Proteomic analysis of ontogenetic and diet-related changes in venom composition of juvenile and adult Dusky Pigmy rattlesnakes (Sistrurus miliarius barbouri)

Gibbs, H. Lisle; Sanz, Libia; Chiucchi, James E.; Farrell, Terence M.; Calvete, Juan J.

doi:10.1016/j.jprot.2011.06.013

Cited by 99 publications

(80 citation statements)

References 42 publications

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“…We did not specifically test for plasticity in this study because venom expression differences have been shown repeatedly to be under genetic control and not environmentally induced (Daltry et al 1996;Gibbs et al 2011;Holding et al 2015;Margres et al 2015b), and the feeding ecology of venomous snakes makes adaptive plasticity unlikely. Because venom is stored for long periods of time (e.g., over winter and between infrequent feeding events) and previous meals may not be robust predictors of future meals, plasticity would be unlikely to provide any adaptive advantage for this trait.…”

Section: Expression Differentiation and Variation Are Constrained To mentioning

confidence: 99%

“…Because venom is stored for long periods of time (e.g., over winter and between infrequent feeding events) and previous meals may not be robust predictors of future meals, plasticity would be unlikely to provide any adaptive advantage for this trait. Gibbs et al (2011) fed different groups of S. miliarius different prey items over extended time periods and did not find any significant changes in venom expression; Margres et al (2015b) documented the ontogenetic shift in venom expression in C. adamanteus in laboratory-raised individuals and found that geographic differences in venom expression held over long periods of time despite the animals being raised under identical conditions in captivity; and Holding et al (2015) recently showed that prey preference is also under genetic control and not affected by previously fed upon items in S. miliarius. Because these studies failed to identify any plastic changes in venoms in the two species in our study that exhibited significant expression differentiation, we rejected the hypothesis that plasticity played any role in generating the observed variation in venom expression.…”

Section: Expression Differentiation and Variation Are Constrained To mentioning

confidence: 99%

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Expression Differentiation Is Constrained to Low-Expression Proteins over Ecological Timescales

Margres¹,

Wray²,

Seavy³

et al. 2015

Genetics

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Protein expression level is one of the strongest predictors of protein sequence evolutionary rate, with high-expression protein sequences evolving at slower rates than low-expression protein sequences largely because of constraints on protein folding and function. Expression evolutionary rates also have been shown to be negatively correlated with expression level across human and mouse orthologs over relatively long divergence times (i.e., 100 million years). Long-term evolutionary patterns, however, often cannot be extrapolated to microevolutionary processes (and vice versa), and whether this relationship holds for traits evolving under directional selection within a single species over ecological timescales (i.e., ,5000 years) is unknown and not necessarily expected. Expression is a metabolically costly process, and the expression level of a particular protein is predicted to be a tradeoff between the benefit of its function and the costs of its expression. Selection should drive the expression level of all proteins close to values that maximize fitness, particularly for high-expression proteins because of the increased energetic cost of production. Therefore, stabilizing selection may reduce the amount of standing expression variation for high-expression proteins, and in combination with physiological constraints that may place an upper bound on the range of beneficial expression variation, these constraints could severely limit the availability of beneficial expression variants. To determine whether rapid-expression evolution was restricted to low-expression proteins owing to these constraints on highly expressed proteins over ecological timescales, we compared venom protein expression levels across mainland and island populations for three species of pit vipers. We detected significant differentiation in protein expression levels in two of the three species and found that rapid-expression differentiation was restricted to low-expression proteins. Our results suggest that various constraints on high-expression proteins reduce the availability of beneficial expression variants relative to lowexpression proteins, enabling low-expression proteins to evolve and potentially lead to more rapid adaptation.KEYWORDS protein expression; selective constraints; evolutionary rates; adaptation T HE expression level of a protein is one of the strongest predictors of protein sequence evolutionary rate; sequences of highly expressed proteins evolve more slowly than low-expression proteins (Duret and Mouchiroud 1999;Pal et al. 2001;Gout et al. 2010;Yang et al. 2012;Nabholz et al. 2013;Park et al. 2013). This relationship may be a function of specific selective constraints on sequences to avoid protein misfolding (Drummond et al. 2005;Geiler-Samerotte et al. 2011), protein misinteractions (Yang et al. 2012, a decrease in protein function (Cherry 2010;Gout et al. 2010), and/or messenger RNA (mRNA) misfolding (Park et al. 2013). Analyses of microarray data have shown that expression evolutionary rate is also negatively...

