Evolution of Venomous and Poisonous Animals

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

Deadline for manuscript submissions: closed (28 February 2023) | Viewed by 28715

Special Issue Editors


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Guest Editor
Department of Biosciences, College of Science, Swansea University, Swansea SA2 8PP, UK
Interests: evolutionary toxinology; macroevolution; diversification; convergent evolution; antipredator defence; herpetology; phylogenetic comparative methods
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Guest Editor
Institute for Global Food Security, School of Biological Sciences, Queen's University Belfast, BT9 5DL Belfast, UK

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Guest Editor
Venom Systems Lab, Ryan Institute, National University of Ireland Galway, H91 TK33 Galway, Ireland
Interests: reptile and arthropod predation strategies; venom – transcriptomics; proteomics; medical importance and therapeutics

Special Issue Information

Dear Colleagues,

The ability to use toxic weaponry such as venoms and poisons has evolved many times across the animal tree of life. Animals have the capacity to produce toxins endogenously, such as venoms, or exogenously via toxin bioaccumulation/sequestration, and such toxins are either actively transferred as venoms or passively secreted as poisons. Regardless of the strategy, having venoms or toxins has led to major evolutionary adaptations in animals and the organisms with which they interact. Unsurprisingly, venoms and toxins have been studied for their therapeutic potential, fueling research on toxin characterization and molecular aspects of venom toxins (e.g., structure–function relationships, molecular evolution of toxins, and venomics). However, in recent years, the field of organismal toxinology has expanded and provided more focus on the evolutionary, ecological, and behavioral context, leading to the discovery of remarkable examples of evolutionary arms races, mimicry, and aposematism.

This Special Issue is focused on gathering contributions in the form of original research articles, reviews, and short communications in the broad area of the evolution of venomous and poisonous animals. More specifically, we welcome papers that consider (but are not limited to) the following: systematics and phylogenetics of targeted groups of venomous or poisonous animals; molecular adaptations of venoms and gene-encoded toxins; studies that link physiology or ecology to the evolution of toxicity or venoms in animals; evolutionary and ecological consequences of toxicity (such as aposematism and mimicry); behavioral or morphological adaptations; host–microbiome interactions in toxic animals; and toxin resistance and sequestration.

Dr. Kevin Arbuckle
Dr. Karen Siu-Ting
Dr. John Dunbar
Guest Editors

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Keywords

  • Venoms
  • Toxins
  • Poisons
  • Animal evolution
  • Evolutionary adaptations
  • Venomics
  • Ecology
  • Alkaloids

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Published Papers (5 papers)

