canescens (Hymenoptera: Ichneumonidae), diploid males resembled their haploid counterparts in most respects, but their mating success was nevertheless lower than that of haploid males, especially when the two types of males were placed in competition. Furthermore, although diploid males transferred viable sperm during copulation, they sired no daughters: the females with which they mated produced only sons, like virgin females. A simulation model combining behavior, genetics and demography demonstrated that for two alternative hypotheses concerning the fertilization success of diploid sperm, the mating success of diploid males strongly affected population dynamics. Conclusion The performance of diploid males should be estimated in competitive situations. It is a crucial determinant of the probability of extinction. Electronic supplementary material The online version of this article (doi:10.1186/s12898-014-0032-6) contains supplementary material, which is available to authorized users.

National audience; Utilization of microcosms to test invasion biology hypotheses. Understanding the factors underlying establishment and spread of exotic species in order to predict invasion risks is a major goal in invasion biology. Many theoretical studies investigated the ecological and evolutionary components of these factors and their impact on the invasive process. Yet, hypothesis tests through experimental approaches are still scarce because of the practical and ethical difficulties associated with the introduction of exotic species in nature. Thus, most empirical results come from a posteriori analyses of fortuitous invasions, which allow correlative approaches at best and give no information about invasion failures. In this paper, we propose microcosms, i.e. reproducible controlled simplified environments, as an alternative to experimental introductions in natura. From a review of the literature, we discuss the distinctive features of microcosms to test theoretical predictions about invasion. Our analysis focuses on studies involving populations in transitory dynamics after a demographic bottleneck and/or subject to an adaptive challenge, two key characteristics of invasive processes. Despite their small number, these studies have been used successfully to explore the influences of various factors, mainly related to the introduction site characteristics (its abiotic conditions and their spatial and temporal heterogeneity), and to a lesser extent to the introduced individuals themselves (propagule pressure, genetic diversity and adaptations in the introduced population) or the invaded community. We argue that microcosms, as model systems, can be powerful tools to test theoretical hypotheses. They must however be used with care, as they do not account for the same complexity as natural systems. They are thus complementary to theoretical studies and field surveys, and contribute to reinforce the predictive value of invasion biology by linking theory and experimentation.

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International audience; In sexual organisms, low population density can result in mating failures and subsequently yields a low population growth rate and high chance of extinction. For species that are in tight interaction, as in host-parasitoid systems, population dynamics are primarily constrained by demographic interdependences, so that mating failures may have much more intricate consequences. Our main objective is to study the demographic consequences of parasitoid mating failures at low density and its consequences on the success of biological control. For this, we developed a deterministic host-parasitoid model with a mate-finding Allee effect, allowing to tackle interactions between the Allee effect and key determinants of host-parasitoid demography such as the distribution of parasitoid attacks and host competition. Our study shows that parasitoid mating failures at low density result in an extinction threshold and increase the domain of parasitoid deterministic extinction. When proned to mate finding difficulties, parasitoids with cyclic dynamics or low searching efficiency go extinct; parasitoids with high searching efficiency may either persist or go extinct, depending on host intraspecific competition. We show that parasitoids suitable as biocontrol agents for their ability to reduce host populations are particularly likely to suffer from mate-finding Allee effects. This study highlights novel perspectives for understanding of the dynamics observed in natural host-parasitoid systems and improving the success of parasitoid introductions.

International audience; Propagule pressure, i.e. the number of individuals introduced, is thought to be a major predictor of the establishment success of introduced populations in the field. Its influence in laboratory experimental systems has however been questioned. In fact, other factors involved in long-term population persistence, like habitat size, were usually found to explain most of the dynamics of experimental populations. To better understand the respective influence of short- and long-term factors and their potential interaction on extinction dynamics in experimental systems, we investigated the influence of propagule pressure, habitat size and genetic background on the early dynamics of laboratory-based populations of a hymenopteran parasitoid. The amount of demographic variance differed between establishment and persistence phase and was influenced by habitat size and genetic background (geographic strain), but independent of propagule pressure. In contrast, the probability of extinction within five generations depended on the genetic background and on the interaction between propagule pressure and habitat size. Vulnerability to extinction in small size habitats was increased when populations were founded with a small number of individuals, but this effect was delayed until the third to fifth generations. These results indicate that demographic stochasticity is influential during population establishment, but is not affected by the genetic variability of propagules. On the other hand, extinction might be influenced by a genetic Allee effect triggered by the combination of low propagule pressure and genetic drift. Finally, we documented consistent differences between genetic backgrounds in both deterministic and stochastic population dynamics patterns, with major consequences on extinction risk and ultimately population establishment.

