Venom evolution in robber flies: An integrative approach applying functional morphology in venomics
Animal Physiology and Biochemistry
Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions
Final Report Abstract
In at least 80 instances venoms evolved convergently in the animal kingdom safeguarding the success of venomous species in all animal lineages. Despite the obvious importance of venoms we still lack of a broader understanding of the processes that drive venom evolution and the general biology of most venomous species, including the morphology of venom delivery systems. So far only few species from groups like snakes, spiders, scorpions and cone-snails are better studied. Insect venoms are as well surprisingly under-represented, only few hymenopteran species are more detailed studied. Robber flies (Asilidae, Diptera) are known since longer to hunt larger and/or well defensive prey, such as dragonflies or hymenopterans and were assumed to employ venom with a neurotoxic component because of the rapid paralysis of their prey. The liquefied extracts of thoracic gland tissue showed after injecting the liquid into different bioassay species neurotoxic effects that vary in strength depending on the asilid species, however, the venom composition remained unknown. In this project we addressed the morphology of the venom gland system in robber flies using synchrotron micro-CT reconstructions. This first high-resolution scans revealed a complex system of muscles and valves that enables a high-speed injection of the venom from the thoracic glands into the proboscis and finally into the prey (The labial glands were rejected as part of the venom delivery system because of a lacking connection into the hypopharynx). The complementary, first proteo-transcriptomic venomics analysis of asilid venoms showed that the major, higher expressed and secreted venom components belong to new unique venom protein classes, which we named asilidins (Asilidin1 - asilidin14). In contrast to other venomous species such as spiders, robber flies secrete only few enzymatic components. However, in all species a neurotoxic component (Asilidin1) was identified that resembles an ICK knottin (Cystein scaffolded knottin) very similar to known neurotoxin variants from scorpions or spiders. First bioassays underpin an obvious neurotoxic effect. The low amount of enzymatic proteins for the three species Machimus arthriticus, Eutolmus rufibarbis and Dasypogon diadema can be explained by our proposed mechanism of envenomation: Asilids first inject venom to paralyze the prey, in a second step they inject likely regurgitated enzymes from the gut content and in a final step they suck up the liquefied prey – all steps are orchestrated by the complex morphology. Finally, we contributed the currently largest analyses using comparative genomics to identify processes that drive toxin gene evolution in robber flies by sequencing also a de novo draft genome of Dasypogon diadema. It is shown that robber fly toxin genes evolve by a diverse, multi-modal mechanism, in which single copy co-opted genes, duplicated genes and lineage unique orphan genes contribute to the complex venom cocktail and the function of its venom proteins. • Erste Studie zu Giftevolution in Raubfliegen veröffentlicht, IdW: https://idw-online.de/de/news687204 • Giftige Killerfliegen, Laborjournal: https://www.laborjournal.de/editorials/1434.php • Frankfurter Allgemeine Sonntagszeitung, Nr 22, 0306.2018: https://www.faz.net/aktuell/wissen/leben-gene/raubfliegen-wie-intelligent-insekten-wirklich-sind-15625395.html • BR Radiowissen: Tiergifte – Naturheilstoffe in der Medizin (21.03.2019): https://www.br.de/mediathek/podcast/radiowissen/tiergifte-naturheilstoffe-in-der-medizin/1505794
Publications
- (2018): A dipterans novel sucker punch: Evolution of arthropod atypical venom with a neurotoxic component in robber flies (Asilidae, Diptera). Toxins 10(1), 29
Drukewitz HS, Fuhrmann N, Undheim EAB, Blanke A, Giribaldi J, Mary Rosanna, Lacond G, Dutertre S, von Reumont BM
(See online at https://doi.org/10.3390/toxins10010029) - Studying small and neglected organisms in modern evolutionary venomics implementing RNASeq (transcriptomics) – a critical guide. (2018): Toxins, 10, 292
von Reumont BM
(See online at https://doi.org/10.3390/toxins10070292) - (2019): Toxins from scratch? – Diverse, multimodal gene origins in predatory robber flies indicate dynamic venom evolution in dipteran insects. GigaScience
Drukewitz SH, Bokelmann L, Undheim E, von Reumont BM
(See online at https://doi.org/10.1093/gigascience/giz081) - The Significance of Comparative Genomics in Modern Evolutionary Venomics. Front. Ecol. Evol. 2019, 7
Drukewitz, S. H.; Reumont, von, BM
(See online at https://doi.org/10.3389/fevo.2019.00163)
