Abstract
BackgroundFor echinoderms with feeding larvae, metamorphic and post-settlement success may be highly dependent on larval nutrition and the accumulation of energetic lipids from the diet. In contrast to the sea urchins, starfish and brittle stars within the Phylum Echinodermata, sea cucumber metamorphosis does not involve formation of a juvenile rudiment, but instead there is a rearrangement of the entire larval body. Successful metamorphosis in sea cucumbers is often associated with the presence in the late auricularia stage of an evolutionary novelty, the hyaline spheres (HS), which form in the base of the larval arms. Known since the 1850s the function of these HS has remained enigmatic—suggestions include assistance with flotation, as an organizer for ciliary band formation during metamorphosis and as a nutrient store for metamorphosis.ResultsHere using multiple methodologies (lipid mapping, resin-section light microscopy, lipid and fatty acid analyses) we show definitively that the HS are used to store neutral lipids that fuel the process of metamorphosis in Australostichopus mollis. Neutral lipids derived from the phytoplankton diet are transported by secondary mesenchyme cells (“lipid transporting cells”, LTC), likely as free fatty acids or lipoproteins, from the walls of the stomach and intestine through the blastocoel to the HS; here, they are converted to triacylglycerol with a higher saturated fatty acid content. During metamorphosis the HS decreased in size as the triacylglycerol was consumed and LTC again transported neutral lipids within the blastocoel.ConclusionThe HS in A. mollis functions as a nutrient storage structure that separates lipid stores from the major morphogenic events that occur during the metamorphic transition from auricularia–doliolaria–pentactula (settled juvenile). The discovery of LTC within the blastocoel of sea cucumbers has implications for other invertebrate larvae with a gel-filled blastocoel and for our understanding of lipid use during metamorphosis in marine invertebrates.
Highlights
For echinoderms with feeding larvae, metamorphic and post-settlement success may be highly dependent on larval nutrition and the accumulation of energetic lipids from the diet
Successful metamorphosis in sea cucumbers is often associated with the presence in the late auricularia stage of enigmatic structures, the hyaline spheres (HS), which form in the larval arms during the feeding phase, increase in diameter in the late auricularia before metamorphosis into the doliolaria stage and decrease in size during the pentactula and juvenile stage [7,8,9,10, 12,13,14,15,16]
Late auricularia Larvae of the sea cucumber Australostichopus mollis reach the late auricularia stage approximately 14 days after fertilization, defined as when the left somatocoel was about half the length of the stomach and there was no elongation of the axohydrocoel (Fig. 1a)
Summary
For echinoderms with feeding larvae, metamorphic and post-settlement success may be highly dependent on larval nutrition and the accumulation of energetic lipids from the diet. In species with feeding larvae, metamorphic and post-settlement success may be highly dependent on larval nutrition and the accumulation of energetic lipids from the diet [3,4,5]. These lipid reserves, Holothuroids are the echinoderm class that most fully represents the ancestral type of indirect larval. HS appear in species from three clades in the recent molecular phylogeny of the Holothuroidea [19], in the families Holothuriidae, Stichopodidae and Synaptidae, but are absent in crinoids and echinoderm classes that form a rudiment during metamorphosis [7]
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