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International audience; In the framework of biological control, the selection of effective natural enemies determines the final pest control. Thus, the genetic improvement of biocontrol agents could enhance the efficiency of biocontrol programs. Although promising, this approach has rarely been applied in this field. At the intraspecific level, hybridization between divergent populations of biocontrol agents is expected to promote hybrid vigor (heterosis), but it is not clear to what extent. An even more difficult task is the ability to predict the fitness of hybrids from the biological characteristics of their parents. We investigated these general questions by crossing seven populations of the parasitoid wasp Trichogramma chilonis (Hymenoptera: Trichogrammatidae). Our results show different levels of mating compatibilities among populations, including asymmetric or almost complete reproductive isolation. Hybrids' performance (fitness of the F 1 generation) ranges from inbreeding depression to heterosis. It was possible, to some extent, to predict hybrid fitness from pairwise genetic and phenotypic distances among parents, in accordance with the dominance hypothesis. This may provide general guidelines for the genetic improvement of biological control agents.

International audience; Populations are introduced into novel environments in different contexts, one being the biological control of pests. Despite intense efforts, less than half introduced biological control agents establish. Among the possible approaches to improve biological control, one is to better understand the processes that underpin introductions and contribute to ecological and evolutionary success. In this perspective, we first review the demographic and genetic processes at play in small populations, be they stochastic or deterministic. We discuss the theoretical outcomes of these different processes with respect to individual fitness, population growth rate, and establishment probability. Predicted outcomes differ subtly in some cases, but enough so that the evaluating results of introductions have the potential to reveal which processes play important roles in introduced populations. Second, we attempt to link the theory we have discussed with empirical data from biological control introductions. A main result is that there are few available data, but we nonetheless report on an increasing number of well-designed, theory-driven, experimental approaches. Combining demography and genetics from both theoretical and empirical perspectives highlights novel and exciting avenues for research on the biology of small, introduced populations, and great potential for improving both our understanding and practice of biological control.

International audience

International audience; In many animals, mating takes place after natal dispersal. Consequently, use of reliable information is required to increase the probability of encounters between the sexes. Most of the studies on mate finding in parasitoid insects have focused on the role of a single information source: a sex pheromone. Other sources have been mostly ignored. We studied the nature of olfactory information used for mate finding by the parasitoid Venturia canescens both at a distance and at host patch level, and investigated how this information is used. We tested which sex attracts the other and whether mate location is improved by combining different sources of information. We found that males simultaneously used two types of olfactory cues to find their mate: information directly related to females and an environmental cue provided by hosts. Male efficiency in locating virgin females was enhanced threefold by the association of females with hosts, whereas host patches, on their own, were unattractive to males. Our results also suggest that females emit a volatile pheromone. At the host patch level, males used chemical marks left by females foraging for hosts. These results led us to consider the distinction between signals and cues and we suggest that the volatile pheromone emitted by the females, always described as a signal, could rather be a cue. Although evidence for a volatile sex pheromone is pervasive in parasitoids, our study stresses the role of other cues in mate-finding strategies.

Publication Inra prise en compte dans l'analyse bibliométrique des publications scientifiques mondiales sur les Fruits, les Légumes et la Pomme de terre. Période 2000-2012. http://prodinra.inra.fr/record/256699; International audience; In agrosystems, pests are submitted to strong human-imposed selective pressures to which they sometimes adapt rapidly, either through selection of genotypes resulting from mutation and/or recombination events, or through phenotypic plasticity. Understanding how insects respond to such selective pressures is of great importance for sustainable pest management strategies, such as the use of resistant plants. In this study, we investigated the genetic and phenotypic variability of anholocyclic Aphis gossypii Glover (Hemiptera: Aphididae) strains, in response to the resistance gene Vat that is present in melon crops. Forty-nine aphid colonies were sampled on several melon crops in southern France, genotyped using 15 microsatellite loci, and tested in phenotypic experiments using Vat or non-Vat melons. The level of genetic polymorphism between these colonies was low, as only seven multilocus genotypes were detected. In contrast, the phenotypic variability for life-history and behavioral traits between colonies, including those sharing the same genotype, was unexpectedly high, with a continuum of response to the Vat gene from complete susceptibility to strong virulence. The low genetic polymorphism associated with a strong phenotypic variability highlights the high adaptive potential of A. gossypii and the major role of environmental cues in shaping phenotypic responses of this aphid to pest management strategies

