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Solenodon genome reveals convergent evolution of venom in eulipotyphlan mammals

Casewell, Nicholas R and Petras, Daniel and Card, Daren C and Suranse, Vivek and Mychajliw, Alexis M and Richards, David and Koludarov, Ivan and Albulescu, Laura-Oana and Slagboom, Julien and Hempel, Benjamin-Florian and Ngum, Neville M and Kennerley, Rosalind J and Brocca, Jorge L and Whiteley, Gareth and Harrison, Robert A and Bolton, Fiona M S and Debono, Jordan and Vonk, Freek J and Alfoldi, Jessica and Johnson, Jeremy and Karlsson, Elinor K and Lindblad-Toh, Kerstin and Mellor, Ian R and Sussmuth, Roderich D and Fry, Bryan G and Kuruppu, Sanjaya and Hodgson, Wayne C and Kool, Jeroen and Castoe, Todd A and Barnes, Ian and Sunagar, Kartik and Undheim, Eivind A B and Turvey, Samuel T (2019) Solenodon genome reveals convergent evolution of venom in eulipotyphlan mammals. In: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 116 (51). pp. 25745-25755.

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Official URL: https://dx.doi.org/10.1073/pnas.1906117116

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: Journal Article
Additional Information: Copyright of this article belongs to NATL ACAD SCIENCES
Keywords: convergent molecular evolution; genotype phenotype; gene duplication; venom systems; kallikrein toxin
Department/Centre: Division of Biological Sciences > Centre for Ecological Sciences
Depositing User: Id for Latest eprints
Date Deposited: 16 Jan 2020 08:02
Last Modified: 16 Jan 2020 08:02
URI: http://eprints.iisc.ac.in/id/eprint/64336

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