Search

SummaryThe management of insect pests has long been dominated by the use of chemical insecticides, with the aim of instantaneously killing enough individuals to limit their damage. To minimize unwanted consequences, environmentally-friendly approaches have been proposed that utilize biological control and take advantage of intrinsic demographic processes to reduce pest populations.We address the feasibility of a novel pest management strategy based on the release of insects infected withWolbachia, which causes cytoplasmic incompatibilities in its host population, into a population with a pre-existing Allee effect. We hypothesize that the transient decline in population size caused by a successful invasion ofWolbachiacan bring the population below its Allee threshold and, consequently, trigger extinction.We develop a stochastic population model that accounts forWolbachia-induced cytoplasmic incompatibilities in addition to an Allee effect arising from mating failures at low population densities. Using our model, we identify conditions under which cytoplasmic incompatibilities and Allee effects successfully interact to drive insect pest populations toward extinction. Based on our results, we delineate control strategies based on introductions ofWolbachia-infected insects.We extend this analysis to evaluate control strategies that implement successive introductions of two incompatibleWolbachiastrains. Additionally, we consider methods that combineWolbachiainvasion with mating disruption tactics to enhance the pre-existing Allee effect.We demonstrate that Wolbachia-induced cytoplasmic incompatibility and the Allee effect act independently from one another: the Allee effect does not modify theWolbachia-invasion threshold, and cytoplasmic incompatibilities only have a marginal effect on the Allee threshold. However, the interaction of these two processes can drive even large populations to extinction. The success of this method can be amplified by the introduction of multipleWolbachiacytotypes as well as the addition of mating disruption.Our study extends the existing literature by proposing the use ofWolbachiaintroductions to capitalize on pre-existing Allee effects and consequently eradicate insect pests. More generally, it highlights the importance of transient dynamics, and the relevance of manipulating a cascade of destabilizatons for pest management.

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.

Like other animals and plants, insects may find it difficult to survive and reproduce in small populations, to the extent that their long-term persistence may be jeopardized. The Allee effect is a theoretical framework that formalizes this decrease in survival or reproduction in small populations, and the resulting decrease in population growth and persistence. Mating failure in low-density populations is likely to generate an Allee effect and, therefore, has a major effect on the functioning of small populations. Here, I review mate-finding Allee effects in insect species, and their consequences for individual mating success, population dynamics, and population management. I focus, in particular, on the comparison of theoretical expectations with observational data. Several studies have reported some degree of mating failure at low density. However, almost none of the datasets available allow comparison with the predictions of classical mate-searching models. A few studies at the population level have reported the co-occurrence of mating failure at low density and a demographic Allee effect, but no study has yet clearly demonstrated a causal relationship between mating failure and lower rates of population growth. Thus, although the theoretical development of management tactics based on Allee effects is considered promising, the current lack of evidence supporting this strategy limits its potential relevance. I call here for a more rigorous approach to the study of mate-finding Allee effects and propose new approaches for this purpose.

In the present study, we investigated the evolution of life-history traits in the main species of a community, after the arrival of a new competitor. Two parasitoid species, Leptopilina heterotoma and Asobara tabida, are present throughout the Rhone and Saone valleys, whereas a third species, Leptopilina boulardi, is slowly extending its distribution northwards. In the presence of L. boulardi, competing parasitoids experience a higher mortality and lower host availability. Resources should thus be re-allocated between traits according to these new factors. We compared life-history traits of populations of L. heterotoma and A. tabida in areas with and without L. boulardi. As predicted by both Price's balanced mortality hypothesis and the theory of life-history traits, we found that investment in reproduction is higher in southern populations for both native species, coupled with higher travelling abilities. However, only A. tabida paid their higher fecundity by a lower longevity. The absence of a clear trade-off between these traits in L. heterotoma may be explained by a lower metabolic rate in southern populations. These results highlight the importance of the community change over climate in the evolution of life-history traits in this parasitoid community. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107, 153-165. ADDITIONAL KEYWORDS: Asobara tabida - competition - evolution - global change - Leptopilina boulardi - Leptopilina heterotoma - maintenance - mobility - reproduction - trade-off.