Many populations introduced into a novel environment fail to establish. One underlying process is the Allee effect, i.e., the difficulty of individuals to survive and reproduce when rare, and the consequently low or negative population growth. Although observations showing a positive relation between initial population size and establishment probability suggest that the Allee effect could be widespread in biological invasions, experimental tests are scarce. Here, we used a biological control program against Diuraphis noxia (Mordvilko) (Hemiptera: Aphididae) in the United States to manipulate initial population size of the introduced parasitoid Aphelinus asychis Walker (Hymenoptera: Aphelinidae) originating from France. For eight populations and three generations after introduction, we studied spatial distribution and spread, density, mate-finding, and population growth. Dispersal was lower in small populations during the first generation. Smaller initial population size nonetheless resulted in lower density during the three generations studied. The proportion of mated females and the population sex ratio were not affected by initial population size or population density. Net reproductive rate decreased with density within each generation, suggesting negative density-dependence. But for a given density, net reproductive rate was smaller in populations initiated with few individuals than in populations initiated with many individuals. Hence, our results demonstrate a demographic Allee effect. Mate-finding is excluded as an underlying mechanism, and other component Allee effects may have been overwhelmed by negative density-dependence in reproduction. Impact of generalist predators could provide one potential explanation for the relationship between initial population size and net reproductive rate. However, the continuing effect of initial population size on population growth suggests genetic processes may have been involved in the observed demographic Allee effect.

Bayesian updating is a form of learning by which individuals can adapt their behaviour to uncertain environments. In the particular situation of optimal foraging in a patchy habitat, animals may estimate the profitability of the patches they encounter to update their estimate of the profitability of the habitat as a whole, and adjust their foraging decisions accordingly. Recent studies have suggested that parasitoid insects may have such abilities, but were based on too few patches for clear conclusions on Bayesian updating. We studied how females of an aphid parasitoid update their estimate of habitat profitability, by recording their behaviour on a series of seven consecutive host patches, each serving both as a potential cue for habitat profitability and as a means to measure the behavioural response to previously collected information. The experiment was designed to test specific predictions based on Bayesian updating with different memory dynamics. The parasitoids clearly perceived the profitability of the patches, but the effect of previous experience on current patch use was different from our predictions. The reinterpretation of previous studies in the light of our results suggests that foraging parasitoids give more weight to early experience.

In haplodiploid organisms, virgin females can produce offspring, albeit only sons. They may therefore face a trade-off between either: (1) searching for hosts and producing sons immediately; or (2) searching for mates and perhaps producing both sons and daughters later in life. Although this trade-off raises a theoretical interest, it has not been approached experimentally. The objective of this article is thus to document the effect of mating status on the foraging behavior of a haplodiploid parasitoid. For this, we recorded the behavior of virgin and mated female Lysiphlebus testaceipes (Hymenoptera: Braconidae) after being released, in the field, on a colony of their aphid hosts. Half of the virgin females were mated by a wild male after less than 10 min of foraging. Evidently, virgin females attract males while foraging on host patches, so that the two activities are not mutually exclusive. Nonetheless, virgin females stayed motionless more often and for longer periods than mated females. Consequently, they attacked aphids at a lower rate, and in turn, attacked fewer aphids on each patch. Moreover, contrary to mated females, virgins did not aggregate their progeny on large patches. We conclude that in L. testaceipes, the trade-off may not be as hypothesized. By dispersing across patches more than mated females, virgins could promote future mating opportunities for their sons and increase their inclusive fitness. However, by moving too frequently, females may lose immediate mating opportunities for themselves and the immediate advantage of producing offspring of both sexes. The observed behavior of virgin L. testaceipes females on host patches could reflect an optimal solution to such a trade-off.

