Egg-laying strategy under natural conditions of Leptopilina boulardi, a hymenopteran parasitoid of Drosophila spp

The hypothesis of optimal host species selection predicts that when a parasitoid has the choice between two host species, it will choose the species thay gives the best survival chances for its progeny. We confirmed this hypothesis by laboratory experiments with Leptopilina boulardi Barb. et al., a cynipid parasitoid which prefers Drosophila melanogaster Meigen (the host species most suitable for parasitoid survival) above D. simulans Sturt. As far as fitness parameters are concerned, the fertility of L. boulardi is higher with D. melanogaster; the egg laying can be spread out over a long period when this host is relatively scarce. This does not occur with D. simulans in which parasitic oviposition stops soon when this host is not abundant.Investigations of this foraging strategy were done under more complex natural conditions. We found that L. boulardi has a type III functional response with D. melanogaster only; furthermore, it seems that a switching effect may exist with this host. Parasitoid females appear to distribute their eggs more regularly on D. melanogaster, thus avoiding superparasitism. This seems to be independent of the relative frequency of this host. However, superparasitism of D. simulans did occur more frequently when this host was scarce.

---

Stratégie de ponte de Leptopilina boulardi (hyménoptère parasite de drosophiles) dans les conditions naturelles

Résumé Le concept de réponse optimale d'un parasite vis-à-vis de l'hôte le plus favorable pour son développement demeure surtout théorique et n'a pu être vérifié que dans les conditions de laboratoire. Nous avons montré que Drosophila melanogaster s'avère être, par rapport à D. simulans, l'hôte le plus favorable pour le développement du cynipide parasite Leptopilina boulardi. Une étude sur le terrain a démontré que ce parasite présente une réponse fonctionnelle densité dépendante vis-à-vis de D. melanogaster et non vis-à-vis de D. simulans, avec un effet de bascule. D'autre part, il s'avère que ce parasite exploite beaucoup mieux son hôte, en évitant le superparasitisme, ceci étant démontré au laboratoire et dans la nature. Enfin, il apparaît qu'il est capable d'allonger sa période de ponte lorsque cet hôte est rare, ce qui ne se produit pas avec D. simulans.

     

Local adaptation of a Drosophila parasitoid: habitat‐specific differences in thermal reaction norms

Local climate is an important source of selection on thermal reaction norms that has been well investigated in cline studies, where populations sampled along altitudinal or latitudinal gradients are compared. Several biotic factors vary with climate, but are rarely integrated as alternative agents of selection to climatic factors. We tested the hypothesis that habitat may select for thermal reaction norms and magnitude of phenotypic plasticity in a drosophila parasitoid, independently of the climate of origin. We sampled populations of Leptopilina boulardi, a Drosophila parasitoid in two different habitats, orchards and forests. Orchards offer laying opportunities over small distances for parasitoids, with a low variability in the number of hosts per patch, while forests offer more dispersed and more variable patches. The sampling was realized in a temperate and a Mediterranean climate. We measured egg load, volume of eggs, longevity and lipid content for parasitoids reared at two temperatures. Reaction norms were opposite for populations from forests and orchards for investment in reproduction, independently of the climate of origin. The maximal investment of resources in reproduction occurred at the lower temperature in orchards and the higher temperature in forests. Host distribution differences between habitats may explain these opposite reaction norms. We also observed a flatter reaction norm for egg load in forests than in orchards. This relative canalization may have been selected in response to the higher variability in laying opportunities observed in forests. Our results demonstrate the potential role of resource distribution in evolution of thermal plasticity.     

