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

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.

Keywords: Venom diversity; defense; predation; toxin function; venom gland; venom metering; venom optimization.

Figure 1

Taxonomic diversity and the main primary functions of venom. A pruned and schematic phylogenetic tree of venomous animals modified after Casewell et al. [23] illustrating the frequency with which venoms have evolved within the animal kingdom. Colored branches highlight venomous lineages, with red branches indicating a predatory/feeding venom function, blue branches indicating a defensive function and dashed green branches indicating a role in intraspecific competition. Taxa for which no direct support of their venomous nature could be found are indicated with a question mark. For an exhaustive list of venomous lineages see Table S1. Arthropod phylogeny follows that of Giribet and Edgecombe [24].

Figure 2

Examples of morphological constraints on the regulation of venom secretions. (A) Species with complex venom glands and heterogeneous distribution of venom components are more likely to be able to qualitatively modulate venom compared to species with simple venom glands. This ability may, in turn, be related to the pharmacological properties of toxins in the venom (see below). (B) Sea anemones do not possess a centralized venom system (venom gland). Instead, the functions of toxins can be inferred from the sea anemone’s functional anatomy. (C) Ants and venomous fish possess rather simple venom glands with only a few different components and are not able to modulate venom secretion. They use their venom to defend themselves against potential predators, but in the case of the ants also to incapacitate prey. (D) Snakes, spiders, and centipedes are also thought to be able to modulate venom composition as venom components are stored heterogeneously throughout the gland. This may enable indirect qualitative venom modulation similar to that which has been demonstrated in scorpions, which possess a roughly similar overall venom gland morphology as snakes, spiders, and centipedes. (E) Cone snails and assassin bugs are able to directly modulate venom composition. They achieve this due to complex venom gland morphology with distinct compartments for predatory and defensive venom components.