Metamorphosis

@book{doi105962bhltitle4801,
    author = "Conklin, Edwin",
    title = "The organization and cell-lineage of the ascidian egg",
    year = "1905",
    journal = "Bulletin of Miscellaneous Information (Royal Gardens Kew)",
    url = "https://doi.org/10.5962/bhl.title.4801",
    doi = "10.5962/bhl.title.4801",
    openalex = "W577221246",
    references = "macbride1898the"
}

ABSTRACT The viviparity recorded for this ascidian parallels that of placental mammals in reduction of the number and size of the eggs, the development of extra-embryonic membranes, and the prolongation of larval development with increase in the gestation period. The ovum is alecithal, 25 μ. in diameter; it develops within an oviducal brood pouch in which the lining cells become distinctly modified and which remains attached to the parent for 5! months. Exposure of the embryo to the lumen of the pouch is brought about by rupture of the overlying follicle cells due to enzyme secretion by the dorsal-most cells of the blastula. Endodermal development is precocious. At the gastrula stage the future oesophageal region, the future stomach, and a pair of endodermal tubes are distinguishable. The paired endodermal tubes are unique in the ascidians. They are larval structures which disappear after metamorphosis and bear no relation to the functional stigmata of the oozooid. They resemble the branchial tubes of the Appendicularia, developing as blind outgrowths which later open through to the exterior; but in this species they open dorsally, not ventrally. They act as passive channels through which material from the pouch passes into the gut (a bolus being present from the gastrula stage onwards) and as anchoring strands for the ectotrophe. This extra-embryonic membrane formed by elevation of the dorsal ectoderm ultimately practically envelops the embryo and becomes apposed to the lining of the pouch. It is extremely simple, exhibits no vascularization, makes no actual liaison with the oviducal epithelium, and shows little cell differentiation. Extra-embryonic material reaches the embryo indirectly by diffusion across the ectotrophe (which unlike the remaining embryonic ectoderm secretes no test), and directly through the endodermal tubes. The latter method is the more important during early stages of development, the former during later stages. The production of an extremely large and complex tadpole with numerous buds at an advanced stage of organogenesis testifies to the success of this type of viviparity.

@article{doi101242jcss39739435,
    author = "Brewin, Beryl I.",
    title = "The Growth and Development of a Viviparous Compound Ascidian, Hypsistozoa fasmeriana",
    year = "1956",
    journal = "Journal of Cell Science",
    abstract = "ABSTRACT The viviparity recorded for this ascidian parallels that of placental mammals in reduction of the number and size of the eggs, the development of extra-embryonic membranes, and the prolongation of larval development with increase in the gestation period. The ovum is alecithal, 25 μ. in diameter; it develops within an oviducal brood pouch in which the lining cells become distinctly modified and which remains attached to the parent for 5! months. Exposure of the embryo to the lumen of the pouch is brought about by rupture of the overlying follicle cells due to enzyme secretion by the dorsal-most cells of the blastula. Endodermal development is precocious. At the gastrula stage the future oesophageal region, the future stomach, and a pair of endodermal tubes are distinguishable. The paired endodermal tubes are unique in the ascidians. They are larval structures which disappear after metamorphosis and bear no relation to the functional stigmata of the oozooid. They resemble the branchial tubes of the Appendicularia, developing as blind outgrowths which later open through to the exterior; but in this species they open dorsally, not ventrally. They act as passive channels through which material from the pouch passes into the gut (a bolus being present from the gastrula stage onwards) and as anchoring strands for the ectotrophe. This extra-embryonic membrane formed by elevation of the dorsal ectoderm ultimately practically envelops the embryo and becomes apposed to the lining of the pouch. It is extremely simple, exhibits no vascularization, makes no actual liaison with the oviducal epithelium, and shows little cell differentiation. Extra-embryonic material reaches the embryo indirectly by diffusion across the ectotrophe (which unlike the remaining embryonic ectoderm secretes no test), and directly through the endodermal tubes. The latter method is the more important during early stages of development, the former during later stages. The production of an extremely large and complex tadpole with numerous buds at an advanced stage of organogenesis testifies to the success of this type of viviparity.",
    url = "https://doi.org/10.1242/jcs.s3-97.39.435",
    doi = "10.1242/jcs.s3-97.39.435",
    openalex = "W2188782393"
}

Abstract Specimens of Ciona intestinalis have been maintained in sea water containing 131I, and the iodinated compounds present in extracts of their endostyles studied by chromatography, using two different two-dimensional systems. Before chromatographic analysis, the extracts have been purified by acetic acid elution from an anion exchange resin, using a procedure based upon that described by Pitt-Rivers & Sacks (1962). The reliability of the technique has been confirmed by prior tests with extracts of the thyroid gland of rats. 3-Monoiodotyrosine and 3,5-diiodotyrosine have been readily identified in 1% and 10% acetic acid eluates of endostylar extracts. There is no evidence that 3, 5, 3' -triiodothyronineis present, but small amounts of thyroxine have been identified in 50% acetic acid eluates; in this instance positive results are only obtained if close attention is given to the conditions in which the experimental animals are maintained. Other radioactive spots are present in the chromatograms, but it has not so far been possible to characterize them. Some reference is made to results obtained with extracts of the remainder of the pharynx, and of the cuticular layer of the tunic. The results are discussed in relation to previous autoradiographic and chromatographic studies of protochordates, and in the light of the well-known development of the thyroid gland of lampreys from the endostyle of the ammocoete larva. Much further investigation of the complex problem of the origin of thyroidal biosynthesis is still needed, but it is concluded at this stage that thyroxine is probably synthesized in the endostyle of Ciona, and that this process is associated with the presence in that organ of a zone of specialized iodinating epithelium. It is, however, impossible as yet to determine whether or not this is a true thyroidal biosynthesis.

@article{doi101098rspb19650063,
    author = "Barrington, E. J. W. and Thorpe, Alan",
    title = "The identification of monoiodotyrosine, diiodotyrosine and thyroxine in extracts of the endostyle of the ascidian, Ciona intestinalis L",
    year = "1965",
    journal = "Proceedings of the Royal Society of London. Series B, Biological sciences",
    abstract = "Abstract Specimens of Ciona intestinalis have been maintained in sea water containing 131I, and the iodinated compounds present in extracts of their endostyles studied by chromatography, using two different two-dimensional systems. Before chromatographic analysis, the extracts have been purified by acetic acid elution from an anion exchange resin, using a procedure based upon that described by Pitt-Rivers \& Sacks (1962). The reliability of the technique has been confirmed by prior tests with extracts of the thyroid gland of rats. 3-Monoiodotyrosine and 3,5-diiodotyrosine have been readily identified in 1\% and 10\% acetic acid eluates of endostylar extracts. There is no evidence that 3, 5, 3' -triiodothyronineis present, but small amounts of thyroxine have been identified in 50\% acetic acid eluates; in this instance positive results are only obtained if close attention is given to the conditions in which the experimental animals are maintained. Other radioactive spots are present in the chromatograms, but it has not so far been possible to characterize them. Some reference is made to results obtained with extracts of the remainder of the pharynx, and of the cuticular layer of the tunic. The results are discussed in relation to previous autoradiographic and chromatographic studies of protochordates, and in the light of the well-known development of the thyroid gland of lampreys from the endostyle of the ammocoete larva. Much further investigation of the complex problem of the origin of thyroidal biosynthesis is still needed, but it is concluded at this stage that thyroxine is probably synthesized in the endostyle of Ciona, and that this process is associated with the presence in that organ of a zone of specialized iodinating epithelium. It is, however, impossible as yet to determine whether or not this is a true thyroidal biosynthesis.",
    url = "https://doi.org/10.1098/rspb.1965.0063",
    doi = "10.1098/rspb.1965.0063",
    openalex = "W2035976475",
    references = "barrington1963comparative, doi101002jmor1051060306, doi1010160006300261904851, doi1010160006300262903487, doi101016000630026290570x, doi1010160010406x60900323, doi1010160016648065900626, doi101017s0025315400009061, doi101017s0025315400014879, doi101017s0025315400017021, doi1023071538464"
}

@article{doi101016s0022532066800515,
    author = "Cloney, Richard A.",
    title = "Cytoplasmic filaments and cell movements: Epidermal cells during ascidian metamorphosis",
    year = "1966",
    journal = "Journal of Ultrastructure Research",
    url = "https://doi.org/10.1016/s0022-5320(66)80051-5",
    doi = "10.1016/s0022-5320(66)80051-5",
    openalex = "W1983645902",
    references = "doi101016b9780121191023x50010, doi101016s0022532061800117, doi101038173971a0, doi101038173973a0, doi101083jcb113736, doi101083jcb172375, doi101083jcb233553, doi101083jcb45529, doi101083jcb92409, doi10310910520296009114754"
}

@article{doi101007bf00335222,
    author = "Cloney, Richard A. and Grimm, Leslie M.",
    title = "Transcellular emigration of blood cells during ascidian metamorphosis",
    year = "1970",
    journal = "Cell and Tissue Research",
    url = "https://doi.org/10.1007/bf00335222",
    doi = "10.1007/bf00335222",
    openalex = "W1992643802"
}

@article{doi101007bf02584045,
    author = "Eakin, Richard M. and Kuda, Aileen M.",
    title = "Ultrastructure of sensory receptors in ascidian tadpoles",
    year = "1970",
    journal = "Cell and Tissue Research",
    url = "https://doi.org/10.1007/bf02584045",
    doi = "10.1007/bf02584045",
    openalex = "W2057576215",
    references = "doi101002jez1400300206, doi101007bf00309735, doi101007bf00321477, doi101007bf02956047, doi1010160012160666900030, doi101073pnas485826, doi101083jcb23319, doi101083jcb24319, doi101242jcss310363393, openalexw589719149"
}

@incollection{doi101016s0065288108603417,
    author = "Millar, R.H.",
    title = "The Biology of Ascidians",
    year = "1971",
    booktitle = "Advances in marine biology",
    url = "https://doi.org/10.1016/s0065-2881(08)60341-7",
    doi = "10.1016/s0065-2881(08)60341-7",
    openalex = "W1173186620",
    references = "doi101007bf00347115, doi101017s0025315400000102, doi101017s002531540001170x, doi101038191786a0, doi101071mf9520205, doi10108000785326196410416277, doi101098rstb19350013, doi101111j109636421970tb00732x, doi101111j1469185x1955tb01546x, doi1023071438975, doi1023071440498, doi1023071948663, doi104319lo1960520138, doi105962bhltitle4801, jørgensen1949feedingrates, openalexw1556897912, openalexw2077200748, openalexw615237313, orton1913the"
}

Abstract Thyroid‐like activity was investigated in the endostyles of Molgula manhattensis, M. occidentalis and Styela plicata. Animals were immersed in sea water containing 125 I for one to 24 hours. Although electron microscopic autoradiography revealed an extracellular accumulation of silver grains associated with zone 8 in all three species and with zone 9 in two of them, intracellular accumulations were found only in zone 7. Within this zone in each of the three species, grains were present over the apical cell membrane, multivesicular bodies and the apical cytoplasmic matrix after brief exposure to 125 I. After longer exposure, grains were also present over large dense bodies and more basal regions of the cytoplasmic matrix. Certain features, suggestive of thyroidal functions, were observed in the cells of zone 7. These included morphological evidence for secretory and pinocytotic activities and cytochemical evidence both for peroxidase activity and for the presence of carbohydrate material which may represent a glycoprotein. It is concluded that active binding of iodine is restricted to zone 7 in the endostyles of Molgula and Styela, where it occurs at both the apical cell membrane and within multivesicular bodies. Some of the iodinated product may be immediately passed into the lumen of the pharynx. The rest is stored intracellularly within multivesicular bodies and dense bodies of zone 7. Intracellular binding and storage of iodine are considered to represent primitive conditions preceding the evolution of the follicular structure of the thyroid gland.

@article{doi101002jez1401880111,
    author = "DUNN, ANN D.",
    title = "Ultrastructural autoradiography and cytochemistry of the iodine‐binding cells in the ascidian endostyle",
    year = "1974",
    journal = "Journal of Experimental Zoology",
    abstract = "Abstract Thyroid‐like activity was investigated in the endostyles of Molgula manhattensis, M. occidentalis and Styela plicata. Animals were immersed in sea water containing 125 I for one to 24 hours. Although electron microscopic autoradiography revealed an extracellular accumulation of silver grains associated with zone 8 in all three species and with zone 9 in two of them, intracellular accumulations were found only in zone 7. Within this zone in each of the three species, grains were present over the apical cell membrane, multivesicular bodies and the apical cytoplasmic matrix after brief exposure to 125 I. After longer exposure, grains were also present over large dense bodies and more basal regions of the cytoplasmic matrix. Certain features, suggestive of thyroidal functions, were observed in the cells of zone 7. These included morphological evidence for secretory and pinocytotic activities and cytochemical evidence both for peroxidase activity and for the presence of carbohydrate material which may represent a glycoprotein. It is concluded that active binding of iodine is restricted to zone 7 in the endostyles of Molgula and Styela, where it occurs at both the apical cell membrane and within multivesicular bodies. Some of the iodinated product may be immediately passed into the lumen of the pharynx. The rest is stored intracellularly within multivesicular bodies and dense bodies of zone 7. Intracellular binding and storage of iodine are considered to represent primitive conditions preceding the evolution of the follicular structure of the thyroid gland.",
    url = "https://doi.org/10.1002/jez.1401880111",
    doi = "10.1002/jez.1401880111",
    openalex = "W1981467931",
    references = "doi1010160016648065900626, doi101016001664806990063x, doi1010160016648071901493, doi1010160016648072902560, doi101017s0025315400017021, doi101083jcb152173, doi101083jcb202313, doi101083jcb352357, doi101083jcb3811, doi101083jcb92409, doi101098rspb19650063, doi101177144291"
}

@article{doi101007bf00229160,
    author = "Schiaffino, Stefano and Burighel, Paolo and Nunzi, M.G.",
    title = "Involution of the caudal musculature during metamorphosis in the ascidian, Botryllus schlosseri",
    year = "1974",
    journal = "Cell and Tissue Research",
    url = "https://doi.org/10.1007/bf00229160",
    doi = "10.1007/bf00229160",
    openalex = "W2058365755"
}

@incollection{doi101016s0065288108604575,
    author = "Goodbody, Ivan",
    title = "The Physiology of Ascidians",
    year = "1975",
    booktitle = "Advances in marine biology",
    url = "https://doi.org/10.1016/s0065-2881(08)60457-5",
    doi = "10.1016/s0065-2881(08)60457-5",
    openalex = "W2178304161",
    references = "barrington1937vi, barrington1963comparative, doi10100797836429105483, doi1010160016648065900626, doi101016001664806990063x, doi1010160305049171901362, doi101016s0065288108603417, doi101017s002531540001170x, doi101017s0025315400017021, doi101038182774a0, doi101071mf9550157, doi101083jcb172375, doi101098rspb19650063, doi101098rspb19680054, doi101242jeb164499, doi101242jeb313424, doi101515bchm219117256494, jørgensen1949feedingrates, openalexw2077200748, openalexw2084845249, openalexw2954279587, orton1913the"
}

@article{doi101007bf00220677,
    author = "Cavey, MichaelJ. and Cloney, RichardA.",
    title = "Ultrastructure and differentiation of ascidian muscle",
    year = "1976",
    journal = "Cell and Tissue Research",
    url = "https://doi.org/10.1007/bf00220677",
    doi = "10.1007/bf00220677",
    openalex = "W2614972014"
}

