Life history constraints contribute to the vulnerability of a declining North American rattlesnake

Waldron, Jayme L.; Welch, Shane M.; Bennett, Stephen H.; Kalinowsky, Wade G.; Mousseau, Timothy A.

doi:10.1016/j.biocon.2012.11.021

Cited by 19 publications

(34 citation statements)

References 41 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…1). Because of the ontogenetic shift in venom composition (Margres et al, 2015b), specimens ≥102 cm were classified as adults and individuals <102 cm were classified as juveniles (Waldron et al, 2013), consistent with previous analyses (Margres et al, 2015a, b; 2016). All venom samples included in this study had been analyzed previously (i.e., reversed-phase high-performance liquid chromatography (RP-HPLC) and statistical analyses; Margres et al, 2015a, b, 2016).…”

Section: Methodsmentioning

confidence: 63%

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

View full text Add to dashboard Cite

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.

show abstract

Section: Methodsmentioning

confidence: 63%

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

View full text Add to dashboard Cite

show abstract

“…Maturity was assessed based on SVL with individuals ≥102 cm classified as adults and individuals <102 cm classified as juveniles (Waldron et al . ). Population designations were taken from Margres et al .…”

Section: Methodsmentioning

confidence: 97%

“…The total data set was then split into two age classes (juveniles and adults) as described above (Waldron et al . ). Principal component analyses were performed on each of these age classes to explore the effect of shape among populations north and south of the Suwannee River drainage.…”

Section: Methodsmentioning

confidence: 97%

Phenotypic integration in the feeding system of the eastern diamondback rattlesnake (Crotalus adamanteus)

et al. 2015

View full text Add to dashboard Cite

Selection can vary geographically across environments and temporally over the lifetime of an individual. Unlike geographic contexts, where different selective regimes can act on different alleles, age-specific selection is constrained to act on the same genome by altering age-specific expression. Snake venoms are exceptional traits for studying ontogeny because toxin expression variation directly changes the phenotype; relative amounts of venom components determine, in part, venom efficacy. Phenotypic integration is the dependent relationship between different traits that collectively produce a complex phenotype and, in venomous snakes, may include traits as diverse as venom, head shape and fang length. We examined the feeding system of the eastern diamondback rattlesnake (Crotalus adamanteus) across environments and over the lifetime of individuals and used a genotype-phenotype map approach, protein expression data and morphological data to demonstrate that: (i) ontogenetic effects explained more of the variation in toxin expression variation than geographic effects, (ii) both juveniles and adults varied geographically, (iii) toxin expression variation was a result of directional selection and (iv) different venom phenotypes covaried with morphological traits also associated with feeding in temporal (ontogenetic) and geographic (functional) contexts. These data are the first to demonstrate, to our knowledge, phenotypic integration between multiple morphological characters and a biochemical phenotype across populations and age classes. We identified copy number variation as the mechanism driving the difference in the venom phenotype associated with these morphological differences, and the parallel mitochondrial, venom and morphological divergence between northern and southern clades suggests that each clade may warrant classification as a separate evolutionarily significant unit.

show abstract

“…Samples were collected across all months and seasons. C. adamanteus reaches sexual maturity at approximately 102-cm snout-vent length (Waldron et al 2013), and M. fulvius becomes sexually mature at approximately 50-cm snout-vent length (Jackson and Franz 1981). All specimens used in our analyses met or exceeded these measurements.…”

Section: Sample Collectionmentioning

confidence: 99%

Contrasting Modes and Tempos of Venom Expression Evolution in Two Snake Species

et al. 2014

View full text Add to dashboard Cite

Selection is predicted to drive diversification within species and lead to local adaptation, but understanding the mechanistic details underlying this process and thus the genetic basis of adaptive evolution requires the mapping of genotype to phenotype. Venom is complex and involves many genes, but the specialization of the venom gland toward toxin production allows specific transcripts to be correlated with specific toxic proteins, establishing a direct link from genotype to phenotype. To determine the extent of expression variation and identify the processes driving patterns of phenotypic diversity, we constructed genotype-phenotype maps and compared range-wide toxin-protein expression variation for two species of snake with nearly identical ranges: the eastern diamondback rattlesnake (Crotalus adamanteus) and the eastern coral snake (Micrurus fulvius). We detected significant expression variation in C. adamanteus, identified the specific loci associated with population differentiation, and found that loci expressed at all levels contributed to this divergence. Contrary to expectations, we found no expression variation in M. fulvius, suggesting that M. fulvius populations are not locally adapted. Our results not only linked expression variation at specific loci to divergence in a polygenic, complex trait but also have extensive conservation and biomedical implications. C. adamanteus is currently a candidate for federal listing under the Endangered Species Act, and the loss of any major population would result in the irrevocable loss of a unique venom phenotype. The lack of variation in M. fulvius has significant biomedical application because our data will assist in the development of effective antivenom for this species. N ATURAL selection can be a powerful force driving rapid diversification within species and is predicted to lead to local adaptation through the increase in frequency of mutations in gene-regulatory or protein-coding regions (Stern 2000;Hoekstra and Coyne 2007;Carroll 2008;Muller 2007). Expression variation at single loci has produced adaptive phenotypic divergence in the beaks of Darwin's finches (Abzhanov et al. 2004), coat color in mice (Manceau et al. 2011), and mimicry in butterflies (Reed et al. 2011). Most traits, however, are products of poorly characterized developmental pathways involving many loci. Many of the fundamental features of evolving systems, such as evolvability, epistasis, pleiotropy, and basic variational properties (Rokyta et al. 2008(Rokyta et al. , 2009(Rokyta et al. , 2011bWager 2008;Chou et al. 2011;Woods et al. 2011;Hill and Zhang 2012), result from the relationship between genotype and phenotype (Stadler et al. 2001;Hansen 2006), but the ability to study this relationship directly in polygenic traits is rare. Therefore, linking gene-regulatory changes to adaptive evolution in polygenic, complex phenotypes remains a challenge (Romero et al. 2012;Savolainen et al. 2013).Snake venoms are complex cocktails of 40-100 proteinaceous toxins (Boldrini-França et ...

show abstract

Life history constraints contribute to the vulnerability of a declining North American rattlesnake

Cited by 19 publications

References 41 publications

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

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

Phenotypic integration in the feeding system of the eastern diamondback rattlesnake (Crotalus adamanteus)

Contrasting Modes and Tempos of Venom Expression Evolution in Two Snake Species

Contact Info

Product

Resources

About