Bet-hedging in parasitoids: when optimization is not the best strategy to cope with climatic extremes.

Bet-hedging occurs when unreliable environments select for genotypes exhibiting a lower variance in fitness at the cost of a lower mean fitness for each batch of progeny. This means that at the level of the genotype, the production of mostly non-optimal phenotypes may be favored when at least some phenotypes are successful. As extreme unreliable climatic events are increasing because of climate change, it is pertinent to investigate the potential of bet-hedging strategies that allow insects to cope with climate change. Evidence for bet-hedging is scarce in most insects, including parasitoids, but the unique lifestyle and biology of parasitoids leads to the expectation that bet-hedging may occur frequently. Here, we evaluate a range of parasitoid traits for which a bet-hedging strategy could be envisioned even if bet-hedging has not been identified as such yet. Under-identification of bet-hedging in nature could have resulted from a major focus of studies on parasitoid life history evolution and foraging behavior on optimality models, predicting how mean fitness can be maximized. Most environmental factors, however, vary unpredictably. Life history and behavioral adaptations are thus expected to be affected by environmental stochasticity. In this paper, we review different aspects of parasitoid behavior, physiology, and life histories and ask the question whether parasitoid traits could have evolved under selection by environmental stochasticity.

No evidence for competition over floral resources between winter-active parasitoids and pollinators in agroecosystems.

Warming temperate winters are resulting in increased insect winter activity. With modern agroecosystems largely homogenous, characterised by low floral diversity, competitive interactions may arise between flower-visiting species, with potential implications for the ecosystem services they provide (e.g. biological control and pollination). Flower strips may be implemented during winter months to support flower-visiting insects and enhance ecosystem service provision. Employing field trials conducted in Brittany, France between 2019 and 2021 and laboratory cage experiments, the current study examined the impact of winter flower strips on aphid biological control performed by parasitoid wasps and the potential for competitive interactions between winter-active parasitoids and pollinators. Results revealed that parasitism rate was not enhanced by the presence of winter flower strips. This lack of effect was not the consequence of pollinator presence, and the current study found no effect of pollinator abundance on parasitism rate. Flower strips may thus be implemented during winter months to support nectar-feeding insects when floral resources are scarce, with no evidence of exploitative competition between pollinators and parasitoids, nor a detrimental impact on biological control provision.

Many parasitoids lack adult fat accumulation, despite fatty acid synthesis: A discussion of concepts and considerations for future research.

Fat reserves, specifically the accumulation of triacylglycerols, are a major energy source and play a key role for life histories. Fat accumulation is a conserved metabolic pattern across most insects, yet in most parasitoid species adults do not gain fat mass, even when nutrients are readily available and provided ad libitum. This extraordinary physiological phenotype has evolved repeatedly in phylogenetically dispersed parasitoid species. This poses a conundrum because it could lead to significant constraints on energy allocation toward key adult functions such as survival and reproduction. Recent work on the underlying genetic and biochemical mechanisms has spurred a debate on fat accumulation versus fat production, because of incongruent interpretation of results obtained using different methodologies. This debate is in part due to semantics, highlighting the need for a synthetic perspective on fat accumulation that reconciles previous debates and provides new insights and terminology. In this paper, we propose updated, unambiguous terminology for future research in the field, including "fatty acid synthesis" and "lack of adult fat accumulation", and describe the distinct metabolic pathways involved in the complex process of lipogenesis. We then discuss the benefits and drawbacks of the main methods available to measure fatty acid synthesis and adult fat accumulation. Most importantly, gravimetric/colorimetric and isotope tracking methods give complementary information, provided that they are applied with appropriate controls and interpreted correctly. We also compiled a comprehensive list of fat accumulation studies performed during the last 25 years. We present avenues for future research that combine chemistry, ecology, and evolution into an integrative approach, which we think is needed to understand the dynamics of fat accumulation in parasitoids.

Parasitoid ecology along geographic gradients: lessons for climate change studies.

One method to study the impact of climate change on host-parasitoid relationships is to compare populations along geographical gradients in latitude, altitude, or longitude. Indeed, temperatures, which vary along geographic gradients, directly shape the life traits of parasitoids and indirectly shift their populations through trophic interactions with hosts and plants. We explored the pros and cons of using these comparisons along gradients. We highlighted that the longitudinal gradients, although understudied, are well correlated to winter warming and summer heat waves and we draw attention to the impact of the increase in extreme events, which will probably be the determining parameters of the effect of climate change on host-parasitoid relationships.

Composition and Food Web Structure of Aphid-Parasitoid Populations on Plum Orchards in Chile.

