The genetics of venom ontogeny in the eastern diamondback rattlesnake (Crotalus adamanteus).

Darin R Rokyta,Elda E Sanchez,Micaiah J Ward,Mark J Margres

doi:10.7717/peerj.3249

Darin R Rokyta, Elda E Sanchez + Show 2 more

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https://doi.org/10.7717/peerj.3249

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Abstract

The same selective forces that give rise to rapid inter- and intraspecific divergence in snake venoms can also favor differences in venoms across life-history stages. Ontogenetic changes in venom composition are well known and widespread in snakes but have not been investigated to the level of unambiguously identifying the specific loci involved. The eastern diamondback rattlesnake was previously shown to undergo an ontogenetic shift in venom composition at sexual maturity, and this shift accounted for more venom variation than geography. To characterize the genetics underlying the ontogenetic venom compositional change in C. adamanteus, we sequenced adult/juvenile pairs of venom-gland transcriptomes from five populations previously shown to have different adult venom compositions. We identified a total of 59 putative toxin transcripts for C. adamanteus, and 12 of these were involved in the ontogenetic change. Three toxins were downregulated, and nine were upregulated in adults relative to juveniles. Adults and juveniles expressed similar total levels of snake-venom metalloproteinases but differed substantially in their featured paralogs, and adults expressed higher levels of Bradykinin-potentiating and C-type natriuretic peptides, nerve growth factor, and specific paralogs of phospholipases A2 and snake venom serine proteinases. Juvenile venom was more toxic to mice, indicating that the expression differences resulted in a phenotypically, and therefore potentially ecologically, significant difference in venom function. We also showed that adult and juvenile venom-gland transcriptomes for a species with known ontogenetic venom variation were equally effective at individually providing a full characterization of the venom genes of a species but that any particular individual was likely to lack several toxins in their transcriptome. A full characterization of a species’ venom-gene complement therefore requires sequencing more than one individual, although the ages of the individuals are unimportant.

Highlights

Snake venoms are traits of moderate genetic complexity comprised largely of proteinaceous toxins that function in predation and defense (Boldrini-Franca et al, 2010; Calvete et al, How to cite this article Rokyta et al (2017), The genetics of venom ontogeny in the eastern diamondback rattlesnake (Crotalus adamanteus)
We have substantially increased this number through a combination of longer reads, which helps the assembly of longer toxins such as snake-venom metalloproteinases (SVMPs), and inclusion of animals from throughout the species’ range
We showed that the ontogenetic change in C. adamanteus has a simple, statistically significant transcriptional basis, which was consistent with the proteomic patterns underlying the ontogenetic change in C. adamanteus described by Margres et al (2015b) and the functional characterizations described by Margres et al (2016a)

Summary

Introduction

Snake venoms are traits of moderate genetic complexity comprised largely of proteinaceous toxins that function in predation and defense (Boldrini-Franca et al, 2010; Calvete et al., How to cite this article Rokyta et al (2017), The genetics of venom ontogeny in the eastern diamondback rattlesnake (Crotalus adamanteus). With some exceptions (Margres et al, 2015a; Margres et al, 2016b), snake venoms have been found to evolve rapidly under positive selection within and between species, involving both changes in toxin expression patterns (Gibbs, Sanz & Calvete, 2009; Rokyta et al, 2015; Margres et al, 2015a; Margres et al, 2015b) and protein sequences (Lynch, 2007; Gibbs & Rossiter, 2008) This rapid evolution is thought to result from the evolutionarily critical roles of venom in feeding and defense (Jansa & Voss, 2011) and the antagonistic coevolutionary interactions with predators and prey (Biardi, Chien & Coss, 2005; Biardi et al, 2011). Ontogenetic changes in venom composition have been identified in numerous snake species (e.g., Mackessy, 1988; Glenn, Straight & Wolf, 1994; López-Lozano et al, 2002; Saldarriaga et al, 2003; Mackessy et al, 2006; Calvete et al, 2010; Zelanis et al, 2010; Durban et al, 2013; Rokyta et al, 2015), but certainly not in all species that have been examined (e.g., Gibbs et al, 2011; Rokyta et al, 2015)

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