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Solenodon genome reveals convergent evolution of venom in eulipotyphlan mammals

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Casewell, Nicholas ORCID: https://orcid.org/0000-0002-8035-4719, Petras, Daniel, Card, Darren, Suranse, Vivek, Mychajliw, Alexis, Richards, David, Koludarov, Ivan, Albulescu, Laura-Oana, Slagboom, Julien, Hempel, Benjamin-Florian, Ngum, Neville, Kennerley, Rosalind, Brocca, Jorge, Whiteley, Gareth, Harrison, Robert, Bolton, Fiona, Debono, Jordan, Vonk, Freek, Alfoldi, Jessica, Johnson, Jeremy, Karlsson, Elinor, Lindblad-Toh, Kerstin, Mellor, Ian, Sussmuth, Roderich, Fry, Bryan, Kuruppu, Sanjaya, Hodgson, Wayne, Kool, Jeroen, Castoe, Todd, Barnes, Ian, Sunagar, Kartik, Undheim, Eivind and Turvey, Samuel (2019) 'Solenodon genome reveals convergent evolution of venom in eulipotyphlan mammals'. Proceedings of the National Academy of Sciences.

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Abstract

Venom systems are key adaptations that have evolved throughout the tree of life and typically facilitate predation or defence. Despite venoms being model systems for studying a variety of evolutionary and physiological processes, many taxonomic groups remain understudied, including venomous mammals. Within the Order Eulipotyphla, multiple shrew species and solenodons have oral venom systems. Despite morphological variation of their delivery systems, it remains unclear whether venom represents the ancestral state in this group or is the result of multiple independent origins. We investigated the origin and evolution of venom in eulipotyphlans by characterising the venom system of the endangered Hispaniolan solenodon (Solenodon paradoxus). We constructed a genome to underpin proteomic identifications of solenodon venom toxins, before undertaking evolutionary analyses of those constituents, and functional assessments of the secreted venom. Our findings show that solenodon venom consists of multiple paralogous kallikrein 1 (KLK1) serine proteases, which cause hypotensive effects in vivo, and seem likely to have evolved to facilitate vertebrate prey capture. Comparative analyses provide convincing evidence that the oral venom systems of solenodons and shrews have evolved convergently, with the four independent origins of venom in eulipotyphlans outnumbering all other venom origins in mammals. We find that KLK1s have been independently co-opted into the venom of shrews and solenodons following their divergence during the late Cretaceous, suggesting that evolutionary constraints may be acting on these genes. Consequently, our findings represent a striking example of convergent molecular evolution, and demonstrate that distinct structural backgrounds can yield equivalent functions.

Item Type: Article
Subjects: QU Biochemistry > Enzymes > QU 136 Hydrolases
QU Biochemistry > Genetics > QU 500 Genetic phenomena
WD Disorders of Systemic, Metabolic or Environmental Origin, etc > Animal Poisons > WD 400 General works
Faculty: Department: Biological Sciences > Department of Tropical Disease Biology
Digital Object Identifer (DOI): https://doi.org/10.1073/pnas.1906117116
Depositing User: Mary Creegan
Date Deposited: 28 Nov 2019 16:50
Last Modified: 09 Dec 2019 12:28
URI: https://archive.lstmed.ac.uk/id/eprint/12990

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