Cross effects of heat stress and three insecticides on the survival of the codling moth Cydia pomonella (L.): Investigating the molecular and biochemical mechanisms.

As temperature is expected to strongly increase in the future, understanding temperature-mediated toxicity of insecticides is determinant to assess pest management efficiency in a warming world. Investigating molecular and biochemical mechanisms associated with cross mechanisms of temperature and insecticides on pests' tolerance would also be useful in this context. This study aimed to investigate cross effects between temperature and insecticides on the survival of a major pest, the codling moth Cydia pomonella, and their underlying mechanisms. The effect of three insecticidal active ingredients, i.e. chlorantraniliprole, emamectin and spinosad, was assessed at different temperatures on: (i) C. pomonella larval survival; (ii) detoxification enzymes activities (cytochrome P450 multi-function oxygenases, carboxylesterases and glutathione S-transferases) and (iii) genes expression of some detoxification enzymes, heat shock proteins and receptors targeted by the insecticides. We observed a decreased efficiency of emamectin and spinosad at high temperature to control the codling moth while no influence of temperature on chlorantraniliprole efficacy was observed. Detoxification enzymes activities were improved by heat stress alone but not by double stress (temperature + insecticides). Moreover, two detoxification genes (Cyp9A61 and Gst1) were over-expressed by a single stress but not by two stresses while Hsp70 and Cyp6B2 genes may be involved in tolerance to two stresses in C. pomonella. These results confirmed the cross effects of temperature and insecticides on C. pomonella for emamectin and spinosad and provided clues to understand how temperature affects the susceptibility of C. pomonella to insecticides. They illustrate however the complexity of molecular and biochemical responses of individuals facing multiple stresses.

Ovigeny index increases with temperature in an aphid parasitoid: Is early reproduction better when it is hot?

Studying relative investment of resources towards early and delayed reproduction is central to understand life history evolution since these traits are generally negatively correlated and traded-off against several other fitness components. For this purpose, ovigeny index (OI), which is calculated as the fraction of the maximum potential lifetime egg complement that is mature upon female emergence, has been developed in insects. Despite the central role of temperature on life history evolution in ectotherms, its influence on ovigeny index has never been tested. Adaptive models imply that OI should increase with temperature because of changes in body size, but the same influence may be expected considering physiological effects of temperature on egg maturation rate or amount of energy available. We investigated in the aphid parasitoid Aphidius ervi the influence of temperature experienced by the immature and/or the adult (from 12 °C to 28 °C) on ovigeny index and oviposition behaviour. As predicted, OI increased between 16 and 28 °C, i.e. females were able to reproduce earlier as temperature increased but this was traded off against a lower delayed reproduction. The highest OI was however observed at 12°, probably because this temperature was too low for females to mature eggs. Females that developed at 20 °C and were transferred as adult at 24 °C and 28 °C had the highest ovigeny index and laid more eggs during the early oviposition period while those transferred at 16 °C laid more eggs at the end of their life. Our results suggest that ovigeny index is not only influenced by body size - i.e. the adaptive explanation - but also by adult egg maturation rate, lifespan or amount of energy available - i.e. a physiological and adaptive explanation.

Response of life-history traits to artificial and natural selection for virulence and nonvirulence in a Drosophila parastitoid, Asobara tabida.

Co-evolution of host-parasitoid interactions is determined by the costs of host resistance, which received empirical evidence, and the costs of parasitoid virulence, which have been mostly hypothesized. Asobara tabida is a parasitoid, which mainly parasitizes Drosophila melanogaster and D. subobscura, the first species being able to resist to the parasitoid development while the second species is not. To parasitize resistant hosts, including D. melanogaster, A. tabida develops sticky eggs, which prevent encapsulation, but this virulence mechanism may be costly. Interindividual and interpopulation variation in the proportion of sticky eggs respectively allowed us to (i) artificially select and compare life-history traits of a virulent and a nonvirulent laboratory strain, and (ii) compare a virulent and a nonvirulent field strain, to investigate the hypothetical costs of virulence. We observed strong differences between the 2 laboratory strains. The nonvirulent strain invested fewer resources in reproduction and walked less than the virulent one but lived longer. Concerning the field strains, we observed that the nonvirulent strain had larger wings while the virulent one walked more and faster. All together, our results suggest that virulence may not always be costly, but rather that different life histories associated with different levels of virulence may coexist at both intra- and interpopulation levels.