By increasing plant diversity in agroecosystems, it has been proposed that one can enhance and stabilize ecosystem functioning by increasing natural enemies' diversity. Food web structure determines ecosystem functioning as species at different trophic levels are linked in interacting networks. We compared the food web structure and composition of the aphid- parasitoid and aphid-hyperparasitoid networks in two differentially managed plum orchards: plums with inter-rows of oats as a cover crop (OCC) and plums with inter-rows of spontaneous vegetation (SV). We hypothesized that food web composition and structure vary between OCC and SV, with network specialization being higher in OCC and a more complex food web composition in SV treatment. We found a more complex food web composition with a higher species richness in SV compared to OCC. Quantitative food web metrics differed significantly among treatments showing a higher generality, vulnerability, interaction evenness, and linkage density in SV, while OCC presented a higher degree of specialization. Our results suggest that plant diversification can greatly influence the food web structure and composition, with bottom-up effects induced by plant and aphid hosts that might benefit parasitoids and provide a better understanding of the activity, abundance, and interactions between aphids, parasitoids, and hyperparasitoids in plum orchards.

Composition and structure of winter aphid-parasitoid food webs along a latitudinal gradient in Chile.

All species interact in complex antagonistic or mutualistic networks that may be driven by turnover in species composition due to spatiotemporal environmental filtering. Therefore, studying differences in insect communities along environmental gradients may improve our understanding of the abiotic and biotic factors that shape the structure of trophic networks. Parasitoids are interesting models to do so, due to their intimate eco-evolutionary relationship with their hosts. We explored the differences in cereal aphid-parasitoid food webs during the winter among nine localities in Chilean central-south valley, along a gradient of 1200 km from north (29° S) to south (40° S). We hypothesized that diapause incidence would increase in the coldest areas, resulting in a lower number of parasitoid species active during the winter. Consequently, network specialization, generality, and vulnerability indexes should increase with decreasing latitude, which implies fewer and more weakly connected links per parasitoid species through an increased fraction of basal host species. Based on the severity of winter, three areas along the explored gradient were distinguished, but clustering did not follow a clear north-south latitudinal gradient. Instead, few differences were observed in overwintering strategies, with very low levels of diapause in all localities, and no major differences in food-web composition. The major differences along the gradient were the relative abundances of the different aphid, parasitoid and hyperparasitoid species, with higher levels of spatial and temporal variation observed for the less abundant species. Our results provide a better understanding of the activity and abundance of aphid parasitoids during winter in relation to climatic conditions.

Effect of a cover crop on the aphid incidence is not explained by increased top-down regulation.

Background: Cover crops can be used as a habitat management strategy to enhance the natural enemies and their temporal synchronization with a target pest. We examined the effect of winter oat intercropping within organic plum orchards on the natural enemy abundance and seasonal dynamics on the biological control of plum aphids in spring in Central Chile. Methods: We compared the incidence and abundance of natural enemies and aphid pests from winter to the end of spring using two treatments: (1) plum trees with an oat cover crop (OCC) and (2) plum trees without a cover crop but with spontaneous vegetation (SV). We hypothesized that cover crops allow the development of winter cereal aphids, promoting the early arrival of natural enemies in spring, resulting in an earlier control of plum aphids. Results: Winter cereal aphids developed well on the OCC, and as a result, a lower plum aphid incidence in spring was observed when compared to the SV. However, the abundance of natural enemies and the parasitism rates cannot explain the positive impacts of the oat cover crop on the aphid populations as there were no differences between treatments. A potential effect of the oat due to chemical and/or physical stimuli (bottom-up effects) could help to explain these results.

Dealing with predictable and unpredictable temperatures in a climate change context: the case of parasitoids and their hosts.

The Earth's climate is changing at a rapid pace. To survive in increasingly fluctuating and unpredictable environments, species can either migrate or evolve through rapid local adaptation, plasticity and/or bet-hedging. For small ectotherm insects, like parasitoids and their hosts, phenotypic plasticity and bet-hedging could be critical strategies for population and species persistence in response to immediate, intense and unpredictable temperature changes. Here, we focus on studies evaluating phenotypic responses to variable predictable thermal conditions (for which phenotypic plasticity is favoured) and unpredictable thermal environments (for which bet-hedging is favoured), both within and between host and parasitoid generations. We then address the effects of fluctuating temperatures on host-parasitoid interactions, potential cascading effects on the food web, as well as biological control services. We conclude our review by proposing a road map for designing experiments to assess if plasticity and bet-hedging can be adaptive strategies, and to disentangle how fluctuating temperatures can affect the evolution of these two strategies in parasitoids and their hosts.

