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Evolutionary Ecology of Venom

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

Deadline for manuscript submissions: closed (14 February 2020) | Viewed by 89273

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Dr. Kevin Arbuckle

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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
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

The molecular biology, evolution, and pathology of venoms have long been fertile areas for research, particularly animal venoms of clinical significance. Some of this work has attempted to interpret biochemical and molecular evolutionary findings in the context of ecology, for instance differences in venom composition being explained by some attributes that differ between species such as diet. However, much rarer is an explicit attempt to study the evolutionary ecology of venom beyond simply using the ecological aspects as an ad hoc and post hoc explanatory framework. Venom also presents a powerful system to address broader questions in evolutionary ecology thanks to its variability at multiple scales, its broad phylogenetic distribution, and its inherently tight link to key fitness components via natural enemy interactions.

The focus of this Special Issue is on understanding how ecology shapes the evolution of venom systems and also how venom influences the ecological attributes and interactions of species. Questions and areas that have been particularly neglected will be particularly favoured and I encourage articles covering any venomous organisms, whether animal, plant, or bacteria. I look forward to editing an exciting collection of research and review articles that will help stimulate interest in the evolutionary ecology of venom.

Best wishes,

Dr. Kevin Arbuckle
Guest Editor

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All papers will be peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

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Keywords

Natural enemy interactions
Coevolution
Ecological niche
Venom toxin resistance
Phylogenetic comparative biology
Venom ecological function
Ecology of venom systems

Published Papers (11 papers)

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Editorial

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4 pages, 222 KiB

Open AccessEditorial

Special Issue: Evolutionary Ecology of Venom

by Kevin Arbuckle

Toxins 2021, 13(5), 310; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins13050310 - 27 Apr 2021

Cited by 1 | Viewed by 2136

Abstract

This Special Issue of Toxins aims to increase the profile and understanding of how ecology shapes the evolution of venom systems, and also how venom influences the ecological attributes of and interactions among species [...] Full article

(This article belongs to the Special Issue Evolutionary Ecology of Venom)

Research

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19 pages, 3953 KiB

Open AccessEditor’s ChoiceArticle

Fangs for the Memories? A Survey of Pain in Snakebite Patients Does Not Support a Strong Role for Defense in the Evolution of Snake Venom Composition

by Harry Ward-Smith, Kevin Arbuckle, Arno Naude and Wolfgang Wüster

Toxins 2020, 12(3), 201; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins12030201 - 22 Mar 2020

Cited by 20 | Viewed by 14639

Abstract

Animals use venoms for multiple purposes, most prominently for prey acquisition and self-defense. In snakes, venom composition often evolves as a result of selection for optimization for local diet. However, whether selection for a defensive function has also played a role in driving the evolution of venom composition has remained largely unstudied. Here, we use an online survey of snakebite victims to test a key prediction of a defensive function, that envenoming should result in the rapid onset of severe pain. From the analysis of 584 snakebite reports, involving 192 species of venomous snake, we find that the vast majority of bites do not result in severe early pain. Phylogenetic comparative analysis shows that where early pain after a bite evolves, it is often lost rapidly. Our results, therefore, do not support the hypothesis that natural selection for antipredator defense played an important role in the origin of venom or front-fanged delivery systems in general, although there may be intriguing exceptions to this rule. Full article

(This article belongs to the Special Issue Evolutionary Ecology of Venom)

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12 pages, 1331 KiB

Open AccessEditor’s ChoiceArticle

Diet Breadth Mediates the Prey Specificity of Venom Potency in Snakes

by Keith Lyons, Michel M. Dugon and Kevin Healy

Toxins 2020, 12(2), 74; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins12020074 - 23 Jan 2020

Cited by 40 | Viewed by 6321

Abstract

Venoms are best known for their ability to incapacitate prey. In predatory groups, venom potency is predicted to reflect ecological and evolutionary drivers relating to diet. While venoms have been found to have prey-specific potencies, the role of diet breadth on venom potencies has yet to be tested at large macroecological scales. Here, using a comparative analysis of 100 snake species, we show that the evolution of prey-specific venom potencies is contingent on the breadth of a species’ diet. We find that while snake venom is more potent when tested on species closely related to natural prey items, we only find this prey-specific pattern in species with taxonomically narrow diets. While we find that the taxonomic diversity of a snakes’ diet mediates the prey specificity of its venom, the species richness of its diet was not found to affect these prey-specific potency patterns. This indicates that the physiological diversity of a species’ diet is an important driver of the evolution of generalist venom potencies. These findings suggest that the venoms of species with taxonomically diverse diets may be better suited to incapacitating novel prey species and hence play an important role for species within changing environments. Full article