Behavioural effects of temperature on ectothermic animals: unifying thermal physiology and behavioural plasticity.

Temperature imposes significant constraints on ectothermic animals, and these organisms have evolved numerous adaptations to respond to these constraints. While the impacts of temperature on the physiology of ectotherms have been extensively studied, there are currently no frameworks available that outline the multiple and often simultaneous pathways by which temperature can affect behaviour. Drawing from the literature on insects, we propose a unified framework that should apply to all ectothermic animals, generalizing temperature's behavioural effects into: (1) kinetic effects, resulting from temperature's bottom-up constraining influence on metabolism and neurophysiology over a range of timescales (from short to long term), and (2) integrated effects, where the top-down integration of thermal information intentionally initiates or modifies a behaviour (behavioural thermoregulation, thermal orientation, thermosensory behavioural adjustments). We discuss the difficulty in distinguishing adaptive behavioural changes from constraints when observing animals' behavioural responses to temperature. We then propose two complementary approaches to distinguish adaptations from constraints, and categorize behaviours according to our framework: (i) 'kinetic null modelling' of temperature's effects on behaviour; and (ii) behavioural ecology experiments using temperature-insensitive mutants. Our framework should help to guide future research on the complex relationship between temperature and behaviour in ectothermic animals.

Influence of temperature on patch residence time in parasitoids: physiological and behavioural mechanisms.

Patch time allocation has received much attention in the context of optimal foraging theory, including the effect of environmental variables. We investigated the direct role of temperature on patch time allocation by parasitoids through physiological and behavioural mechanisms and its indirect role via changes in sex allocation and behavioural defences of the hosts. We compared the influence of foraging temperature on patch residence time between an egg parasitoid, Trichogramma euproctidis, and an aphid parasitoid, Aphidius ervi. The latter attacks hosts that are able to actively defend themselves, and may thus indirectly influence patch time allocation of the parasitoid. Patch residence time decreased with an increase in temperature in both species. The increased activity levels with warming, as evidenced by the increase in walking speed, partially explained these variations, but other mechanisms were involved. In T. euproctidis, the ability to externally discriminate parasitised hosts decreased at low temperature, resulting in a longer patch residence time. Changes in sex allocation with temperature did not explain changes in patch time allocation in this species. For A. ervi, we observed that aphids frequently escaped at intermediate temperature and defended themselves aggressively at high temperature, but displayed few defence mechanisms at low temperature. These defensive behaviours resulted in a decreased patch residence time for the parasitoid and partly explained the fact that A. ervi remained for a shorter time at the intermediate and high temperatures than at the lowest temperature. Our results suggest that global warming may affect host-parasitoid interactions through complex mechanisms including both direct and indirect effects on parasitoid patch time allocation.

Rising temperature reduces divergence in resource use strategies in coexisting parasitoid species.

Coexistence of species sharing the same resources is often possible if species are phylogenetically divergent in resource acquisition and allocation traits, decreasing competition between them. Developmental and life-history traits related to resource use are influenced by environmental conditions such as temperature, but thermal trait responses may differ among species. An increase in ambient temperature may, therefore, affect trait divergence within a community, and potentially species coexistence. Parasitoids are interesting models to test this hypothesis, because multiple species commonly attack the same host, and employ divergent larval and adult host use strategies. In particular, development mode (arrested or continued host growth following parasitism) has been recognized as a major organiser of parasitoid life histories. Here, we used a comparative trait-based approach to determine thermal responses of development time, body mass, egg load, metabolic rate and energy use of the coexisting Drosophila parasitoids Asobara tabida, Leptopilina heterotoma, Trichopria drosophilae and Spalangia erythromera. We compared trait values between species and development modes, and calculated trait divergence in response to temperature, using functional diversity indices. Parasitoids differed in their thermal response for dry mass, metabolic rate and lipid use throughout adult life, but only teneral lipid reserves and egg load were affected by developmental mode. Species-specific trait responses to temperature were probably determined by their adaptations in resource use (e.g. lipogenesis or ectoparasitism). Overall, trait values of parasitoid species converged at the higher temperature. Our results suggest that local effects of warming could affect host resource partitioning by reducing trait diversity in communities.

