Intra-organismal distribution of tetrodotoxin in two species of blue-ringed octopuses (Hapalochlaena fasciata and H. lunulata)

Williams, Becky L.; Caldwell, Roy L.

doi:10.1016/j.toxicon.2009.05.019

Cited by 53 publications

(58 citation statements)

References 55 publications

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“…Matsui et al 1982;Matsumura 1996;Noguchi et al 2006;Saito et al 1984). However, the TTX levels found in adult H. lunulata from this area (Bali, Indonesia) are comparable to levels found in other species of the genus (Williams and Caldwell 2009;Yotsu-Yamashita et al 2007). Also, TTX stores increase in developing embryos of H. lunulata in captivity after eggs have been laid but before hatching, suggesting that the mechanism of TTX production remains intact (Williams et al 2011).…”

Section: Discussionsupporting

confidence: 56%

Chemical defense in pelagic octopus paralarvae: Tetrodotoxin alone does not protect individual paralarvae of the greater blue-ringed octopus (Hapalochlaena lunulata) from common reef predators

et al. 2011

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Some pelagic marine larvae possess anti-predator chemical defenses. Occasionally, toxic adults imbue their young with their own defensive cocktails. We examined paralarvae of the greater blue-ringed octopus (Hapalochlaena lunulata) for the deadly neurotoxin tetrodotoxin (TTX), and if present, whether TTX conferred protection to individual paralarvae. Paralarvae of H. lunulata possessed 150 ± 17 ng TTX each. These paralarvae appeared distasteful to a variety of fish and stomatopod predators, yet food items spiked with 200 ng TTX were readily consumed by predators. We conclude that TTX alone does not confer individual protection to paralarvae of H. lunulata, and that they possess an alternative defense. In larger doses, tetrodotoxin is a deterrent to the predatory stomatopod Haptosquilla trispinosa (mean dose = 3.97 lg/g). This corresponds to 12-13 paralarvae per predator based on the TTX levels of the clutch we examined. Thus, the basic assumption that individual paralarvae of H. lunulata are defended by TTX alone was disproved. Instead, functionality of TTX levels in paralarvae may arise through alternative selective pathways, such as deterrence to parasites, through kin selection, or against predator species not tested here.

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Section: Discussionsupporting

confidence: 56%

Chemical defense in pelagic octopus paralarvae: Tetrodotoxin alone does not protect individual paralarvae of the greater blue-ringed octopus (Hapalochlaena lunulata) from common reef predators

et al. 2011

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“…This is because TTX is likely produced by bacteria symbiotically associated with their hosts, or else, taken up from the food chain by animals that prey on TTX-accumulating organisms (51). In any event, unlike peptide toxins that are sequestered within a gland, TTX passes through cell membranes so that although it may be concentrated in certain tissues, all tissues are more or less exposed to it (52). Thus, those animals that sequester high concentrations of TTX have evolved mechanisms to protect themselves from its effects (53,54).…”

Section: Adaptive Evolution Of Nav Channels: Tetrodotoxin Resistancementioning

confidence: 99%

Adaptive evolution of voltage-gated sodium channels: The first 800 million years

Zakon

2012

Proc. Natl. Acad. Sci. U.S.A.

143

141

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Voltage-gated Na + -permeable (Nav) channels form the basis for electrical excitability in animals. Nav channels evolved from Ca 2+ channels and were present in the common ancestor of choanoflagellates and animals, although this channel was likely permeable to both Na + and Ca 2+. Thus, like many other neuronal channels and receptors, Nav channels predated neurons. Invertebrates possess two Nav channels (Nav1 and Nav2), whereas vertebrate Nav channels are of the Nav1 family. Approximately 500 Mya in early chordates Nav channels evolved a motif that allowed them to cluster at axon initial segments, 50 million years later with the evolution of myelin, Nav channels "capitalized" on this property and clustered at nodes of Ranvier. The enhancement of conduction velocity along with the evolution of jaws likely made early gnathostomes fierce predators and the dominant vertebrates in the ocean. Later in vertebrate evolution, the Nav channel gene family expanded in parallel in tetrapods and teleosts (∼9 to 10 genes in amniotes, 8 in teleosts). This expansion occurred during or after the late Devonian extinction, when teleosts and tetrapods each diversified in their respective habitats, and coincided with an increase in the number of telencephalic nuclei in both groups. The expansion of Nav channels may have allowed for more sophisticated neural computation and tailoring of Nav channel kinetics with potassium channel kinetics to enhance energy savings. Nav channels show adaptive sequence evolution for increasing diversity in communication signals (electric fish), in protection against lethal Nav channel toxins (snakes, newts, pufferfish, insects), and in specialized habitats (naked mole rats).gene duplication | nervous system M ulticellular animals evolved >650 million years ago (1). The nervous system and muscles evolved shortly thereafter. The phylogeny of basal metazoans is poorly resolved, likely because of the rapid radiation of these then-new life forms (2), so depending on the phylogeny one embraces, the nervous system evolved once, once with a loss in sponges, or twice independently in ctenophora and bilateria + cnidaria or bilateria and cnidaria + ctenophora (3, 4). However, in all animals with nervous systems, neurons generate action potentials (APs), release excitatory and inhibitory neurotransmitters, form circuits, receive sensory input, innervate muscle, and direct behavior.The history of brain evolution and its key neural genes would fill volumes. I will use voltage-dependent Na + (Nav, Na-permeable voltage-dependent = protein; scn, sodium channel = gene) channels as an exemplar to tell this story because all neuronal excitability depends on Nav channels, there is a good understanding of their function and regulation from biophysical, biochemical, and modeling studies, and there are fascinating examples of ecologically relevant adaptations. An additional rationale is that although many proteins, such as immunoglobins, sperm and egg receptors, olfactory receptors, opsins, and surface proteins of pathogens, a...