1. Animals usually require information about the current state of their habitat to optimize their behaviour. For this, they can use a learning process through which their estimate is continually updated according to the cues they perceive. Identifying these cues is a long-standing but still inveterate challenge for ecologists. 2. The use of plant cues by aphid parasitoids for the assessment of habitat profitability and the adaptation of patch exploitation was studied. Grounding on predictions from optimal foraging theory, we tested whether parasitoids exploited host patches less intensively after visiting heavily infested plants than after visiting plants bearing fewer aphids. 3. As predicted, after visiting heavily infested plants parasitoids reduced their residence time and attacked fewer hosts in the next patch. This was the case regardless of whether the aphids were actually present on the first plant, indicating that the cue came from the plant. Moreover, the level of infestation of a plant at some distance from the first plant visited affected parasitoid patch exploitation on the second plant in a similar manner, indicating that the cue was volatile. 4. These results highlight a novel role of herbivore-induced volatiles in parasitoid foraging behaviour, different from the widely studied attraction at a distance.

International audience; The ideal free distribution (IFD) is a stable distribution of competitors among resource patches. For equally efficient competitors, equilibrium is reached when the per capita rate of intake equalizes across patches. The seminal version of the IFD assumes omniscience, but populations may still converge toward the equilibrium provided that competitors 1) accurately assess their environment by learning and 2) remain for an optimal (rate-maximizing) time on each encountered patch. In the companion article (Tentelier C, Desouhant E, Fauvergue X. 2006. Habitat assessment by parasitoids: mechanisms for patch time allocation. Behav Ecol. Forthcoming), it is shown that the parasitoid wasp Lysiphlebus testaceipes adapts its exploitation of aphid host colonies based on previous experience, in a manner consistent with these two conditions. We therefore predicted that a randomly distributed population of initially naive wasps should converge toward the IFD. We tested this prediction by introducing 1300 L. testaceipes females into a 110-m(2) greenhouse containing 40 host patches. Just after introduction, the parasitoid rate of gain was positively affected by host number and negatively affected by parasitoid number but, as predicted, these effects vanished in the course of the experiment. Six hours after introduction, the expected rate of gain reached a constant. Surprisingly, this passage through equilibrium was not accompanied by a decrease in the coefficient of variation among gain rates or by a shift from a random to an aggregated distribution of parasitoids. These results challenge our understanding of the link between individual behavior and population distribution.

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International audience; 1. Optimal foraging models ultimately predict that female parasitoids should exploit rich host patches for longer than poorer ones. At the proximate level, mechanistic models and experimental studies show that parasitoids use both chemicals produced by their hosts and direct encounters with their hosts to estimate patch quality. Although it has been extensively studied in the context of host location, the use of herbivore-induced plant response by insect parasitoids has never been considered in the context of patch time allocation. 2. In this study, the respective roles of herbivore-induced plant response and direct contact with hosts on the foraging behaviour of Lisiphlebus testaceipes females on an aphid patch were quantified. For this, the level of herbivore-induced plant response and the number of aphids on the leaf bearing the patch were manipulated independently. Different levels of plant response were obtained by varying the duration of infestation on another leaf. 3. Parasitoid residence time and number of attacks increased with both the level of plant response and the number of aphids. 4. These results suggest that L. testaceipes females use the combination of herbivore-induced response of plants and direct encounters with hosts to assess patch quality and adjust their patch use behaviour

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Neurotoxic insecticides are widely used for crop protection. One consequence is that changes in behaviour can be expected in surviving beneficial insects because of an impairment of host perception and motor abilities. Under laboratory conditions, we studied the impact of deltamethrin, a pyrethroid, on the oviposition behaviour of two hymenopterous parasitoids of aphids, Aphidius matricariae (Haliday) and Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae). They both para- sitize Myzus persicae (Sulzer) (Homoptera: Aphididae), which is the preferred host of A. matricariae, regardless of the host plant, whereas D. rapae is a major parasitoid of aphids on Cruciferae crops, including M. persicae. After exposure to deltamethrin, the different items of oviposition behaviour and the total time spent on the patch were recorded. The results showed that the patch time allocation by both parasitoid species was not significantly affected by deltamethrin treatment, when compared with the controls. Nor were the frequencies and sequences of behavioural items modified (e.g., frequency of sting). It therefore appeared that the patch use of A. matricariae and D. rapae on new colonies of M. persicae was not disturbed by deltamethrin at the three doses tested. The possibility that parasitoid strains are partially tolerant to deltamethrin is discussed.