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Section: Expression Differentiation and Variation Are Constrained To mentioning

confidence: 99%

Section: Expression Differentiation and Variation Are Constrained To mentioning

confidence: 99%

Expression Differentiation Is Constrained to Low-Expression Proteins over Ecological Timescales

Margres¹,

Wray²,

Seavy³

et al. 2015

Genetics

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“…In addition, variation in phenotypes that are directly coupled with predation or herbivory can be associated with variation in the availability or characteristics of nutritional resources. Relevant examples of such phenotypes include beaks of Darwin's finches [6], gill rakers of alewives [7] and sticklebacks [8], radular teeth and drilling behaviours of marine snails [9,10], and venoms of snakes [11][12][13]. Associations between phenotypes and resources may be genetically based [7,10,14], but limited knowledge of genes associated with resource acquisition limits our ability to determine the impact of geographical mosaics of species interactions on the genetic differentiation of populations [3].…”

Section: Introductionmentioning

confidence: 99%

Effects of geographical heterogeneity in species interactions on the evolution of venom genes

2015

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Geographical heterogeneity in the composition of biotic interactions can create a mosaic of selection regimes that may drive the differentiation of phenotypes that operate at the interface of these interactions. Nonetheless, little is known about effects of these geographical mosaics on the evolution of genes encoding traits associated with species interactions. Predatory marine snails of the family Conidae use venom, a cocktail of conotoxins, to capture prey. We characterized patterns of geographical variation at five conotoxin genes of a vermivorous species, Conus ebraeus, at Hawaii, Guam and American Samoa, and evaluated how these patterns of variation are associated with geographical heterogeneity in prey utilization. All populations show distinct patterns of prey utilization. Three 'highly polymorphic' conotoxin genes showed significant geographical differences in allelic frequency, and appear to be affected by different modes of selection among populations. Two genes exhibited low levels of diversity and a general lack of differentiation among populations. Levels of diversity of 'highly polymorphic' genes exhibit a positive relationship with dietary breadth. The different patterns of evolution exhibited by conotoxin genes suggest that these genes play different roles in prey capture, and that some genes are more greatly affected by differences in predator-prey interactions than others. Moreover, differences in dietary breadth appear to have a greater influence on the differentiation of venoms than differences in the species of prey.

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“…Functional and applied studies and antivenom producers using venoms from adult snakes can likely rely on repeatable samples from captive colonies (Simpson & Jacobsen 2009;Whitaker & Whitaker 2012), assuming diet is held constant (Gibbs et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

“…More recent studies have leveraged high resolution forms of analysis-namely chromatographic separation and mass spectrometry-and found that long-term alteration of rattlesnake diets (Gibbs et al 2011) and long-term captivity (Freitas-de-Sousa et al, 2015) did induce modest changes in protein composition. Confounding effects of captivity stress, growth in captivity, diet, and season exist in each of the aforementioned studies, often paired with a lack of replication due to the use of pooled venom samples.…”

Section: Introductionmentioning

confidence: 99%

Stress Ecology of the Pacific Rattlesnakes (Crotalus Oreganus and Crotalus Helleri)

Claunch¹

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Proteomic analysis of ontogenetic and diet-related changes in venom composition of juvenile and adult Dusky Pigmy rattlesnakes (Sistrurus miliarius barbouri)

Cited by 99 publications

References 42 publications

Expression Differentiation Is Constrained to Low-Expression Proteins over Ecological Timescales

Expression Differentiation Is Constrained to Low-Expression Proteins over Ecological Timescales

Effects of geographical heterogeneity in species interactions on the evolution of venom genes

Stress Ecology of the Pacific Rattlesnakes (Crotalus Oreganus and Crotalus Helleri)

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