Solenodon genome reveals convergent evolution of venom in eulipotyphlan mammals

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 JohnsonElinor 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, Samuel T. Turvey

*Corresponding author for this work

Research output: Contribution to JournalArticle

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.

Original languageEnglish
Pages (from-to)25745-25755
Number of pages11
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number51
Early online date26 Nov 2019
DOIs
Publication statusPublished - 17 Dec 2019

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Keywords

  • Convergent molecular evolution
  • Gene duplication
  • Genotype phenotype
  • Kallikrein toxin
  • Venom systems

Cite this

Casewell, N. R., Petras, D., Card, D. C., Suranse, V., Mychajliw, A. M., Richards, D., ... Turvey, S. 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), 25745-25755. https://doi.org/10.1073/pnas.1906117116