@article{doi101007bf00225658,
    author = "Cloney, RichardA.",
    title = "Larval adhesive organs and metamorphosis in ascidians",
    year = "1977",
    journal = "Cell and Tissue Research",
    url = "https://doi.org/10.1007/bf00225658",
    doi = "10.1007/bf00225658",
    openalex = "W2324713557"
}

@incollection{cloney1978ascidian1,
    author = "Cloney, R. A",
    editor = "Chia, F. S. and Rice, M. E.",
    title = "Ascidian metamorphosis: review and analysis",
    year = "1978",
    booktitle = "Settlement and Metamorphosis of Marine Invertebrate Larvae",
    publisher = "New York, Elsevier, p. 255-282",
    note = "talkorigins\_source = {true}; raw\_reference = {Cloney, R. A., 1978, Ascidian metamorphosis: review and analysis, in Chia, F. S., and Rice, M. E., eds., Settlement and Metamorphosis of Marine Invertebrate Larvae: New York, Elsevier, p. 255-282.}"
}

@article{doi101038271061a0,
    author = "Thorndyke, Michael C.",
    title = "Evidence for a ‘mammalian’ thyroglobulin in endostyle of the ascidian Styela clava",
    year = "1978",
    journal = "Nature",
    url = "https://doi.org/10.1038/271061a0",
    doi = "10.1038/271061a0",
    openalex = "W2016378702",
    references = "doi101002jez1401880111, doi1010160016648065900626"
}

@article{openalexw2273005662,
    author = "Chia, Fu‐Shiang and Rice, Mary E.",
    title = "Settlement and metamorphosis of marine invertebrate larvae",
    year = "1978",
    openalex = "W2273005662"
}

gamma-Aminobutyric acid (a simple amino acid and potent neurotransmitter in human brain and other tissues of higher animals) and certain of its congeners rapidly and synchronously induce planktonic larvae of the red abalone, Haliotis rufescens, to settle and commence behavioral and developmental metamorphosis. These naturally occurring inducers of algal origin apparently are responsible, in part, for the substrate-specific recruitment, induction of settling, and the onset of metamorphosis of abalone and other planktonic larvae upon specific algae which provide naturally favorable habitats for the young of these species in coastal waters. These observations provide a convenient experimental model for further analysis of the basic molecular mechanisms by which environmental and endogenous factors control the recruitment and development of planktonic larvae. Halogenated organic pesticides significantly interfere with larval settling, as quantified in a new bioassay based upon these findings.

@article{doi101126science2044391407,
    author = "Morse, Daniel E. and Hooker, Neal and Duncan, Helen and Jensen, Lloyd",
    title = "γ-Aminobutyric Acid, a Neurotransmitter, Induces Planktonic Abalone Larvae to Settle and Begin Metamorphosis",
    year = "1979",
    journal = "Science",
    abstract = "gamma-Aminobutyric acid (a simple amino acid and potent neurotransmitter in human brain and other tissues of higher animals) and certain of its congeners rapidly and synchronously induce planktonic larvae of the red abalone, Haliotis rufescens, to settle and commence behavioral and developmental metamorphosis. These naturally occurring inducers of algal origin apparently are responsible, in part, for the substrate-specific recruitment, induction of settling, and the onset of metamorphosis of abalone and other planktonic larvae upon specific algae which provide naturally favorable habitats for the young of these species in coastal waters. These observations provide a convenient experimental model for further analysis of the basic molecular mechanisms by which environmental and endogenous factors control the recruitment and development of planktonic larvae. Halogenated organic pesticides significantly interfere with larval settling, as quantified in a new bioassay based upon these findings.",
    url = "https://doi.org/10.1126/science.204.4391.407",
    doi = "10.1126/science.204.4391.407",
    openalex = "W2061371525"
}

@article{doi1010160016648080900118,
    author = "DUNN, ANN D.",
    title = "Studies on iodoproteins and thyroid hormones in ascidians",
    year = "1980",
    journal = "General and Comparative Endocrinology",
    url = "https://doi.org/10.1016/0016-6480(80)90011-8",
    doi = "10.1016/0016-6480(80)90011-8",
    openalex = "W2074333642",
    references = "doi101002jez1401880111"
}

@article{doi1010160022098180901732,
    author = "Young, Craig M. and Braithwaite, Lee F.",
    title = "Larval behavior and post-settling morphology in the ascidian, Chelyosoma productum Stimpson",
    year = "1980",
    journal = "Journal of Experimental Marine Biology and Ecology",
    url = "https://doi.org/10.1016/0022-0981(80)90173-2",
    doi = "10.1016/0022-0981(80)90173-2",
    openalex = "W1984538738"
}

@article{doi101007bf00249213,
    author = "Patricolo, Eleonora and Ortolani, G and Cascio, Antonio",
    title = "The effect of L-thyroxine on the metamorphosis of Ascidia malaca",
    year = "1981",
    journal = "Cell and Tissue Research",
    url = "https://doi.org/10.1007/bf00249213",
    doi = "10.1007/bf00249213",
    openalex = "W2053521525"
}

Abstract The structure of the body‐wall muscle of the ascidian, Halocynthia roretzi, was investigated by electron and light microscopy. Thin (about 8 nm in diameter), (18–20 nm in diameter), and 10‐nm filaments were seen in this muscle cell. These filaments, however, did not have the regular arrangement of a striated or oblique structure. We also found by three‐dimensional reconstruction that this muscle cell is multinucleated. Based on these observations, we report that the body‐wall muscle of the ascidian, Halocynthia roretzi, is smooth and multinucleated.

@article{doi101002jez1402210203,
    author = "Shinohara, Yoshiko and Konishi, Kazuhiko",
    title = "Ultrastructure of the body‐wall muscle of the ascidian Halocynthia roretzi: Smooth muscle cell with multiple nuclei",
    year = "1982",
    journal = "Journal of Experimental Zoology",
    abstract = "Abstract The structure of the body‐wall muscle of the ascidian, Halocynthia roretzi, was investigated by electron and light microscopy. Thin (about 8 nm in diameter), (18–20 nm in diameter), and 10‐nm filaments were seen in this muscle cell. These filaments, however, did not have the regular arrangement of a striated or oblique structure. We also found by three‐dimensional reconstruction that this muscle cell is multinucleated. Based on these observations, we report that the body‐wall muscle of the ascidian, Halocynthia roretzi, is smooth and multinucleated.",
    url = "https://doi.org/10.1002/jez.1402210203",
    doi = "10.1002/jez.1402210203",
    openalex = "W1984328257"
}

@article{doi101007bf00213854,
    author = "Cloney, Richard A. and Cavey, Michael J.",
    title = "Ascidian larval tunic: Extraembryonic structures influence morphogenesis",
    year = "1982",
    journal = "Cell and Tissue Research",
    url = "https://doi.org/10.1007/bf00213854",
    doi = "10.1007/bf00213854",
    openalex = "W2056799713"
}

SYNOPSIS. Ascidian larvae settle and metamorphose after only a brief free—swimming period; they are all lecilhotrophic. Extrinsic factors (chemical and physical) may trigger metamorphosis but none are known to be essential. The major larval structures may be classified as transitory larval organs (TLO), prospective juvenile organs (PJO) or larvaljuvenile organs (LJO). TLO are phagocytized or otherwise destroyed at metamorphosis; the PJO and LJO become the functional parts of the juvenile or oozooid. Metamorphosis involves some rapid and some slow morphogenetic movements. Variations in larval morphology are reflected in metamorphosis. Some of the events of metamorphosis are fairly well known in terms of the role of specific cells but we know little about how the various events are initiated and coordinated. The nervous system is more complex than had been previously assumed. The nervous system, neuroid conduction and diffusion of one or more humoral factors are probably all involved in controlling metamorphosis.

@article{doi101093icb224817,
    author = "Cloney, Richard A.",
    title = "Ascidian Larvae and the Events of Metamorphosis",
    year = "1982",
    journal = "American Zoologist",
    abstract = "SYNOPSIS. Ascidian larvae settle and metamorphose after only a brief free—swimming period; they are all lecilhotrophic. Extrinsic factors (chemical and physical) may trigger metamorphosis but none are known to be essential. The major larval structures may be classified as transitory larval organs (TLO), prospective juvenile organs (PJO) or larvaljuvenile organs (LJO). TLO are phagocytized or otherwise destroyed at metamorphosis; the PJO and LJO become the functional parts of the juvenile or oozooid. Metamorphosis involves some rapid and some slow morphogenetic movements. Variations in larval morphology are reflected in metamorphosis. Some of the events of metamorphosis are fairly well known in terms of the role of specific cells but we know little about how the various events are initiated and coordinated. The nervous system is more complex than had been previously assumed. The nervous system, neuroid conduction and diffusion of one or more humoral factors are probably all involved in controlling metamorphosis.",
    url = "https://doi.org/10.1093/icb/22.4.817",
    doi = "10.1093/icb/22.4.817",
    openalex = "W1967582304",
    references = "doi101007bf00213854, doi101007bf00220677, doi101007bf00225658, doi101007bf00229160, doi101007bf00249213, doi101007bf00307009, doi101007bf00335222, doi101007bf02584045, doi1010160022098180901732, doi101016s0022532066800515, doi101242jcss39739435"
}

@article{doi1010160012160687901886,
    author = "Nishida, Hiroki",
    title = "Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme",
    year = "1987",
    journal = "Developmental Biology",
    url = "https://doi.org/10.1016/0012-1606(87)90188-6",
    doi = "10.1016/0012-1606(87)90188-6",
    openalex = "W1596141725",
    references = "doi101242jcss310363393, openalexw574596740"
}

@article{openalexw2489624142,
    author = "Svane, Ib and Young, Craig M.",
    title = "The ecology and behavior of ascidian larvae",
    year = "1989",
    journal = "Oceanography and Marine Biology/Oceanography and marine biology - an annual review",
    openalex = "W2489624142"
}

Abstract In the laboratory, the swimming larvae of benthic marine invertebrates are generally capable of prolonging their larval period beyond the time that they first become physiologically competent to metamorphose. Larvae seem to differ markedly in their ability to postpone metamorphosis, both interspecifically and intraspecifically. The proportion of this variability that is genetically controlled has not yet been determined; if under genetic control, both pre-competent and competent periods would be subject to selection, although the selective pressures and the physiological or developmental mechanisms through which such pressures might operate remain purely speculative. Limited data strongly suggest that at least a few species delay metamorphosis in the field. The frequency with which they do so, and under what conditions they do so, and for how long, are unexplored questions. Some of these issues can now be explored, with the finding that various inorganic and organic substances can trigger the metamorphosis of competent larvae in a number of species; competence, and the extent to which larvae delay their metamorphosis, may now be assessed directly for field populations and in laboratory cultures, rather than by means of unreliable morphological or behavioral criteria. Careful laboratory studies may enable greater prediction of minimum and maximum dispersal periods in the field by revealing the extent to which environmental factors, such as temperature and salinity, influence pre-competent and competent periods in different species. The extent to which postponing metamorphosis alters post-metamorphic fitness is also now subject to investigation through laboratory studies and possible field transplants.

@article{doi10108000785236199010422025,
    author = "Pechenik, Jan A.",
    title = "Delayed metamorphosis by larvae of benthic marine invertebrates: Does it occur? Is there a price to pay?",
    year = "1990",
    journal = "Ophelia",
    abstract = "Abstract In the laboratory, the swimming larvae of benthic marine invertebrates are generally capable of prolonging their larval period beyond the time that they first become physiologically competent to metamorphose. Larvae seem to differ markedly in their ability to postpone metamorphosis, both interspecifically and intraspecifically. The proportion of this variability that is genetically controlled has not yet been determined; if under genetic control, both pre-competent and competent periods would be subject to selection, although the selective pressures and the physiological or developmental mechanisms through which such pressures might operate remain purely speculative. Limited data strongly suggest that at least a few species delay metamorphosis in the field. The frequency with which they do so, and under what conditions they do so, and for how long, are unexplored questions. Some of these issues can now be explored, with the finding that various inorganic and organic substances can trigger the metamorphosis of competent larvae in a number of species; competence, and the extent to which larvae delay their metamorphosis, may now be assessed directly for field populations and in laboratory cultures, rather than by means of unreliable morphological or behavioral criteria. Careful laboratory studies may enable greater prediction of minimum and maximum dispersal periods in the field by revealing the extent to which environmental factors, such as temperature and salinity, influence pre-competent and competent periods in different species. The extent to which postponing metamorphosis alters post-metamorphic fitness is also now subject to investigation through laboratory studies and possible field transplants.",
    url = "https://doi.org/10.1080/00785236.1990.10422025",
    doi = "10.1080/00785236.1990.10422025",
    openalex = "W2081148041",
    references = "doi101007bf00380003, doi1010160022098185900590, doi1010160302352475900389, doi101016b9780122825057x50015, doi10108000785326196510409596, doi101098rspb19790086, doi101111j1469185x1950tb00585x, doi101111j1469185x1983tb00380x, doi101126science11538249, doi101146annureves16110185002011, doi1023071540075, doi1023071540409, hartnoll1975chemoreception, knightjones1953laboratory, openalexw2273005662"
}

@article{openalexw48629314,
    author = "Satoh, Noriyuki and Jeffrey, William R.",
    title = "Developmental Biology of Ascidians",
    year = "1995",
    openalex = "W48629314"
}

The Msx homeobox genes are expressed in complex patterns during vertebrate development in conjunction with inductive tissue interactions. As a means of understanding the archetypal role of Msx genes in chordates, we have isolated and characterized an Msx gene in ascidians, protochordates with a relatively simple body plan. The Mocu Msx-a and McMsx-a genes, isolated from the ascidians Molgula oculata and Molgula citrina, respectively, have homeodomains that place them in the msh-like subclass of Msx genes. Therefore, the Molgula Msx-a genes are most closely related to the msh genes previously identified in a number of invertebrates. Southern blot analysis suggests that there are one or two copies of the Msx-a gene in the Molgula genome. Northern blot and RNase protection analysis indicate that Msx-a transcripts are restricted to the developmental stages of the life cycle. In situ hybridization showed that Msx-a mRNA first appears just before gastrulation in the mesoderm (presumptive notochord and muscle) and ectoderm (neural plate) cells. Transcript levels decline in mesoderm cells after the completion of gastrulation, but are enhanced in the folding neural plate during neurulation. Later, Msx-a mRNA is also expressed in the posterior ectoderm and in a subset of the tail muscle cells. The ectoderm and mesoderm cells that express Msx-a are undergoing morphogenetic movements during gastrulation, neurulation, and tail formation. Msx-a expression ceases after these cells stop migrating. The ascidian M. citrina, in which adult tissues and organs begin to develop precociously in the larva, was used to study Msx-a expression during adult development. Msx-a transcripts are expressed in the heart primordium and the rudiments of the ampullae, epidermal protrusions with diverse functions in the juvenile. The heart and ampullae develop in regions where mesenchyme cells interact with endodermal or epidermal epithelia. A comparison of the expression patterns of the Molgula genes with those of their vertebrate congeners suggests that the archetypal roles of the Msx genes may be in morphogenetic movements during embryogenesis and in mesenchymal-epithelial interactions during organogenesis.

