Assessing the Relationship between Venom Complexity and Diet Diversity in Rattlesnakes Using a Novel, Genome-Wide Phylogeny

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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