Charnov's marginal value theorem predicts that female parasitoids should exploit patches of their hosts until their instantaneous rate of fitness gain reaches a marginal value. The consequences of this are that: (1) better patches should be exploited for a longer time; (2) as travel time between patches increases, so does the patch residence time; and (3) all exploited patches should be reduced to the same level of profitability. Patch residence time was measured in an egg parasitoid Anaphes victus (Hymenoptera: Mymaridae) when patch quality and travel time, approximated here as an increased delay between emergence and patch exploitation, varied. As predicted, females stayed longer when patch quality and travel time increased. However, the marginal value of fitness gain when females left the patch increased with patch quality and decreased with travel time. A. victus females appear to base their patch quality estimate on the first patch encountered rather than on a fixed innate estimate, as was shown for another egg parasitoid Trichogramma brassicae. Such a strategy could be optimal when inter-generational variability in patch quality is high and within-generational variability is low.

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Populations spatially structured at the time of mating may experience local mate competition (LMC) and inbreeding, two factors known to select, in haplodiploid organisms, for a female biased sex ratio. Populations of the two Drosophila parasitoids Leptopilina boulardi and L. heterotoma could have such a structure because although males and females develop from different hosts, many hosts are clumped within fruits decaying on the ground. However, contrary to theoretical expectations. we found field sex ratios to be only slightly female biased (L. heterotoma) or even male biased (L. boulardi). This raised the question of whether populations of these two species experience any level of LMC and inbreeding. To address this question. we studied male and female spatio-temporal patterns of emergence, dispersal, and male attraction to females. We found that within days, emergence was synchronized, with males starting to emerge slightly before females. However, when emergence was analyzed day-by-day for individuals laid during the same oviposition bout, males and females emerged on different days. A similar analysis for fruits collected in the field showed that about 20% of males and 20% of females emerged in the absence of any potential mate Furthermore, males dispersed from their natal sites soon after emergence, at a rate similar to that of conspecific females. With laboratory and field experiments, we found that dispersing males were attracted to virgin females via in-flight orientation mediated by a volatile sex pheromone. These data suggest that the mating structures of L. boulardi and L. heterotoma differ from that assumed by classic LMC models. Because males disperse and search for females from other patches, local mate competition and inbreeding will be reduced to an extent depending on male mating success after dispersal. Inbreeding could also be reduced because synchronous emergence of males and females mainly results from asynchronous oviposition bouts, so that on-patch matings should concern unrelated individuals, Such a mating structure explains the absence of a strong sex ratio bias toward females in these two species. More generally, through a review of the published literature on sex pheromones, we suggest that mating structures with a non-negligible fraction of off-patch matings could be widespread among parasitoids.

International audience

International audience; This chapter describes the main principles of the sterile insect technique (SIT), a pest control method that seeks to gradually reduce insect reproduction by releasing sterilized males in large numbers. We highlight the potential and limitations of the use of SIT and explore various future research avenues. SIT is generally one important component of an area-wide integrated pest management programme. The aim is no longer to protect individual crop fields but rather entire regions, which requires cooperation among many stakeholders. This larger focus also underscores the need for transdisciplinary cooperation among researchers in the biological sciences and humanities and social sciences as well as key stakeholders from the early stages of a programme, whether pilot or operational. We explore examples from France, which has seen the development of several pilot projects in agriculture and health in the recent years.

International audience; Augmentative biological control is based on the repeated introduction of mass-produced biological control agents as predators or parasitoids with the aim of temporarily controlling or even eradicating pest populations. The different augmentative strategies form a continuum ranging from preventive releases of small numbers of natural enemies prior to the arrival of the pests for a delayed impact (inoculation) to intense, short-term mass releases for a quick and drastic impact on the pest population (inundation). These strategies may also be combined with practices that aim to favour the individual fitness and/or the population establishment of the biological control agents. After briefly reviewing the history of such practices, this chapter explores different challenges currently faced by augmentative biological control linked to the production of biocontrol agents, the underlying business models and the potential existence of non-target effects. Finally, different ways to improve augmentative biological control are investigated, from better selection of biocontrol agent strains to innovations in rearing conditions or supplementation of resources to support the introduced natural enemies. The need to better understand the population dynamics at play or the possible combination of augmentative biological control with entomovectoring techniques are also discussed.

