Assessing the Relationship between Venom Complexity and Diet Diversity in Rattlesnakes Using a Novel

Holding, Matthew L.

matthewholding28@gmail.com

Department of Biological Science

Florida State University Tallahassee, Florida, USA

Strickland, Jason L.

Rautsaw, Rhett M.

Mason, Andrew J.

Hofmann, Erich P.

Department of Biological Sciences

Clemson University Clemson, South Carolina, USA

Hogan, Michael P.

Ellsworth, Schyler Nystrom, Gunnar Department of Biological Science

Florida State University Tallahassee, Florida, USA

Margres, Mark M.

Department of Biological Sciences Clemson University Clemson, South Carolina, USA

Colston, Timothy J.

Department of Biological Science

Florida State University

Tallahassee, Florida, USA

Borja, Miguel

Facultad de Ciencias Biológicas Universidad

Juárez del Estado de Durango Gómez Palacio, Durango, Mexico

Grüwald, Christoph I.

Jones, Jason M.

Herp.mx A.C.

Villa del Álvarez, Colima, Mexico

Castañeda, Gamaliel

Facultad de Ciencias Biológicas Universidad

Juárez del Estado de Durango

Gómez Palacio, Durango, Mexico

de Sousa, Lucia A. F.

da Silva, Ana Moura

Laboratório de Imunopatologia Instituto Butantan

São Paulo, Brazil

Azevedo, Inacio

Grazziotin, Felipe G.

Laboratório Especial de Toxinologia Aplicada

Instituto Butantan

São Paulo, Brazil

Gibbs, H. Lisle

Department of Evolution, Ecology, and Organismal Biology

Ohio State University

Columbus, Ohio, USA

Rokyta, Darin R.

Department of Biological Science

Florida State University

Tallahassee, Florida, USA

Parkinson, Christopher L.

Department of Biological Sciences

Department of Forestry and Environmental Conservation

Clemson University

Clemson, South Carolina, USA

Organisms are more than the sum of their parts, making the study of complex integrated phenotypes imperative for understanding the interplay between the evolution of traits and the evolution of species. Molecular trait complexity is particularly important in species interactions, where more diverse networks of species interactions may select for molecular complexity in offensive or defensive traits, such as secreted toxins. Animal venoms, as injected secretions with a tractable genetic basis, are optimal systems for testing the hypothesis that the evolution of more complex molecular traits is associated with interacting with diverse prey taxa. The rattlesnakes (Crotalus and Sistrurus) are the most speciose group of vipers, consisting of ~50 currently described species. Rattlesnakes are medically important as they contribute the majority of snakebites in North America. Additionally, they are flagships for curiosity, culture, and conservation of snakes. We have collected venom glands of 147 individual snakes, representing most rattlesnake lineages. We use > 1500 nontoxin sequences from venom gland transcriptomes to infer the phylogeny of rattlesnakes, and characterize the composition and complexity of toxin expression in the transcriptomes and in chromatographic profiles of whole venom. We combine a novel, dated phylogeny of rattlesnakes, venom gene expression data, and published diet data to test the hypothesis that more complex venoms evolve in response to a more taxonomically complex diet. Our work provides new insight into the evolutionary history of this complex and iconic group, and relates complexity in patterns of gene expression to the complexity of ecological interactions an organism must face.


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