Jetske de Boer

Hyperparasitoids are some of the most diverse members of insect food webs. True hyperparasitoids parasitize the larvae of other parasitoids, reaching these larvae with their ovipositor through the herbivore that hosts the parasitoid larva. During pupation, primary parasitoids also may be attacked by pseudohyperparasitoids that lay their eggs on the parasitoid (pre)pupae. By attacking primary parasitoids, hyperparasitoids may affect herbivore population dynamics, and they have been identified as a major challenge in biological control. Over the past decades, research, especially on aphid- and caterpillar-associated hyperparasitoids, has revealed that hyperparasitoids challenge rules on nutrient use efficiency in trophic chains, account for herbivore outbreaks, or stabilize competitive interactions in lower trophic levels, and they may use cues derived from complex interaction networks to locate their hosts. This review focuses on the fascinating ecology of hyperparasitoids related to how they exploit and locate their often inconspicuous hosts and the insect community processes in which hyperparasitoids are prominent players.

Parasitoids lay their eggs in or on a host, usually another insect. During foraging, parasitoids can encounter insects that differ in terms of host suitability and quality. At one extreme end of this spectrum are non-hosts that are unsuitable for offspring development. Non-hosts are generally ignored but parasitization does occur and occasionally also results in egg deposition. Here, the authors investigate how oviposition in a non-host influences subsequent foraging behaviour of a parasitoid and whether this is mediated by learning. The study system consists of the endoparasitoid Cotesia glomerata and the presumed non-host caterpillar Mamestra brassicae. In the presence of Pieris brassicae hosts and/or their traces (frass), C. glomerata inserted its ovipositor into M. brassicae caterpillars. Eggs were deposited, but all eggs disappeared within 96 h, confirming the non-host status of M. brassicae. In contrast to the expectation, there was no memory retention after oviposition in a non-host and parasitoids did not alter their behaviour with respect to non-host contacts and ovipositions. Instead, C. glomerata became more motivated to forage on a non-host infested leaf. The authors propose that egg deposition in non-hosts by C. glomerata might be due to their high egg load, which is thought to make parasitoids less selective on host quality, especially when they have few reproductive opportunities. In such cases, fitness costs to individual females are low. Egg deposition in non-hosts might ultimately lead to host range expansion if parasitoids overcome the defence response of non-hosts over evolutionary time.

Adults of many mosquito species feed on plants to obtain metabolic energy and to enhance reproduction. Mosquitoes primarily rely on olfaction to locate plants and are known to respond to a range of plant volatiles. We studied the olfactory response of the yellow fever mosquito Aedes aegypti to methyl jasmonate (MeJA) and cis-jasmone (CiJA), volatile compounds originating from the octadecanoid signaling pathway that plays a key role in plant defense against herbivores. Specifically, we investigated how Ae. aegypti of different ages responded to elevated levels of CiJA in two attractive odor contexts, either derived from Lima bean plants or human skin. Aedes aegypti females landed significantly less often on a surface with CiJA and MeJA compared to the solvent control, CiJA exerting a stronger reduction in landing than MeJA. Odor context (plant or human) had no significant main effect on the olfactory responses of Ae. aegypti females to CiJA. Mosquito age significantly affected the olfactory response, older females (7–9 d) responding more strongly to elevated levels of CiJA than young females (1–3 d) in either odor context. Our results show that avoidance of CiJA by Ae. aegypti is independent of odor background, suggesting that jasmonates are inherently aversive cues to these mosquitoes. We propose that avoidance of plants with elevated levels of jasmonates is adaptive to mosquitoes to reduce the risk of encountering predators that is higher on these plants, i.e. by avoiding ‘enemy-dense-space’.

Endogenous viruses form an important proportion of eukaryote genomes and a source of novel functions. How large DNA viruses integrated into a genome evolve when they confer a benefit to their host, however, remains unknown. Bracoviruses are essential for the parasitism success of parasitoid wasps, into whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome at a chromosomal scale, that bracovirus genes colonized all ten chromosomes of Cotesia congregata. Most form clusters of genes involved in particle production or parasitism success. Genomic comparison with another wasp, Microplitis demolitor, revealed that these clusters were already established ~53 mya and thus belong to remarkably stable genomic structures, the architectures of which are evolutionary constrained. Transcriptomic analyses highlight temporal synchronization of viral gene expression without resulting in immune gene induction, suggesting that no conflicts remain between ancient symbiotic partners when benefits to them converge.