EFFECTS OF PARTHENOGENESIS AND GEOGRAPHIC ISOLATION ON FEMALE SEXUAL TRAITS IN A PARASITOID WASP

Population divergence in sexual traits is affected by different selection pressures, depending on the mode of reproduction. In allopatric sexual populations, aspects of sexual behavior may diverge due to sexual selection. In parthenogenetic populations, loss‐of‐function mutations in genes involved in sexual functionality may be selectively neutral or favored by selection. We assess to what extent these processes have contributed to divergence in female sexual traits in the parasitoid wasp Leptopilina clavipes in which some populations are infected with parthenogenesis‐inducing Wolbachia bacteria. We find evidence consistent with both hypotheses. Both arrhenotokous males and males derived from thelytokous strains preferred to court females from their own population. This suggests that these populations had already evolved population‐specific mating preferences when the latter became parthenogenetic. Thelytokous females did not store sperm efficiently and fertilized very few of their eggs. The nonfertility of thelytokous females was due to mutations in the wasp genome, which must be an effect of mutation accumulation under thelytoky. Divergence in female sexual traits of these two allopatric populations has thus been molded by different forces: independent male/female coevolution while both populations were still sexual, followed by female‐only evolution after one population switched to parthenogenesis.     

Egg distributions and the information a solitary parasitoid has and uses for its oviposition decisions

Approximately three decades ago the question was first answered whether parasitoids are able to assess the number or origin of eggs in a host for a solitary parasitoid, Leptopilina heterotoma, by fitting theoretically derived distributions to empirical ones. We extend the set of different theoretically postulated distributions of eggs among hosts by combining searching modes and abilities in assessing host quality. In the models, parasitoids search either randomly (Poisson) (1) or by vibrotaxis (Negative Binomial) (2). Parasitoids are: (a) assumed to treat all hosts equally, (b) able to distinguish them in unparasitised and parasitised hosts only, (c) able to distinguish them by the number of eggs they contained, or (d) able to recognise their own eggs. Mathematically tractable combinations of searching mode (1 and 2) and abilities (a,b,c,d) result in seven different models (M1a, M1b, M1c, M1d, M2a, M2b and M2c). These models have been simulated for a varying number of searching parasitoids and various mean numbers of eggs per host. Each resulting distribution is fitted to all theoretical models. The model with the minimum Akaike's information criterion (AIC) is chosen as the best fitting for each simulated distribution. We thus investigate the power of the AIC and for each distribution with a specified mean number of eggs per host we derive a frequency distribution for classification.Firstly, we discuss the simulations of models including random search (M1a, M1b, M1c and M1d). For M1a, M1c and M1d the simulated distributions are correctly classified in at least 70% of all cases. However, in a few cases model M1b is only properly classified for intermediate mean values of eggs per host. The models including vibrotaxis as searching behaviour (M2a, M2b and M2c) cannot be distinguished from those with random search if the mean number of eggs per host is low. Among the models incorporating vibrotaxis the three abilities are detected analogously as in models with random search.Experiments with two species of solitary parasitoids (L. heterotoma and Asobara tabida) are conducted. All theoretically postulated distributions are separately fitted to the resulting experimental egg distributions. The AIC criterion is used to choose the best fitting theoretical distribution. For both parasitoid species the frequency distribution of best fitting models for experimental data is compared to the classification of distributions generated by simulations. This leads to the conclusion that both L. heterotoma and A. tabida are able to distinguish between parasitised and unparasitised hosts. For L. heterotoma the results point to an ability to assess the number of eggs in a host, whereas A. tabida does not seem to have this ability. This difference suggests that an egg is more valuable for L. heterotoma than for A. tabida.     

Selection in the absence of males does not affect male-female conflict in the parasitoid wasp Leptopilina clavipes (Hymenoptera: Figitidae)

Divergent reproductive interests of males and females can lead to sexually antagonistic coevolution (SAC). In the absence of males, adaptations evolved under SAC are released from selection and expected to deteriorate. In this study, we investigated this prediction using two populations of the parasitoid wasp Leptopilina clavipes, one arrhenotokous and one thelytokous. Thelytokous females were induced to produce sons by curing them of their Wolbachia-infection. We examined whether thelytokous males were less able to inhibit female remating than arrhenotokous males and whether thelytokous females were more susceptible to male-induced longevity reduction than arrhenotokous females. The results showed that females were monandrous, regardless of whether mated with an arrhenotokous or thelytokous male. While ongoing courtship of males reduced female life span, there was no longevity cost of mating for either arrhenotokous or thelytokous females. Our results therefore do not support the idea that adaptations evolved under SAC deteriorate under prolonged female-only selection.     