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“…For detailed reviews of cephalopod development, see von Boletzky (1989Boletzky ( , 2003. Tetrodotoxin content in the posterior salivary glands (PSG) was used as a proxy for total female TTX levels because these two quantities are highly correlated and PSG is more easily assayed (Williams and Caldwell, 2009). Toxicity assays are destructive, thus female samples were collected at the reproductive stage indicated by eggs/paralarvae.…”

Section: Methodsmentioning

confidence: 99%

“…Toxicity assays are destructive, thus female samples were collected at the reproductive stage indicated by eggs/paralarvae. Previously, we found TTX in oviducal glands of H. fasciata (Williams and Caldwell, 2009); thus, three oviducal glands of H. lunulata and one of H. fasciata also were sampled.…”

Section: Methodsmentioning

confidence: 99%

“…Adult blue-ring octopuses are wellknown for possessing the potent neurotoxin, TTX, which has been identified in 3 species of blue-ringed octopus, Hapalochlaena fasciata (e.g., Sheumack et al, 1978;Williams and Caldwell, 2009), H. maculosa (e.g., YotsuYamashita et al, 2007), and H. lunulata (e.g., Williams and Caldwell, 2009). Based on symptoms of human envenomation (e.g., McMichael, 1964), other species of Hapalochlaena also appear to contain TTX.…”

Section: Introductionmentioning

confidence: 99%

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Ontogeny of Tetrodotoxin Levels in Blue-ringed Octopuses: Maternal Investment and Apparent Independent Production in Offspring of Hapalochlaena lunulata

et al. 2010

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Many organisms provision offspring with antipredator chemicals. Adult blue-ringed octopuses (Hapalochlaena spp.) harbor tetrodotoxin (TTX), which may be produced by symbiotic bacteria. Regardless of the ultimate source, we find that females invest TTX into offspring and offspring TTX levels are significantly correlated with female TTX levels. Because diversion of TTX to offspring begins during the earliest stages of egg formation, when females are still actively foraging and looking for mates, females may face an evolutionary tradeoff between provisioning larger stores of TTX in eggs and retaining that TTX for their own defense and offense (venom). Given that total TTX levels appear to increase during development and that female TTX levels correlate with those of offspring, investment may be an active adaptive process. Even after eggs have been laid, TTX levels continue to increase, suggesting that offspring or their symbionts begin producing TTX independently. The maternal investment of TTX in offspring of Hapalochlaena spp. represents a rare examination of chemical defenses, excepting ink, in cephalopods.

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Intra-organismal distribution of tetrodotoxin in two species of blue-ringed octopuses (Hapalochlaena fasciata and H. lunulata)

Cited by 53 publications

References 55 publications

Chemical defense in pelagic octopus paralarvae: Tetrodotoxin alone does not protect individual paralarvae of the greater blue-ringed octopus (Hapalochlaena lunulata) from common reef predators

Chemical defense in pelagic octopus paralarvae: Tetrodotoxin alone does not protect individual paralarvae of the greater blue-ringed octopus (Hapalochlaena lunulata) from common reef predators

Adaptive evolution of voltage-gated sodium channels: The first 800 million years

Ontogeny of Tetrodotoxin Levels in Blue-ringed Octopuses: Maternal Investment and Apparent Independent Production in Offspring of Hapalochlaena lunulata

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