Suitability and Profitability of a Cereal Aphid for the Parasitoid Aphidius platensis in the Context of Conservation Biological Control of Myzus persicae in Orchards.

The use of cover crops can promote the abundance and early arrival of populations of natural enemies. Cereal cover crops between orchards rows could encourage the early arrival of the parasitoid Aphidius platensis, as they offer alternative winter hosts (e.g., Rhopalosiphum padi), enhancing the control of Myzus persicae in spring. However, the preference for and suitability of the alternative host must be addressed beforehand. To evaluate the potential of this strategy, we assessed host preference using behavioural choice tests, as well as no-choice tests measuring fitness traits, when developing on both host species. One source field for each aphid population from the above hosts was chosen. There was a clear choice for R. padi compared to M persicae, independently of the source, probably due to more defensive behaviours of M. persicae (i.e., kicks and escapes). Nevertheless, both aphid species were suitable for parasitoids' development. The female progeny developed on R. padi were larger in size, irrespective of their origin. According to our results, in peach orchards with cereals sown between peach trees during the autumn, where we expect when R. padi populations will no longer be available during spring, A. platensis should be able to switch to M. persicae.

Transdisciplinary Bioblitz: Rapid biotic and abiotic inventory allows studying environmental changes over 60 years at the Biological Field Station of Paimpont (Brittany, France) and opens new interdisciplinary research opportunities.

BACKGROUND: The Biological Field Station of Paimpont (Station Biologique de Paimpont, SBP), owned by the University of Rennes and located in the Brocéliande Forest of Brittany (France), has been hosting student scientific research and field trips during the last 60 years. The study area of the SBP is a landscape mosaic of 17 ha composed of gorse moors, forests, prairies, ponds and creeks. Land use has evolved over time. Historical surveys by students and researchers focused on insects and birds. With this study, we aimed to increase the range of taxa observations, document changes in species composition and landscape and provide a basis for interdisciplinary research perspectives. We gathered historical data, implemented an all-taxon biodiversity inventory (ATBI) in different habitats of the SBP study area, measured abiotic factors in the air, water and soil and performed a photographical landscape observation during the BioBlitz held in July 2017. NEW INFORMATION: During the 24 h BioBlitz, organised by the SBP and the EcoBio lab from the University of Rennes and the French National Center of Scientific Research (CNRS), different habitats were individually sampled. Seventy-seven experts, accompanied by 120 citizens and 12 young people participating in the European Volunteer Service, observed, identified and databased 660 species covering 5 kingdoms, 8 phyla, 21 classes, 90 orders and 247 families. In total, there were 1819 occurrences including records identified to higher taxon ranks, thereby adding one more kingdom and four more phyla. Historical data collection resulted in 1176 species and 4270 occurrences databased. We also recorded 13 climatic parameters, 10 soil parameters and 18 water parameters during the BioBlitz. Current habitats were mapped and socio-ecological landscape changes were assessed with a diachronic approach using 32 historical photographs and historical maps. The coupling of historical biodiversity data with new biotic and abiotic data and a photographic comparison of landscape changes allows an integrative understanding of how the SBP changed from agriculturally-used land to a managed natural area within the last 60 years. Hence, this BioBlitz represents an important holistic sampling of biodiversity for studies on trophic webs or on trophic interactions or on very diverse, but connected, habitats. The integration of social, biotic and abiotic data opens innovative research opportunities on the evolution of socio-ecosystems and landscapes.

Interspecific competition among aphid parasitoids: molecular approaches reveal preferential exploitation of parasitized hosts.

When a guild of species exploit the same limited resources, interspecific competition induces the exclusion of inferior competitors, in which case, interspecific recognition mechanisms are needed. Here, we address resource partitioning and interspecific competition among three main solitary parasitoid species attacking the same host resource, the aphid Sitobion avenae in wheat fields. Optimal host acceptance models predict that parasitoid species should prefer attacking unparasitized hosts when they are available in order to maximize their fitness, as already parasitized hosts are less valuable for laying eggs, especially for inferior competitors. Therefore, we expected the level of competition (multiparasitism) in the field to increase at low host density. By using a combination of taxonomical (determination) and molecular (PCR-based) approaches, we assessed the species of all parasitoid adults and immature stages within aphid hosts. Our results demonstrate that, early in the season, the multiparasitism rates were low, whereas they were high in the mid-late season, corresponding to an aphid density decrease over time. Moreover, parasitoid species could not have been exploiting host resources randomly and the better competitor, Aphidius ervi, seemed to be foraging preferentially on hosts already parasitized by the inferior competitor A. rhopalosiphi, even when unparasitized hosts were still available. This could be due to differences in their host detection capability, as species with a narrow host range may be better at detecting their hosts in comparison with species with a greater host range, such as A. ervi, with a greater host range within the guild. Our study suggests differences in the host exploitation of two prevalent parasitoid species through the main period of aphid colonization, which still allowed the coexistence of a third inferior competitor (A. rhopalosiphi) within the assemblage, in spite of some negative interactions (multiparasitism) and redundancies.

