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Transcriptional profiling of spiny lobster metamorphosis reveals three new additions to the nuclear receptor superfamily.

ABSTRACT: BACKGROUND:The Crustacea are an evolutionarily diverse taxon which underpins marine food webs and contributes significantly to the global economy. However, our knowledge of crustacean endocrinology and development is far behind that of terrestrial arthropods. Here we present a unique insight into the molecular pathways coordinating crustacean metamorphosis, by reconciling nuclear receptor (NR) gene activity from a 12-stage, 3-replicate transcriptome in the ornate spiny lobster (Panulirus ornatus) during larval development. RESULTS:We annotated 18 distinct nuclear receptor genes, including three novel NRs which are upregulated prior to metamorphosis and have hence been named the "molt-associated receptors" (MARs). We also demonstrate the ecdysone-responsive expression of several known molt-related NRs including ecdysone receptor, fushi-tarazu-F1 and E75. Phylogenetic analysis of the curated NR family confirmed gene annotations and suggested that the MARs are a recent addition to the crustacean superfamily, occurring across the Malacostraca from the Stomatopoda to the Decapoda. The ligand-binding domain of these receptors appears to be less conserved than that of typical group-1 NRs. Expression data from two other crustacean species was utilized to examine MAR expression. The Y-organ of the tropical land crab showed a decline in expression of all MARs from intermolt to post-molt. Tissue distributions showed gonad-enriched expression in the Eastern rock lobster and antennal gland-enriched expression in the tropical land crab, although expression was evident across most tissues. CONCLUSION:By mining transcriptome data, we have curated an extensive list of NR genes expressed during the metamorphic molts of P. ornatus, including three novel crustacean NRs which appear to play a role in the molting process. Divergence of the E-region of these new receptors indicates that they may have adopted a function that is unconventional for NRs. Based on expression patterns, we can confirm that a number of NRs play a role in the ecdysone cassette which regulates molting in crustaceans. This study describes in detail the molecular events surrounding crustacean molting and metamorphosis by taking advantage of the distinctive life history unique to achelatan crustaceans.

SUBMITTER: Hyde CJ

PROVIDER: S-EPMC6599367 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:One of the major impediments to spiny lobster aquaculture is the high cost of hatchery production due to the long and complex larval cycle and poor survival during the many moult stages, especially at metamorphosis. We examined if the key trait of larval survival can be improved through selection by determining if genetic variance exists for this trait. Specifically, we report, for the first time, genetic parameters (heritability and correlations) for early survival rates recorded at five larval phases; early-phyllosoma stages (instars 1-6; S1), mid-phyllosoma stages (instars; 7-12; S2), late-phyllosoma stages (instars 13-17; S3), metamorphosis (S4) and puerulus stage (S5) in hatchery-reared spiny lobster Sagmariasus verreauxi. RESULTS:The data were collected from a total of 235,060 larvae produced from 18 sires and 30 dams over nine years (2006 to 2014). Parentage of the offspring and full-sib families was verified using ten microsatellite markers. Analysis of variance components showed that the estimates of heritability for all the five phases of larval survival obtained from linear mixed model were generally similar to those obtained from threshold logistic generalised models (0.03-0.47 vs. 0.01-0.50). The heritability estimates for survival traits recorded in the early larval phases (S1 and S2) were higher than those estimated in later phases (S3, S4 and S5). The existence of the additive genetic component in larval survival traits indicate that they could be improved through selection. Both phenotypic and genetic correlations among the five survival measures studied were moderate to high and positive. The genetic associations between successive rearing periods were stronger than those that are further apart. CONCLUSIONS:Our estimates of heritability and genetic correlations reported here in a spiny lobster species indicate that improvement in the early survival especially during metamorphosis can be achieved through genetic selection in this highly economic value species.

Project description:The non-feeding postlarva (puerulus) of spiny lobsters actively swims from the open ocean to the coastal habitats where it settles and molts to the first-stage juvenile (JI). Because pueruli use much of their energy reserves swimming and preparing for the post-settlement molt, the survival of JIs presumably depends on resuming feeding as soon as possible. To test this hypothesis, the resistance to starvation of JIs of the Caribbean spiny lobster, Panulirus argus, was evaluated by measuring their point-of-no-return (PNR, minimum time of initial starvation preventing recovery after later feeding) and point-of-reserve-saturation (PRS, minimum time of initial feeding allowing for food-independent development through the rest of the molting cycle) in a warm and a cold season. Each experiment consisted of eight groups: a continuously fed control (FC) group, a continuously starved control (SC) group, and six groups subjected to differential periods of either initial starvation and subsequent feeding (PNR experiments) or initial feeding and subsequent starvation (PSR experiments). No JIs molted under continuous absence of food (SC). In both PNR experiments (temperature in warm season: 29.79 ± 0.07°C, mean ± 95% CI; in cold season: 25.63 ± 0.12°C) mortality increased sharply after 9 d of initial starvation and intermolt periods increased with period of initial starvation, but were longer in the cold season. The PNR50 was longer in the warm season (12.1 ± 1.2 d, mean ± 95% CI) than in the cold season (9.5 ± 2.1 d). In PRS experiments (temperature in warm season: 29.54 ± 0.07 °C; in cold season: 26.20 ± 0.12 °C), JIs that molted did so near the end of the feeding period; all JIs initially fed for up to 6 d succumbed, and no JIs molted after 13 d of starvation despite having fed previously. The PRS50 did not differ between the cold (13.1 ± 0.7 d) and warm seasons (12.1 ± 1.1 d). JIs of P. argus exhibit a remarkable resistance to starvation considering that the previous non-feeding, energy-demanding puerulus phase lasts for ∼3 weeks. However, JIs appear to have a relatively higher degree of dependence on food to complete development to JII during the cold season than during the warm season. Therefore, JIs of P. argus would appear to be more resistant to starvation during the warm season.

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Transcriptional profiling of spiny lobster metamorphosis reveals three new additions to the nuclear receptor superfamily.

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