1 - The Drosophilia suzukii fly, native to Asia, is a fly that devastates many fruit crops (especially berries). This fruit fly has recently invaded Europe and is currently at the heart of projects aimed at developing an integrative fight against it. The technique of management by cytoplasmic incompatibility (ICM) is a self-control technique. It works by releasing individuals of the target species infected by the Wolbachia bacterium, a disruptive symbionte that generates cytoplasmic incompatibilities, a phenomenon that can lead to the laying of non-viable eggs. Combined with positive density dependence effects (Allee effects), invasion by Wolbachia can lead to the disappearance of the host population. Our objectives in this course are to understand the interaction between (i) demographic stochasticity (ii) density dependence and Wolbachia invasion. 2 - (i) Stochasticity has little effect on the invasion process under conditions that are conducive to invasion. (ii) The invasion process is little affected by density dependence in the form of the Allee effect, whereas in the form of competition it seems to have a negative effect. During the study the invasion times obtained are very long. Finally, we did not observe a monotonous decrease in host populations during the invasion, a result which diverges from the results of previous generalist models.; 1 – La mouche Drosophilia suzukii, originaire d’Asie est une mouche ravageant de nombreuses cultures fruitières (notamment les petits fruits). Cette mouche du fruit à récemment envahi l’Europe et est actuellement au cœur de projets visant à développer contre elle une lutte intégrative. La technique de gestion par incompatibilité cytoplasmique (GIC), est une technique de lutte autocide. Elle fonctionne par lâchés d’individus de l’espèce cible, infectés par la bactérie Wolbachia, un symbionte perturbateur générant des incompatibilités cytoplasmique, phénomène pouvant entrainer la ponte d’œufs non viables. Combinés avec des effets de densité dépendance positive (effets Allee) l’invasion par Wolbachia peut entrainer la disparition de la population hôte. Nous avons pour objectifs dans ce stage de comprendre l’interaction entre (i) stochasticité démographiques (ii) densité - dépendance et l’invasion par Wolbachia.2 – (i) La stochasticité affecte peu le processus d’invasion, dans des conditions propices à l’invasion. (ii) Le processus d’invasion est peu affecté par la densité dépendance sous forme d’effet Allee, tandis que sous forme de compétition, elle semble avoir un effet négatif. Durant l’étude les temps d’invasions obtenus sont très longs. Enfin nous n’avons pas observé de diminution monotone des populations hôtes lors de l’invasion, résultats qui diverge avec les résultats des précédents modèles généralistes.

International audience

Inbreeding and hybridization are two genetic processes that may have antagonistic effects in biological control agents (BCAs) rearing. Hybridization can minimize the risk of inbreeding depression (decrease in fitness of inbred individuals), and favor the emergence of advantageous phenotypes. Although the mechanisms of inbreeding depression and the consequences of hybridization are well known, very few studies have been carried out in the context of biological control. The actual effects of inbreeding and hybridization on the fitness of BCAs should be assessed to guide the practices of the biocontrol industry. In a public-private collaboration, data were generated on the effects of inbreeding in the four BCAs Allotropa burrelli, Chrysoperla near comanche, Cryptolaemus montrouzieri and Macrolophus pygmaeus. Inbreeding resulted in a 30% decrease in reproductive success in M. pygmaeus. A thorough study of the consequences of intra-specific hybridization was then carried out using four populations of M. pygmaeus. Three genetic groups separated by strong reproductive isolation were identified. Nevertheless, a fitness advantage for individuals from crosses between genetically distant parents has been highlighted within each genetic group. This work brings data usable in the short term by the partner companies. It also helps to create a corpus of data to better evaluate the real importance of genetic effects in BCAs rearing.; La consanguinité et l’hybridation sont deux processus génétiques pouvant avoir des effets antagonistes dans les élevages d’auxiliaires de lutte biologique. L’hybridation peut minimiser les risques de dépression de consanguinité (diminution de fitness des individus consanguins), et favoriser l’apparition de phénotypes avantageux. Bien que les mécanismes de la dépression de consanguinité et des conséquences de l’hybridation soient bien connus, très peu d’études ont été réalisées dans le cadre de la lutte biologique. Il convient d’évaluer les effets réels de la consanguinité et de l’hybridation sur la fitness des auxiliaires pour orienter les pratiques de l’industrie de la lutte biologique. Dans le cadre d’une collaboration public-privé, des données ont été produites sur les effets de la consanguinité chez les quatre auxiliaires Allotropa burrelli, Chrysoperla near comanche, Cryptolaemus montrouzieri et Macrolophus pygmaeus. La consanguinité a notamment provoqué une baisse de 30% du succès reproducteur chez M. pygmaeus. Une étude approfondie des conséquences de l’hybridation intra-spécifique a alors été réalisée en utilisant quatre populations de M. pygmaeus. Trois groupes génétiques séparés par un fort isolement reproducteur ont été mis en évidence. Néanmoins, un avantage de fitness pour les individus issus de croisements entre parents génétiquement distants a été mis en évidence au sein de chaque groupe génétique. Ce travail de thèse apporte des données utilisables à court-terme par les entreprises partenaires. Il contribue par ailleurs à créer un corpus de données pour mieux évaluer l’importance réelle des effets génétiques dans les élevages d’auxiliaires.

