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Population genomics of venom genes in Speckled Rattlesnakes


Highland, Dylan K.



Farleigh, Keaka                                                                                                                                         

Alderman, Megan G.                                                                                                                                   

Department of Biology                                                                                                                                 

University of Virginia                                                                                                                             

Charlottesville, Virginia USA


Hirst, Samuel R.                                                                                                                                           

Department of Integrative Biology                                                                                                               

University of South Florida                                                                                                                            

Tampa, Florida USA


Perry, Blair W.                                                                                                                                               

Ecology and Evolutionary Biology                                                                                                              

University of California Santa Cruz                                                                                                                

Santa Cruz, California USA


Margres, Mark J.                                                                                                                                             

Department of Integrative Biology                                                                                                               

University of South Florida                                                                                                                            

Tampa, Florida USA


Holding, Matthew L.                                                                                                                                          

Life Sciences Institute                                                                                                                                 

University of Michigan                                                                                                                                       

Ann Arbor, Michigan USA


Schield, Drew                                                                                                                                    

Department of Biology                                                                                                                                 

University of Virginia                                                                                                                            

Charlottesville, Virginia USA


Understanding the evolution of complex, ecologically-relevant traits in closely related species is key to linking patterns of selection to organismal fitness. Such traits may exhibit substantial inter- and intraspecific variation in both expressed phenotypes and their underlying genetic basis. In rattlesnakes (genus Crotalus), venom is under intense selection due to its requirement for prey acquisition and predator defense. Venom is encoded by numerous gene families and venom expression is known to be impacted by many factors, including genetics, age, environment, prey diversity, and resistance in prey species. Here, we use a population genomic dataset to study venom gene regions in Speckled Rattlesnakes to identify how venom has been variably shaped by forms of natural selection. We first assembled a new chromosome-level reference genome for the Southwestern Speckled Rattlesnake (Crotalus pyrrhus) from Arizona and performed detailed annotation of venom genes. Then, using both within and between-population comparisons at shallow and deeper evolutionary timescales, we applied a series of population genetic tests designed to detect footprints of natural selection. We find that several of the major venom gene families (e.g., snake venom metalloproteinases and several snake venom serine proteases) harbor excess trans-species polymorphism consistent with long-term balancing selection on these components of the venom phenotype. Other genes (e.g., highly-expressed phospholipase A2s) show signatures of recent positive selection, highlighting distinct evolutionary responses to variable selection pressures at major effect venom loci. Our findings further lend population genetic perspectives supporting the broad conclusion that the genetic architecture of venom facilitates the efficiency of selection via independent assortment of unlinked multi-gene venom gene families.

 
 
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