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Numerous cases of evolutionary trait loss and regain have been reported over the years. Here, we argue that such reverse evolution can also become apparent when trait expression is plastic in response to the environment. We tested this idea for the loss and regain of fat synthesis in parasitic wasps. We first show experimentally that the wasp Leptopilina heterotoma switches lipogenesis on in a fat-poor environment, and completely off in a fat-rich environment. Plasticity suggests that this species did not regain fat synthesis, but that it can be switched off in some environmental settings. We then compared DNA sequence variation and protein domains of several more distantly related parasitoid species thought to have lost lipogenesis, and found no evidence for non-functionality of key lipogenesis genes. This suggests that other parasitoids may also show plasticity of fat synthesis. Last, we used individual-based simulations to show that a switch for plastic expression can remain functional in the genome for thousands of generations, even if it is only used sporadically. The evolution of plasticity could thus also explain other examples of apparent reverse evolution.

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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.

Current predictions forthe effects of the climate crisis on biodiversity loss have so far ignored the effects of learning ability and sexual selection. Using the African butterfly Bicyclus anynana,which showsstrong phenotypic plasticity in response to temperature,we showthat learning produces a maladaptive mate preference under climate warming. We modelled climate warming and foundthat as temperature becomes an unreliable cue atthe onset of the dry season,adult butterflies displayed the wet season rather than the dry season form. Femalelearning further suppressed their innate, adaptive sexual preference for dry season males. Instead,females learned to prefer a phenotype transiently present during the seasonal transition. Female fertility and longevity were also affectedby learning,reducingfemalefitness following climate warming. Our results emphasize the importance ofsexual selection,learning,and their fitness consequences for understanding(mal)adaptation of natural populations to climate warming.

Unraveling theorigin of molecular pathways underlying the evolution of adaptive traits is essential forunderstandinghow new lineagesemerge, including the relative contribution ofconserved, ancestral traits, and newly evolved, derived traits. Here, we investigated the evolutionary divergence of sex pheromone communication from moths (mostly nocturnal) to butterflies (mostly diurnal)that occurred~98million years ago. In moths, females typically emit pheromones to attract male mates, but in butterflies pheromonesand used by females for mate choice. The molecular bases of sex pheromone communication arewellunderstood in moths, but haveremained virtually unexplored in butterflies. We useda combination of transcriptomics, real time qPCR, and phylogenetics, to identify genes involved in different steps of sex pheromone communication in the butterflyBicyclus anynana. Our results show that the biosynthesis and reception of sex pheromonesrelies both on moth-specific gene families (reductases) and onmore ancestral insect gene families (desaturases, olfactory receptors, odorant binding proteins). Interestingly, B. anynana further appears to use what was believed to be the moth-specific neuropeptide Pheromone Biosynthesis Activating Neuropeptide (PBAN) for regulationof sex pheromone production. Altogether, our results suggest that a mosaic pattern best explains how sex pheromone communication evolved in butterflies, with some molecular components derived from moths, and others conserved from more ancient insect ancestors. This is the first large-scale analysis of the genetic pathways underlying sex pheromone communication in a butterfly.

Effects of plants on herbivores can cascade up the food web and modulate the abundance of higher trophic levels. In agro-ecosystems, plant viruses can affect the interactions between crops, crop pests, and natural enemies. Little is known, however, about the effects of viruses on higher trophic levels, including parasitoids and their ability for pest regulation. We tested the hypothesis that a plant virus affects parasitoid foraging behaviour through cascading effects on higher trophic levels. We predicted that the semi-persistent Beet yellows virus (BYV) would influence plant (Beta vulgaris) quality, as well as aphid host (Aphis fabae) quality for a parasitoid Lysiphlebus fabarum. We determined amino acid and sugar content in healthy and infected plants (first trophic level), lipid content and body size of aphids (second trophic level) fed on both plants, as well as foraging behaviour and body size of parasitoids (third trophic level) that developed on aphids fed on both plants. Our results showed that virus infection increased sugars and decreased total amino acid content in B. vulgaris. We further observed an increase in aphid size without modification in host aphid quality (i.e., lipid content), and a slight effect on parasitoid behaviour through an increased number of antennal contacts with host aphids. Although the BYV virus clearly affected the first two trophic levels, it did not affect development or emergence of parasitoids. As the parasitoid L. fabarum does not seem to be affected by the virus, we discuss the possibility of using it for the development of targeted biological control against aphids.