Animals can alter their foraging behavior through associative learning, where an encounter with an essential resource (e.g., food or a reproductive opportunity) is associated with nearby environmental cues (e.g., volatiles). This can subsequently improve the animal's foraging efficiency. However, when these associated cues are encountered again, the anticipated resource is not always present. Such an unrewarding experience, also called a memory-extinction experience, can change an animal's response to the associated cues. Although some studies are available on the mechanisms of this process, they rarely focus on cues and rewards that are relevant in an animal's natural habitat. In this study, we tested the effect of different types of ecologically relevant memory-extinction experiences on the conditioned plant volatile preferences of the parasitic wasp Cotesia glomerata that uses these cues to locate its caterpillar hosts. These extinction experiences consisted of contact with only host traces (frass and silk), contact with nonhost traces, or oviposition in a nonhost near host traces, on the conditioned plant species. Our results show that the lack of oviposition, after contacting host traces, led to the temporary alteration of the conditioned plant volatile preference in C. glomerata, but this effect was plant species-specific. These results provide novel insights into how ecologically relevant memory-extinction experiences can fine-tune an animal's foraging behavior. This fine-tuning of learned behavior can be beneficial when the lack of finding a resource accurately predicts current, but not future foraging opportunities. Such continuous reevaluation of obtained information helps animals to prevent maladaptive foraging behavior.

Malaria parasites (Plasmodium) can change the attractiveness of their vertebrate hosts to Anopheles vectors, leading to a greater number of vector-host contacts and increased transmission. Indeed, naturally Plasmodium-infected children have been shown to attract more mosquitoes than parasite-free children. Here, we demonstrate Plasmodium-induced increases in the attractiveness of skin odor in Kenyan children and reveal quantitative differences in the production of specific odor components in infected vs. parasite-free individuals. We found the aldehydes heptanal, octanal, and nonanal to be produced in greater amounts by infected individuals and detected by mosquito antennae. In behavioral experiments, we demonstrated that these, and other, Plasmodium-induced aldehydes enhanced the attractiveness of a synthetic odor blend mimicking "healthy" human odor. Heptanal alone increased the attractiveness of "parasite-free" natural human odor. Should the increased production of these aldehydes by Plasmodium-infected humans lead to increased mosquito biting in a natural setting, this would likely affect the transmission of malaria.

The host preferences of the anthropophilic mosquito species in the Anopheles gambiae complex (Diptera: Culicidae) are mediated by skin bacterial volatiles. However, it is not known whether these mosquitoes respond differentially to skin bacterial volatiles from non-human host species. In this study, the responses of two malaria mosquito species in the An. gambiae complex, Anopheles gambiae s.s. (hereafter, An. gambiae) and Anopheles arabiensis, with different host preferences, to volatiles released from skin bacteria were tested. Skin bacteria collected from human, cow and chicken skin significantly increased trap catches; traps containing bacteria collected from human skin caught the highest proportions of An. gambiae and An. arabiensis. Traps with bacteria of human origin caught a significantly higher proportion of An. gambiae than of An. arabiensis, whereas bacterial volatiles from the chicken attracted significantly higher numbers of An. arabiensis than of An. gambiae. Additionally, An. gambiae showed a specialized response to volatiles from four specific bacteria, whereas An. arabiensis responded equally to all species of bacteria tested. Skin bacterial volatiles may therefore play important roles in guiding mosquitoes with different host preferences. The identification of these bacterial volatiles can contribute to the development of an odour blend that attracts mosquitoes with different host preferences.

An attractive way to improve our understanding of sex determination evolution is to study the underlying mechanisms in closely related species and in a phylogenetic perspective. Hymenopterans are well suited owing to the diverse sex determination mechanisms, including different types of Complementary Sex Determination (CSD) and maternal control sex determination. We investigated different types of CSD in four species within the braconid wasp genus Asobara that exhibit diverse life-history traits. Nine to thirteen generations of inbreeding were monitored for diploid male production, brood size, offspring sex ratio, and pupal mortality as indicators for CSD. In addition, simulation models were developed to compare these observations to predicted patterns for multilocus CSD with up to ten loci. The inbreeding regime did not result in diploid male production, decreased brood sizes, substantially increased offspring sex ratios nor in increased pupal mortality. The simulations further allowed us to reject CSD with up to ten loci, which is a strong refutation of the multilocus CSD model. We discuss how the absence of CSD can be reconciled with the variation in life-history traits among Asobara species, and the ramifications for the phylogenetic distribution of sex determination mechanisms in the Hymenoptera.

Natural enemies may go through genetic bottlenecks during the process of biological control introductions. Such bottlenecks are expected to be particularly detrimental in parasitoid Hymenoptera that exhibit complementary sex determination (CSD). CSD is associated with a severe form of inbreeding depression because homozygosity at one or multiple sex loci leads to the production of diploid males that are typically unviable or sterile. We observed that diploid males occur at a relatively high rate (8-13% of diploid adults) in a field population of Cotesia rubecula in Minnesota, USA, where this parasitoid was introduced for biological control of the cabbage white Pieris rapae. However, our laboratory crosses suggest two-locus CSD in a native Dutch population of C. rubecula and moderately high diploid males survival (approximately 70%), a scenario expected to produce low proportions of diploid males. We also show that courtship behavior of diploid males is similar to that of haploid males, but females mated to diploid males produce only very few daughters that are triploid. We use our laboratory data to estimate sex allele diversity in the field population of C. rubecula and discuss the possibility of a sex determination meltdown from two-locus CSD to effective single-locus CSD during or after introduction.