@article{doi101002sici109701771996032053308aidaja1030co20,
    author = "Ma, Liang and Swalla, Billie J. and Zhou, Jing and Dobias, Sonia L. and Bell, Jeffrey R. and Chen, Juan and Maxson, Robert E. and Jeffery, William R.",
    title = "Expression of anMsx homeobox gene in ascidians: Insights into the archetypal chordate expression pattern",
    year = "1996",
    journal = "Developmental Dynamics",
    abstract = "The Msx homeobox genes are expressed in complex patterns during vertebrate development in conjunction with inductive tissue interactions. As a means of understanding the archetypal role of Msx genes in chordates, we have isolated and characterized an Msx gene in ascidians, protochordates with a relatively simple body plan. The Mocu Msx-a and McMsx-a genes, isolated from the ascidians Molgula oculata and Molgula citrina, respectively, have homeodomains that place them in the msh-like subclass of Msx genes. Therefore, the Molgula Msx-a genes are most closely related to the msh genes previously identified in a number of invertebrates. Southern blot analysis suggests that there are one or two copies of the Msx-a gene in the Molgula genome. Northern blot and RNase protection analysis indicate that Msx-a transcripts are restricted to the developmental stages of the life cycle. In situ hybridization showed that Msx-a mRNA first appears just before gastrulation in the mesoderm (presumptive notochord and muscle) and ectoderm (neural plate) cells. Transcript levels decline in mesoderm cells after the completion of gastrulation, but are enhanced in the folding neural plate during neurulation. Later, Msx-a mRNA is also expressed in the posterior ectoderm and in a subset of the tail muscle cells. The ectoderm and mesoderm cells that express Msx-a are undergoing morphogenetic movements during gastrulation, neurulation, and tail formation. Msx-a expression ceases after these cells stop migrating. The ascidian M. citrina, in which adult tissues and organs begin to develop precociously in the larva, was used to study Msx-a expression during adult development. Msx-a transcripts are expressed in the heart primordium and the rudiments of the ampullae, epidermal protrusions with diverse functions in the juvenile. The heart and ampullae develop in regions where mesenchyme cells interact with endodermal or epidermal epithelia. A comparison of the expression patterns of the Molgula genes with those of their vertebrate congeners suggests that the archetypal roles of the Msx genes may be in morphogenetic movements during embryogenesis and in mesenchymal-epithelial interactions during organogenesis.",
    url = "https://doi.org/10.1002/(sici)1097-0177(199603)205:3<308::aid-aja10>3.0.co;2-0",
    doi = "10.1002/(sici)1097-0177(199603)205:3<308::aid-aja10>3.0.co;2-0",
    openalex = "W2020401689",
    references = "doi101093icb224817, doi101098rstb19350013"
}

@article{doi1010160168952596100329,
    author = "Thummel, Carl S.",
    title = "Flies on steroids — Drosophila metamorphosis and the mechanisms of steroid hormone action",
    year = "1996",
    journal = "Trends in Genetics",
    url = "https://doi.org/10.1016/0168-9525(96)10032-9",
    doi = "10.1016/0168-9525(96)10032-9",
    openalex = "W1976851982"
}

@article{doi101006dbio19978772,
    author = "Hirano, Toshio and Nishida, Hiroki",
    title = "Developmental Fates of Larval Tissues after Metamorphosis in AscidianHalocynthia roretzi",
    year = "1997",
    journal = "Developmental Biology",
    url = "https://doi.org/10.1006/dbio.1997.8772",
    doi = "10.1006/dbio.1997.8772",
    openalex = "W1970028013",
    references = "doi101007bf02956047"
}

M any marine invertebrate species have complex life cycles, in which one or more free-living developmental stages eventually metamorphoses to a morphologically-and often ecologically and physiologically-distinct juvenile stage. Such life cycles are also common among insects, amphibians, and marine fishes. Among marine invertebrates, complex life cycles are widely distributed among such diverse animals as sponges; turbellarian and trematode flatworms; gastropod and bivalved mollusks; polychaete worms; lobsters, crabs, barnacles, and other crustaceans; bryozoans; and echinoderms (Thorson 1950). Marine invertebrate larvae may feed on phytoplankton and other particulates or subsist entirely on yolk or other nutrients provided by the mother. They may spend as little as a few minutes or as long as several to many months in the plankton before metamorphosing to adult form and habitat (Pechenik 1990). Marine invertebrate larvae are

@article{doi1023071313294,
    author = "Pechenik, Jan A. and Wendt, Dean E. and Jarrett, Jeremiah N.",
    title = "Metamorphosis Is Not a New Beginning",
    year = "1998",
    journal = "BioScience",
    abstract = "M any marine invertebrate species have complex life cycles, in which one or more free-living developmental stages eventually metamorphoses to a morphologically-and often ecologically and physiologically-distinct juvenile stage. Such life cycles are also common among insects, amphibians, and marine fishes. Among marine invertebrates, complex life cycles are widely distributed among such diverse animals as sponges; turbellarian and trematode flatworms; gastropod and bivalved mollusks; polychaete worms; lobsters, crabs, barnacles, and other crustaceans; bryozoans; and echinoderms (Thorson 1950). Marine invertebrate larvae may feed on phytoplankton and other particulates or subsist entirely on yolk or other nutrients provided by the mother. They may spend as little as a few minutes or as long as several to many months in the plankton before metamorphosing to adult form and habitat (Pechenik 1990). Marine invertebrate larvae are",
    url = "https://doi.org/10.2307/1313294",
    doi = "10.2307/1313294",
    openalex = "W2087770966",
    references = "doi10108000785236199010422025, knightjones1953laboratory"
}

The endostyle is a pharyngeal organ for the internal filter feeding of urochordates, cephalochordates, and larval lamprey. This organ is also considered to be homologous to the follicular thyroid gland of higher vertebrates. Thyroglobulin (Tg) and thyroid peroxidase (TPO) are specifically expressed in the thyroid gland of higher vertebrates, and they play an important role in iodine metabolism for the synthesis of thyroid hormones. Previous histochemical observations showed that iodine-concentrating and peroxidase activities were detected in zones 7, 8, and 9 of the ascidian endostyle, suggesting that these zones contains cells that are equivalent to those in the vertebrate follicular thyroid. In order to investigate the molecular developmental mechanisms involved in the formation and function of the endostyle, with special reference to the evolution of the thyroid gland, in the present study, we isolated and characterized cDNA clones for TPO genes, CiTPO from Ciona intestinalis and HrTPO from Halocynthia roretzi. Northern blot and in situ hybridization analyses revealed that the expression of the ascidian TPO genes was restricted to zone 7, one of the elements equivalent to the thyroid. These results provide the first evidence at the gene expression level for shared function between a part of the ascidian endostyle and the vertebrate follicular thyroid gland. J. Exp. Zool. (Mol. Dev. Evol.) 285:158-169, 1999.

@article{doi101002sici1097010x199908152852158aidjez830co20,
    author = "Ogasawara, Michio and Lauro, Roberto Di and Satoh, Nori",
    title = "Ascidian homologs of mammalian thyroid peroxidase genes are expressed in the thyroid-equivalent region of the endostyle",
    year = "1999",
    journal = "Journal of Experimental Zoology",
    abstract = "The endostyle is a pharyngeal organ for the internal filter feeding of urochordates, cephalochordates, and larval lamprey. This organ is also considered to be homologous to the follicular thyroid gland of higher vertebrates. Thyroglobulin (Tg) and thyroid peroxidase (TPO) are specifically expressed in the thyroid gland of higher vertebrates, and they play an important role in iodine metabolism for the synthesis of thyroid hormones. Previous histochemical observations showed that iodine-concentrating and peroxidase activities were detected in zones 7, 8, and 9 of the ascidian endostyle, suggesting that these zones contains cells that are equivalent to those in the vertebrate follicular thyroid. In order to investigate the molecular developmental mechanisms involved in the formation and function of the endostyle, with special reference to the evolution of the thyroid gland, in the present study, we isolated and characterized cDNA clones for TPO genes, CiTPO from Ciona intestinalis and HrTPO from Halocynthia roretzi. Northern blot and in situ hybridization analyses revealed that the expression of the ascidian TPO genes was restricted to zone 7, one of the elements equivalent to the thyroid. These results provide the first evidence at the gene expression level for shared function between a part of the ascidian endostyle and the vertebrate follicular thyroid gland. J. Exp. Zool. (Mol. Dev. Evol.) 285:158-169, 1999.",
    url = "https://doi.org/10.1002/(sici)1097-010x(19990815)285:2<158::aid-jez8>3.0.co;2-0",
    doi = "10.1002/(sici)1097-010x(19990815)285:2<158::aid-jez8>3.0.co;2-0",
    openalex = "W1976501744",
    references = "doi101002j146020751989tb08391x, doi101002j146020751994tb06649x, doi101002jez1401880111, doi101006abio19879999, doi101007s004270050250, doi1010160003269787900212, doi101016001664806990063x, doi101017s0025315400017021, doi101021bi00436a054, doi101038182774a0, doi101093emboj16113185, doi101128mcb1294230, doi1031810037972721444098"
}

All chordates share several characteristic features including a dorsal hollow neural tube, a notochord, a pharynx and an endostyle. Unlike other chordate taxa, ascidians have a biphasic life-history with two distinct body plans. During metamorphosis, the larval nerve cord and notochord degenerate and the pharyngeal gill slits and endostyle form. While ascidians, like other marine invertebrates, metamorphose in response to specific environmental cues, it remains unclear how these cues trigger metamorphosis. We have identified a novel gene (Hemps) which encodes a protein with a putative secretion signal sequence and four epidermal growth factor (EGF)-like repeats which is a key regulator of metamorphosis in the ascidian Herdmania curvata. Expression of Hemps increases markedly when the swimming tadpole larva becomes competent to undergo metamorphosis and then during the first 24 hours of metamorphosis. The Hemps protein is localised to the larval papillae and anterior epidermis of the larva in the region known to be required for metamorphosis. When the larva contacts an inductive cue the protein is released, spreading posteriorly and into the tunic as metamorphosis progresses. Metamorphosis is blocked by incubating larvae in anti-Hemps antibodies prior to the addition of the cue. Addition of recombinant Hemps protein to competent larvae induces metamorphosis in a concentration-dependent manner. A subgroup of genes are specifically induced during this process. These results demonstrate that the Hemps protein is a key regulator of ascidian metamorphosis and is distinct from previously described inducers of this process in terrestrial arthropods and aquatic vertebrates.

@article{doi101242dev126245809,
    author = "Eri, Rajaraman and Arnold, Jeremy M. and Hinman, Veronica F. and Green, Kathryn M. and Jones, Malcolm K. and Degnan, Bernard M. and Lavin, Martin F.",
    title = "Hemps, a novel EGF-like protein, plays a central role in ascidian metamorphosis",
    year = "1999",
    journal = "Development",
    abstract = "All chordates share several characteristic features including a dorsal hollow neural tube, a notochord, a pharynx and an endostyle. Unlike other chordate taxa, ascidians have a biphasic life-history with two distinct body plans. During metamorphosis, the larval nerve cord and notochord degenerate and the pharyngeal gill slits and endostyle form. While ascidians, like other marine invertebrates, metamorphose in response to specific environmental cues, it remains unclear how these cues trigger metamorphosis. We have identified a novel gene (Hemps) which encodes a protein with a putative secretion signal sequence and four epidermal growth factor (EGF)-like repeats which is a key regulator of metamorphosis in the ascidian Herdmania curvata. Expression of Hemps increases markedly when the swimming tadpole larva becomes competent to undergo metamorphosis and then during the first 24 hours of metamorphosis. The Hemps protein is localised to the larval papillae and anterior epidermis of the larva in the region known to be required for metamorphosis. When the larva contacts an inductive cue the protein is released, spreading posteriorly and into the tunic as metamorphosis progresses. Metamorphosis is blocked by incubating larvae in anti-Hemps antibodies prior to the addition of the cue. Addition of recombinant Hemps protein to competent larvae induces metamorphosis in a concentration-dependent manner. A subgroup of genes are specifically induced during this process. These results demonstrate that the Hemps protein is a key regulator of ascidian metamorphosis and is distinct from previously described inducers of this process in terrestrial arthropods and aquatic vertebrates.",
    url = "https://doi.org/10.1242/dev.126.24.5809",
    doi = "10.1242/dev.126.24.5809",
    openalex = "W2104818624",
    references = "doi101006abio19931170, doi1010160168952596100329, doi1010160378111988900054, doi1010160753332289901303, doi1010160968000489903071, doi101126science1354393, doi105860choice353280, openalexw2144634347, openalexw37545008, openalexw48629314"
}

@article{doi101007s004270050011,
    author = "Hirano, Takahiro and Nishida, Hiroki",
    title = "Developmental fates of larval tissues after metamorphosis in the ascidian, Halocynthia roretzi",
    year = "2000",
    journal = "Development Genes and Evolution",
    url = "https://doi.org/10.1007/s004270050011",
    doi = "10.1007/s004270050011",
    openalex = "W2411940210",
    references = "doi101002jez1402210203, doi101006dbio19978772, doi1010160012160683902014, doi1010160012160687901886, doi101016s0040816670800106, doi101016s0065288108603417, doi101016s0065288108604575, doi101098rspb19760090, doi101242dev1034625, doi105962bhltitle4801"
}

Treatment of larvae of the ascidians Boltenia villosa (Family: Pyuridae) and Cnemidocarpa finmarkiensis (Family: Styelidae) with drugs that inhibit the function of the molecular chaperone HSP90 increased the frequency of tail resorption, the primary morphogenetic event of metamorphosis. If treatment was initiated at hatching, metamorphic events subsequent to tail resorption failed to occur, indicating an ongoing role for HSP90 during morphogenesis. Removal of tails from heads of mature, but not newly hatched larvae, induced metamorphosis of the head. Decapitation experiments indicate that the capacity of tails to shorten in response to inhibition of HSP90 function requires communication with heads. To identify candidate proteins with which HSP90 may interact to regulate metamorphosis, we noted that in mammalian cells, nitric oxide synthase (NOS) interacts with HSP90 and its activity is sensitive to drugs that inhibit HSP90 function. In addition, nitric oxide (NO) signaling in the marine snail Ilyanassa obsoleta is an important regulator of metamorphosis. Inhibition of NOS activity in these ascidian larvae with L-NAME increased the frequency of metamorphosis, consistent with a putative interaction of NOS and HSP90. NOS is present in tail muscle cells, implicating them as targets for the drug treatments, consistent with the decapitation experiments. Inhibition of soluble guanylyl cyclase, the most common effector of NO signaling, also increased the frequency of metamorphosis. In contrast to treatment with anti-HSP90 drugs, metamorphosis induced with L-NAME or ODQ was complete. The results presented suggest that an HSP90-dependent, NO-based regulatory mechanism localized in tails represses ascidian metamorphosis. We discuss these results in relation to the induction of ascidian metamorphosis by several unrelated agents.