Genetic and demographic processes can drive small populations to extinction. Their interaction can generate extinction vortices. In Hymenoptera, males are haploid and females are diploid. In species with single-locus complementary sex determination (sl-CSD), hemizygous at the CSD gene develop in males and heterozygous diploids, in females. Homozygous develop in diploids males, often unviable or sterile. Theoretical studies suggest that the production of diploid males associated with demographic and environmental stochasticity may drive small populations into an extinction vortex.The first objective is to stimulate collaboration between genetics and demography by proposing a definition for component Allee effects generated by genetic processes. Component and demographic genetic Allee effects were detected in the literature.The second objective was to investigate the presence of a genetic, and maybe demographic, Allee effect in populations of the parasitoid Venturia canescens, a Hymenoptera with sl-CSD. Microsatellite markers were developed and used to show a negative relationship between genetic diversity and proportion of diploid males in isolated and bottlenecked populations. Diploid males can mate but they are sterile. Inbreeding depression affecting females is negligible. We created and monitored experimental populations of V. canescens with different levels of genetic diversity. A genetic Allee effect due to the production of diploid males was detected but it did not influence the growth rate or the probability of extinction of populations. Extinction events observed thus seem mainly due to demographic stochasticity.; L’interaction de processus génétiques et démographiques peut générer des vortex d’extinction. Chez les hyménoptères, les mâles sont haploïdes et les femelles diploïdes. Chez les espèces avec sl-CSD (single-locus complementary sex determination), les haploïdes, se développent en mâles et les diploïdes hétérozygotes au gène du CSD, en femelles. Les diploïdes homozygotes sont des mâles non viables ou stériles. Des études théoriques suggèrent que la production de mâles diploïdes peut entraîner les petites populations d’hyménoptères dans un vortex d’extinction. Le premier objectif est d’encourager le dialogue entre génétique et démographie en proposant une définition des effets Allee élémentaires générés par des processus génétiques, dont nous avons identifié des exemples dans la littérature. Le deuxième objectif est de rechercher l’existence d’un effet Allee génétique dans des populations de Venturia canescens, un hyménoptère parasitoïde avec sl-CSD. Des marqueurs microsatellites ont été élaborés et utilisés pour montrer une relation négative entre diversité génétique et proportion de mâles diploïdes dans des populations isolées ou goulotées. Les mâles diploïdes s’accouplent mais sont stériles. La dépression de consanguinité affectant les femelles est faible. Nous avons créé et suivi des populations expérimentales de V. canescens avec différents niveaux de diversité génétique. Un effet Allee génétique dû à la production de mâles diploïdes a été détecté mais il n’influençait ni le taux d’accroissement ni la probabilité d’extinction des populations. Les extinctions observées semblent surtout due à la stochasticité démographique.