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Research

13 pages, 1531 KiB  
Article
Diversity Begets Diversity When Diet Drives Snake Venom Evolution, but Evenness Rather Than Richness Is What Counts
by Romane Schaeffer, Victoria J. Pascolutti, Timothy N. W. Jackson and Kevin Arbuckle
Toxins 2023, 15(4), 251; https://doi.org/10.3390/toxins15040251 - 29 Mar 2023
Cited by 3 | Viewed by 6405
Abstract
Snake venoms are primarily used to subjugate prey, and consequently, their evolution has been shown to be predominantly driven by diet-related selection pressure. Venoms tend to be more lethal to prey than non-prey species (except in cases of toxin resistance), prey-specific toxins have [...] Read more.
Snake venoms are primarily used to subjugate prey, and consequently, their evolution has been shown to be predominantly driven by diet-related selection pressure. Venoms tend to be more lethal to prey than non-prey species (except in cases of toxin resistance), prey-specific toxins have been identified, and preliminary work has demonstrated an association between the diversity of diet classes and that of toxicological activities of whole venom. However, venoms are complex mixtures of many toxins, and it remains unclear how toxin diversity is driven by diet. Prey-specific toxins do not encompass the molecular diversity of venoms, and whole venom effects could be driven by one, few, or all components, so the link between diet and venom diversity remains minimally understood. Here, we collated a database of venom composition and diet records and used a combination of phylogenetic comparative methods and two quantitative diversity indices to investigate whether and how diet diversity relates to the toxin diversity of snake venoms. We reveal that venom diversity is negatively related to diet diversity using Shannon’s index but positively related using Simpson’s index. Since Shannon’s index predominantly considers the number of prey/toxins, whereas Simpson’s index more strongly reflects evenness, we provide insights into how the diet–venom diversity link is driven. Specifically, species with low diet diversity tend to have venoms dominated by a few abundant (possibly specialised) toxin families, whereas species with diverse diets tend to ‘hedge their bets’ by having venoms with a more even composition of different toxin classes. Full article
(This article belongs to the Special Issue Evolution of Venomous and Poisonous Animals)
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23 pages, 2255 KiB  
Article
The Fast and the Furriest: Investigating the Rate of Selection on Mammalian Toxins
by Leah Lucy Joscelyne Fitzpatrick, Vincent Nijman, Rodrigo Ligabue-Braun and K. Anne-Isola Nekaris
Toxins 2022, 14(12), 842; https://doi.org/10.3390/toxins14120842 - 1 Dec 2022
Cited by 2 | Viewed by 3741
Abstract
The evolution of venom and the selection pressures that act on toxins have been increasingly researched within toxinology in the last two decades, in part due to the exceptionally high rates of diversifying selection observed in animal toxins. In 2015, Sungar and Moran [...] Read more.
The evolution of venom and the selection pressures that act on toxins have been increasingly researched within toxinology in the last two decades, in part due to the exceptionally high rates of diversifying selection observed in animal toxins. In 2015, Sungar and Moran proposed the ‘two-speed’ model of toxin evolution linking evolutionary age of a group to the rates of selection acting on toxins but due to a lack of data, mammals were not included as less than 30 species of venomous mammal have been recorded, represented by elusive species which produce small amounts of venom. Due to advances in genomics and transcriptomics, the availability of toxin sequences from venomous mammals has been increasing. Using branch- and site-specific selection models, we present the rates of both episodic and pervasive selection acting upon venomous mammal toxins as a group for the first time. We identified seven toxin groups present within venomous mammals, representing Chiroptera, Eulipotyphla and Monotremata: KLK1, Plasminogen Activator, Desmallipins, PACAP, CRiSP, Kunitz Domain One and Kunitz Domain Two. All but one group (KLK1) was identified by our results to be evolving under both episodic and pervasive diversifying selection with four toxin groups having sites that were implicated in the fitness of the animal by TreeSAAP (Selection on Amino Acid Properties). Our results suggest that venomous mammal ecology, behaviour or genomic evolution are the main drivers of selection, although evolutionary age may still be a factor. Our conclusion from these results indicates that mammalian toxins are following the two-speed model of selection, evolving predominately under diversifying selection, fitting in with other younger venomous taxa like snakes and cone snails—with high amounts of accumulating mutations, leading to more novel adaptions in their toxins. Full article
(This article belongs to the Special Issue Evolution of Venomous and Poisonous Animals)
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18 pages, 2845 KiB  
Article
Worldwide Web: High Venom Potency and Ability to Optimize Venom Usage Make the Globally Invasive Noble False Widow Spider Steatoda nobilis (Thorell, 1875) (Theridiidae) Highly Competitive against Native European Spiders Sharing the Same Habitats
by Sean Rayner, Aiste Vitkauskaite, Kevin Healy, Keith Lyons, Leona McSharry, Dayle Leonard, John P. Dunbar and Michel M. Dugon
Toxins 2022, 14(9), 587; https://doi.org/10.3390/toxins14090587 - 26 Aug 2022
Cited by 4 | Viewed by 6220
Abstract
Venom compositions include complex mixtures of toxic proteins that evolved to immobilize/dissuade organisms by disrupting biological functions. Venom production is metabolically expensive, and parsimonious use is expected, as suggested by the venom optimisation hypothesis. The decision-making capacity to regulate venom usage has never [...] Read more.
