Solenodon genome reveals convergent evolution of venom in eulipotyphlan mammals

Casewell, Nicholas R, Petras, Daniel, Card, Daren C, Suranse, Vivek, Mychajliw, Alexis M, Richards, David, Koludarov, Ivan, Albulescu, Laura-Oana, Slagboom, Julien, Hempel, Benjamin-Florian, Ngum, Neville M, Kennerley, Rosalind J, Brocca, Jorge L, Whiteley, Gareth, Harrison, Robert A, Bolton, Fiona M S, Debono, Jordan, Vonk, Freek J, Alföldi, Jessica, Johnson, Jeremy, Karlsson, Elinor K, Lindblad-Toh, Kerstin, Mellor, Ian R, Süssmuth, Roderich D, Fry, Bryan G, Kuruppu, Sanjaya, Hodgson, Wayne C, Kool, Jeroen, Castoe, Todd A, Barnes, Ian, Sunagar, Kartik, Undheim, Eivind A B and Turvey, Samuel T (2019) Solenodon genome reveals convergent evolution of venom in eulipotyphlan mammals. Proceedings of the National Academy of Sciences of the United States of America, 116 (51). pp. 25745-25755. ISSN 1091-6490

[img]
Preview
PDF (Published_Version) - Published Version
Available under License Creative Commons Attribution.

Download (1MB) | Preview

Abstract

Venom systems are key adaptations that have evolved throughout the tree of life and typically facilitate predation or defense. 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 characterizing 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 4 independent origins of venom in eulipotyphlans outnumbering all other venom origins in mammals. We find that KLK1s have been independently coopted 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
Additional Information: Copyright © 2019 the Author(s). Published by PNAS.
Faculty \ School: Faculty of Science > School of Biological Sciences
Depositing User: LivePure Connector
Date Deposited: 03 Dec 2019 02:13
Last Modified: 19 Mar 2020 02:40
URI: https://ueaeprints.uea.ac.uk/id/eprint/73238
DOI: 10.1073/pnas.1906117116

Actions (login required)

View Item View Item