International audience; Classical biological control-the introduction of exotic species to permanently control pests-offers an applied framework to test ecological and evolutionary hypotheses derived from invasion biology. One such hypothesis is that intraspecific hybridization can facilitate invasions because hybrids express higher phenotypic mean and/or variance than their parents. We tested this hypothesis using the parasitoid wasp Psyttalia lounsburyi, a candidate biocontrol agent for the olive fly Bactrocera oleae. Under laboratory conditions, we found marked differentiations between two populations of wasps, from South Africa and Kenya, in terms of life history strategies. South African females were better reproducers than Kenyan females, but the opposite was observed for males. Reaction norms showed different effects of developmental temperature on fecundity depending on the genotype. However, neither heterosis nor hybrid breakdown were observed. Hence, in this system, sex-specific effects of hybridization and genotype-by-environment interactions jeopardize any straightforward prediction on the fitness of hybrids. Therefore, our paper contributes to tone down the hybrid advantage hypothesis in invasion biology.

International audience; Numerous arthropod species are genetically differentiated across their distribution area. Diversifying the geographical origins of a biocontrol agent species can be used to favour their perennial establishment by the sampling of pre-adapted genotypes and/or the production of new genotypes through hybridization. Hybridization can be nevertheless challenged by reproductive isolations induced by some common microbial endosymbionts. In this study, we aimed at characterizing (i) the genetic diversity of six populations of Psyttalia lounsburyi (Hymenoptera: Braconidae), a candidate biocontrol agent of the olive fruit fly Bactrocera oleae (Diptera: Tephritidae) and (ii) the diversity of their Wolbachia endosymbionts. Both mitochondrial and microsatellite markers evidence clustering between the South African population and several Kenyan/Namibian populations. The survey of the Wolbachia also distinguished two main variants with a spatial heterogeneity in the infection status. All these results are discussed in the context of the use of these P. lounsburyi populations for hybridization and further field releases.

Habitat selection by dispersers is the focus of much theoretical models, most of which are based on the assumption of negative density dependence. The archetype of these models is the ideal free distribution, characterized by an evolutionary stable state where more competitors aggregate in better habitats, so that the fitness benefit of resource abundance is equally offset by the cost of competition in all habitats. In this study, we used parentage analysis on microsatellite genotypes to test the ideal free distribution in a natural population of aphid parasitoids. Parentage analysis was conducted on parasitoids emerging from aphid colonies. We inferred the number of foundress females which had reproduced in each colony, as well as the number of offspring for each foundress. As predicted by the ideal free distribution, the number of offspring per foundress per colony did not depend on the number of hosts per colony. However, contrary to ideal free distribution predictions, it was affected by the number of foundresses per colony. In surprising contrast with the basic assumption of negative density dependence, individual fitness increased with the number of foundresses. Moreover, parentage analysis revealed a very low number of offspring per foundress per colony (mean = 1.8). This observed distribution questions the validity of classical models of habitat choice based on competition. Indeed, our results provide a new illustration reinforcing a growing body of theory and data on positive density dependence. Our results also suggest that the avoidance of hyperparasitism and predation, although generally neglected, may shape the distribution of parasitoids in the field.

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.

Animals foraging for patchily distributed resources may optimize their foraging decisions concerning the patches they encounter, provided that they base these decisions on reliable information about the profitability of the habitat as a whole. Females of the parasitoid Lysiphlebus testaceipes exploit aphid hosts, which typically aggregate in discrete colonies. We show here how betweencolony travel time and the number of aphids in previously visited colonies affect parasitoid foraging behavior. We first assumed that parasitoids use travel time and previous colony size to estimate a mean rate of fitness gain in the habitat and derived quantitative predictions concerning the effect of these two variables on patch residence time and patch-leaving rate of attack. We then tested these theoretical predictions in laboratory experiments in which female parasitoids were allowed to visit two successive colonies. As predicted, the observed residence time in the second colony increased with increasing travel time and decreasing size of the first colony. Patch-leaving rate of attack decreased with increasing travel time but was not affected by previous colony size. These results suggest that parasitoids use these two variables to assess habitat quality. However, discrepancies between the data obtained and quantitative predictions show that the effect of travel time on patch use may be more complex than assumed in our model. Key words: learning, Lysiphlebus testaceipes, marginal value theorem, optimal foraging theory, patch size, travel time. [Behav Ecol]

