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.