Using Genomics to Understand Venom Evolution

A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Animal Venoms".

Deadline for manuscript submissions: closed (30 November 2022) | Viewed by 14012

Special Issue Editors


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Guest Editor
Department of Integrative Biology, University of South Florida, Tampa, FL 33620, USA
Interests: evolutionary genomics; adaptation; coevolution; gene regulation; gene expression; population venomics

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Guest Editor
Department of Biology, University of South Alabama, Mobile, AL 36688, USA
Interests: comparative genomics; gene family evolution; gene expression; population venomics; trait evolution

Special Issue Information

Dear Colleagues,

Venoms are complex cocktails of peptides, proteins, and/or organic molecules that have multiple origins across the animal tree of life. Animal venoms have emerged as a model system for understanding the genotype–phenotype relationship in polygenic traits because of their genetic tractability, contributions to fitness, and exceptionally high evolutionary rates. Although venoms are commonly investigated using transcriptomics and proteomics, genomic information is required to understand the processes and mechanisms that underlie venoms’ multiple origins, as well as the mechanisms producing the exceptional degree of variation known in these systems. High-quality genome data for venomous species are still sparse relative to those for other systems, although several recent studies have begun addressing this knowledge gap, in particular venomous lineages. The aim of this Special Issue is to publish genomics-based research to further our understanding of venom evolution using data generated through whole-genome sequencing, sequence capture, RAD-seq, BAC clones, Sanger sequencing, and other genomic approaches. This issue is expected to publish original research articles, reviews, and short communications in the broad area of venom genomics (but will not include studies solely relying on transcriptomes or proteomes). Since Toxins is a well-known journal in the field of venom research, we strongly believe that the articles published in this issue will reach a wide audience and aid in the generation of genomic data as a public resource and offer insight into the macro- and microevolutionary trends of venom evolution across a wide range of taxa.

Dr. Mark J. Margres
Dr. Jason L. Strickland
Guest Editors

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Keywords

  • genomics
  • venom
  • adaptation
  • selection
  • gene expression
  • evolution
  • genetic architecture
  • sequence-capture
  • RAD-seq
  • whole-genome sequencing

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Published Papers (2 papers)

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Research

17 pages, 25855 KiB  
Article
Varying Intensities of Introgression Obscure Incipient Venom-Associated Speciation in the Timber Rattlesnake (Crotalus horridus)
by Mark J. Margres, Kenneth P. Wray, Dragana Sanader, Preston J. McDonald, Lauren M. Trumbull, Austin H. Patton and Darin R. Rokyta
Toxins 2021, 13(11), 782; https://doi.org/10.3390/toxins13110782 - 5 Nov 2021
Cited by 8 | Viewed by 3857
Abstract
Ecologically divergent selection can lead to the evolution of reproductive isolation through the process of ecological speciation, but the balance of responsible evolutionary forces is often obscured by an inadequate assessment of demographic history and the genetics of traits under selection. Snake venoms [...] Read more.
Ecologically divergent selection can lead to the evolution of reproductive isolation through the process of ecological speciation, but the balance of responsible evolutionary forces is often obscured by an inadequate assessment of demographic history and the genetics of traits under selection. Snake venoms have emerged as a system for studying the genetic basis of adaptation because of their genetic tractability and contributions to fitness, and speciation in venomous snakes can be associated with ecological diversification such as dietary shifts and corresponding venom changes. Here, we explored the neurotoxic (type A)–hemotoxic (type B) venom dichotomy and the potential for ecological speciation among Timber Rattlesnake (Crotalus horridus) populations. Previous work identified the genetic basis of this phenotypic difference, enabling us to characterize the roles geography, history, ecology, selection, and chance play in determining when and why new species emerge or are absorbed. We identified significant genetic, proteomic, morphological, and ecological/environmental differences at smaller spatial scales, suggestive of incipient ecological speciation between type A and type B C. horridus. Range-wide analyses, however, rejected the reciprocal monophyly of venom type, indicative of varying intensities of introgression and a lack of reproductive isolation across the range. Given that we have now established the phenotypic distributions and ecological niche models of type A and B populations, genome-wide data are needed and capable of determining whether type A and type B C. horridus represent distinct, reproductively isolated lineages due to incipient ecological speciation or differentiated populations within a single species. Full article
(This article belongs to the Special Issue Using Genomics to Understand Venom Evolution)
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20 pages, 3335 KiB  
Article
Widespread Evolution of Molecular Resistance to Snake Venom α-Neurotoxins in Vertebrates
by Muzaffar A. Khan, Daniel Dashevsky, Harald Kerkkamp, Dušan Kordiš, Merijn A. G. de Bakker, Roel Wouters, Jory van Thiel, Bianca op den Brouw, Freek J. Vonk, R. Manjunatha Kini, Jawad Nazir, Bryan G. Fry and Michael K. Richardson
Toxins 2020, 12(10), 638; https://doi.org/10.3390/toxins12100638 - 2 Oct 2020
Cited by 24 | Viewed by 9265
Abstract
Venomous snakes are important subjects of study in evolution, ecology, and biomedicine. Many venomous snakes have alpha-neurotoxins (α-neurotoxins) in their venom. These toxins bind the alpha-1 nicotinic acetylcholine receptor (nAChR) at the neuromuscular junction, causing paralysis and asphyxia. Several venomous snakes and their [...] Read more.
Venomous snakes are important subjects of study in evolution, ecology, and biomedicine. Many venomous snakes have alpha-neurotoxins (α-neurotoxins) in their venom. These toxins bind the alpha-1 nicotinic acetylcholine receptor (nAChR) at the neuromuscular junction, causing paralysis and asphyxia. Several venomous snakes and their predators have evolved resistance to α-neurotoxins. The resistance is conferred by steric hindrance from N-glycosylated asparagines at amino acids 187 or 189, by an arginine at position 187 that has been hypothesized to either electrostatically repulse positively charged neurotoxins or sterically interfere with α-neurotoxin binding, or proline replacements at positions 194 or 197 of the nAChR ligand-binding domain to inhibit α-neurotoxin binding through structural changes in the receptor. Here, we analyzed this domain in 148 vertebrate species, and assessed its amino acid sequences for resistance-associated mutations. Of these sequences, 89 were sequenced de novo. We find widespread convergent evolution of the N-glycosylation form of resistance in several taxa including venomous snakes and their lizard prey, but not in the snake-eating birds studied. We also document new lineages with the arginine form of inhibition. Using an in vivo assay in four species, we provide further evidence that N-glycosylation mutations reduce the toxicity of cobra venom. The nAChR is of crucial importance for normal neuromuscular function and is highly conserved throughout the vertebrates as a result. Our research shows that the evolution of α-neurotoxins in snakes may well have prompted arms races and mutations to this ancient receptor across a wide range of sympatric vertebrates. These findings underscore the inter-connectedness of the biosphere and the ripple effects that one adaption can have across global ecosystems. Full article
(This article belongs to the Special Issue Using Genomics to Understand Venom Evolution)
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