Understanding the molecular mechanisms that underlie snake venom variability provides important clues for understanding how the biological functions of this powerful toxic arsenal evolve. Here we analyzed in detail individual transcripts and venom protein isoforms produced by five specimens of a venomous snake (Bothrops atrox) from two nearby but genetically distinct populations from the Brazilian Amazon rainforest showing functional similarities in venom properties. Individual variation was observed among the venoms of these specimens, but the overall abundance of each general toxin family was conserved both in transcripts and in venom protein levels. However, when expression of independent paralogues was analyzed, remarkable differences were observed within and among each toxin group both between individuals and between populations. Transcripts for functionally essential venom proteins (“housekeeping” proteins) are highly expressed in all specimens and show similar transcription/translation rates. In contrast, other paralogues show lower expression levels and the toxins they code for vary among different individuals. These results provide support for the idea that that expression and translational differences play a greater role in defining adaptive variation in venom phenotypes than does sequence variation in protein coding genes and that convergent adaptive venom phenotypes can be generated through different molecular mechanisms.
This content will become publicly available on April 1, 2023
Venom Gene Sequence Diversity and Expression Jointly Shape Diet Adaptation in Pitvipers
Abstract Understanding the joint roles of protein sequence variation and differential expression during adaptive evolution is a fundamental, yet largely unrealized goal of evolutionary biology. Here, we use phylogenetic path analysis to analyze a comprehensive venom-gland transcriptome dataset spanning three genera of pitvipers to identify the functional genetic basis of a key adaptation (venom complexity) linked to diet breadth (DB). The analysis of gene-family-specific patterns reveals that, for genes encoding two of the most important venom proteins (snake venom metalloproteases and snake venom serine proteases), there are direct, positive relationships between sequence diversity (SD), expression diversity (ED), and increased DB. Further analysis of gene-family diversification for these proteins showed no constraint on how individual lineages achieved toxin gene SD in terms of the patterns of paralog diversification. In contrast, another major venom protein family (PLA2s) showed no relationship between venom molecular diversity and DB. Additional analyses suggest that other molecular mechanisms—such as higher absolute levels of expression—are responsible for diet adaptation involving these venom proteins. Broadly, our findings argue that functional diversity generated through sequence and expression variations jointly determine adaptation in the key components of pitviper venoms, which mediate complex molecular interactions between the snakes and their prey.
- Editors:
- Yoder, Anne
- Award ID(s):
- 1638872
- Publication Date:
- NSF-PAR ID:
- 10376741
- Journal Name:
- Molecular Biology and Evolution
- Volume:
- 39
- Issue:
- 4
- ISSN:
- 0737-4038
- Sponsoring Org:
- National Science Foundation
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