(This article belongs to the Special Issue Evolutionary Ecology of Venom)

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17 pages, 714 KiB

Open AccessArticle

Characterization of Venom Components and Their Phylogenetic Properties in Some Aculeate Bumblebees and Wasps

by Kyungjae Andrew Yoon, Kyungmun Kim, Woo-Jin Kim, Woo Young Bang, Neung-Ho Ahn, Chang-Hwan Bae, Joo-Hong Yeo and Si Hyeock Lee

Toxins 2020, 12(1), 47; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins12010047 - 14 Jan 2020

Cited by 17 | Viewed by 4159

Abstract

To identify and compare venom components and expression patterns, venom gland-specific transcriptome analyses were conducted for 14 Aculeate bees and wasps. TPM (transcripts per kilobase million) values were normalized using the average transcription level of a reference housekeeping gene (dimethyladenosine transferase). Orthologous venom component genes across the 14 bee and wasp species were identified, and their relative abundance in each species was determined by comparing normalized TPM values. Based on signal sequences in the transcripts, the genes of novel venom components were identified and characterized to encode potential allergens. Most of the allergens and pain-producing factors (arginine kinase, hyaluronidase, mastoparan, phospholipase A1, phospholipase A2, and venom allergen 5) showed extremely high expression levels in social wasps. Acid phosphatase, neprilysin, and tachykinin, which are known allergens and neurotoxic peptides, were found in the venom glands of solitary wasps more often than in social wasps. In the venom glands of bumblebees, few or no transcripts of major allergens or pain-producing factors were identified. Taken together, these results indicate that differential expression patterns of the venom genes in some Aculeate species imply that some wasps and bumblebee species have unique groups of highly expressed venom components. Some venom components reflected the Aculeate species phylogeny, but others did not. This unique evolution of specific venom components in different groups of some wasps and bumblebee species might have been shaped in response to both ecological and behavioral influences. Full article

(This article belongs to the Special Issue Evolutionary Ecology of Venom)

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14 pages, 306 KiB

Open AccessEditor’s ChoiceArticle

Coevolution of Snake Venom Toxic Activities and Diet: Evidence that Ecological Generalism Favours Toxicological Diversity

by Emma-Louise Davies and Kevin Arbuckle

Toxins 2019, 11(12), 711; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins11120711 - 06 Dec 2019

Cited by 42 | Viewed by 6569

Abstract

Snake venom evolution is typically considered to be predominantly driven by diet-related selection pressures. Most evidence for this is based on lethality to prey and non-prey species and on the identification of prey specific toxins. Since the broad toxicological activities (e.g., neurotoxicity, coagulotoxicity, etc.) sit at the interface between molecular toxinology and lethality, these classes of activity may act as a key mediator in coevolutionary interactions between snakes and their prey. Indeed, some recent work has suggested that variation in these functional activities may be related to diet as well, but previous studies have been limited in geographic and/or taxonomic scope. In this paper, we take a phylogenetic comparative approach to investigate relationships between diet and toxicological activity classes on a global scale across caenophidian snakes, using the clinically oriented database at toxinology.com. We generally find little support for specific prey types selecting for particular toxicological effects except that reptile-feeders are more likely to be neurotoxic. We find some support for endothermic prey (with higher metabolic rates) influencing toxic activities, but differently from previous suggestions in the literature. More broadly, we find strong support for a general effect of increased diversity of prey on the diversity of toxicological effects of snake venom. Hence, we provide evidence that selection pressures on the toxicological activities of snake venom has largely been driven by prey diversity rather than specific types of prey. These results complement and extend previous work to suggest that specific matching of venom characteristics to prey may occur at the molecular level and translate into venom lethality, but the functional link between those two is not constrained to a particular toxicological route. Full article

(This article belongs to the Special Issue Evolutionary Ecology of Venom)

12 pages, 1491 KiB

Open AccessEditor’s ChoiceArticle

High Specific Efficiency of Venom of Two Prey-Specialized Spiders

by Ondřej Michálek, Lucia Kuhn-Nentwig and Stano Pekár

Toxins 2019, 11(12), 687; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins11120687 - 23 Nov 2019

