Abstract
BackgroundSnake venom is shaped by the ecology and evolution of venomous species, and signals of positive selection in toxins have been consistently documented, reflecting the role of venoms as an ecologically critical phenotype. New World coral snakes (Elapidae) are represented by three genera and over 120 species and subspecies that are capable of causing significant human morbidity and mortality, yet coral-snake venom composition is poorly understood in comparison to that of Old World elapids. High-throughput sequencing is capable of identifying thousands of loci, while providing characterizations of expression patterns and the molecular evolutionary forces acting within the venom gland.ResultsWe describe the de novo assembly and analysis of the venom-gland transcriptome of the eastern coral snake (Micrurus fulvius). We identified 1,950 nontoxin transcripts and 116 toxin transcripts. These transcripts accounted for 57.1% of the total reads, with toxins accounting for 45.8% of the total reads. Phospholipases A2 and three-finger toxins dominated expression, accounting for 86.0% of the toxin reads. A total of 15 toxin families were identified, revealing venom complexity previously unknown from New World coral snakes. Toxins exhibited high levels of heterozygosity relative to nontoxins, and overdominance may favor gene duplication leading to the fixation of advantageous alleles. Phospholipase A2 expression was uniformly distributed throughout the class while three-finger toxin expression was dominated by a handful of transcripts, and phylogenetic analyses indicate that toxin divergence may have occurred following speciation. Positive selection was detected in three of the four most diverse toxin classes, suggesting that venom diversification is driven by recurrent directional selection.ConclusionsWe describe the most complete characterization of an elapid venom gland to date. Toxin gene duplication may be driven by heterozygote advantage, as the frequency of polymorphic toxin loci was significantly higher than that of nontoxins. Diversification among toxins appeared to follow speciation reflecting species-specific adaptation, and this divergence may be directly related to dietary shifts and is suggestive of a coevolutionary arms race.
Highlights
Snake venom is shaped by the ecology and evolution of venomous species, and signals of positive selection in toxins have been consistently documented, reflecting the role of venoms as an ecologically critical phenotype
High venom complexity revealed by means of sequencing Our high-throughput transcriptomic analysis revealed high venom complexity in M. fulvius, comparable to the diversity of toxin components recently identified in the venom-gland transcriptome of the eastern diamondback rattlesnake (Crotalus adamanteus: Viperidae) [16]
We have described the most comprehensive transcriptomic characterization of an elapid venom gland to date, revealing venom complexity previously unknown from any New World coral snake [11,13,15,22,43,44,45]
Summary
Snake venom is shaped by the ecology and evolution of venomous species, and signals of positive selection in toxins have been consistently documented, reflecting the role of venoms as an ecologically critical phenotype. Positive selection has been repeatedly detected in toxin genes and reflects the significant contribution of venoms to fitness [2,3,4] These molecular signals of adaptive evolution coupled with compositional variation suggest that toxin diversification is an adaptation to diet and may reflect a predator-prey arms race [5]. A full characterization of all venom components may allow the design of more effective polyvalent antivenom [13,14], but coral-snake venom composition is poorly understood in comparison to that of Old World elapids [15], mainly due to the difficulty of procuring sufficient venom quantities during milking for standard proteomic techniques [13]. We sequenced the venom-gland transcriptome of M. fulvius with Illumina technology using the paired-end approach of Rokyta et al [16], and used the generated sequence data to examine the relationship between toxin heterozygosity and gene duplication events and uncover distinct expression patterns in highly expressed and extremely diverse toxin gene families
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