Sequestration of nematocysts by divergent cnidarian predators: mechanism, function, and evolution

Abstract

Animals have evolved diverse mechanisms to protect themselves from predators. Although such defenses are typically generated endogenously, some species have evolved the ability to acquire defenses by sequestering defensive chemicals or structures from other species. Chemical sequestration is widespread among animals, but the ability to sequester entire structures, such as organelles, appears to be rare. Here, we review information on the seques-tration of functional nematocysts, the stinging organelles produced by Cnidaria, by divergent predators. Nematocyst sequestration has evolved multiple times, having been documented in Ctenophora, Acoelomorpha, Platyhelminthes, and Mollusca. For each of these phyla, we review the phylogenetic distribution, mechanisms, and possible functions of nematocyst sequestration. We estimate that nematocyst sequestration has evolved 9-17 times across these four phyla. Although data on the mechanism of sequestration remain limited, similarities across several groups are evident. For example, in multiple groups, nematocysts are transported within cells from the gut to peripheral tissues, and certain types of nematocysts are selectively sequestered over others, suggesting convergent evolution in some aspects of the sequestration process across phyla. Similarly, although the function of nematocyst sequestra-tion has not been well documented, several studies do suggest that the nematocysts seques-tered by these groups are effective for defense. We highlight several traits that are common to Ctenophora, Acoelomorpha, Platyhelminthes, and Mollusca and suggest hypotheses for how these traits could have played a role in the evolution of nematocyst sequestration. Finally, we propose a generalized working model for the steps that may lead to the evolution of nemato-cyst sequestration and discuss important areas for future research.

The Precursor Hypothesis of Sponge Kleptocnidism: Development of Nematocysts in Haliclona cnidata sp. nov. (Porifera, Demospongiae, Haplosclerida)

“…Little is known about the acquisition of exogenous defense structures like the sequestration of nematocysts and the ecological implications for the sequestering species. Recently, Goodheart and Bely provided a generalized working model as well as traits facilitating the evolution of kleptocnidism in metazoans, i.e., preying on cnidarians, a soft-body, a branched digestive system that allows unhampered distribution of nematocysts, and the ability to regenerate (Goodheart and Bely, 2017). Interestingly, sponges comply mostly with these traits by having an aquiferous system throughout their soft body combined with regenerative power (Hooper and Van Soest, 2002), which likely facilitate the distribution of nematocysts.…”

“…These immature nematocytes are maintained in the sponge and may even mature to specific types of fully functioning nematocytenematocyst complexes. Such maturation of sequestered nematocysts is known for some nudibranchs (Goodheart and Bely, 2017). Free-floating immature nematocytes may, for example, be released into the water body after corallivorous predator attacks either from predator feces (Martin, 2003;Goodheart and Bely, 2017) or potentially from injured coral tissues.…”

“…Based on the alternative term for nematocyst (i.e., cnidocyst), the sum of all nematocyst types being present in a species is called cnidom (Fautin, 2009). However, some noncnidarians like nudibranch gastropods can acquire functional nematocysts via feeding and apply these as "cellular weapons" (sensu Tardent, 1995) for their own defense (reviewed in Greenwood, 2009;Goodheart and Bely, 2017). This phenomenon is referred to as kleptocnidism and the sequestered nematocysts are called kleptocnidae.…”

“…This phenomenon is referred to as kleptocnidism and the sequestered nematocysts are called kleptocnidae. Kleptocnidism has evolved multiple times in at least four phyla-Ctenophora, Acoelomorpha, Platyhelminthes, and Mollusca (Goodheart and Bely, 2017). Among sponges, this trait has so far only been reported in a single species, the Australian taxon "Haliclona sp.…”

“…628, " which presumably sequesters the nematocysts from a coral donor (Garson et al, 1998;Russell et al, 2003). Kleptocnidism in the phylum Porifera is surprising, however, as filter-feeding sponges do not feed on cnidarian prey, which has been considered a prerequisite for sequestering nematocysts (Goodheart and Bely, 2017).…”