A recent study showed that a wingless parasitoid, Gelis agilis, exhibits a suite of ant-like traits that repels attack from wolf spiders. When agitated, G. agilis secreted 6-methyl-5-hepten-2-one (sulcatone), which a small number of ant species produce as an alarm/panic pheromone. Here, we tested four Gelis parasitoid species, occurring in the same food chain and microhabitats, for the presence of sulcatone and conducted two-species choice bioassays with wolf spiders to determine their degree of susceptibility to attack. All four Gelis species, including both winged and wingless species, produced sulcatone, whereas a closely related species, Acrolyta nens, and the more distantly related Cotesia glomerata, did not. In two-choice bioassays, spiders overwhelmingly rejected the wingless Gelis species, preferring A. nens and C. glomerata. However, spiders exhibited no preference for either A. nens or G. areator, both of which are winged. Wingless gelines exhibited several ant-like traits, perhaps accounting for the reluctance of spiders to attack them. On the other hand, despite producing sulcatone, the winged G. areator more closely resembles other winged cryptines like A. nens, making it harder for spiders to distinguish between these two species. C. glomerata was also preferred by spiders over A. nens, suggesting that other non-sulcatone producing cryptines nevertheless possess traits that make them less attractive as prey. Phylogenetic reconstruction of the Cryptinae reveals that G. hortensis and G. proximus are ‘sister’species, with G. agilis, and G.areator in particular evolving along more distant trajectories. We discuss the possibility that wingless Gelis species have evolved a suite of ant-like traits as a form, of mimicry to repel predators on the ground.

Olfactory communication can be of critical importance for mate choice decisions. Lepidoptera are key model systems for understanding olfactory communication, particularly considering sex pheromone signaling in the context of sexual selection. Solvent extraction or rinsing of pheromone-producing structures is a widespread method for quantifying sex pheromones, but such measures reflect what is stored and may not represent what is actually emitted by an individual during courtship. Here, we address this point for the first time by quantifying the components of the male sex pheromone (MSP) of interacting Bicyclus anynana butterflies, a species for which much information is available onthe role played by MSPs in affecting mating success. Using headspace sampling during courtship and solvent extraction after completion of experiments using the same males, we were able to track individual traits. Our results show that solvent extracts do not reflect quantities of MSP components emitted by live butterflies. We further show that MSP amounts obtained using headspace sampling correlated with male mating success, but solvent extracts did not. Our results further strongly suggest that males actively control MSP emission when faced with increased male-male competition. Common practice solvent extracts may thus not serve as an adequate proxy for male sex pheromone signaling as they are perceived by choosy females. Our study serves as a proof of principle that quantification of male sex pheromone components depends on the method of collection, which could apply to many other insects using short-range chemical signals. This affects our understanding of how sexual selection shapes the evolution of sexually-selected chemical traits.

Aphids are attacked by a broad range of natural enemies, notably parasitoids. These insects lay their egg inside aphids and the larva feed on aphid haemolymph and tissues. Female parasitoids have to make decisions in order to maximize their offspring success, which mainly depends on the host quality. Winged aphids are produced in the colony when environmental conditions are detrimental. This thesis is interested in the nutritional value of winged and wingless aphids and the oviposition choices made by parasitoids and hyperparasitoids (parasitoids that parasitize primary parasitoids). Winged aphids are usually considered as low-quality hosts for parasitoids, because nutrients are required for the production of wings and subsequent flight. We demonstrated that winged aphids of the species Myzus persicae were heavier than wingless aphids and contained more free sugars, lipids and proteins. They are, in our case, hosts of higher quality compared to wingless aphids. Consequently, parasitoids of the species Aphidius colemani and hyperparasitoids of the species Asaphes vulgaris that developed in immature winged aphids were fatter. We were unable, however, to identify a choice between immature winged and wingless hosts as parasitism rates were similar on different morphs in the laboratory. We did, however, show that winged aphids displayed fewer defensive behaviours against parasitoids compared to wingless aphids. In the field, we showed that parasitism rates on winged aphids were far lower than on wingless aphids. Winged aphids contain more nutrients and are less defensive; hence we could expect that winged aphids constitute a risk for parasitoids if they disperse., (SC - Sciences) -- UCL, 2018