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Divergent venom effectors correlate with ecological niche in neuropteran predators

ABSTRACT: Neuropteran larvae are fierce predators that use venom to feed on arthropods, but their venom system is poorly understood. The iconic antlions (Myrmeleontidae) are adapted to dry, sandy habitats, where they use pitfall traps and venom to catch and subdue large arthropod prey. The aphid lions, larvae of green lacewings (Chrysopidae) primarily hunt for smaller prey, such as aphids. Here, we investigate the tissue origin, composition and ecological role of venom in the European antlion Euroleon nostras and the green lacewing Chrysoperla carnea. We show that E. nostras venom has potent insecticidal activity, indicating its importance for efficient immobilization of large prey. C. carnea venom exerted no toxic effects, reflecting their specialization to small, non-defensive prey. Histological and proteotranscriptomic analysis revealed that antlion venom is produced in three distinct glands that secrete different proteins, indicating a functional compartmentalization of venom compounds. The venom system of E. nostras contains no bacteria, providing strong evidence that all venom compounds are of insect origin and not produced by bacterial symbionts as previously suggested. Our study provides a detailed analysis of the neuropteran venom system and new insights into venom biochemistry and function that may underpin the adaptation of antlions to their unique ecological niche.

INSTRUMENT(S): Q Exactive Plus

ORGANISM(S): Chrysoperla Carnea Euroleon Nostras

SUBMITTER: Jennifer Schwarz

LAB HEAD: Dr. Heiko

PROVIDER: PXD047026 | Pride | 2024-08-13

REPOSITORIES: Pride

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Project description:We found that assassin bugs from the earliest-diverging subfamily of higher Reduviidae (Peiratinae), as well as a subfamily closely related to Triatominae (Stenopodainae) have venom that is highly similar in composition to that produced by previously examined reduviids from Harpactorinae and Reduviinae. This finding suggests that venom composition has been largely stable due to purifying selection among the higher Reduviidae, which is consistent with the ancient origin of venom in the ancestors of Heteroptera 250–300 million years ago (Sunagar and Moran 2015; Walker et al. 2018a). This near homogeneity of venom composition is perhaps surprising considering that reduviid predators have evolved numerous instances of prey specialization and specialized hunting strategies that might be expected to co-evolve with venom. Possibly, further studies focussing on species with more specialized hunting strategies, or different kinds of venom bioactivities, will uncover more nuanced venom adaptations. Alternatively, it is possible that the protease-rich venoms of predatory reduviids are simply well-suited to myriad different hunting strategies. These data are consistent with other examples where venoms are surprisingly similar despite great differences in biology, for example between solitary and eusocial bees. A more detailed picture of venom evolution in Reduviidae would examine venom produced by the early-diverging Phymatine complex as well as venoms of non-reduviid cimicomorphs, prey specialists such as the arachnophagous Emesinae and the myrmecophagous Holoptilinae, and some of the many groups that employ hunting specializations, such as the use of plant resins to catch prey (Hwang and Weirauch 2012). Within Triatominae, examination of saliva produced by additional species from multiple lineages (especially those that switched to blood-feeding independently, if the subfamily is shown to be polyphyletic) and including generalists and specialists on different host taxa and species associated especially with nests and burrows will be informative. The venoms of predatory reduviids such as Zelurus spp. and Opisthacidius spp. that are most closely related to Triatominae, and share some behaviours such as habitation of bird nests by Opisthacidius spp. may also provide more information about the evolution of triatomine saliva.

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Divergent venom effectors correlate with ecological niche in neuropteran predators

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