Geographic variations of life history traits and potential trade-offs in different populations of the parasitoid Leptopilina heterotoma.

Energy allocation is determined by resource availability and trade-offs among traits, and so organisms have to give some traits priority over others to maximize their fitness according to their environment. In this study, we investigated the geographic variations in life history traits and potential trade-offs in populations of the parasitoid Leptopilina heterotoma (Hymenoptera: Figitidae) originating from the north and the south of the Rhône-Saône valley (over a gradient of 300 km, South-East France). We measured a set of traits related to reproduction, maintenance, and mobility using several estimators of each of these main functions determined at different times. We did not find any clear differences between populations from contrasting areas, whereas the southern populations, which were all assumed to be exposed to similar environmental conditions, displayed contrasting patterns of energy allocation. Thus, the most likely explanation seems to be that the evolution of the life history of L. heterotoma is probably shaped by local selective pressures, such as microclimate, microhabitats, or intensity of competition, rather than by regional ecological conditions. Using our study as an example, we discuss the interest of considering several traits and using different ways of measuring them, concluding that multiple measurements should be performed in future studies to ensure the robustness of the results.

Evolution of metabolic rate in a parasitic wasp: the role of limitation in intrinsic resources.

Metabolic rate, a physiological trait closely related to fitness traits, is expected to evolve in response to two main environmental variables: (1) climate, low metabolic rates being found in dry and hot regions when comparing populations originating from different climates in a common garden experiment and (2) resource limitations, low metabolic rates being selected when resources are limited. The main goal of this study was to investigate if differences in intrinsic resource limitations may have disrupted the expected evolution of metabolic rate in response to climate in a parasitic wasp. We compared CO(2) production of females from 4 populations of a Drosophila parasitoid, Leptopilina boulardi, as an estimate of their metabolic rate. Two populations from a hot and dry area able to synthesise lipids de novo at adult stage were compared with two populations originating from a mild and humid climate where no lipid accumulation during adult life was observed. These last females are thus more limited in lipids than the first ones. We observed that a high metabolic rate has been selected in hot and dry environments, contrarily to the results of a great majority of studies. We suggest that lipogenesis occurring there may have allowed the selection of a higher metabolic rate, as females are less limited in energetic resources than females from the mild environment. A high metabolic rate may have been selected there as it partly compensates for the long distances that females have to cross to find laying opportunities in distant orchards. We suggest that intrinsic resources should be integrated when investigating geographical variations in metabolism as this factor may disrupt evolution in response to climate.

Temperature and parasitism by Asobara tabida (Hymenoptera: Braconidae) influence larval pupation behaviour in two Drosophila species.

In holometabolous insects, pupation site selection behaviour has large consequences for survival. Here, we investigated the combined effects of temperature and parasitism by the parasitoid Asobara tabida on larval pupation behaviour in two of its main Drosophila sp. hosts differing in their climate origin. We found that larvae of Drosophila melanogaster--a species with a (sub)tropical origin--placed at 25°C pupated higher in rearing jars than those placed at 15°C. The opposite pattern was observed for Drosophila subobscura larvae--a species from temperate regions--which pupated lower, i.e. on or near the substrate at 25°C, than those placed at 15°C. When placed at 25°C, parasitized larvae of both species pupated closer to the substrate than unparasitized ones. Moreover, the Drosophila larvae that had been exposed and probably stung by A. tabida, but were not parasitized, pupated lower than the control unparasitized larvae. These results provide new insights of host behaviour manipulation by A. tabida larvae.