Sex makes them sleepy: host reproductive status induces diapause in a parasitoid population experiencing harsh winters

Abstract

When organisms coevolve, any change in one species can induce phenotypic changes in traits and ecology of the other species. The role such interactions play in ecosystems is central, but their mechanistic bases remain underexplored. Upper trophic level species have to synchronize their life-cycle to both abiotic conditions and to lower trophic level species’ phenology and phenotypic variations. We tested the effect of host seasonal strategy on parasitoid diapause induction by using a holocyclic clone of the pea aphid Acyrthosiphon pisum producing asexual and sexual morphs that are viviparous females (i.e. laying embryos) and oviparous females (laying eggs), respectively, the latter being only present at the end of the growing season. Aphidius ervi parasitoids from populations of contrasted climatic origin (harsh vs. mild winter areas) were allowed to parasitize each morph in a split-brood design and developing parasitoids were next reared under either fall-like or summer-like temperature-photoperiod conditions. We next examined aspects of the host physiological state by comparing the relative proportion of forty-seven metabolites and lipid reserves in both morphs produced under the same conditions. We found that oviparous morphs are cues per se for diapause induction; parasitoids entered diapause at higher levels when developing in oviparous hosts (19.4 ± 3.0%) than in viviparous ones (3.6 ± 1.3%), under summer-like conditions (i.e., when oviparous aphids appear in the fields). This pattern was only observed in parasitoids from the harsh winter area since low diapause levels were observed in the other population, suggesting local adaptations to overwintering cues. Metabolomics analyses show parasitoids’ response to be mainly influenced by the host’s physiology, with higher proportion of polyols and sugars, and more fat reserves being found in oviparous morphs. Host quality thus varies across the seasons and represents one of the multiple environmental parameters affecting parasitoid diapause. Our results underline strong coevolutionary processes between hosts and parasitoids in their area of origin, likely leading to phenological synchronization, and we point out the importance of such bottom-up effects for trait expression, and for the provision of ecosystem services such as biological control in the context of climate change.

Prey–predator phenological mismatch under climate change

“…For example, some parasitoids can enter and terminate prolonged diapause when their hosts adopt the same strategy, indicating that they both are timed by the same external cues, potentially due to strong coevolution [67]. Predictions are more challenging for parasitoid and host species that rely on multiple diapause-inducing cues [68]. Secondly, it will depend on the response of consumer-resource interaction as a whole [69] and on the degree of intimacy among resources and consumers between trophic levels and the strength of their ecological link.…”

Cold tolerance and diapause within and across trophic levels: endoparasitic wasps and their fly host have similar phenotypes

“…For example, the greater tendency of D. alloeum and U. canaliculatus to avert diapause may result in poor energy reserve accumulation (Hahn and Denlinger, 2011) and higher mortality due to energy drain at mild winter temperatures. Conversely, characteristics of host physiology, such as diet or whether the host is in diapause, can have strong effects on parasitoid cold tolerance physiology (Li et al, 2015; Tougeron et al, 2019; but see Alford et al, 2017). Given that all the wasps in our cold tolerance experiments were collected from the same population of hawthorn-infesting R. pomonella , many of the wasps likely had access to similar host-related resources, resulting in similar overwintering success (Hahn and Denlinger, 2011; Toxopeus and Sinclair, 2018).…”

How climate change affects the seasonal ecology of insect parasitoids

“…However, because aphid diapause and aphid sexual morphs are often induced by the same cues as for parasitoid diapause, it is unlikely that conflicting cues would appear for parasitoids between host signals and abiotic signals. In warm environments, aphid parasitoids would more likely stop using aphid sexual morphs as a diapause‐inducing signal (Tougeron et al ., ).…”

“…The host plant plays a crucial role in the seasonal polymorphism and heteroecy of aphids because most aphid species shift from a secondary to a primary host plant at the end of the growing season. This shift is accompanied by the production of sexual aphid morphs (Dixon, 1985), which can be a signal for diapause induction in parasitoids (Polgár et al, 1991;Tougeron et al, 2019). As another example, diapausing larvae of the pecan nut casebearer Acrobasis nuxvorella (Lepidoptera: Pyralidae) resume growth and development when exposed to pecan volatiles during the onset of pecan bud growth in spring (Vargas-Arispuro et al, 2013).…”

“…Predictions are more challenging for parasitoid species that rely on multiple diapause-inducing cues, including those from their host. For example, the parasitoids Aphidius matricariae and A. ervi (Hymenoptera: Braconidae) enter diapause at high levels when parasitising sexual aphids, probably in response to aphid metabolic or hormonal content, whereas diapause is induced by photoperiod and temperature when parasitoids exploit asexual aphids (Polgár et al, 1991;Tougeron et al, 2019). Indeed, sexual female morphs of the pea aphid have been shown to contain more polyols and sugar molecules than asexual females, which may increase diapause incidence in aphid parasitoids .…”