@article{doi101002jez1019,
    author = "Bishop, Cory D. and Bates, William and Brandhorst, Bruce P.",
    title = "Regulation of metamorphosis in ascidians involves NO\/cGMP signaling and HSP90",
    year = "2001",
    journal = "Journal of Experimental Zoology",
    abstract = "Treatment of larvae of the ascidians Boltenia villosa (Family: Pyuridae) and Cnemidocarpa finmarkiensis (Family: Styelidae) with drugs that inhibit the function of the molecular chaperone HSP90 increased the frequency of tail resorption, the primary morphogenetic event of metamorphosis. If treatment was initiated at hatching, metamorphic events subsequent to tail resorption failed to occur, indicating an ongoing role for HSP90 during morphogenesis. Removal of tails from heads of mature, but not newly hatched larvae, induced metamorphosis of the head. Decapitation experiments indicate that the capacity of tails to shorten in response to inhibition of HSP90 function requires communication with heads. To identify candidate proteins with which HSP90 may interact to regulate metamorphosis, we noted that in mammalian cells, nitric oxide synthase (NOS) interacts with HSP90 and its activity is sensitive to drugs that inhibit HSP90 function. In addition, nitric oxide (NO) signaling in the marine snail Ilyanassa obsoleta is an important regulator of metamorphosis. Inhibition of NOS activity in these ascidian larvae with L-NAME increased the frequency of metamorphosis, consistent with a putative interaction of NOS and HSP90. NOS is present in tail muscle cells, implicating them as targets for the drug treatments, consistent with the decapitation experiments. Inhibition of soluble guanylyl cyclase, the most common effector of NO signaling, also increased the frequency of metamorphosis. In contrast to treatment with anti-HSP90 drugs, metamorphosis induced with L-NAME or ODQ was complete. The results presented suggest that an HSP90-dependent, NO-based regulatory mechanism localized in tails represses ascidian metamorphosis. We discuss these results in relation to the induction of ascidian metamorphosis by several unrelated agents.",
    url = "https://doi.org/10.1002/jez.1019",
    doi = "10.1002/jez.1019",
    openalex = "W1976270214",
    references = "doi101007bf00689048, doi101016s0026895x25102332, doi101016s0092867400802032, doi101016s0092867400803141, doi10103824550, doi10103833934, doi101038372546a0, doi101073pnas91188324, doi101093emboj17164829, doi1031810037972721744252"
}

Abstract In this study we investigated the presence and localization of thyroxine in Ciona intestinalis larvae and its involvement in metamorphosis. To date, the mechanisms regulating the metamorphosis of ascidians remain largely unknown. In vivo treatment of swimming larvae with exogenous L‐thyroxine and thiourea, and in vitro experiments utilizing high performance liquid chromatography, radioimmunoassay, and immunoperoxidase staining demonstrate the presence of thyroxine at the larval stage. This suggests that this hormone may participate in the control of metamorphosis and thus play a different role from that observed in adults. J. Exp. Zool. 290:426–430, 2001. © 2001 Wiley‐Liss, Inc.

@article{doi101002jez1084,
    author = "Patricolo, Eleonora and Cammarata, Matteo and D’Agati, Paolo",
    title = "Presence of thyroid hormones in ascidian larvae and their involvement in metamorphosis",
    year = "2001",
    journal = "Journal of Experimental Zoology",
    abstract = "Abstract In this study we investigated the presence and localization of thyroxine in Ciona intestinalis larvae and its involvement in metamorphosis. To date, the mechanisms regulating the metamorphosis of ascidians remain largely unknown. In vivo treatment of swimming larvae with exogenous L‐thyroxine and thiourea, and in vitro experiments utilizing high performance liquid chromatography, radioimmunoassay, and immunoperoxidase staining demonstrate the presence of thyroxine at the larval stage. This suggests that this hormone may participate in the control of metamorphosis and thus play a different role from that observed in adults. J. Exp. Zool. 290:426–430, 2001. © 2001 Wiley‐Liss, Inc.",
    url = "https://doi.org/10.1002/jez.1084",
    doi = "10.1002/jez.1084",
    openalex = "W2052710716",
    references = "doi101002jez1401880111, doi101002sici1097010x199908152852158aidjez830co20, doi101006abio19769999, doi101007bf00249213, doi1010160003269776905273, doi1010160016648080900118, doi101038271061a0, doi101098rspb19650063, doi1031810037972721444098, openalexw654005152"
}

External chemical signals provide a mechanism for broadcast-spawning scleractinian corals to recognise suitable substrata for larval settlement and metamorphosis. These morphogens can be extracted from crustose coralline algae (CCA) and the skeletons of some coral species, however the precise origin of the chemical inducers has not yet been conclusively demonstrated. Microorganisms have been reported to induce metamorphosis in various species of echinoderms, molluscs, polychaetes and cnidarians. We report that Strain A3, a species of Pseudoalteromonas isolated from the CCA Hydrolithon onkodes (Heydrich), was able to induce significant levels (up to 51.5% 5.8 SE) of metamorphosis of Acropora willisae Veron & Wallace, 1984 and A. millepora (Ehrenberg, 1834) larvae in laboratory assays. This experiment was repeated daily over 4 d, and the spat developed normally into juvenile polyps in flow-through aquaria. Approximately the same number of larvae underwent partial metamorphosis, forming flattened discs that were not attached to the substrata. Larvae underwent full settlement, attachment and metamorphosis only in the presence of Pseudoalteromonas A3 plus inert chips of the coral skeleton Porites sp., indicating that the calcareous matrix may play a role in the synthesis of inducers from Pseudoalteromonas Strain A3. This discovery provides evidence for a widening range of morphogenic sources and demonstrates the role that microorganisms may play in fine-scale coral recruitment. In addition, the synthesis of chemical inducers by Pseudoalteromonas Strain A3 may have biotechnological applications for reef re-seeding.

@article{doi103354meps223121,
    author = "Negri, AP and Webster, Nicole S. and Hill, Russell T. and Heyward, AJ",
    title = "Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae",
    year = "2001",
    journal = "Marine Ecology Progress Series",
    abstract = "External chemical signals provide a mechanism for broadcast-spawning scleractinian corals to recognise suitable substrata for larval settlement and metamorphosis. These morphogens can be extracted from crustose coralline algae (CCA) and the skeletons of some coral species, however the precise origin of the chemical inducers has not yet been conclusively demonstrated. Microorganisms have been reported to induce metamorphosis in various species of echinoderms, molluscs, polychaetes and cnidarians. We report that Strain A3, a species of Pseudoalteromonas isolated from the CCA Hydrolithon onkodes (Heydrich), was able to induce significant levels (up to 51.5\% 5.8 SE) of metamorphosis of Acropora willisae Veron \& Wallace, 1984 and A. millepora (Ehrenberg, 1834) larvae in laboratory assays. This experiment was repeated daily over 4 d, and the spat developed normally into juvenile polyps in flow-through aquaria. Approximately the same number of larvae underwent partial metamorphosis, forming flattened discs that were not attached to the substrata. Larvae underwent full settlement, attachment and metamorphosis only in the presence of Pseudoalteromonas A3 plus inert chips of the coral skeleton Porites sp., indicating that the calcareous matrix may play a role in the synthesis of inducers from Pseudoalteromonas Strain A3. This discovery provides evidence for a widening range of morphogenic sources and demonstrates the role that microorganisms may play in fine-scale coral recruitment. In addition, the synthesis of chemical inducers by Pseudoalteromonas Strain A3 may have biotechnological applications for reef re-seeding.",
    url = "https://doi.org/10.3354/meps223121",
    doi = "10.3354/meps223121",
    openalex = "W2044350324"
}

Ascidian metamorphosis represents a powerful model for comparative work on chordate development that has remained largely unexplored. We isolated transcripts differentially expressed during metamorphosis in the ascidian Boltenia villosa by suppressive PCR subtractions of staged larval and juvenile cDNAs. We employed a series of three subtractions to dissect gene expression during metamorphosis. We have isolated 132 different protein coding sequences, and 65 of these transcripts show significant matches to GenBank proteins. Some of these genes have putative functions relevant to key metamorphic events including the differentiation of smooth muscle, blood cells, heart tissue and adult nervous system from larval rudiments. In addition, a significant fraction of the differentially expressed transcripts match identified genes from the innate immune system. Innate immunity confers a rapid response to pathogen-specific molecules and/or compromised self-tissues. The activation of innate immunity genes during metamorphosis may represent the programmed maturation of the adult immune system. In addition, this immune response may be necessary for phagocytosis and re-structuring of larval tissues. An innate immune-related inflammatory response may also underlie two waves of trans-epidermal blood cell migration that occur during the swimming larval period and immediately upon settlement. We characterized these trans-epidermal migrations and discovered that some migratory cells leave the animal entirely through an anterior tunnel in the tunic. We show that these cells are positioned to detect external settlement cues and hypothesize that the innate immune system may also be employed to detect and rapidly respond to environmental settlement cues.

@article{doi101242dev129204739,
    author = "Davidson, Brad and Swalla, Billie J.",
    title = "A molecular analysis of ascidian metamorphosis reveals activation of an innate immune response",
    year = "2002",
    journal = "Development",
    abstract = "Ascidian metamorphosis represents a powerful model for comparative work on chordate development that has remained largely unexplored. We isolated transcripts differentially expressed during metamorphosis in the ascidian Boltenia villosa by suppressive PCR subtractions of staged larval and juvenile cDNAs. We employed a series of three subtractions to dissect gene expression during metamorphosis. We have isolated 132 different protein coding sequences, and 65 of these transcripts show significant matches to GenBank proteins. Some of these genes have putative functions relevant to key metamorphic events including the differentiation of smooth muscle, blood cells, heart tissue and adult nervous system from larval rudiments. In addition, a significant fraction of the differentially expressed transcripts match identified genes from the innate immune system. Innate immunity confers a rapid response to pathogen-specific molecules and/or compromised self-tissues. The activation of innate immunity genes during metamorphosis may represent the programmed maturation of the adult immune system. In addition, this immune response may be necessary for phagocytosis and re-structuring of larval tissues. An innate immune-related inflammatory response may also underlie two waves of trans-epidermal blood cell migration that occur during the swimming larval period and immediately upon settlement. We characterized these trans-epidermal migrations and discovered that some migratory cells leave the animal entirely through an anterior tunnel in the tunic. We show that these cells are positioned to detect external settlement cues and hypothesize that the innate immune system may also be employed to detect and rapidly respond to environmental settlement cues.",
    url = "https://doi.org/10.1242/dev.129.20.4739",
    doi = "10.1242/dev.129.20.4739",
    openalex = "W2103316815",
    references = "doi101002sici109701772000062182235aiddvdy230co2g, doi101016s0952791500001916, doi10103835021228, doi101093nar25173389, doi101126science1071059, doi101152physrev1999791181, doi101172jci12609, doi105962bhltitle4801, openalexw48629314, openalexw654005152"
}

It is becoming widely recognized that extending the larval period of marine invertebrates, especially of species with non-feeding larvae, can affect post-larval performance. As these carry-over effects are presumed to be caused by the depletion of larval energy reserves, we predicted that the level of larval activity would also affect post-larval performance. This prediction was tested with the cosmopolitan colonial ascidian Diplosoma listerianum in field experiments in southern Australia. Diplosoma larvae, brooded in the parent colony, are competent to settle immediately after spawning, and they remain competent to metamorphose for >15 h. Some larvae were induced to metamorphose 0 to 6 h after release, whilst others were induced to swim actively by alternating light and dark periods for up to 3 h prior to metamorphosis. Juvenile colonies were then transplanted to a subtidal field site in Port Phillip Bay and left to grow for up to 3 wk. Extending the larval period and increasing the amount of swimming both produced carry-over effects on post-larval performance. Colonies survived at different rates among experiments, but larval experience did not affect survival rates. Delays in metamorphosis and increased swimming activity did, however, reduce colony growth rates dramatically, resulting in 50% fewer zooids per colony. Moreover, such colonies produced initial zooids with smaller feeding structures, with the width of branchial baskets reduced by 10 to 15%. These differences in branchial basket size persisted and were still apparent in newly budded zooids 3 wk after metamorphosis. Our results suggest that, for D. listerianum, larval maintenance, swimming, and metamorphosis all use energy from a common pool, and increases in the allocation to maintenance or swimming come at the expense of post-larval performance.

@article{doi103354meps246153,
    author = "Marshall, Dustin J. and Pechenik, JA and Keough, Michael J.",
    title = "Larval activity levels and delayed metamorphosis affect post-larval performance in the colonial ascidian Diplosoma listerianum",
    year = "2003",
    journal = "Marine Ecology Progress Series",
    abstract = "It is becoming widely recognized that extending the larval period of marine invertebrates, especially of species with non-feeding larvae, can affect post-larval performance. As these carry-over effects are presumed to be caused by the depletion of larval energy reserves, we predicted that the level of larval activity would also affect post-larval performance. This prediction was tested with the cosmopolitan colonial ascidian Diplosoma listerianum in field experiments in southern Australia. Diplosoma larvae, brooded in the parent colony, are competent to settle immediately after spawning, and they remain competent to metamorphose for >15 h. Some larvae were induced to metamorphose 0 to 6 h after release, whilst others were induced to swim actively by alternating light and dark periods for up to 3 h prior to metamorphosis. Juvenile colonies were then transplanted to a subtidal field site in Port Phillip Bay and left to grow for up to 3 wk. Extending the larval period and increasing the amount of swimming both produced carry-over effects on post-larval performance. Colonies survived at different rates among experiments, but larval experience did not affect survival rates. Delays in metamorphosis and increased swimming activity did, however, reduce colony growth rates dramatically, resulting in 50\% fewer zooids per colony. Moreover, such colonies produced initial zooids with smaller feeding structures, with the width of branchial baskets reduced by 10 to 15\%. These differences in branchial basket size persisted and were still apparent in newly budded zooids 3 wk after metamorphosis. Our results suggest that, for D. listerianum, larval maintenance, swimming, and metamorphosis all use energy from a common pool, and increases in the allocation to maintenance or swimming come at the expense of post-larval performance.",
    url = "https://doi.org/10.3354/meps246153",
    doi = "10.3354/meps246153",
    openalex = "W2048252622",
    references = "doi101007bf00377130, doi101016s0022098187800126, doi10108000785236199010422025, doi1018900012965820010821597osapiv20co2, doi1023071313294, doi1023071540075, doi103354meps177269, openalexw2489624142, openalexw3213326676, thorson1950reproductive"
}

Hemps, a novel epidermal growth factor (EGF)-like protein, is expressed during larval development and early metamorphosis in the ascidian Herdmania curvata and plays a direct role in triggering metamorphosis. In order to identify downstream genes in the Hemps pathway we used a gene expression profiling approach, in which we compared post-larvae undergoing normal metamorphosis with larval metamorphosis blocked with an anti-Hemps antibody. Molecular profiling revealed that there are dynamic changes in gene expression within the first 30 minutes of normal metamorphosis with a significant portion of the genome (approximately 49%) being activated or repressed. A more detailed analysis of the expression of 15 of these differentially expressed genes through embryogenesis, larval development and metamorphosis revealed that while there is a diversity of temporal expression patterns, a number of genes are transiently expressed during larval development and metamorphosis. These and other differentially expressed genes were localised to a range of specific cell and tissue types in Herdmania larvae and post-larvae. The expression of approximately 24% of the genes that were differentially expressed during early metamorphosis was affected in larvae treated with the anti-Hemps antibody. Knockdown of Hemps activity affected the expression of a range of genes within 30 minutes of induction, suggesting that the Hemps pathway directly regulates early response genes at metamorphosis. In most cases, it appears that the Hemps pathway contributes to the modulation of gene expression, rather than initial gene activation or repression. A total of 151 genes that displayed the greatest alterations in expression in response to anti-Hemps antibody were sequenced. These genes were implicated in a range of developmental and physiological roles, including innate immunity, signal transduction and in the regulation of gene transcription. These results suggest that there is significant gene activity during the very early stages of H. curvata metamorphosis and that the Hemps pathway plays a key role in regulating the expression of many of these genes.