Venom compositions include complex mixtures of toxic proteins that evolved to immobilize/dissuade organisms by disrupting biological functions. Venom production is metabolically expensive, and parsimonious use is expected, as suggested by the venom optimisation hypothesis. The decision-making capacity to regulate venom usage has never been demonstrated for the globally invasive Noble false widow Steatoda nobilis (Thorell, 1875) (Theridiidae). Here, we investigated variations of venom quantities available in a wild population of S. nobilis and prey choice depending on venom availability. To partially determine their competitiveness, we compared their attack rate success, median effective dose (ED50) and lethal dose (LD50), with four sympatric synanthropic species: the lace webbed spider Amaurobius similis, the giant house spider Eratigena atrica, the missing sector orb-weaver Zygiella x-notata, and the cellar spider Pholcus phalangioides. We show that S. nobilis regulates its venom usage based on availability, and its venom is up to 230-fold (0.56 mg/kg) more potent than native spiders. The high potency of S. nobilis venom and its ability to optimize its usage make this species highly competitive against native European spiders sharing the same habitats. Full article
(This article belongs to the Special Issue Evolution of Venomous and Poisonous Animals)
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16 pages, 2664 KiB  
Article
Initial Phylotranscriptomic Confirmation of Homoplastic Evolution of the Conspicuous Coloration and Bufoniform Morphology of Pumpkin-Toadlets in the Genus Brachycephalus
by Mariana L. Lyra, Juliane P. C. Monteiro, Loïs Rancilhac, Iker Irisarri, Sven Künzel, Eugenia Sanchez, Thais H. Condez, Omar Rojas-Padilla, Mirco Solé, Luís Felipe Toledo, Célio F. B. Haddad and Miguel Vences
Toxins 2021, 13(11), 816; https://doi.org/10.3390/toxins13110816 - 19 Nov 2021
Cited by 6 | Viewed by 3472
Abstract
The genus Brachycephalus is a fascinating group of miniaturized anurans from the Brazilian Atlantic Forest, comprising the conspicuous, brightly colored pumpkin-toadlets and the cryptic flea-toads. Pumpkin-toadlets are known to contain tetrodotoxins and therefore, their bright colors may perform an aposematic function. Previous studies [...] Read more.
The genus Brachycephalus is a fascinating group of miniaturized anurans from the Brazilian Atlantic Forest, comprising the conspicuous, brightly colored pumpkin-toadlets and the cryptic flea-toads. Pumpkin-toadlets are known to contain tetrodotoxins and therefore, their bright colors may perform an aposematic function. Previous studies based on a limited number of mitochondrial and nuclear-encoded markers supported the existence of two clades containing species of pumpkin-toadlet phenotype, but deep nodes remained largely unresolved or conflicting between data sets. We use new RNAseq data of 17 individuals from nine Brachycephalus species to infer their evolutionary relationships from a phylogenomic perspective. Analyses of almost 5300 nuclear-encoded ortholog protein-coding genes and full mitochondrial genomes confirmed the existence of two separate pumpkin-toadlet clades, suggesting the convergent evolution (or multiple reversals) of the bufoniform morphology, conspicuous coloration, and probably toxicity. In addition, the study of the mitochondrial gene order revealed that three species (B. hermogenesi, B. pitanga, and B. rotenbergae) display translocations of different tRNAs (NCY and CYA) from the WANCY tRNA cluster to a position between the genes ATP6 and COIII, showing a new mitochondrial gene order arrangement for vertebrates. The newly clarified phylogeny suggests that Brachycephalus has the potential to become a promising model taxon to understand the evolution of coloration, body plan and toxicity. Given that toxicity information is available for only few species of Brachycephalus, without data for any flea-toad species, we also emphasize the need for a wider screening of toxicity across species, together with more in-depth functional and ecological study of their phenotypes. Full article
(This article belongs to the Special Issue Evolution of Venomous and Poisonous Animals)
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18 pages, 7061 KiB  
Article
Morphology of the Cutaneous Poison and Mucous Glands in Amphibians with Particular Emphasis on Caecilians (Siphonops annulatus)
by Beatriz Mauricio, Pedro Luiz Mailho-Fontana, Luciana Almeida Sato, Flavia Ferreira Barbosa, Renato Mancini Astray, Alexander Kupfer, Edmund D. Brodie, Jr., Carlos Jared and Marta Maria Antoniazzi
Toxins 2021, 13(11), 779; https://doi.org/10.3390/toxins13110779 - 4 Nov 2021
Cited by 6 | Viewed by 5659
Abstract
Caecilians (order Gymnophiona) are apodan, snake-like amphibians, usually with fossorial habits, constituting one of the most unknown groups of terrestrial vertebrates. As in orders Anura (frogs, tree frogs and toads) and Caudata (salamanders and newts), the caecilian skin is rich in mucous glands, [...] Read more.
Caecilians (order Gymnophiona) are apodan, snake-like amphibians, usually with fossorial habits, constituting one of the most unknown groups of terrestrial vertebrates. As in orders Anura (frogs, tree frogs and toads) and Caudata (salamanders and newts), the caecilian skin is rich in mucous glands, responsible for body lubrication, and poison glands, producing varied toxins used in defence against predators and microorganisms. Whereas in anurans and caudatans skin gland morphology has been well studied, caecilian poison glands remain poorly elucidated. Here we characterised the skin gland morphology of the caecilian Siphonops annulatus, emphasising the poison glands in comparison to those of anurans and salamanders. We showed that S. annulatus glands are similar to those of salamanders, consisting of several syncytial compartments full of granules composed of protein material but showing some differentiated apical compartments containing mucus. An unusual structure resembling a mucous gland is frequently observed in lateral/apical position, apparently connected to the main duct. We conclude that the morphology of skin poison glands in caecilians is more similar to salamander glands when compared to anuran glands that show a much-simplified structure. Full article
(This article belongs to the Special Issue Evolution of Venomous and Poisonous Animals)
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