Cited by 19 | Viewed by 5800

Abstract

The venom of predators should be under strong selection pressure because it is a costly substance and prey may potentially become resistant. Particularly in prey-specialized predators, venom should be selected for its high efficiency against the focal prey. Very effective venom paralysis has been observed in specialized predators, such as spiders preying on dangerous prey. Here, we compared the toxicity of the venoms of two prey-specialized species, araneophagous Palpimanus sp. and myrmecophagous Zodarion nitidum, and their related generalist species. We injected different venom concentrations into two prey types—the prey preferred by a specialist and an alternative prey—and observed the mortality and the paralysis of the prey within 24 h. We found that the venoms of specialists were far more potent towards the preferred prey than alternative prey. The venoms of generalists were similarly potent towards both prey types. In addition, we tested the efficacy of two venom fractions (smaller and larger than 10 kDa) in araneophagous Palpimanus sp. Compounds larger than 10 kDa paralyzed both prey types, but smaller compounds (<10 kDa) were effective only on preferred prey, suggesting the presence of prey-specific compounds in the latter fraction. Our results confirm that prey-specialized spiders possess highly specific venom that allows them to subdue dangerous prey. Full article

(This article belongs to the Special Issue Evolutionary Ecology of Venom)

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19 pages, 3206 KiB

Open AccessEditor’s ChoiceArticle

Rapid and Differential Evolution of the Venom Composition of a Parasitoid Wasp Depending on the Host Strain

by Fanny Cavigliasso, Hugo Mathé-Hubert, Laurent Kremmer, Christian Rebuf, Jean-Luc Gatti, Thibaut Malausa, Dominique Colinet and Marylène Poirié

Toxins 2019, 11(11), 629; https://doi.org/10.3390/toxins11110629 - 29 Oct 2019

Cited by 20 | Viewed by 3669

Abstract

Parasitoid wasps rely primarily on venom to suppress the immune response and regulate the physiology of their host. Intraspecific variability of venom protein composition has been documented in some species, but its evolutionary potential is poorly understood. We performed an experimental evolution initiated with the crosses of two lines of Leptopilina boulardi of different venom composition to generate variability and create new combinations of venom factors. The offspring were maintained for 10 generations on two strains of Drosophila melanogaster differing in resistance/susceptibility to the parental parasitoid lines. The venom composition of individuals was characterized by a semi-automatic analysis of 1D SDS-PAGE electrophoresis protein profiles whose accuracy was checked by Western blot analysis of well-characterized venom proteins. Results made evident a rapid and differential evolution of the venom composition on both hosts and showed that the proteins beneficial on one host can be costly on the other. Overall, we demonstrated the capacity of rapid evolution of the venom composition in parasitoid wasps, important regulators of arthropod populations, suggesting a potential for adaptation to new hosts. Our approach also proved relevant in identifying, among the diversity of venom proteins, those possibly involved in parasitism success and whose role deserves to be deepened. Full article

(This article belongs to the Special Issue Evolutionary Ecology of Venom)

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13 pages, 921 KiB

Open AccessEditor’s ChoiceArticle

Prey and Venom Efficacy of Male and Female Wandering Spider, Phoneutria boliviensis (Araneae: Ctenidae)

by Juan Carlos Valenzuela-Rojas, Julio César González-Gómez, Arie van der Meijden, Juan Nicolás Cortés, Giovany Guevara, Lida Marcela Franco, Stano Pekár and Luis Fernando García

Toxins 2019, 11(11), 622; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins11110622 - 27 Oct 2019

Cited by 14 | Viewed by 6729

Abstract

Spiders rely on venom to catch prey and few species are even capable of capturing vertebrates. The majority of spiders are generalist predators, possessing complex venom, in which different toxins seem to target different types of prey. In this study, we focused on the trophic ecology and venom toxicity of Phoneutria boliviensis F. O. Pickard-Cambridge, 1897, a Central American spider of medical importance. We tested the hypothesis that its venom is adapted to catch vertebrate prey by studying its trophic ecology and venom toxicity against selected vertebrate and invertebrate prey. We compared both trophic ecology (based on acceptance experiments) and toxicity (based on bioassays) among sexes of this species. We found that P. boliviensis accepted geckos, spiders, and cockroaches as prey, but rejected frogs. There was no difference in acceptance between males and females. The venom of P. boliviensis was far more efficient against vertebrate (geckos) than invertebrate (spiders) prey in both immobilization time and LD50. Surprisingly, venom of males was more efficient than that of females. Our results suggest that P. boliviensis has adapted its venom to catch vertebrates, which may explain its toxicity to humans. Full article