@article{doi101242dev01120,
    author = "Woods, Rick and Roper, Kathrein E. and Gauthier, Marie and Bebell, Lisa M. and Sung, Kristin and Degnan, Bernard M. and Lavin, Martin F.",
    title = "Gene expression during early ascidian metamorphosis requires signalling by Hemps, an EGF-like protein",
    year = "2004",
    journal = "Development",
    abstract = "Hemps, a novel epidermal growth factor (EGF)-like protein, is expressed during larval development and early metamorphosis in the ascidian Herdmania curvata and plays a direct role in triggering metamorphosis. In order to identify downstream genes in the Hemps pathway we used a gene expression profiling approach, in which we compared post-larvae undergoing normal metamorphosis with larval metamorphosis blocked with an anti-Hemps antibody. Molecular profiling revealed that there are dynamic changes in gene expression within the first 30 minutes of normal metamorphosis with a significant portion of the genome (approximately 49\%) being activated or repressed. A more detailed analysis of the expression of 15 of these differentially expressed genes through embryogenesis, larval development and metamorphosis revealed that while there is a diversity of temporal expression patterns, a number of genes are transiently expressed during larval development and metamorphosis. These and other differentially expressed genes were localised to a range of specific cell and tissue types in Herdmania larvae and post-larvae. The expression of approximately 24\% of the genes that were differentially expressed during early metamorphosis was affected in larvae treated with the anti-Hemps antibody. Knockdown of Hemps activity affected the expression of a range of genes within 30 minutes of induction, suggesting that the Hemps pathway directly regulates early response genes at metamorphosis. In most cases, it appears that the Hemps pathway contributes to the modulation of gene expression, rather than initial gene activation or repression. A total of 151 genes that displayed the greatest alterations in expression in response to anti-Hemps antibody were sequenced. These genes were implicated in a range of developmental and physiological roles, including innate immunity, signal transduction and in the regulation of gene transcription. These results suggest that there is significant gene activity during the very early stages of H. curvata metamorphosis and that the Hemps pathway plays a key role in regulating the expression of many of these genes.",
    url = "https://doi.org/10.1242/dev.01120",
    doi = "10.1242/dev.01120",
    openalex = "W2163647417",
    references = "doi101007s004270050011, doi101242dev126245809"
}

Following the reading of its draft genome sequence and the collection of a large quantity of cDNA information, Ciona intestinalis is now becoming a model organism for whole-genome analyses of the expression and function of developmentally relevant genes. Although most studies have focused on larval structures, the development of the adult form is also very interesting in relation to tissues and organs of vertebrate body. Here we conducted detailed observations of the development of tissues and organs in Ciona intestinalis larva and juveniles until so-called the 2nd ascidian stage. These observations included examination of the oral siphon, tentacle, oral pigments and atrial pigments, atrial siphon, ganglion and neural gland, longitudinal muscle, stigmata, transverse bar and languet, longitudinal bar and papilla, heart, digestive organ, gonad, endostyle, and stalk and villi. The findings from these observations make a new staging system for juvenile development possible. Based on the development of the internal organs, we propose here nine stages (stage 0-stage 8) starting with swimming larvae and proceeding through juveniles until the 2nd ascidian stage. These descriptions and staging system provide a basis for studying cellular and molecular mechanisms underlying the development of adult organs and tissues of this basal chordate.

@article{doi102108zsj21285,
    author = "Chiba, Shota and Sasaki, Akane and Nakayama, A. and Takamura, Katsumi and Satoh, Nori",
    title = "Development of Ciona intestinalis Juveniles (Through 2nd Ascidian Stage)",
    year = "2004",
    journal = "ZOOLOGICAL SCIENCE",
    abstract = "Following the reading of its draft genome sequence and the collection of a large quantity of cDNA information, Ciona intestinalis is now becoming a model organism for whole-genome analyses of the expression and function of developmentally relevant genes. Although most studies have focused on larval structures, the development of the adult form is also very interesting in relation to tissues and organs of vertebrate body. Here we conducted detailed observations of the development of tissues and organs in Ciona intestinalis larva and juveniles until so-called the 2nd ascidian stage. These observations included examination of the oral siphon, tentacle, oral pigments and atrial pigments, atrial siphon, ganglion and neural gland, longitudinal muscle, stigmata, transverse bar and languet, longitudinal bar and papilla, heart, digestive organ, gonad, endostyle, and stalk and villi. The findings from these observations make a new staging system for juvenile development possible. Based on the development of the internal organs, we propose here nine stages (stage 0-stage 8) starting with swimming larvae and proceeding through juveniles until the 2nd ascidian stage. These descriptions and staging system provide a basis for studying cellular and molecular mechanisms underlying the development of adult organs and tissues of this basal chordate.",
    url = "https://doi.org/10.2108/zsj.21.285",
    doi = "10.2108/zsj.21.285",
    openalex = "W2145670106",
    references = "doi101002sici1097010x199908152852158aidjez830co20, doi101007bf02956047, doi101007s004270050011, doi101016s0065288108604575"
}

Tunicates are the only animals that perform cellulose biosynthesis. The tunicate gene for cellulose synthase, Ci-CesA, was likely acquired by horizontal transfer from bacteria and was a key innovation in the evolution of tunicates. Transposon-based mutagenesis in an ascidian, Ciona intestinalis, has generated a mutant, swimming juvenile (sj). Ci-CesA is the gene responsible for the sj mutant, in which a drastic reduction in cellulose was observed in the tunic. Furthermore, during metamorphosis, which in ascidians convert the vertebrate-like larva into a sessile filter feeder, sj showed abnormalities in the order of metamorphic events. In normal larvae, the metamorphic events in the trunk region are initiated after tail resorption. In contrast, sj mutant larvae initiated the metamorphic events in the trunk without tail resorption. Thus, sj larvae show a "swimming juvenile" phenotype, the juvenile-like trunk structure with a complete tail and the ability to swim. It is likely that ascidian cellulose synthase is required for the coordination of the metamorphic events in the trunk and tail in addition to cellulose biosynthesis.

@article{doi101073pnas0503640102,
    author = "Sasakura, Yasunori and Nakashima, Keisuke and Awazu, Satoko and Matsuoka, Terumi and Nakayama, A. and Azuma, Junichi and Satoh, Nori",
    title = "Transposon-mediated insertional mutagenesis revealed the functions of animal cellulose synthase in the ascidian Ciona intestinalis",
    year = "2005",
    journal = "Proceedings of the National Academy of Sciences",
    abstract = {Tunicates are the only animals that perform cellulose biosynthesis. The tunicate gene for cellulose synthase, Ci-CesA, was likely acquired by horizontal transfer from bacteria and was a key innovation in the evolution of tunicates. Transposon-based mutagenesis in an ascidian, Ciona intestinalis, has generated a mutant, swimming juvenile (sj). Ci-CesA is the gene responsible for the sj mutant, in which a drastic reduction in cellulose was observed in the tunic. Furthermore, during metamorphosis, which in ascidians convert the vertebrate-like larva into a sessile filter feeder, sj showed abnormalities in the order of metamorphic events. In normal larvae, the metamorphic events in the trunk region are initiated after tail resorption. In contrast, sj mutant larvae initiated the metamorphic events in the trunk without tail resorption. Thus, sj larvae show a "swimming juvenile" phenotype, the juvenile-like trunk structure with a complete tail and the ability to swim. It is likely that ascidian cellulose synthase is required for the coordination of the metamorphic events in the trunk and tail in addition to cellulose biosynthesis.},
    url = "https://doi.org/10.1073/pnas.0503640102",
    doi = "10.1073/pnas.0503640102",
    openalex = "W1990343858",
    references = "doi101093icb224817"
}

For many years ecologists have documented the remarkable within-species variation inherent in natural systems-for example, variability in juvenile growth rates, mortality rates, fecundities, time to reproductive maturity, the outcomes of competitive interactions, and tolerance to pollutants. Over the past 20 years, it has become increasingly apparent that at least some of this variation may reflect differences in embryonic or larval experiences. Such experiences may include delayed metamorphosis, short term starvation, short term salinity stress, or exposure to sublethal concentrations of pollutants or sublethal levels of ultra violet irradiation. Latent effects-effects that have their origins in early development but that are first exhibited in juveniles or adults-have now been documented among gastropods, bivalves, echinoderms, polychaetes, crustaceans, bryozoans, urochordates, and vertebrates. The extent to which latent effects alter ecological outcomes in natural populations in the field, and the mechanisms through which they are mediated are largely unexplored.

@article{doi101093icbicj028,
    author = "Pechenik, Jan A.",
    title = "Larval experience and latent effects--metamorphosis is not a new beginning",
    year = "2006",
    journal = "Integrative and Comparative Biology",
    abstract = "For many years ecologists have documented the remarkable within-species variation inherent in natural systems-for example, variability in juvenile growth rates, mortality rates, fecundities, time to reproductive maturity, the outcomes of competitive interactions, and tolerance to pollutants. Over the past 20 years, it has become increasingly apparent that at least some of this variation may reflect differences in embryonic or larval experiences. Such experiences may include delayed metamorphosis, short term starvation, short term salinity stress, or exposure to sublethal concentrations of pollutants or sublethal levels of ultra violet irradiation. Latent effects-effects that have their origins in early development but that are first exhibited in juveniles or adults-have now been documented among gastropods, bivalves, echinoderms, polychaetes, crustaceans, bryozoans, urochordates, and vertebrates. The extent to which latent effects alter ecological outcomes in natural populations in the field, and the mechanisms through which they are mediated are largely unexplored.",
    url = "https://doi.org/10.1093/icb/icj028",
    doi = "10.1093/icb/icj028",
    openalex = "W2114315821",
    references = "doi10103843425, doi101056nejm197608122950701, doi10108000785236199010422025, doi101093jn13492169, doi101111j001438202003tb00298x, doi101128mcb2315529353002003, doi1023071312173, doi1023071933500, doi1023071937462, doi1023071943173, doi103354meps177269, doi103354meps246153, knightjones1953laboratory"
}

Metamorphosis in marine invertebrate larvae is a dynamic, environmentally dependent process that integrates ontogeny with habitat selection. The capacity of many marine invertebrate larvae to survive and maintain metamorphic competence in the absence of environmental cues has been hypothesized to be an adaptive convergence (Hadfield and others 2001). A survey of the literature reveals that a single generalized hypothesis about metamorphic competence as an adaptive convergence is not sufficient to account for interspecific variation in this character. In an attempt to capture this variation, we discuss the "desperate larva hypothesis" and propose two additional hypotheses called the "variable retention hypothesis" and the "death before dishonor hypothesis." To validate these additional hypotheses we collected data on taxa from the published literature and performed a contingency analysis to detect correlations between spontaneous metamorphosis, habitat specificity and/or larval life-history mode, three characters relevant to environmentally induced settlement and metamorphosis. In order to account for phylogenetic bias in these correlations, we also constructed a phylogeny of these taxa and again performed a character-correlation analysis. Both these tests suggest that juvenile habitat specificity is correlated to the capacity of individuals to retain the competent larval state in the absence of substrate cues and therefore validate the existence of more than one hypothesis about metamorphic competence. We provide new data from the sea urchin Lytechinus pictus that suggest that nitric oxide (NO) and thyroxine hormone signaling interact to determine the probability of settlement in response to a settlement cue. Similarly, we provide evidence that thyroxine signaling in the sand dollar Dendraster excentricus increases spontaneous metamorphosis in the absence of cues from adult conspecifics in a manner that is independent of larval age.

@article{doi101093icbicl043,
    author = "Bishop, Cory D. and Huggett, Megan J. and Heyland, Andreas and Hodin, Jason and Brandhorst, Bruce P.",
    title = "Interspecific variation in metamorphic competence in marine invertebrates: the significance for comparative investigations into the timing of metamorphosis",
    year = "2006",
    journal = "Integrative and Comparative Biology",
    abstract = {Metamorphosis in marine invertebrate larvae is a dynamic, environmentally dependent process that integrates ontogeny with habitat selection. The capacity of many marine invertebrate larvae to survive and maintain metamorphic competence in the absence of environmental cues has been hypothesized to be an adaptive convergence (Hadfield and others 2001). A survey of the literature reveals that a single generalized hypothesis about metamorphic competence as an adaptive convergence is not sufficient to account for interspecific variation in this character. In an attempt to capture this variation, we discuss the "desperate larva hypothesis" and propose two additional hypotheses called the "variable retention hypothesis" and the "death before dishonor hypothesis." To validate these additional hypotheses we collected data on taxa from the published literature and performed a contingency analysis to detect correlations between spontaneous metamorphosis, habitat specificity and/or larval life-history mode, three characters relevant to environmentally induced settlement and metamorphosis. In order to account for phylogenetic bias in these correlations, we also constructed a phylogeny of these taxa and again performed a character-correlation analysis. Both these tests suggest that juvenile habitat specificity is correlated to the capacity of individuals to retain the competent larval state in the absence of substrate cues and therefore validate the existence of more than one hypothesis about metamorphic competence. We provide new data from the sea urchin Lytechinus pictus that suggest that nitric oxide (NO) and thyroxine hormone signaling interact to determine the probability of settlement in response to a settlement cue. Similarly, we provide evidence that thyroxine signaling in the sand dollar Dendraster excentricus increases spontaneous metamorphosis in the absence of cues from adult conspecifics in a manner that is independent of larval age.},
    url = "https://doi.org/10.1093/icb/icl043",
    doi = "10.1093/icb/icl043",
    openalex = "W2092013273",
    references = "doi101002jez1019, doi1010160967065393914159, doi101017cbo9780511806384, doi101038387489a0, doi101086284325, doi101086383584, doi101098rspb19940006, doi101242dev126245809, doi1023074615733, openalexw1586553371, openalexw2611511275"
}

The ascidian tadpole larva represents the basic body plan of all chordates in a relatively small number of cells and tissue types. Although it had been considered that ascidians develop largely in a determinative way, whereas vertebrates develop in an inductive way, recent studies at the molecular and cellular levels have uncovered several similarities in the way developmental fates are specified. In this review, we describe ascidian embryogenesis and its cell lineages, introduce several characteristics of ascidian embryos, describe recent advances in understanding of the mechanisms of cell fate specification, and discuss them in the context of what is known in vertebrates and other organisms.

@article{doi101002dvdy21108,
    author = "Kumano, Gaku and Nishida, Hiroki",
    title = "Ascidian embryonic development: An emerging model system for the study of cell fate specification in chordates",
    year = "2007",
    journal = "Developmental Dynamics",
    abstract = "The ascidian tadpole larva represents the basic body plan of all chordates in a relatively small number of cells and tissue types. Although it had been considered that ascidians develop largely in a determinative way, whereas vertebrates develop in an inductive way, recent studies at the molecular and cellular levels have uncovered several similarities in the way developmental fates are specified. In this review, we describe ascidian embryogenesis and its cell lineages, introduce several characteristics of ascidian embryos, describe recent advances in understanding of the mechanisms of cell fate specification, and discuss them in the context of what is known in vertebrates and other organisms.",
    url = "https://doi.org/10.1002/dvdy.21108",
    doi = "10.1002/dvdy.21108",
    openalex = "W1967796034",
    references = "doi101007s004270050011, doi101242dev126225149"
}

@article{doi101007s0042700701570,
    author = "Roberts, Brock and Davidson, Brad and MacMaster, Glen and Lockhart, Victoria and Ma, Eva and Wallace, Shannon Smith and Swalla, Billie J.",
    title = "A complement response may activate metamorphosis in the ascidian Boltenia villosa",
    year = "2007",
    journal = "Development Genes and Evolution",
    url = "https://doi.org/10.1007/s00427-007-0157-0",
    doi = "10.1007/s00427-007-0157-0",
    openalex = "W1981998259",
    references = "doi101002jez1019, doi101006jmbi19931305, doi101007s0025100306065, doi101038nature04336, doi101038nri800, doi101093icb224817, doi101093molbevmsi225, doi101093nargkg500, doi101126science1080049, doi101242dev126245809, doi105860choice353280, openalexw2273005662, openalexw48629314"
}

In ascidian tadpoles, metamorphosis is triggered by a polarized wave of apoptosis, via mechanisms that are largely unknown. We demonstrate that the MAP kinases ERK and JNK are both required for the wave of apoptosis and metamorphosis. By employing a gene-profiling-based approach, we identified the network of genes controlled by either ERK or JNK activity that stimulate the onset of apoptosis. This approach identified a gene network involved in hormonal signalling, in innate immunity, in cell-cell communication and in the extracellular matrix. Through gene silencing, we show that Ci-sushi, a cell-cell communication protein controlled by JNK activity, is required for the wave of apoptosis that precedes tail regression. These observations lead us to propose a model of metamorphosis whereby JNK activity in the CNS induces apoptosis in several adjacent tissues that compose the tail by inducing the expression of genes such as Ci-sushi.

