New publication: Solenodon genome reveals convergent evolution of venom in eulipotyphlan mammals

By Nicholas R. Casewell et al. (including Eivind A. B. Undheim*) in PNAS

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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.


PNAS
December 17, 2019 116 (51) 25745-25755
First published November 26, 2019
DOI: 10.1073/pnas.1906117116
Publication webpage.


Nicholas R. Casewell, Daniel Petras, Daren C. Card, Vivek Suranse, Alexis M. Mychajliw, David Richards, Ivan Koludarov, Laura-Oana Albulescu, Julien Slagboom, Benjamin-Florian Hempel, Neville M. Ngum, Rosalind J. Kennerley, Jorge L. Brocca, Gareth Whiteley, Robert A. Harrison, Fiona M. S. Bolton, Jordan Debono, Freek J. Vonk, Jessica Alföldi, Jeremy Johnson, Elinor K. Karlsson, Kerstin Lindblad-Toh, Ian R. Mellor, Roderich D. Süssmuth, Bryan G. Fry, Sanjaya Kuruppu, Wayne C. Hodgson, Jeroen Kool, Todd A. Castoe, Ian Barnes, Kartik Sunagar, Eivind A. B. Undheim*, and Samuel T. Turvey


* Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo, Norway. See the publication webpage for full author information.

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Published Dec. 20, 2019 3:58 PM - Last modified Dec. 20, 2019 4:28 PM