Maternal investment and nutrient utilization during early larval development of the sea cucumber Australostichopus mollis

Peters-Didier, Josefina; Sewell, Mary A.

doi:10.1007/s00227-017-3209-7

Cited by 8 publications

(5 citation statements)

References 54 publications

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“…Early-stage auricularia developed two granular masses, similar to those described by Semon [24] and Mortensen [12] in the two posterolateral arms (Fig. 3a).…”

Section: Resultssupporting

confidence: 82%

“…Australostichopus mollis larvae were obtained from 4 L rearing tanks of 1-µm-filtered sea water (FSW) set-up with gentle aeration under constant light and temperature conditions (12:12-h light:dark cycle at 19 ± 0.5 °C) as outlined in detail in Peters-Didier and Sewell [24]. Larvae were fed a 1:1:1 diet of microalgae Isochrysis galbana, Dunaliella tertiolecta and Chaetoceros muelleri (CSIRO Australia) supplied at a final concentration of 3000 microalgae cells per ml twice daily.…”

Section: Methodsmentioning

confidence: 99%

“…Lipid extraction and analysis using Iatroscan thin-layer chromatography–flame ionization detection (TLC–FID) was performed as described in Peters-Didier and Sewell [24] on larval samples (14 days, 20 days, 22 days; N = 200 individuals) and pentactula/juveniles ( N = 60). Traditional TLC was also conducted on lipid extracts (45) from auricularia pre-HS (14 days) and with HS (20 days, N = 1000 individuals).…”

Section: Methodsmentioning

confidence: 99%

“…Here, using auricularia larvae of the New Zealand sea cucumber Australostichopus mollis we directly test the hypothesis of a nutritional function for the HS using lipid mapping, resin-section light microscopy and lipid and fatty acid analyses. Our previous work has shown that, like asteroids and echinoids, A. mollis use the neutral lipids TAG and FFA to build the larval body [24], and we predicted that, as in other echinoderms [3, 4], these lipids would also be used to fuel metamorphosis. Consequently, our approach to study the HS was to use specific dyes to stain lipids—firstly the lipophilic Nile Red and then using more specific neutral lipid and phospholipid fluorescent probes.…”

Section: Introductionmentioning

confidence: 99%

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The role of the hyaline spheres in sea cucumber metamorphosis: lipid storage via transport cells in the blastocoel

Peters-Didier

Sewell

2019

EvoDevo

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Background 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 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. Results Here 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. Conclusion The 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.

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“…Early-stage auricularia developed two granular masses, similar to those described by Semon [24] and Mortensen [12] in the two posterolateral arms (Fig. 3a).…”

Section: Resultssupporting

confidence: 82%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

The role of the hyaline spheres in sea cucumber metamorphosis: lipid storage via transport cells in the blastocoel

Peters-Didier

Sewell

2019

EvoDevo

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“…Mechanistically, maternal contributions to shifts in tolerance of the progeny could manifest in two ways -1) as maternal energetic investment in the eggs, and/or 2) as maternally-derived egg transcripts and proteins working to reduce cellular damage due to heat stress during early development. Historically maternal energetic investment has been assessed through measurements of egg size and biochemical composition (i.e., lipids and proteins) where studies have shown that egg size and nutritional macromolecules are significant in determining conditions and performance of developing progeny in echinoderms (Jaeckle, 1995;Prowse et al, 2008;Moran et al, 2013;Peters-Didier and Sewell, 2017). Given these data on echinoderm eggs, we hypothesized that observed differences in offspring phenotype would be due to differences in maternal energetic provisioning (i.e., egg size and biochemical composition).…”

Section: Maternal Provisioning As a General Mechanism Of Tgpmentioning

confidence: 99%

Transgenerational plasticity as a mechanism of response to marine heatwaves in the purple sea urchin, Strongylocentrotus purpuratus

2023

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Kelp forests of the California Current System have experienced prolonged marine heatwave (MHW) events that overlap in time with the phenology of life history events (e.g., gametogenesis and spawning) of many benthic marine invertebrates. To study the effect of thermal stress from MHWs during gametogenesis in the purple sea urchin (Strongylocentrotus purpuratus) and further, whether MHWs might induce transgenerational plasticity (TGP) in thermal tolerance of progeny, adult urchins were acclimated to two conditions in the laboratory – a MHW temperature of 18°C and a non-MHW temperature of 13°C. Following a four-month long acclimation period (October–January), adults were spawned and offspring from each parental condition were reared at MHW (18°C) and non-MHW temperatures (13°C), creating a total of four embryo treatment groups. To assess transgenerational effects for each of the four groups, we measured thermal tolerance of hatched blastula embryos in acute thermal tolerance trials. Embryos from MHW-acclimated females were more thermally tolerant with higher LT50 values as compared to progeny from non-MHW-acclimated females. Additionally, there was an effect of female acclimation state on offspring body size at two stages of embryonic development - early gastrulae and prism, an early stage echinopluteus larvae. To assess maternal provisioning as means to also alter embryo performance, we assessed gamete traits from the differentially acclimated females, by measuring size and biochemical composition of eggs. MHW-acclimated females had eggs with higher protein concentrations, while egg size and lipid content showed no differences. Our results indicate that TGP plays a role in altering the performance of progeny as a function of the thermal history of the female, especially when thermal stress coincides with gametogenesis. In addition, the data on egg provisioning show that maternal experience can influence embryo traits via egg protein content. Although this is a laboratory-based study, the results suggest that TGP may play a role in the resistance and tolerance of S. purpuratus early stages in the natural kelp forest setting.

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Bait-subsidized diets and their effects on ovigerous North American lobsters (Homarus americanus)

Goldstein

Shields

2018

Aquacult Int

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Maternal investment and nutrient utilization during early larval development of the sea cucumber Australostichopus mollis

Cited by 8 publications

References 54 publications

The role of the hyaline spheres in sea cucumber metamorphosis: lipid storage via transport cells in the blastocoel

The role of the hyaline spheres in sea cucumber metamorphosis: lipid storage via transport cells in the blastocoel

Transgenerational plasticity as a mechanism of response to marine heatwaves in the purple sea urchin, Strongylocentrotus purpuratus

Bait-subsidized diets and their effects on ovigerous North American lobsters (Homarus americanus)

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