@article{doi101242dev002220,
    author = "Chambon, Jean‐Philippe and Nakayama, A. and Takamura, Katsumi and McDougall, Alex and Satoh, Noriyuki",
    title = "ERK- and JNK-signalling regulate gene networks that stimulate metamorphosis and apoptosis in tail tissues of ascidian tadpoles",
    year = "2007",
    journal = "Development",
    abstract = "In ascidian tadpoles, metamorphosis is triggered by a polarized wave of apoptosis, via mechanisms that are largely unknown. We demonstrate that the MAP kinases ERK and JNK are both required for the wave of apoptosis and metamorphosis. By employing a gene-profiling-based approach, we identified the network of genes controlled by either ERK or JNK activity that stimulate the onset of apoptosis. This approach identified a gene network involved in hormonal signalling, in innate immunity, in cell-cell communication and in the extracellular matrix. Through gene silencing, we show that Ci-sushi, a cell-cell communication protein controlled by JNK activity, is required for the wave of apoptosis that precedes tail regression. These observations lead us to propose a model of metamorphosis whereby JNK activity in the CNS induces apoptosis in several adjacent tissues that compose the tail by inducing the expression of genes such as Ci-sushi.",
    url = "https://doi.org/10.1242/dev.002220",
    doi = "10.1242/dev.002220",
    openalex = "W2160667462",
    references = "doi101002jez1084"
}

Metamorphosis displays a striking diversity in chordates, a deuterostome phylum that comprises vertebrates, urochordates (tunicates), and cephalochordates (amphioxus). In anuran amphibians, the tadpole loses its tail, develops limbs, and undergoes profound changes at the behavioral, physiological, biochemical, and ecological levels. In ascidian tunicates, the tail is lost and the head tissues are drastically remodeled into the adult animal, whereas in amphioxus, the highly asymmetric larva transforms into a relatively symmetric adult. This wide diversity has led to the proposal that metamorphosis evolved several times independently in the different chordate lineages during evolution. However, the molecular mechanisms involved in metamorphosis are largely unknown outside amphibians and teleost fishes, in which metamorphosis is regulated by the thyroid hormones (TH) T3 and T4 binding to their receptors (thyroid hormone receptors). In this review, we compare metamorphosis in chordates and then propose a unifying definition of the larva-to-adult transition, based on the conservation of the role of THs and some of their derivatives as the main regulators of metamorphosis. According to this definition, all chordates (if not, all deuterostomes) have a homologous metamorphosis stage during their postembryonic development. The intensity and the nature of the morphological remodeling varies extensively among taxa, from drastic remodeling like in some ascidians or amphibians to more subtle events, as in mammals.

@article{doi101002dvg20443,
    author = "Paris, Mathilde and Laudet, Vincent",
    title = "The history of a developmental stage: Metamorphosis in chordates",
    year = "2008",
    journal = "genesis",
    abstract = "Metamorphosis displays a striking diversity in chordates, a deuterostome phylum that comprises vertebrates, urochordates (tunicates), and cephalochordates (amphioxus). In anuran amphibians, the tadpole loses its tail, develops limbs, and undergoes profound changes at the behavioral, physiological, biochemical, and ecological levels. In ascidian tunicates, the tail is lost and the head tissues are drastically remodeled into the adult animal, whereas in amphioxus, the highly asymmetric larva transforms into a relatively symmetric adult. This wide diversity has led to the proposal that metamorphosis evolved several times independently in the different chordate lineages during evolution. However, the molecular mechanisms involved in metamorphosis are largely unknown outside amphibians and teleost fishes, in which metamorphosis is regulated by the thyroid hormones (TH) T3 and T4 binding to their receptors (thyroid hormone receptors). In this review, we compare metamorphosis in chordates and then propose a unifying definition of the larva-to-adult transition, based on the conservation of the role of THs and some of their derivatives as the main regulators of metamorphosis. According to this definition, all chordates (if not, all deuterostomes) have a homologous metamorphosis stage during their postembryonic development. The intensity and the nature of the morphological remodeling varies extensively among taxa, from drastic remodeling like in some ascidians or amphibians to more subtle events, as in mammals.",
    url = "https://doi.org/10.1002/dvg.20443",
    doi = "10.1002/dvg.20443",
    openalex = "W1983834103",
    references = "barrington1963comparative, doi101002jez1084, doi101098rspb19650063, doi101186147121487127, stokes1995ciliary"
}

@article{doi101016jcub200805039,
    author = "Lemaire, Patrick and Smith, William C. and Nishida, Hiroki",
    title = "Ascidians and the Plasticity of the Chordate Developmental Program",
    year = "2008",
    journal = "Current Biology",
    url = "https://doi.org/10.1016/j.cub.2008.05.039",
    doi = "10.1016/j.cub.2008.05.039",
    openalex = "W1965991185",
    references = "doi101007s004270050011, doi101093icb224817, doi101242dev126245809"
}

Hydroides elegans is a common marine fouling organism in most tropical and subtropical waters. The life cycle of H. elegans includes a planktonic larval stage in which swimming larvae normally take 5 days to attain competency to settle. Larval metamorphosis marks the beginning of its benthic life; however, the endogenous molecular mechanisms that regulate metamorphosis remain largely unknown. In this study, a PCR-based suppressive subtractive hybridization (SSH) library was constructed to screen the genes expressed in competent larvae but not in precompetent larvae. Among the transcripts isolated from the library, 21 significantly matched sequences in the GenBank. Many of these isolated transcripts have putative roles in the reactive oxygen species (ROS) signal transduction pathway or in response to ROS stress. A putative novel p38 mitogen-activated protein kinase (MAPK), which was also isolated with SSH screen, was then cloned and characterized. The MAPK inhibitors assay showed that both p38 MAPK inhibitors SB202190 and SB203580 effectively inhibited the biofilm-induced metamorphosis of H. elegans. A cell stressors assay showed that H(2)O(2) effectively induced larval metamorphosis of H. elegans, but the inductivity of H(2)O(2) was also inhibited by both SB inhibitors. The catalase assay showed that the catalase could effetely inhibit H. elegans larvae from responding to inductive biofilm. These results showed that the p38 MAPK-dependent pathway plays critical role in controlling larval metamorphosis of the marine polychaete H. elegans, and the reactive oxygen radicals produced by biofilm could be the cue inducing larval metamorphosis.

@article{doi101002jezb21344,
    author = "Wang, Hao and Qian, Pei‐Yuan",
    title = "Involvement of a novel p38 mitogen‐activated protein kinase in larval metamorphosis of the polychaete Hydroides elegans (Haswell)",
    year = "2010",
    journal = "Journal of Experimental Zoology Part B Molecular and Developmental Evolution",
    abstract = "Hydroides elegans is a common marine fouling organism in most tropical and subtropical waters. The life cycle of H. elegans includes a planktonic larval stage in which swimming larvae normally take 5 days to attain competency to settle. Larval metamorphosis marks the beginning of its benthic life; however, the endogenous molecular mechanisms that regulate metamorphosis remain largely unknown. In this study, a PCR-based suppressive subtractive hybridization (SSH) library was constructed to screen the genes expressed in competent larvae but not in precompetent larvae. Among the transcripts isolated from the library, 21 significantly matched sequences in the GenBank. Many of these isolated transcripts have putative roles in the reactive oxygen species (ROS) signal transduction pathway or in response to ROS stress. A putative novel p38 mitogen-activated protein kinase (MAPK), which was also isolated with SSH screen, was then cloned and characterized. The MAPK inhibitors assay showed that both p38 MAPK inhibitors SB202190 and SB203580 effectively inhibited the biofilm-induced metamorphosis of H. elegans. A cell stressors assay showed that H(2)O(2) effectively induced larval metamorphosis of H. elegans, but the inductivity of H(2)O(2) was also inhibited by both SB inhibitors. The catalase assay showed that the catalase could effetely inhibit H. elegans larvae from responding to inductive biofilm. These results showed that the p38 MAPK-dependent pathway plays critical role in controlling larval metamorphosis of the marine polychaete H. elegans, and the reactive oxygen radicals produced by biofilm could be the cue inducing larval metamorphosis.",
    url = "https://doi.org/10.1002/jez.b.21344",
    doi = "10.1002/jez.b.21344",
    openalex = "W2138831814",
    references = "doi101242dev126245809"
}

Comparative genomics of representative basal metazoans leaves little doubt that the most recent common ancestor to all modern metazoans was morphogenetically complex. Here, we support this interpretation by demonstrating that the demosponge Amphimedon queenslandica has a biphasic pelagobenthic life cycle resembling that present in a wide range of bilaterians and anthozoan cnidarians. The A. queenslandica life cycle includes a compulsory planktonic larval phase that can end only once the larva develops competence to respond to benthic signals that induce settlement and metamorphosis. The temporal onset of competence varies between individuals as revealed by idiosyncratic responses to inductive cues. Thus, the biphasic life cycle with a dispersing larval phase of variable length appears to be a metazoan synapomorphy and may be viewed as an ancestral polyphenic trait. Larvae of a particular age that are subjected to an inductive cue either maintain the larval form or metamorphose into the post-larval/juvenile form. Variance in the development of competence dictates that only a subset of a larval cohort will settle and undergo metamorphosis at a given time, which in turn leads to variation in dispersal distance and in location of settlement. Population divergence and allopatric speciation are likely outcomes of this conserved developmental polyphenic trait.

@article{doi101098rstb20090248,
    author = "Degnan, Sandie M. and Degnan, Bernard M.",
    title = "The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life-cycle evolution",
    year = "2010",
    journal = "Philosophical Transactions of the Royal Society B Biological Sciences",
    abstract = "Comparative genomics of representative basal metazoans leaves little doubt that the most recent common ancestor to all modern metazoans was morphogenetically complex. Here, we support this interpretation by demonstrating that the demosponge Amphimedon queenslandica has a biphasic pelagobenthic life cycle resembling that present in a wide range of bilaterians and anthozoan cnidarians. The A. queenslandica life cycle includes a compulsory planktonic larval phase that can end only once the larva develops competence to respond to benthic signals that induce settlement and metamorphosis. The temporal onset of competence varies between individuals as revealed by idiosyncratic responses to inductive cues. Thus, the biphasic life cycle with a dispersing larval phase of variable length appears to be a metazoan synapomorphy and may be viewed as an ancestral polyphenic trait. Larvae of a particular age that are subjected to an inductive cue either maintain the larval form or metamorphose into the post-larval/juvenile form. Variance in the development of competence dictates that only a subset of a larval cohort will settle and undergo metamorphosis at a given time, which in turn leads to variation in dispersal distance and in location of settlement. Population divergence and allopatric speciation are likely outcomes of this conserved developmental polyphenic trait.",
    url = "https://doi.org/10.1098/rstb.2009.0248",
    doi = "10.1098/rstb.2009.0248",
    openalex = "W2119848352",
    references = "doi101242dev126245809"
}

@article{doi101016jcub201107030,
    author = "Laudet, Vincent",
    title = "The Origins and Evolution of Vertebrate Metamorphosis",
    year = "2011",
    journal = "Current Biology",
    url = "https://doi.org/10.1016/j.cub.2011.07.030",
    doi = "10.1016/j.cub.2011.07.030",
    openalex = "W2004471830",
    references = "doi101002jez1084, doi101002jez1402670309"
}

@article{doi101016jydbio201205038,
    author = "Brown, Federico D. and Swalla, Billie J.",
    title = "Evolution and development of budding by stem cells: Ascidian coloniality as a case study",
    year = "2012",
    journal = "Developmental Biology",
    url = "https://doi.org/10.1016/j.ydbio.2012.05.038",
    doi = "10.1016/j.ydbio.2012.05.038",
    openalex = "W2011613147",
    references = "doi101007s004270050011, doi101098rstb19350013"
}

@article{doi101016jfsi201304044,
    author = "Balseiro, Pablo and Moreira, Rebeca and Chamorro, Rubén and Figueras, António and Novoa, Beatriz",
    title = "Immune responses during the larval stages of Mytilus galloprovincialis: Metamorphosis alters immunocompetence, body shape and behavior",
    year = "2013",
    journal = "Fish \& Shellfish Immunology",
    url = "https://doi.org/10.1016/j.fsi.2013.04.044",
    doi = "10.1016/j.fsi.2013.04.044",
    openalex = "W2083818397",
    references = "doi101093icbicl043, doi101242dev129204739"
}

Globally, ascidians are a significant contributor to benthic marine fouling communities, but have remained poorly studied in this context. In some cases, such as in shellfish and finfish aquaculture, ascidians are the most problematic of all fouling organisms. The disproportionate impact of ascidian fouling in some specific geographic locations has been related directly to anthropogenic translocation of these organisms around the globe. In the case of ascidians, therefore, the economic issue of biofouling and the ecological ramifications of invasion are inextricably linked. This mini-review briefly discusses the introduction of non-native ascidians to areas where they have subsequently proven to be a significant fouling pest. The elements of ascidian reproductive ecology that support their aggressive fouling character are discussed and the scant information pertaining to their adhesion and adhesives is presented. Finally, strategies for mitigating ascidian fouling are examined. It is suggested that sufficient working knowledge currently exists to support the inclusion of one or more common ascidian species as 'standard' test organisms used for evaluation of novel fouling-resistant surfaces.

@article{doi101080089270142013866653,
    author = "Aldred, Nick and Clare, Anthony S.",
    title = "Mini-review: Impact and dynamics of surface fouling by solitary and compound ascidians",
    year = "2014",
    journal = "Biofouling",
    abstract = "Globally, ascidians are a significant contributor to benthic marine fouling communities, but have remained poorly studied in this context. In some cases, such as in shellfish and finfish aquaculture, ascidians are the most problematic of all fouling organisms. The disproportionate impact of ascidian fouling in some specific geographic locations has been related directly to anthropogenic translocation of these organisms around the globe. In the case of ascidians, therefore, the economic issue of biofouling and the ecological ramifications of invasion are inextricably linked. This mini-review briefly discusses the introduction of non-native ascidians to areas where they have subsequently proven to be a significant fouling pest. The elements of ascidian reproductive ecology that support their aggressive fouling character are discussed and the scant information pertaining to their adhesion and adhesives is presented. Finally, strategies for mitigating ascidian fouling are examined. It is suggested that sufficient working knowledge currently exists to support the inclusion of one or more common ascidian species as 'standard' test organisms used for evaluation of novel fouling-resistant surfaces.",
    url = "https://doi.org/10.1080/08927014.2013.866653",
    doi = "10.1080/08927014.2013.866653",
    openalex = "W2081630674",
    references = "doi103354meps246153"
}

Diverse animal taxa metamorphose between larval and juvenile phases in response to bacteria. Although bacteria-induced metamorphosis is widespread among metazoans, little is known about the molecular changes that occur in the animal upon stimulation by bacteria. Larvae of the tubeworm Hydroides elegans metamorphose in response to surface-bound Pseudoalteromonas luteoviolacea bacteria, producing ordered arrays of phage tail-like metamorphosis-associated contractile structures (MACs). Sequencing the Hydroides genome and transcripts during five developmental stages revealed that MACs induce the regulation of groups of genes important for tissue remodeling, innate immunity, and mitogen-activated protein kinase (MAPK) signaling. Using two MAC mutations that block P. luteoviolacea from inducing settlement or metamorphosis and three MAPK inhibitors, we established a sequence of bacteria-induced metamorphic events: MACs induce larval settlement; then, particular properties of MACs encoded by a specific locus in P. luteoviolacea initiate cilia loss and activate metamorphosis-associated transcription; finally, signaling through p38 and c-Jun N-terminal kinase (JNK) MAPK pathways alters gene expression and leads to morphological changes upon initiation of metamorphosis. Our results reveal that the intricate interaction between Hydroides and P. luteoviolacea can be dissected using genomic, genetic, and pharmacological tools. Hydroides' dependency on bacteria for metamorphosis highlights the importance of external stimuli to orchestrate animal development. The conservation of Hydroides genome content with distantly related deuterostomes (urchins, sea squirts, and humans) suggests that mechanisms of bacteria-induced metamorphosis in Hydroides may have conserved features in diverse animals. As a major biofouling agent, insight into the triggers of Hydroides metamorphosis might lead to practical strategies for fouling control.