What are the costs of learning? Modest trade-offs and constitutive costs do not set the price of fast associative learning ability in a parasitoid wasp.

Learning ability has been associated with energetic costs that typically become apparent through trade-offs in a wide range of developmental, physiological, and life-history traits. Costs associated with learning ability can be either constitutive or induced, depending on whether they are always incurred or only when information is actively learned and memorized. Using lines of the parasitoid wasp Nasonia vitripennis that were selected for fast associative learning ability, we assessed a range of traits that have previously been identified as potential costs associated with learning. No difference in longevity, lipid reserves, tibia length, egg load, or fecundity was observed between the selected and control lines. All of these traits are considered to potentially lead to constitutive costs in the setup of this study. A gradual reversal to baseline learning after two forms of relaxed selection was indicative of a small constitutive cost of learning ability. We also tested for a trade-off with other memory types formed at later stages, but found no evidence that the mid-term memory that was selected for caused a decrease in performance of other memory types. In conclusion, we observe only one minor effect of a constitutive cost and none of the other costs and trade-offs that are reported in the literature to be of significant value in this case. We, therefore, argue for better inclusion of ecological and economic costs in studies on costs and benefits of learning ability.

When parasitoids deal with the spatial distribution of their hosts: consequences for both partners.

Insect parasitoids developing inside hosts face a true challenge: hosts are scattered in the field and their localization and selection require the use of complex and sometime confusing information. It was assumed for a long time that small-brained organisms like parasitoids have evolved simple and efficient behavioral mechanisms, leading them to be adapted to a given ecological situation, for example, the spatial distribution of hosts in the habitat. However, hosts are not static and their distribution may also vary through generations and within the life of parasitoid individuals. We investigated if and how parasitoids deal with such a spatial complexity in a mesocosm experiment. We used the Aphidius rhopalosiphi/Sitobion avenae parasitoid/host system to investigate if parasitoid females experiencing different host aggregation levels exhibit different foraging behaviors independently of the number of hosts in the environment. We showed that A. rhopalosiphi females exploited hosts more intensively both within and among patches at higher host aggregation levels. We discussed the adaptiveness of such behaviors in the light of evolution and biological control.

Selection for associative learning of color stimuli reveals correlated evolution of this learning ability across multiple stimuli and rewards.

We are only starting to understand how variation in cognitive ability can result from local adaptations to environmental conditions. A major question in this regard is to what extent selection on cognitive ability in a specific context affects that ability in general through correlated evolution. To address this question, we performed artificial selection on visual associative learning in female Nasonia vitripennis wasps. Using appetitive conditioning in which a visual stimulus was offered in association with a host reward, the ability to learn visual associations was enhanced within 10 generations of selection. To test for correlated evolution affecting this form of learning, the ability to readily form learned associations in females was also tested using an olfactory instead of a visual stimulus in the appetitive conditioning. Additionally, we assessed whether the improved associative learning ability was expressed across sexes by color-conditioning males with a mating reward. Both females and males from the selected lines consistently demonstrated an increased associative learning ability compared to the control lines, independent of learning context or conditioned stimulus. No difference in relative volume of brain neuropils was detected between the selected and control lines.

Intraspecific maternal competition induces summer diapause in insect parasitoids.

