The transcriptomic and proteomic basis for the evolution of a novel venom phenotype within the Timber Rattlesnake (Crotalus horridus)

Rokyta, Darin R.; Wray, Kenneth P.; McGivern, James J.; Margres, Mark J.

doi:10.1016/j.toxicon.2015.02.015

Cited by 74 publications

(80 citation statements)

References 42 publications

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“…The ilr transformation for statistical analysis of venom samples was recently employed by Margres et al [20] to compare venom toxin expression variation between different populations of two nearly sympatric snake species, C. adamanteus and Micrurus fulvius. The same group has also applied Clr transformation of the raw percentages of toxin transcripts to compare toxin-class expression between adult and juvenile type A (neurotoxic venom) and type B (hemorrhagic venom) Timber rattlesnake (C. horridus) specimens [82], and to test for changes in venom composition that take place in the first few weeks of life of C. adamanteus and C. horridus neonates, after the postnatal shedding event [83].…”

Section: Comparing Venom Proteomes: Removing the Constant-sum Constraintmentioning

confidence: 99%

Constructing comprehensive venom proteome reference maps for integrative venomics

Eichberg

Sanz

Calvete

et al. 2015

Expert Review of Proteomics

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Section: Comparing Venom Proteomes: Removing the Constant-sum Constraintmentioning

confidence: 99%

Constructing comprehensive venom proteome reference maps for integrative venomics

Eichberg

Sanz

Calvete

et al. 2015

Expert Review of Proteomics

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“…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).…”

Section: Introductionmentioning

confidence: 99%

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

Rokyta

Margres

Ward

et al. 2017

PeerJ

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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.

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“…Snake venoms are modular, polygenic traits that are critical for feeding (Biardi et al, 2000) and defense (Jansa and Voss, 2011), resulting in strong selective pressures on the genes encoding venom components at the sequence (Kordiš and Gubenšek, 2000; Lynch, 2007; Gibbs and Rossiter, 2008; Juárez et al, 2008; Rokyta et al, 2011; Margres et al, 2013; Vonk et al, 2013) and expression levels (Daltry et al, 1996; Barlow et al, 2009; Rokyta et al, 2015; Margres et al, 2016). These strong selective pressures are believed to be responsible for the extensive interspecific (Mackessy, 2008; Sanz et al, 2008; Rokyta et al, 2013; McGivern et al, 2014), intraspecific (Daltry et al, 1996; Creer et al, 2003; Gibbs et al, 2009; Boldrini-França et al, 2010; Margres et al, 2015a, 2016; Rokyta et al, 2015), and ontogenetic venom variation (Mackessy, 1988; Mackessy et al, 2003; Guércio et al, 2006; Madrigal et al, 2012; Zelanis et al, 2012; Durban et al, 2013; Margres et al, 2015b; Wray et al, 2015) because venom variation has been shown to be associated with dietary shifts (Daltry et al, 1996; Barlow et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

“…These strong selective pressures are believed to be responsible for the extensive interspecific (Mackessy, 2008; Sanz et al, 2008; Rokyta et al, 2013; McGivern et al, 2014), intraspecific (Daltry et al, 1996; Creer et al, 2003; Gibbs et al, 2009; Boldrini-França et al, 2010; Margres et al, 2015a, 2016; Rokyta et al, 2015), and ontogenetic venom variation (Mackessy, 1988; Mackessy et al, 2003; Guércio et al, 2006; Madrigal et al, 2012; Zelanis et al, 2012; Durban et al, 2013; Margres et al, 2015b; Wray et al, 2015) because venom variation has been shown to be associated with dietary shifts (Daltry et al, 1996; Barlow et al, 2009). These spatial and temporal shifts in resource use presumably lead to shifts in phenotypic optima and should be accompanied by functional divergence (Jensen et al, 2012; Margres et al, 2015b).…”

Section: Introductionmentioning

confidence: 99%

Functional characterizations of venom phenotypes in the eastern diamondback rattlesnake (Crotalus adamanteus) and evidence for expression-driven divergence in toxic activities among populations

Margres

Walls

Suntravat

et al. 2016

Toxicon

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Phenotypes frequently vary across and within species. The connection between specific phenotypic effects and function, however, is less understood despite being essential to our understanding of the adaptive process. Snake venoms are ideal for identifying functionally important phenotypic variation because venom variation is common, and venoms can be functionally characterized through simple assays and toxicity measurements. Previous work with the eastern diamondback rattlesnake (Crotalus adamanteus) used multivariate statistical approaches to identify six unique venom phenotypes. We functionally characterized hemolytic, gelatinase, fibrinogenolytic, and coagulant activity for all six phenotypes, as well as one additional venom, to determine if the statistically significant differences in toxin expression levels previously documented corresponded to differences in venom activity. In general, statistical differences in toxin expression predicted the identified functional differences, or lack thereof, in toxic activity, demonstrating that the statistical approach used to characterize C. adamanteus venoms was a fair representation of biologically meaningful differences. Minor differences in activity not accounted for by the statistical model may be the result of amino-acid differences and/or post-translational modifications, but overall we were able to link variation in protein expression levels to variation in function as predicted by multivariate statistical approaches.

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The transcriptomic and proteomic basis for the evolution of a novel venom phenotype within the Timber Rattlesnake (Crotalus horridus)

Cited by 74 publications

References 42 publications

Constructing comprehensive venom proteome reference maps for integrative venomics

Constructing comprehensive venom proteome reference maps for integrative venomics

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

Functional characterizations of venom phenotypes in the eastern diamondback rattlesnake (Crotalus adamanteus) and evidence for expression-driven divergence in toxic activities among populations

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