Abstract
Venomousness is a complex functional trait that has evolved independently many times in the animal kingdom, although it is rare among mammals. Intriguingly, most venomous mammal species belong to Eulipotyphla (solenodons, shrews). This fact may be linked to their high metabolic rate and a nearly continuous demand of nutritious food, and thus it relates the venom functions to facilitation of their efficient foraging. While mammalian venoms have been investigated using biochemical and molecular assays, studies of their ecological functions have been neglected for a long time. Therefore, we provide here an overview of what is currently known about eulipotyphlan venoms, followed by a discussion of how these venoms might have evolved under ecological pressures related to food acquisition, ecological interactions, and defense and protection. We delineate six mutually nonexclusive functions of venom (prey hunting, food hoarding, food digestion, reducing intra- and interspecific conflicts, avoidance of predation risk, weapons in intraspecific competition) and a number of different subfunctions for eulipotyphlans, among which some are so far only hypothetical while others have some empirical confirmation. The functions resulting from the need for food acquisition seem to be the most important for solenodons and especially for shrews. We also present several hypotheses explaining why, despite so many potentially beneficial functions, venomousness is rare even among eulipotyphlans. The tentativeness of many of the arguments presented in this review highlights our main conclusion, i.e., insights regarding the functions of eulipotyphlan venoms merit additional study.
Highlights
Key Contribution: The purpose of this review is to summarize the current knowledge on the Eulipotyphla venoms, their toxicity and composition, and delineate the hypotheses explaining evolution of their ecological functions
It is not surprising that most studies have focused on biochemical analyses of animal venoms, due to their potential medical applications and severe human morbidity and mortality caused by snake bites or scorpion stings [12,13,14]
In Haberl’s [162] experiments, the handling times of mealworm larvae were shorter for venomous water shrews (N. fodiens and N. anomalus) than for nonvenomous species (Sorex araneus, S. minutus, Crocidura suaveolens), with the differences, depending on the interspecies comparison, ranging from 3.2 to even 33.9 s for handling a single larva
Summary
The dynamic development and application of molecular techniques to the study of venom (referred to as venomics; [1,2,3,4,5]) during recent decades have identified and characterized many natural toxins [5,6,7] and have offered a great opportunity for their use as pharmacological tools. Despite comprehensive studies on toxic molecules, including their purification and descriptions of their physiological and pharmacological mechanisms, our knowledge of the ecology and evolution of natural toxins is scarce. To fully understand the evolution of animal venoms, it is necessary to examine their biological functions and toxic effects on their natural targets (wild prey and/or enemies) instead of commonly used models such as laboratory mice, rats, rabbits or humans. Ecological studies focusing on natural, predator–prey interactions and using venom in prey hunting, competition, and avoiding predation, parasites and pathogens can shed new light on the evolution of animal venom systems [15,16,17]
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