Organisms often live in unpredictable environments and have to adopt life history strategies that optimize their fitness under these conditions. According to bet-hedging theory, individuals can reduce variation in fitness outcomes by investing in different strategies at the same time. For arthropods, facultative summer diapause enables survival during dry and hot periods of the year, and can be triggered by a decrease in resource abundance. However, the effect of resource depletion on diapause induction has never been disentangled from the effect of the perception of the presence of competitors. Using two solitary parasitoid species of cereal aphids as a model system, Aphidius avenae (Haliday) and Aphidius rhopalosiphi (De Stefani-Perez) (Hymenoptera: Braconidae), we tested whether (i) low absolute host density and/or (ii) high levels of parasitoid females' competition lead to maternal-induced summer diapause in parasitoid offspring. Under summer-like climatic conditions, emerging parasitoid females were (i) reared alone and exposed to different host densities (from 5 to 130 aphids), or (ii) reared together with competing females (from 2 to 20 females) and then exposed individually to 50 aphids. For both parasitoid species, low aphid densities did not induce summer diapause. However, the incidence of summer diapause increased up to a maximum of 11% with increasing levels of competition experienced by female parasitoids. More than 60% of the females produced both diapausing and nondiapausing offspring after being kept at the two highest competition densities. Such a "spreading-the-risk" strategy has likely evolved to optimize parasitoid fitness by preventing the following generation from exposure to low populations of suitable hosts and high mortality from superparasitism. These results provide the first experimental evidence of direct maternal competition-induced diapause in insects, and may change the way we apprehend the evolution of arthropod seasonal ecology, by considering intraspecific competition.

Pesticide stress on plants negatively affects parasitoid fitness through a bypass of their phytophage hosts.

Pesticides taken up by plants from the soil or interstitial (pore) water can cascade to higher trophic levels, which are expected to be more affected due to cumulative bottom-up effects. Knowledge about the impact of indirect exposure to pesticides on non-target terrestrial trophic chains, however, is still lacking. Therefore, we examined the direct and indirect effects of three concentrations of the herbicide 2,6-dichlorobenzonitrile (DCBN) and an insecticide with a similar molecular structure (1,4-dichlorobenzene, DCB) on the fitness traits of a tritrophic system: the wheat plant Triticum aestivum, the aphid Sitobion avenae and its specialist parasitoid Aphidius rhopalosiphi. To mimic exposure via interstitial water the toxicants were added to the growth medium of the plant. Passive dosing between the medium and a silicon layer was used to achieve constant exposure of the poorly soluble pesticides. Wheat plants exposed to both pesticides grew smaller and had reduced biomasses. Negative effects on the reproductive rate, biomass and the number of aphids were only observable at the highest concentration of DCBN. Overall parasitism rate decreased when exposed to both pesticides and parasitoid attack rates decreased at lower concentrations of DCBN and at the highest DCB concentration. The parasitoid sex ratio was extremely male-biased in the presence of DCBN. Our results demonstrate that pesticides can alter the performance of higher trophic levels by sublethal effects, through a bypass of the second trophic level. In addition, the novel test system used was suitable for detecting such carryover effects on non-target organisms.

Are aphid parasitoids from mild winter climates losing their winter diapause?

Temperature is both a selective pressure and a modulator of the diapause expression in insects from temperate regions. Thus, with climate warming, an alteration of the response to seasonal changes is expected, either through genetic adaptations to novel climatic conditions or phenotypic plasticity. Since the 1980s in western France, the winter guild of aphid parasitoids (Hymenoptera: Braconidae) in cereal fields has been made up of two species: Aphidius rhopalosiphi and Aphidius matricariae. The recent activity of two other species, Aphidius avenae and Aphidius ervi, during the winter months suggests that a modification of aphid parasitoid overwintering strategies has taken place within the guild. In this study, we first performed a field survey in the winter of 2014/15 to assess levels of parasitoid diapause incidence in agrosystems. Then, we compared the capacity of the four parasitoid species to enter winter diapause under nine different photoperiods and temperature conditions in the laboratory. As predicted, historically winter-active species (A. rhopalosiphi and A. matricariae) never entered diapause, whereas the species more recently active during winter (A. avenae and A. ervi) did enter diapause but at a low proportion (maximum of 13.4 and 11.2%, respectively). These results suggest rapid shifts over the last three decades in the overwintering strategies of aphid parasitoids in Western France, probably due to climate warming. This implies that diapause can be replaced by active adult overwintering, with potential consequences for species interactions, insect community composition, ecosystem functioning, and natural pest control.

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.

Evolutionary ecology of the interactions between aphids and their parasitoids.

Many organisms, including entomopathogenous fungi, predators or parasites, use aphids as ressources. Parasites of aphids are mostly endoparasitoid insects, i.e. insects which lay eggs inside the body of an other insect which will die as a result of their development. In this article, we review the consequences of the numerous pecularities of aphid biology and ecology for their endoparasitoids, notably the Aphidiinae (Hymenoptera: Braconidae). We first examine the various mechanisms used by aphids for defence against these enemies. We then explore the strategies used by aphidiine parasitoids to exploit their aphid hosts. Finally, we consider the responses of both aphids and parasitoids to ecological constraints induced by seasonal cycles and to environmental variations linked to host plants and climate. The fundamental and applied interest of studying these organisms is discussed.