Genetic and demographic processes can drive small populations to extinction. Their interaction can generate extinction vortices. In Hymenoptera, males are haploid and females are diploid. In species with single-locus complementary sex determination (sl-CSD), hemizygous at the CSD gene develop in males and heterozygous diploids, in females. Homozygous develop in diploids males, often unviable or sterile. Theoretical studies suggest that the production of diploid males associated with demographic and environmental stochasticity may drive small populations into an extinction vortex.The first objective is to stimulate collaboration between genetics and demography by proposing a definition for component Allee effects generated by genetic processes. Component and demographic genetic Allee effects were detected in the literature.The second objective was to investigate the presence of a genetic, and maybe demographic, Allee effect in populations of the parasitoid Venturia canescens, a Hymenoptera with sl-CSD. Microsatellite markers were developed and used to show a negative relationship between genetic diversity and proportion of diploid males in isolated and bottlenecked populations. Diploid males can mate but they are sterile. Inbreeding depression affecting females is negligible. We created and monitored experimental populations of V. canescens with different levels of genetic diversity. A genetic Allee effect due to the production of diploid males was detected but it did not influence the growth rate or the probability of extinction of populations. Extinction events observed thus seem mainly due to demographic stochasticity.; L’interaction de processus génétiques et démographiques peut générer des vortex d’extinction. Chez les Hyménoptères, les mâles sont haploïdes et les femelles diploïdes. Chez les espèces avec sl-CSD (single-locus complementary sex determination), les haploïdes, se développent en mâles et les diploïdes hétérozygotes au gène du CSD, en femelles. Les diploïdes homozygotes sont des mâles non viables ou stériles. Des études théoriques suggèrent que la production de mâles diploïdes peut entraîner les petites populations d’Hyménoptères dans un vortex d’extinction. Le premier objectif est d’encourager le dialogue entre génétique et démographie en proposant une définition des effets Allee élémentaires générés par des processus génétiques, dont nous avons identifié des exemples dans la littérature. Le deuxième objectif est de rechercher l’existence d’un effet Allee génétique dans des populations de Venturia canescens, un Hyménoptère parasitoïde avec sl-CSD. Des marqueurs microsatellites ont été élaborés et utilisés pour montrer une relation négative entre diversité génétique et proportion de mâles diploïdes dans des populations isolées ou goulotées. Les mâles diploïdes s’accouplent mais sont stériles. La dépression de consanguinité affectant les femelles est faible. Nous avons créé et suivi des populations expérimentales de V. canescens avec différents niveaux de diversité génétique. Un effet Allee génétique dû à la production de mâles diploïdes a été détecté mais il n’influençait ni le taux d’accroissement ni la probabilité d’extinction des populations. Les extinctions observées semblent surtout due à la stochasticité démographique.

1 Annexe; 7 articles scientifiques (dont 6 en anglais) Diplôme : Dr. d'Universite; Lorsque l’environnement est variable, les comportements plastiques sont adaptés, à condition d’être basés sur des informations fiables. Dans le cas de la dispersion, les informations importantes concernent la comparaison entre la fitness qu’il est possible de gagner dans un site et celle qu’il est possible de gagner ailleurs dans l’habitat. Dans cette thèse, les décisions de dispersion d’un parasitoïde de pucerons sont étudiées expérimentalement, dans le cadre théorique de l’optimisation et de la théorie des jeux. Les résultats d’expériences au laboratoire montrent que les parasitoïdes perçoivent et mémorisent des signaux volatils émis par les plantes en réponse à la présence de pucerons pour estimer la profitabilité des colonies de pucerons, et adapter leur temps de résidence dans les colonies. D’une part, les parasitoïdes restent plus longtemps dans une colonie lorsqueles signaux des plantes indiquent que la colonie contient de nombreux pucerons. D’autre part, les parasitoïdes augmentent leur temps de résidence si la plante précédemment visitée indique que le reste de l’habitat contient relativement peu d’hôtes. La manière dont les parasitoïdes mettent à jour leur estimation de l’habitat en fonction de leur expérience n’est pas très clairement résolue. La dispersion des parasitoïdes est aussi étudiée en population naturelle, en testant les prédictions de la distribution libre idéale. Le génotype microsatellite des individus émergeant de pucerons parasités permet de déterminer le nombre de femelles de la génération précédente ayant pondu dans une colonie et le nombre de descendants produits par la femelle dans chaque colonie. Les résultats montrent que les femelles ne sont pas distribuées de manière idéale. Leur forte propension à disperser semble plutôt être sélectionnée par des pressions venant des niveaux trophiques supérieurs, comme les prédateurs et les hyperparasitoïdes. L’ensemble des résultats obtenus dans cette thèse indique que les décisions de dispersion des parasitoïdes sont plastiques et se basent probablement sur des informations provenant des différents niveaux trophiques présents dans les communautés. L’effet relatif de chaque information sur les décisions des parasitoïdes reste une question ouverte, qui mériterait une approche d’écologie des communautés.