Phenotypic Variation in Mojave Rattlesnake (Crotalus scutulatus) Venom Is Driven by Four Toxin Families.

Jason L Strickland,Darin R Rokyta,Andrew J Mason,Christopher L Parkinson

doi:10.3390/toxins10040135

Jason L Strickland, Darin R Rokyta + Show 2 more

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https://doi.org/10.3390/toxins10040135

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Abstract

Phenotypic diversity generated through altered gene expression is a primary mechanism facilitating evolutionary response in natural systems. By linking the phenotype to genotype through transcriptomics, it is possible to determine what changes are occurring at the molecular level. High phenotypic diversity has been documented in rattlesnake venom, which is under strong selection due to its role in prey acquisition and defense. Rattlesnake venom can be characterized by the presence (Type A) or absence (Type B) of a type of neurotoxic phospholipase A (PLA), such as Mojave toxin, that increases venom toxicity. Mojave rattlesnakes (Crotalus scutulatus), represent this diversity as both venom types are found within this species and within a single panmictic population in the Sonoran Desert. We used comparative venom gland transcriptomics of nine specimens of C. scutulatus from this region to test whether expression differences explain diversity within and between venom types. Type A individuals expressed significantly fewer toxins than Type B individuals owing to the diversity of C-type lectins (CTLs) and snake venom metalloproteinases (SVMPs) found in Type B animals. As expected, both subunits of Mojave toxin were exclusively found in Type A individuals but we found high diversity in four additional PLAs that was not associated with a venom type. Myotoxin a expression and toxin number variation was not associated with venom type, and myotoxin a had the highest range of expression of any toxin class. Our study represents the most comprehensive transcriptomic profile of the venom type dichotomy in rattlesnakes and C. scutulatus. Even intra-specifically, Mojave rattlesnakes showcase the diversity of snake venoms and illustrate that variation within venom types blurs the distinction of the venom dichotomy.

Highlights

Differential gene expression is a primary component with respect to the genotype and phenotype that facilitates rapid evolutionary response in the face of changing environmental pressures by generating phenotypic diversity [1]
Desert in the U.S.A. (Table 1, Figure 1). These individuals were chosen after determining their venom phenotype using reverse-phased high performance liquid chromatography (RP-HPLC) (Figure 2) to maximize the venom variation in C. scutulatus
We found evidence for a phospholipase A2 (PLA2) allele in one C. scutulatus individual that was more similar to a congener, C. viridis, than the other eight C. scutulatus specimens

Summary

Introduction

Differential gene expression is a primary component with respect to the genotype and phenotype that facilitates rapid evolutionary response in the face of changing environmental pressures by generating phenotypic diversity [1]. Comparative transcriptomics has emerged as the tool to understand these responses by linking the phenotype to the genotype through mRNA sequencing. Changes within the venom phenotype occur through regulatory shifts in protein expression [6], through loss of specific genes [7], duplication [8], and point mutations [9]. Transcriptomics cannot detect all possible mechanisms resulting in phenotypic diversity, with regard to genes in the genome that are not expressed or have multiple copies [10]. For those genes that are expressed, transcriptomics offer an effective means of linking sequence-based and regulatory variation to changes in a composite phenotype [11]. With the increase in availability of high-throughput proteomic, transcriptomic, and genomic resources, rattlesnakes and their venom have become a model system to understand these mechanisms as they exhibit high phenotypic diversity [12,13,14,15]

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