In fall, Myzus persicae (Sulzer) (Homoptera: Aphididae) may exhibit population resurgence in winter oilseed rape in France. This resurgence may arise from pyrethroid treatments against Coleoptera (Psylliodes chrysocephala L.) that either kill parasitoids present during treatment or prevent recolonization by off-crop parasitoids. We studied the impact of Diaeretiella rapae (M'Intosh) (Hymenoptera: Braconidae) on populations of M. persicae when parasitoids were introduced on deltamethrin-treated plants at increasing intervals after treatment. Parasitoids were introduced 1, 2, 7, or 14 d posttreatment on individually caged plants infested with established populations of M. persicae. Aphids were counted 7, 14 and 21 d after parasitoid introduction. First, we observed that both the pesticide and the parasitoid reduced aphid population growth and that their effects were additive. Second, there was no mortality of parasitoids exposed to treated leaves in a device with a refuge area, and only 20% of mortality without the refuge area. Furthermore, deltamethrin residues had no effect on the reproduction of D. rapae females. Compared with the known toxicity of deltamethrin to D. rapae on glass, this low mortality may have been due to both the high liposolubility of deltamethrin (leading to a rapid diffusion of residues in the oilseed rape leaf cuticle) and to the existence of a refuge area. This work suggests that D. rapae could limit populations of M. persicae in the fall, even after pyrethroid treatment, because the presence of deltamethrin residues had little impact on the parasitoid.

International audience

International audience; Inbreeding and inbreeding depression are key processes in small or isolated populations and are therefore central concerns for the management of threatened or (re) introduced organisms. Haplodiploid species of the order Hymenoptera have a particular status with regard to inbreeding depression. Although recessive deleterious alleles that are expressed in males should be purged, an alternative form of inbreeding depression exists in species with single-locus complementary sex determination (sl-CSD). Under sl-CSD, genetically-related parents have a high probability of producing sterile sons instead of fertile daughters. In this article, we study inbreeding depression in Venturia canescens (Hymenoptera: Ichneumonidae), a parasitoid wasp with sl-CSD. We used a crossing design to manipulate relatedness according to three levels: within-family, between-family and between-population. For each level, several fitness components were measured on parents and female offspring. We found a 20% reduction in egg load at emergence for inbred crosses. Inbred crosses also yielded a higher proportion of males, as expected in a species with sl-CSD. Mating probability, presence of daughters among offspring, body size, symmetry and longevity were unaffected by inbreeding.

The patch exploitation strategy of females of the insect parasitoid Trichogramma brassicae was studied on patches containing different proportions of hosts that were previously attacked by conspecific females. On average, T. brassicae females spent more time on patches of higher quality, and all patches were reduced to the same level of profitability before being left. This appeared to be in accordance to the optimal predictions of the Charnov Marginal Value Theorem. The proximate leaving mechanisms involved were analyzed by means of a Cox proportional hazards model. Each oviposition in a healthy host appeared to have an incremental influence on the patch residence time, whereas each rejection of a healthy host or of a host that was previously attacked by the same female (i.e., self-superparasitism) had a decremental effect. These patch leaving mechanisms did not change according to the quality of the patch the females were exploiting. A Monte Carlo simulation was developed around the results of the Cox regression model. The results suggest that this set of patch leaving rules seems to provide the females with a sufficient way to reach the predictions of the Charnov model. Among the different mechanisms involved, the incremental effect associated with each oviposition in a healthy host appeared to play the most important role. The relationship between the proximate mechanistic rules adopted by the females and the ultimate prediction of the Charnov model is discussed. Key words: patch leaving rules, Marginal Value Theorem, Cox regression model, parasitoids, Trichogramma, Monte Carlo simulation. [Behav Ecol 11:577–586 (2000)]

We have developed 21 dinucleotide repeat microsatellite loci from African populations of Psyttalia lounsburyi (Silvestri) (Hymenoptera: Braconidae), a parasitoid wasp of the olive fruit fly, as part of a study assessing the role of introgression/hybridization in the success of a biological control introduction. We proposed suitable conditions for polymerase chain reaction multiplexing. All 21 loci were polymorphic with two to 21 alleles per locus within the Kenyan and South African populations tested. Most of them were successfully amplified in two other Psyttalia species.