Variability and genetic components of innate fruit odour recognition in a parasitoid of Drosophila

Abstract This study aims to investigate the genetic variability of olfactory responses to odours from the host habitat, involved in host selection by insect parasitoids. The probing response of females to fruit and non-fruit odours was studied in Leptopilina boulardi Barbotin et al . (Hymenoptera, Figitidae), a parasitoid of the frugivorous Drosophila melanogaster larvae. Responses of two strains (from Nasrallah, Tunisia, and from Brazzaville, Congo) and their hybrids were compared. Probing is a searching mode by repeated ovipositor insertions into the breeding substrate to locate digging larvae. Most Brazzaville females exhibited innate ovipositor probing into agar in response to the fruit aromas (banana, orange, pear, prickly pear), whereas this was rare in the Nasrallah strain. These four fruits are all breeding sites for D. melanogaster, whereas mushroom is not. Mushroom odour did not trigger any probing response in either strain. In addition, the latency of the probing response was shorter in Brazzaville females. Results from hybrid females (F1 and Backcross) showed that both probability to probe in response to a fruit aroma and latency of the response were strongly heritable. Regarding the probability to probe, there was an apparent complete dominance of Nasrallah characteristics, whereas additive inheritance was found in the Brazzaville lineage. The contrast between reciprocal F1 hybrids suggested a strong interaction with non-chromosomal factors. It is suggested that a cytoplasmic factor in the Nasrallah strain decreases females' propensity to probe in response to significant odours. The latency of probing appeared to be under a chromosomal influence. Thus, this study identifies a strong genetic component in the responses to odours from the host habitat. It also provides information on the genetic basis of the two characters studied.     

Geographical variation in encapsulation ability ofDrosophila melanogaster larvae and evidence for parasitoid-specific components

Summary The ability ofDrosophila melanogaster larvae in Europe to encapsulate the eggs of their most important parasitoids,Asobara tabida andLeptopilina boulardi, shows a large amount of geographical variation. Interestingly, encapsulation ability againstA. tabida is not correlated with encapsulation ability againstL. boulardi. This indicates that the encapsulation system ofD. melanogaster larvae has parasitoid-specific components. The variation in encapsulation ability can only partly be explained by the incidence of parasitism on the larvae. This means that factors other than the two parasitoid species must be selection pressures on the encapsulation ability ofD. melanogaster larvae.     

Prevalence of a virus inducing behavioural manipulation near species range border

The densities of conspecific individuals may vary through space, especially at the edge of species range. This variation in density is predicted to influence the diffusion of species‐specific horizontally transmitted symbionts. However, to date there is very little data on how parasite prevalence varies around the border of a host species. Using a molecular epidemiology approach, we studied the prevalence of a vertically and horizontally transmitted virus at the edge of the geographic range of its insect host, the Drosophila parasitoid wasp Leptopilina boulardi. L. boulardi is a Mediterranean parasitoid species showing a recent range expansion to the north (in France). The LbFV virus manipulates the behaviour of females, increasing their tendency to lay additional eggs in already parasitized Drosophila larvae (superparasitism). This is beneficial for the virus because it allows the virus to be horizontally transferred during superparasitism. We show that LbFV prevalence is very high in central populations, intermediate in marginal populations and almost absent from newly established peripheral populations of L. boulardi. We failed to detect any influence of temperature and diapause on viral transmission efficiency but we observed a clear relationship between prevalence and parasitoid density, and between parasitoid density and the occurrence of superparasitism, as predicted by our epidemiological model. Viral strains were all efficient at inducing the behavioural manipulation and viral gene sequencing revealed very low sequence variation. We conclude that the prevalence reached by the virus critically depends on density‐dependent factors, i.e. superparasitism, underlying the selective pressures acting on the virus to manipulate the behaviour of the parasitoid.