(This article belongs to the Special Issue Evolutionary Ecology of Venom)

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13 pages, 18236 KiB

Open AccessEditor’s ChoiceArticle

Venom in Furs: Facial Masks as Aposematic Signals in a Venomous Mammal

by K. Anne-Isola Nekaris, Ariana Weldon, Muhammad Ali Imron, Keely Q. Maynard, Vincent Nijman, Stephanie A. Poindexter and Thais Queiroz Morcatty

Toxins 2019, 11(2), 93; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins11020093 - 05 Feb 2019

Cited by 19 | Viewed by 8981

Abstract

The function of colouration in animals includes concealment, communication and signaling, such as the use of aposematism as a warning signal. Aposematism is unusual in mammals, and exceptions help us to understand its ecology and evolution. The Javan slow loris is a highly territorial venomous mammal that has a distinctive facial mask and monochromatic vision. To help understand if they use aposematism to advertise their venom to conspecifics or predators with different visual systems, we studied a population in Java, Indonesia. Using ImageJ, we selected colours from the facial masks of 58 individuals, converted RBG colours into monochromatic, dichromatic and trichromatic modes, and created a contrast index. During 290 captures, we recorded venom secretion and aggressiveness. Using Non-metric Multidimensional Scaling and generalised additive models for location, scale and shape, we found that young slow lorises differ significantly from adults, being both more contrasting and more aggressive, with aggressive animals showing fewer wounds. We suggest aposematic facial masks serve multiple purposes in slow lorises based on age. Change in colouration through development may play a role in intraspecific competition, and advertise toxicity or aggressiveness to competitors and/or predators in juveniles. Aposematic signals combined with intraspecific competition may provide clues to new venomous taxa among mammals. Full article

(This article belongs to the Special Issue Evolutionary Ecology of Venom)

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Review

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22 pages, 2439 KiB

Open AccessEditor’s ChoiceReview

The Diversity of Venom: The Importance of Behavior and Venom System Morphology in Understanding Its Ecology and Evolution

by Vanessa Schendel, Lachlan D. Rash, Ronald A. Jenner and Eivind A. B. Undheim

Toxins 2019, 11(11), 666; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins11110666 - 14 Nov 2019

Cited by 126 | Viewed by 17652

Abstract

Venoms are one of the most convergent of animal traits known, and encompass a much greater taxonomic and functional diversity than is commonly appreciated. This knowledge gap limits the potential of venom as a model trait in evolutionary biology. Here, we summarize the taxonomic and functional diversity of animal venoms and relate this to what is known about venom system morphology, venom modulation, and venom pharmacology, with the aim of drawing attention to the importance of these largely neglected aspects of venom research. We find that animals have evolved venoms at least 101 independent times and that venoms play at least 11 distinct ecological roles in addition to predation, defense, and feeding. Comparisons of different venom systems suggest that morphology strongly influences how venoms achieve these functions, and hence is an important consideration for understanding the molecular evolution of venoms and their toxins. Our findings also highlight the need for more holistic studies of venom systems and the toxins they contain. Greater knowledge of behavior, morphology, and ecologically relevant toxin pharmacology will improve our understanding of the evolution of venoms and their toxins, and likely facilitate exploration of their potential as sources of molecular tools and therapeutic and agrochemical lead compounds. Full article

(This article belongs to the Special Issue Evolutionary Ecology of Venom)

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21 pages, 2392 KiB

Open AccessEditor’s ChoiceReview

Evolutionary Ecology of Fish Venom: Adaptations and Consequences of Evolving a Venom System

by Richard J. Harris and Ronald A. Jenner

Toxins 2019, 11(2), 60; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins11020060 - 22 Jan 2019

Cited by 33 | Viewed by 10950

Abstract

Research on venomous animals has mainly focused on the molecular, biochemical, and pharmacological aspects of venom toxins. However, it is the relatively neglected broader study of evolutionary ecology that is crucial for understanding the biological relevance of venom systems. As fish have convergently evolved venom systems multiple times, it makes them ideal organisms to investigate the evolutionary ecology of venom on a broader scale. This review outlines what is known about how fish venom systems evolved as a result of natural enemy interactions and about the ecological consequences of evolving a venom system. This review will show how research on the evolutionary ecology of venom in fish can aid in understanding the evolutionary ecology of animal venoms more generally. Further, understanding these broad ecological questions can shed more light on the other areas of toxinology, with applications across multiple disciplinary fields. Full article

(This article belongs to the Special Issue Evolutionary Ecology of Venom)

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