In haplodiploid organisms, unmated or sperm depleted females are "constrained" to produce only male progeny. If such constrained females reproduce, the popula­ tion sex ratio will shift toward males and unconstrained females will be selected to produce more females. Assuming that a female's own time spent constrained is an index of the population-wide level of constrained oviposition, and that constrained and unconstrained females reproduce at the same rate, the proportion of sons that females produce when unconstrained should decrease with increasing time spent constrained. Alternatively, if females cannot measure time spent constrained or if time spent constrained is not an index to the level of constrained oviposition in the popUlation, the proportion of sons among progeny produced when unconstrained should not depend upon time spent constrained and should be female biased to an extent depending upon the average time spent constrained over evolutionary time. To test these predictions, we manipulated the amount of time spent virgin in the parasitoid wasp Aphelinus asychis Walker (Hymenoptera: Aphelinidae) and mea

International audience; Microsatellite loci were isolated from the aphid parasitoid Lysiphlebus testaceipes (Hymenoptera: Braconidae). Ten loci were obtained from an enriched partial genomic library. Genetic diversity was analysed at seven of these loci and two natural populations, one on oleander and one on citrus. The observed number of alleles ranged from one to 17, and the observed heterozygosity ranged from 0.37 to 0.82. In both populations, no departure from Hardy-Weinberg equilibrium was detected except for one locus. The differentiation between the two populations was characterized by an F-ST Of 0-09.

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.

National audience

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.

Habitat selection by dispersers is the focus of much theoretical models, most of which are based on the assumption of negative density dependence. The archetype of these models is the ideal free distribution, characterized by an evolutionary stable state where more competitors aggregate in better habitats, so that the fitness benefit of resource abundance is equally offset by the cost of competition in all habitats. In this study, we used parentage analysis on microsatellite genotypes to test the ideal free distribution in a natural population of aphid parasitoids. Parentage analysis was conducted on parasitoids emerging from aphid colonies. We inferred the number of foundress females which had reproduced in each colony, as well as the number of offspring for each foundress. As predicted by the ideal free distribution, the number of offspring per foundress per colony did not depend on the number of hosts per colony. However, contrary to ideal free distribution predictions, it was affected by the number of foundresses per colony. In surprising contrast with the basic assumption of negative density dependence, individual fitness increased with the number of foundresses. Moreover, parentage analysis revealed a very low number of offspring per foundress per colony (mean = 1.8). This observed distribution questions the validity of classical models of habitat choice based on competition. Indeed, our results provide a new illustration reinforcing a growing body of theory and data on positive density dependence. Our results also suggest that the avoidance of hyperparasitism and predation, although generally neglected, may shape the distribution of parasitoids in the field.

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.

International audience; One frequent explanation for the failure of biological invasions is the Allee effect: due to positive density dependence, initially small invading populations may fail to establish and spread. Populations released for biological control are similar to fortuitous invading populations and may therefore suffer from Allee effects. However, unlike fortuitous invasions, biological control allows the experimental manipulation of initial population size and, thus, offers a unique opportunity to test for the occurrence of Allee effects. We manipulated the initial size of 45 populations of a parasitoid wasp introduced for the biological control of a phytophagous insect and followed the population dynamics of both parasitoids and hosts during three years. Our results suggest an absence of Allee effects but clear negative density dependence instead: (1) the probability of establishment after three years was not affected by initial population size; (2) net reproductive rate was highest at low parasitoid density and high host density; (3) the sex ratio, reflecting the proportion of virgin females, did not increase at low density, suggesting that low densities did not impede mate-finding; (4) the depression of host populations did not depend upon the number of parasitoids introduced. This is, to our knowledge, the first experimental test of the Allee effect in an invading parasitoid. It leads us to propose that a number of behavioral and life-history features of many parasitoids could protect them from Allee effects.

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.

National audience

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