@article{doi101073pnas1603142113,
    author = "Shikuma, Nicholas J. and Antoshechkin, Igor and Medeiros, João M. and Pilhofer, Martin and Newman, Dianne K.",
    title = "Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling",
    year = "2016",
    journal = "Proceedings of the National Academy of Sciences",
    abstract = "Diverse animal taxa metamorphose between larval and juvenile phases in response to bacteria. Although bacteria-induced metamorphosis is widespread among metazoans, little is known about the molecular changes that occur in the animal upon stimulation by bacteria. Larvae of the tubeworm Hydroides elegans metamorphose in response to surface-bound Pseudoalteromonas luteoviolacea bacteria, producing ordered arrays of phage tail-like metamorphosis-associated contractile structures (MACs). Sequencing the Hydroides genome and transcripts during five developmental stages revealed that MACs induce the regulation of groups of genes important for tissue remodeling, innate immunity, and mitogen-activated protein kinase (MAPK) signaling. Using two MAC mutations that block P. luteoviolacea from inducing settlement or metamorphosis and three MAPK inhibitors, we established a sequence of bacteria-induced metamorphic events: MACs induce larval settlement; then, particular properties of MACs encoded by a specific locus in P. luteoviolacea initiate cilia loss and activate metamorphosis-associated transcription; finally, signaling through p38 and c-Jun N-terminal kinase (JNK) MAPK pathways alters gene expression and leads to morphological changes upon initiation of metamorphosis. Our results reveal that the intricate interaction between Hydroides and P. luteoviolacea can be dissected using genomic, genetic, and pharmacological tools. Hydroides' dependency on bacteria for metamorphosis highlights the importance of external stimuli to orchestrate animal development. The conservation of Hydroides genome content with distantly related deuterostomes (urchins, sea squirts, and humans) suggests that mechanisms of bacteria-induced metamorphosis in Hydroides may have conserved features in diverse animals. As a major biofouling agent, insight into the triggers of Hydroides metamorphosis might lead to practical strategies for fouling control.",
    url = "https://doi.org/10.1073/pnas.1603142113",
    doi = "10.1073/pnas.1603142113",
    openalex = "W2511592890",
    references = "doi101002jez1019, doi101007s0042700701570, doi101016s0300908402014220, doi101038nature11696, doi101038nri2998, doi101073pnas1218525110, doi101073pnas251194298, doi101073pnas4861014, doi101091mbce02050259, doi101093bioinformaticsbtm071, doi101110ps03554604, doi101146annurevmarine120709142753, doi1011861471213x1214, doi101242dev129204739"
}

Dispersing organisms often cannot assess habitat quality directly, so they employ proxies (cues) to choose habitats that maximise fitness. Theory suggests organisms should settle as soon as they find appropriate cues in order to reduce physiological costs and mortality risk incurred whilst searching. We propose that for planktotrophic marine larvae, when resources are plentiful, development of adult structures during an extended larval phase provide post-metamorphosis benefits that offset the costs of remaining in the plankton. To test this, we measured fitness consequences of metamorphosis in response to habitat cues at a range of developmental maturities in 2 sea urchin larvae, Tripneustes gratilla and Centrostephanus rodgersii. We found larvae that were capable of responding to cues and settling accrued significant benefits if they extended their pelagic development. Compared to more developed larvae, larvae without adult structures took longer to metamorphose, and after metamorphosis were 11 to 25% smaller, 0.1 to 6 times more likely to lack defensive structures and 3 to 13 times more likely to have abnormal morphology. Most early settlers died within 1 wk compared to >40% survival for more developed larvae. We found larvae avoid the costs of early metamorphosis by only responding to low concentrations of cues in the water column once they have adult structures. Our results contrast with models of habitat selection that suggest organisms should settle in habitat quickly to minimise search costs. Incorporating the trade-off between the benefits of larval development and search costs into current models of habitat selection may provide new insights into how fitness consequences affect habitat selection.

@article{doi103354meps11914,
    author = "Mos, Benjamin and Dworjanyn, Symon A.",
    title = "Early metamorphosis is costly and avoided by young, but physiologically competent, marine larvae",
    year = "2016",
    journal = "Marine Ecology Progress Series",
    abstract = "Dispersing organisms often cannot assess habitat quality directly, so they employ proxies (cues) to choose habitats that maximise fitness. Theory suggests organisms should settle as soon as they find appropriate cues in order to reduce physiological costs and mortality risk incurred whilst searching. We propose that for planktotrophic marine larvae, when resources are plentiful, development of adult structures during an extended larval phase provide post-metamorphosis benefits that offset the costs of remaining in the plankton. To test this, we measured fitness consequences of metamorphosis in response to habitat cues at a range of developmental maturities in 2 sea urchin larvae, Tripneustes gratilla and Centrostephanus rodgersii. We found larvae that were capable of responding to cues and settling accrued significant benefits if they extended their pelagic development. Compared to more developed larvae, larvae without adult structures took longer to metamorphose, and after metamorphosis were 11 to 25\% smaller, 0.1 to 6 times more likely to lack defensive structures and 3 to 13 times more likely to have abnormal morphology. Most early settlers died within 1 wk compared to >40\% survival for more developed larvae. We found larvae avoid the costs of early metamorphosis by only responding to low concentrations of cues in the water column once they have adult structures. Our results contrast with models of habitat selection that suggest organisms should settle in habitat quickly to minimise search costs. Incorporating the trade-off between the benefits of larval development and search costs into current models of habitat selection may provide new insights into how fitness consequences affect habitat selection.",
    url = "https://doi.org/10.3354/meps11914",
    doi = "10.3354/meps11914",
    openalex = "W2528928385",
    references = "doi101002jez1019, doi101002jez1401990212, doi101007s0044200810439, doi10108000785236199010422030, doi101086285141, doi101111j13652486200801734x, doi101111j14429993200101070ppx, doi101146annureves25110194003041, doi1011861471213x1214, doi1023071313294, doi103354meps097193, doi103354meps177269, doi105343bms20101051"
}

@misc{doi101016bsmcb201811004,
    author = "Hodin, Jason and Heyland, Andreas and Mercier, Annie and Pernet, Bruno and Cohen, David and Hamel, Jean‐François and Allen, Jonathan D. and McAlister, Justin S. and Byrne, Maria and Cisternas, Paula and George, Sophie B.",
    title = "Culturing echinoderm larvae through metamorphosis",
    year = "2018",
    booktitle = "Methods in cell biology",
    url = "https://doi.org/10.1016/bs.mcb.2018.11.004",
    doi = "10.1016/bs.mcb.2018.11.004",
    openalex = "W2907552364",
    references = "doi1011861471213x1214"
}

The ivory shell, Babylonia areolata, is a commercially important aquaculture species in the southeast coast of mainland China. The middle veliger stage, later veliger stage, and juvenile stage are distinct larval stages in B. areolata development. In this study, we used label-free quantification proteomics analysis of the three developmental stages of B. areolata. We identified a total of 5,583 proteins, of which 1,419 proteins expression level showed significant differential expression. The results of gene ontology enrichment analysis showed that the number of proteins involved in metabolic and cellular processes were the most abundant. Those proteins mostly had functions such as binding, catalytic activity and transporter activity. The results of Kyoto Encyclopedia of Genes and Genomes enrichment analysis showed that the number of proteins involved in the ribosome, carbon metabolism, and lysosome pathways were the most abundant, indicating that protein synthesis and the immune response were active during the three stages of development. This is the first study to use proteomics and real-time PCR to study the early developmental stages of B. areolata, which could provide relevant data on gastropod development. Our results provide insights into the novel aspects of protein function in shell formation, body torsion, changes in feeding habits, attachment and metamorphosis, immune-related activities in B. areolata larvae.

@article{doi101038s4159801824645z,
    author = "Shen, Minghui and Di, Guilan and Li, Min and Fu, Jingqiang and Dai, Qi and Miao, Xiulian and Huang, Miaoqin and You, Weiwei and Ke, Caihuan",
    title = "Proteomics Studies on the three Larval Stages of Development and Metamorphosis of Babylonia areolata",
    year = "2018",
    journal = "Scientific Reports",
    abstract = "The ivory shell, Babylonia areolata, is a commercially important aquaculture species in the southeast coast of mainland China. The middle veliger stage, later veliger stage, and juvenile stage are distinct larval stages in B. areolata development. In this study, we used label-free quantification proteomics analysis of the three developmental stages of B. areolata. We identified a total of 5,583 proteins, of which 1,419 proteins expression level showed significant differential expression. The results of gene ontology enrichment analysis showed that the number of proteins involved in metabolic and cellular processes were the most abundant. Those proteins mostly had functions such as binding, catalytic activity and transporter activity. The results of Kyoto Encyclopedia of Genes and Genomes enrichment analysis showed that the number of proteins involved in the ribosome, carbon metabolism, and lysosome pathways were the most abundant, indicating that protein synthesis and the immune response were active during the three stages of development. This is the first study to use proteomics and real-time PCR to study the early developmental stages of B. areolata, which could provide relevant data on gastropod development. Our results provide insights into the novel aspects of protein function in shell formation, body torsion, changes in feeding habits, attachment and metamorphosis, immune-related activities in B. areolata larvae.",
    url = "https://doi.org/10.1038/s41598-018-24645-z",
    doi = "10.1038/s41598-018-24645-z",
    openalex = "W2883091403",
    references = "doi101007s0042700701570"
}

BACKGROUND: Molecular mechanisms underlying coral larval competence, the ability of larvae to respond to settlement cues, determine their dispersal potential and are potential targets of natural selection. Here, we profiled competence, fluorescence and genome-wide gene expression in embryos and larvae of the reef-building coral Acropora millepora daily throughout 12 days post-fertilization. RESULTS: Gene expression associated with competence was positively correlated with transcriptomic response to the natural settlement cue, confirming that mature coral larvae are "primed" for settlement. Rise of competence through development was accompanied by up-regulation of sensory and signal transduction genes such as ion channels, genes involved in neuropeptide signaling, and G-protein coupled receptor (GPCRs). A drug screen targeting components of GPCR signaling pathways confirmed a role in larval settlement behavior and metamorphosis. CONCLUSIONS: These results gives insight into the molecular complexity underlying these transitions and reveals receptors and pathways that, if altered by changing environments, could affect dispersal capabilities of reef-building corals. In addition, this dataset provides a toolkit for asking broad questions about sensory capacity in multicellular animals and the evolution of development.

@article{doi101186s1286401743920,
    author = "Strader, Marie E. and Aglyamova, Galina V. and Matz, Mikhail V.",
    title = "Molecular characterization of larval development from fertilization to metamorphosis in a reef-building coral",
    year = "2018",
    journal = "BMC Genomics",
    abstract = {BACKGROUND: Molecular mechanisms underlying coral larval competence, the ability of larvae to respond to settlement cues, determine their dispersal potential and are potential targets of natural selection. Here, we profiled competence, fluorescence and genome-wide gene expression in embryos and larvae of the reef-building coral Acropora millepora daily throughout 12 days post-fertilization. RESULTS: Gene expression associated with competence was positively correlated with transcriptomic response to the natural settlement cue, confirming that mature coral larvae are "primed" for settlement. Rise of competence through development was accompanied by up-regulation of sensory and signal transduction genes such as ion channels, genes involved in neuropeptide signaling, and G-protein coupled receptor (GPCRs). A drug screen targeting components of GPCR signaling pathways confirmed a role in larval settlement behavior and metamorphosis. CONCLUSIONS: These results gives insight into the molecular complexity underlying these transitions and reveals receptors and pathways that, if altered by changing environments, could affect dispersal capabilities of reef-building corals. In addition, this dataset provides a toolkit for asking broad questions about sensory capacity in multicellular animals and the evolution of development.},
    url = "https://doi.org/10.1186/s12864-017-4392-0",
    doi = "10.1186/s12864-017-4392-0",
    openalex = "W2782024581",
    references = "doi101093icbicl043, doi101242dev126245809"
}

BACKGROUND: Although retinoic acid (RA) signaling plays a crucial role in the body patterning of chordates, its function in non-chordate invertebrates, other than its mediation of environmental cues triggering metamorphosis in cnidarians, is largely unknown. We investigated the role of RA signaling in the metamorphosis of starfish (Echinodermata). RESULTS: We found that exogenous RA treatment induced metamorphosis in starfish larvae. In contrast, inhibitors of RA synthesis and RA receptors suppressed metamorphosis triggered by attachment to a substrate. Gene expressions of the RA signaling component were detected in competent larvae. CONCLUSIONS: This study provides insight into the ancestral function of RA signaling, which is conserved in the metamorphosis of cnidarians and starfish.

@article{doi101186s132270180098x,
    author = "Yamakawa, Shumpei and Morino, Yoshiaki and Honda, Masanao and Wada, Hiroshi",
    title = "The role of retinoic acid signaling in starfish metamorphosis",
    year = "2018",
    journal = "EvoDevo",
    abstract = "BACKGROUND: Although retinoic acid (RA) signaling plays a crucial role in the body patterning of chordates, its function in non-chordate invertebrates, other than its mediation of environmental cues triggering metamorphosis in cnidarians, is largely unknown. We investigated the role of RA signaling in the metamorphosis of starfish (Echinodermata). RESULTS: We found that exogenous RA treatment induced metamorphosis in starfish larvae. In contrast, inhibitors of RA synthesis and RA receptors suppressed metamorphosis triggered by attachment to a substrate. Gene expressions of the RA signaling component were detected in competent larvae. CONCLUSIONS: This study provides insight into the ancestral function of RA signaling, which is conserved in the metamorphosis of cnidarians and starfish.",
    url = "https://doi.org/10.1186/s13227-018-0098-x",
    doi = "10.1186/s13227-018-0098-x",
    openalex = "W2804750144",
    references = "doi1011861471213x1214"
}

Most marine organisms present an indirect lifecycle where a planktonic larval stage reaches competency before settling to the substrate and metamorphosing. Despite the critical importance of these early life history stages, little is known about how global change-related stressors, in particular ocean acidification (OA), affect marine larval settlement and metamorphosis. To date, 48 studies have investigated the effects of OA on larval settlement, focussing mostly on tropical corals (16), echinoderms (11) and fish (8). Most studies show negative effects of OA during settlement and post-settlement processes. For instance, reduced settlement is typically seen along natural pH gradients and in experimentally lowered pH treatments. This generally results in reduced settlement selectivity and metamorphosis and poorer post-settlement fitness. Carryover effects of OA exposure can also occur, with larval environmental history influencing early post-settlement performance. We conclude that OA may (1) alter larval supply for settlement by altering horizontal swimming be haviour or vertical migration; (2) directly influence settlement success through changes in the nature and distribution of suitable settlement substrates (e.g. biofilm, crustose coralline algae); and (3) mediate carryover effects at settlement by altering larval development or larval energy budgets. In contrast to fish larvae, there is little evidence for most invertebrate larvae that their perception of settlement cues is directly influenced by reduced pH. A summation of how OA affects the settlement and metamorphosis of marine invertebrates is timely, since altered settlement rates will influence the future distributions, abundances and ecology of marine benthic communities.

