Abstract
Thousands of armed predatory species, distributed widely across the metazoan tree-of-life, consume only hard-shell or exoskeleton-bearing organisms (called “durophagy”). Prey armor clearly has evolved in response to selection by predators, but there is little evidence of the contrary, counter-adaptation by predators. Evolved consumer responses to prey, in general, might be more readily expressed in ways other than morphological traits, including via sensory cues. Here, we explored the chemosensory basis for durophagy in a model predator-prey system, and identified intimate associations between durophagous predators and their shelled prey. Barnacles (Balanus glandula and Semibalanus cariosus) bear hard shells and secrete, respectively, a 199 or 201 kDa glycoprotein ortholog (named “MULTIFUNCin”), with expression limited to the body armor (epidermis, cuticle, and live shell). To test for effects of MULTIFUNCin on predators, we constructed faux prey to mimic meaningful physical and chemical characteristics of live barnacles. In separate experiments, each consumer species was presented MULTIFUNCin, purified from either B. glandula or S. cariosus, at a typical armor concentration. All six predatory species (sea star, Pisaster ochraceus; whelks, Acanthinucella spirata, Nucella emarginata, N. ostrina, N. canaliculata, and N. lamellosa) attacked and ate MULTIFUNCin-infused faux prey significantly more than controls. Akin to barnacles, secretion of glycoprotein-rich extracellular matrices is common among armored prey species—from marine sponges to terrestrial vertebrates. Our results, therefore, suggest that chemosensory exploitation of glycoproteins could be widespread, with notable consequences for life on land and in the sea.
Highlights
A myriad of metazoan species have evolved armor in morphological defenses
The arms race analogy has been applied to a wide array of natural enemies, even though the degree of reciprocity and details of selection vary among antagonistic encounters
Each barnacle species (B. glandula and S. cariosus) secretes, respectively, a 199 or 201 kDa glycoprotein ortholog, with expression limited to the body armor (Ferrier et al, 2016a; Figure 1)
Summary
A myriad of metazoan species have evolved armor in morphological defenses. The scales of fishes and reptiles, cuticles and carapaces of insects and crustaceans, as well as skeletons and shells of corals, mollusks, brachiopods, echinoderms, and sponges, all protect against the “slings and arrows” of a dangerous world (Kruppert et al, 2020). Chemosensory Exploitation and Arms Races species as arms races between natural enemies (Brodie and Brodie, 1999). The arms race analogy has been applied to a wide array of natural enemies, even though the degree of reciprocity and details of selection vary among antagonistic encounters. Elaborated jaws, and other weapons, increase the ability of consumers to capture prey. Such innovations evolve in response to selection pressures imposed by higherorder predators and by competitors for food, space, and mates (Vermeij, 1994, 2013; Bicknell and Paterson, 2018; Aristide and Morlon, 2019). Enhanced capacity to capture prey can be an unintended consequence of escalation in a particular antipredator, or anti-competitor, morphological or behavioral trait
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