Insect population dynamics under Wolbachia-induced cytoplasmic incompatibility: Puzzle more than buzz in Drosophila suzukii.

In theory, the introduction of individuals infected with an incompatible strain of Wolbachia pipientis into a recipient host population should result in the symbiont invasion and reproductive failures caused by cytoplasmic incompatibility (CI). Modelling studies combining Wolbachia invasion and host population dynamics show that these two processes could interact to cause a transient population decline and, in some conditions, extinction. However, these effects could be sensitive to density dependence, with the Allee effect increasing the probability of extinction, and competition reducing the demographic impact of CI. We tested these predictions with laboratory experiments in the fruit fly Drosophila suzukii and the transinfected Wolbachia strain wTei. Surprisingly, the introduction of wTei into D. suzukii populations at carrying capacity did not result in the expected wTei invasion and transient population decline. In parallel, we found no Allee effect but strong negative density dependence. From these results, we propose that competition interacts in an antagonistic way with Wolbachia-induced cytoplasmic incompatibility on insect population dynamics. If future models and data support this hypothesis, pest management strategies using Wolbachia-induced CI should target populations with negligible competition but a potential Allee effect, for instance at the beginning of the reproductive season.

Insects and incest: Sib-mating tolerance in natural populations of a parasitoid wasp.

Sib-mating avoidance is a pervasive behaviour that is expected to evolve in species subject to inbreeding depression. Although laboratory studies provide elegant demonstrations, small-scaled bioassays minimize the costs of mate finding and choice, and thus may produce spurious findings. We therefore combined laboratory experiments with field observations to examine the existence of inbreeding avoidance using the parasitoid wasp Venturia canescens. In the laboratory, our approach consisted of mate-choice experiments to assess kin discrimination in population cages with competitive interactions. A higher mating probability after sib rejections suggested that females could discriminate their sibs; however, in contrast to previous findings, sib-mating avoidance was not observed. To compare our laboratory results to field data, we captured 241 individuals from two populations. Females laid eggs in the lab, and 226 daughters were obtained. All individuals were genotyped at 18 microsatellite loci, which allowed inference of the genotype of each female's mate and subsequently the relatedness within each mating pair. We found that the observed rate of sib-mating did not differ from the probability that sibs encountered one another at random in the field, which is consistent with an absence of sib-mating avoidance. In addition, we detected a weak but significant male-biased dispersal, which could reduce encounters between sibs. We also found weak fitness costs associated with sib-mating. As such, the sex-biased dispersal that we found is probably sufficient to mitigate these costs. These results imply that kin discrimination has probably evolved for purposes other than mate choice, such as superparasitism avoidance.

Effects of inbreeding on a gregarious parasitoid wasp with complementary sex determination.

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 (nonsib) crosses, across five generations, to examine the consequences of inbreeding in this species. We found that in inbred lines, nonreproducing females live less, the number of daughters produced was lower, and 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.

A cascade of destabilizations: Combining Wolbachia and Allee effects to eradicate insect pests.

The 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 with Wolbachia, 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 of Wolbachia can bring the population below its Allee threshold and, consequently, trigger extinction. We develop a stochastic population model that accounts for Wolbachia-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 towards extinction. Based on our results, we delineate control strategies based on introductions of Wolbachia-infected insects. We extend this analysis to evaluate control strategies that implement successive introductions of two incompatible Wolbachia strains. Additionally, we consider methods that combine Wolbachia invasion 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 the Wolbachia 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 multiple Wolbachia cytotypes as well as the addition of mating disruption. Our study extends the existing literature by proposing the use of Wolbachia introductions 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.

Infochemical use and dietary specialization in parasitoids: a meta-analysis.

Many parasitoid species use olfactory cues to locate their hosts. In tritrophic systems, parasitoids of herbivores can exploit the chemical blends emitted by plants in reaction to herbivore-induced damage, known as herbivore-induced plant volatiles (HIPVs). In this study, we explored the specificity and innateness of parasitoid responses to HIPVs using a meta-analysis of data from the literature. Based on the concept of dietary specialization and infochemical use, we hypothesized that (i) specialist parasitoids (i.e., with narrow host ranges) should be attracted to specific HIPV signals, whereas generalist parasitoids (i.e., with broad host ranges) should be attracted to more generic HIPV signals and (ii) specialist parasitoids should innately respond to HIPVs, whereas generalist parasitoids should have to learn to associate HIPVs with host presence. We characterized the responses of 66 parasitoid species based on published studies of parasitoid behavior. Our meta-analysis showed that (i) as predicted, specialist parasitoids were attracted to more specific signals than were generalist parasitoids but, (ii) contrary to expectations, response innateness depended on a parasitoid's target host life stage rather than on its degree of host specialization: parasitoids of larvae were more likely to show an innate response to HIPVs than were parasitoids of adults. This result changes our understanding of dietary specialization and highlights the need for further theoretical research that will help clarify infochemical use by parasitoids.

No inbreeding depression in laboratory-reared individuals of the parasitoid wasp Allotropa burrelli.

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.

Trophic interactions may reverse the demographic consequences of inbreeding.

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.

Diploid male production correlates with genetic diversity in the parasitoid wasp Venturia canescens: a genetic approach with new microsatellite markers.

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), when individuals 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 microsatellite markers in order to assess and compare genetic diversity and diploid male proportion (DMP) in populations from three distinct habitat types - mainland, island, or captive -, in the parasitoid wasp Venturia canescens. Eroded genetic diversity and higher DMP were found in island and captive populations, and habitat type had large effect on genetic diversity. Therefore, DMP 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.

Temporal autocorrelation in host density increases establishment success of parasitoids in an experimental system.

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.

Sterile males in a parasitoid wasp with complementary sex determination: from fitness costs to population extinction.

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.

The male mate search: an optimal foraging issue?

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.

Inbreeding depression in a parasitoid wasp with single-locus complementary sex determination.

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.

Host-parasitoid dynamics and the success of biological control when parasitoids are prone to allee effects.

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.

Time-lag in extinction dynamics in experimental populations: evidence for a genetic Allee effect?

1. 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. 2. 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. 3. 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. 4. 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.

The biology of small, introduced populations, with special reference to biological control.

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.

Intraspecific variability in the parasitoid wasp Trichogramma chilonis: can we predict the outcome of hybridization?

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.

Virgins in the wild: mating status affects the behavior of a parasitoid foraging 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.

Microsatellite-based parentage analysis reveals non-ideal free distribution in a parasitoid population.

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.

Invading parasitoids suffer no Allee effect: a manipulative field experiment.

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.

Herbivore-induced plant volatiles as cues for habitat assessment by a foraging parasitoid.

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.