@article{doi103354meps12754,
    author = "Espinel-Velasco, N and Hoffmann, L. and Agüera, Antonio and Byrne, Maria and Dupont, Sam and Uthicke, Sven and Webster, Nicole S. and Lamare, Miles D.",
    title = "Effects of ocean acidification on the settlement and metamorphosis of marine invertebrate and fish larvae: a review",
    year = "2018",
    journal = "Marine Ecology Progress Series",
    abstract = "Most marine organisms present an indirect lifecycle where a planktonic larval stage reaches competency before settling to the substrate and metamorphosing. Despite the critical importance of these early life history stages, little is known about how global change-related stressors, in particular ocean acidification (OA), affect marine larval settlement and metamorphosis. To date, 48 studies have investigated the effects of OA on larval settlement, focussing mostly on tropical corals (16), echinoderms (11) and fish (8). Most studies show negative effects of OA during settlement and post-settlement processes. For instance, reduced settlement is typically seen along natural pH gradients and in experimentally lowered pH treatments. This generally results in reduced settlement selectivity and metamorphosis and poorer post-settlement fitness. Carryover effects of OA exposure can also occur, with larval environmental history influencing early post-settlement performance. We conclude that OA may (1) alter larval supply for settlement by altering horizontal swimming be haviour or vertical migration; (2) directly influence settlement success through changes in the nature and distribution of suitable settlement substrates (e.g. biofilm, crustose coralline algae); and (3) mediate carryover effects at settlement by altering larval development or larval energy budgets. In contrast to fish larvae, there is little evidence for most invertebrate larvae that their perception of settlement cues is directly influenced by reduced pH. A summation of how OA affects the settlement and metamorphosis of marine invertebrates is timely, since altered settlement rates will influence the future distributions, abundances and ecology of marine benthic communities.",
    url = "https://doi.org/10.3354/meps12754",
    doi = "10.3354/meps12754",
    openalex = "W2891296021",
    references = "doi103354meps11914"
}

@article{doi101007s0022701935763,
    author = "Pechenik, Jan A. and Pires, Anthony and Trudel, J. and Levy, Morgan and Dooley, T. J. and Resnikoff, Alissa R. and Taylor, Rulaiha",
    title = "Impact of ocean acidification on growth, onset of competence, and perception of cues for metamorphosis in larvae of the slippershell snail, Crepidula fornicata",
    year = "2019",
    journal = "Marine Biology",
    url = "https://doi.org/10.1007/s00227-019-3576-3",
    doi = "10.1007/s00227-019-3576-3",
    openalex = "W2973544975",
    references = "doi101242jeb167478"
}

Many animals depend on microbial symbionts to provide nutrition, defence or other services. Holometabolous insects, as well as other animals that undergo metamorphosis, face unique constraints on symbiont maintenance. Microbes present in larvae encounter a radical transformation of their habitat and may also need to withstand chemical and immunological challenges. Metamorphosis also provides an opportunity, in that symbiotic associations can be decoupled over development. For example, some holometabolous insects maintain the same symbiont as larvae and adults, but house it in different tissues; in other species, larvae and adults may harbour entirely different types or numbers of microbes, in accordance with shifts in host diet or habitat. Such flexibility may provide an advantage over hemimetabolous insects, in which selection on adult-stage microbial associations may be constrained by its negative effects on immature stages, and vice versa. Additionally, metamorphosis itself can be directly influenced by symbionts. Across disparate insect taxa, microbes protect hosts from pathogen infection, supply nutrients essential for rebuilding the adult body and provide cues regulating pupation. However, microbial associations remain completely unstudied for many families and even orders of Holometabola, and future research will undoubtedly reveal more links between metamorphosis and microbiota, two widespread features of animal life. This article is part of the theme issue 'The evolution of complete metamorphosis'.

@article{doi101098rstb20190068,
    author = "Hammer, Tobin J. and Moran, Nancy A.",
    title = "Links between metamorphosis and symbiosis in holometabolous insects",
    year = "2019",
    journal = "Philosophical Transactions of the Royal Society B Biological Sciences",
    abstract = "Many animals depend on microbial symbionts to provide nutrition, defence or other services. Holometabolous insects, as well as other animals that undergo metamorphosis, face unique constraints on symbiont maintenance. Microbes present in larvae encounter a radical transformation of their habitat and may also need to withstand chemical and immunological challenges. Metamorphosis also provides an opportunity, in that symbiotic associations can be decoupled over development. For example, some holometabolous insects maintain the same symbiont as larvae and adults, but house it in different tissues; in other species, larvae and adults may harbour entirely different types or numbers of microbes, in accordance with shifts in host diet or habitat. Such flexibility may provide an advantage over hemimetabolous insects, in which selection on adult-stage microbial associations may be constrained by its negative effects on immature stages, and vice versa. Additionally, metamorphosis itself can be directly influenced by symbionts. Across disparate insect taxa, microbes protect hosts from pathogen infection, supply nutrients essential for rebuilding the adult body and provide cues regulating pupation. However, microbial associations remain completely unstudied for many families and even orders of Holometabola, and future research will undoubtedly reveal more links between metamorphosis and microbiota, two widespread features of animal life. This article is part of the theme issue 'The evolution of complete metamorphosis'.",
    url = "https://doi.org/10.1098/rstb.2019.0068",
    doi = "10.1098/rstb.2019.0068",
    openalex = "W2969429284",
    references = "doi101073pnas1603142113"
}

gene is required for inducing metamorphosis. Purified Mif1 is sufficient for triggering metamorphosis when electroporated into tubeworm larvae. Our results indicate that the delivery of protein effectors by contractile injection systems may orchestrate microbe-animal interactions in diverse contexts.

@article{doi107554elife46845,
    author = "Ericson, Charles F. and Eisenstein, Fabian and Medeiros, João M. and Malter, Kyle E. and Cavalcanti, Giselle S. and Zeller, Robert W. and Newman, Dianne K. and Pilhofer, Martin and Shikuma, Nicholas J.",
    title = "A contractile injection system stimulates tubeworm metamorphosis by translocating a proteinaceous effector",
    year = "2019",
    journal = "eLife",
    abstract = "gene is required for inducing metamorphosis. Purified Mif1 is sufficient for triggering metamorphosis when electroporated into tubeworm larvae. Our results indicate that the delivery of protein effectors by contractile injection systems may orchestrate microbe-animal interactions in diverse contexts.",
    url = "https://doi.org/10.7554/elife.46845",
    doi = "10.7554/elife.46845",
    openalex = "W2974869024",
    references = "doi101073pnas1603142113"
}

Ciona robusta (Ciona intestinalis type A), a model organism for biological studies, belongs to ascidians, the main class of tunicates, which are the closest relatives of vertebrates. In Ciona, a project on the ontology of both development and anatomy is ongoing for several years. Its goal is to standardize a resource relating each anatomical structure to developmental stages. Today, the ontology is codified until the hatching larva stage. Here, we present its extension throughout the swimming larva stages, the metamorphosis, until the juvenile stages. For standardizing the developmental ontology, we acquired different time-lapse movies, confocal microscope images and histological serial section images for each developmental event from the hatching larva stage (17.5 h post fertilization) to the juvenile stage (7 days post fertilization). Combining these data, we defined 12 new distinct developmental stages (from Stage 26 to Stage 37), in addition to the previously defined 26 stages, referred to embryonic development. The new stages were grouped into four Periods named: Adhesion, Tail Absorption, Body Axis Rotation, and Juvenile. To build the anatomical ontology, 203 anatomical entities were identified, defined according to the literature, and annotated, taking advantage from the high resolution and the complementary information obtained from confocal microscopy and histology. The ontology describes the anatomical entities in hierarchical levels, from the cell level (cell lineage) to the tissue/organ level. Comparing the number of entities during development, we found two rounds on entity increase: in addition to the one occurring after fertilization, there is a second one during the Body Axis Rotation Period, when juvenile structures appear. Vice versa, one-third of anatomical entities associated with the embryo/larval life were significantly reduced at the beginning of metamorphosis. Data was finally integrated within the web-based resource "TunicAnatO", which includes a number of anatomical images and a dictionary with synonyms. This ontology will allow the standardization of data underpinning an accurate annotation of gene expression and the comprehension of mechanisms of differentiation. It will help in understanding the emergence of elaborated structures during both embryogenesis and metamorphosis, shedding light on tissue degeneration and differentiation occurring at metamorphosis.

@article{doi101038s41598020735449,
    author = "Hotta, K. and Dauga, Delphine and Manni, L.",
    title = "The ontology of the anatomy and development of the solitary ascidian Ciona: the swimming larva and its metamorphosis",
    year = "2020",
    journal = "Scientific Reports",
    abstract = {Ciona robusta (Ciona intestinalis type A), a model organism for biological studies, belongs to ascidians, the main class of tunicates, which are the closest relatives of vertebrates. In Ciona, a project on the ontology of both development and anatomy is ongoing for several years. Its goal is to standardize a resource relating each anatomical structure to developmental stages. Today, the ontology is codified until the hatching larva stage. Here, we present its extension throughout the swimming larva stages, the metamorphosis, until the juvenile stages. For standardizing the developmental ontology, we acquired different time-lapse movies, confocal microscope images and histological serial section images for each developmental event from the hatching larva stage (17.5 h post fertilization) to the juvenile stage (7 days post fertilization). Combining these data, we defined 12 new distinct developmental stages (from Stage 26 to Stage 37), in addition to the previously defined 26 stages, referred to embryonic development. The new stages were grouped into four Periods named: Adhesion, Tail Absorption, Body Axis Rotation, and Juvenile. To build the anatomical ontology, 203 anatomical entities were identified, defined according to the literature, and annotated, taking advantage from the high resolution and the complementary information obtained from confocal microscopy and histology. The ontology describes the anatomical entities in hierarchical levels, from the cell level (cell lineage) to the tissue/organ level. Comparing the number of entities during development, we found two rounds on entity increase: in addition to the one occurring after fertilization, there is a second one during the Body Axis Rotation Period, when juvenile structures appear. Vice versa, one-third of anatomical entities associated with the embryo/larval life were significantly reduced at the beginning of metamorphosis. Data was finally integrated within the web-based resource "TunicAnatO", which includes a number of anatomical images and a dictionary with synonyms. This ontology will allow the standardization of data underpinning an accurate annotation of gene expression and the comprehension of mechanisms of differentiation. It will help in understanding the emergence of elaborated structures during both embryogenesis and metamorphosis, shedding light on tissue degeneration and differentiation occurring at metamorphosis.},
    url = "https://www.nature.com/articles/s41598-020-73544-9.pdf",
    doi = "10.1038/s41598-020-73544-9",
    is_oa = "true",
    number = "1",
    semanticscholar_citation_count = "44",
    semanticscholar_id = "5d4626a8cfef73e4d3673532c431a1c0fedf2c31",
    volume = "10",
    references = "doi101007s004270050011, doi101093icb224817"
}

, we have begun to identify bacterial cues that stimulate animal metamorphosis and test hypotheses addressing their mechanisms of action. By understanding the mechanisms by which bacteria promote animal metamorphosis, we begin to illustrate how, and explore why, the developmental decision of metamorphosis relies on cues from environmental bacteria.

@article{doi101146annurevmicro011320012753,
    author = "Cavalcanti, Giselle S. and Alker, Amanda T. and Delherbe, Nathalie and Malter, Kyle E. and Shikuma, Nicholas J.",
    title = "The Influence of Bacteria on Animal Metamorphosis",
    year = "2020",
    journal = "Annual Review of Microbiology",
    abstract = ", we have begun to identify bacterial cues that stimulate animal metamorphosis and test hypotheses addressing their mechanisms of action. By understanding the mechanisms by which bacteria promote animal metamorphosis, we begin to illustrate how, and explore why, the developmental decision of metamorphosis relies on cues from environmental bacteria.",
    url = "https://doi.org/10.1146/annurev-micro-011320-012753",
    doi = "10.1146/annurev-micro-011320-012753",
    openalex = "W3083806510",
    references = "doi101007s0042700701570"
}

. This study not only reveals the role of the ADK-AMPK-FoxO pathway in larval settlement and metamorphosis of marine invertebrates but it also deepens our understanding of the functions and evolution of adenosine signaling, a process that is widespread in biology and important in medicine.

@article{doi101021acschembio1c00175,
    author = "He, Jian and Wu, Zhiwen and Chen, Liying and Dai, Qi and Hao, Huanhuan and Su, Pei and Ke, Caihuan and Feng, Danqing",
    title = "Adenosine Triggers Larval Settlement and Metamorphosis in the Mussel Mytilopsis sallei through the ADK-AMPK-FoxO Pathway",
    year = "2021",
    journal = "ACS Chemical Biology",
    abstract = ". This study not only reveals the role of the ADK-AMPK-FoxO pathway in larval settlement and metamorphosis of marine invertebrates but it also deepens our understanding of the functions and evolution of adenosine signaling, a process that is widespread in biology and important in medicine.",
    url = "https://doi.org/10.1021/acschembio.1c00175",
    doi = "10.1021/acschembio.1c00175",
    openalex = "W3182273632",
    references = "doi101371journalpone0088744"
}

How larvae of the many phyla of marine invertebrates find places appropriate for settlement, metamorphosis, growth, and reproduction is an enduring question in marine science. Biofilm-induced metamorphosis has been observed in marine invertebrate larvae from nearly every major marine phylum. Despite the widespread nature of this phenomenon, the mechanism of induction remains poorly understood. The serpulid polychaete Hydroides elegans is a well established model for investigating bacteria-induced larval development. A broad range of biofilm bacterial species elicit larval metamorphosis in H. elegans via at least two mechanisms, including outer membrane vesicles (OMVs) and complexes of phage-tail bacteriocins. We investigated the interaction between larvae of H. elegans and the inductive bacterium Cellulophaga lytica, which produces an abundance of OMVs but not phage-tail bacteriocins. We asked whether the OMVs of C. lytica induce larval settlement due to cell membrane components or through delivery of specific cargo. Employing a biochemical structure–function approach with a strong ecological focus, the cells and OMVs produced by C. lytica were interrogated to determine the class of the inductive compounds. Here, we report that larvae of H. elegans are induced to metamorphose by lipopolysaccharide produced by C. lytica. The widespread prevalence of lipopolysaccharide and its associated taxonomic and structural variability suggest it may be a broadly employed cue for bacterially induced larval settlement of marine invertebrates.

@article{doi101073pnas2200795119,
    author = "Freckelton, Marnie L. and Nedved, Brian T. and Cai, You‐Sheng and Cao, Shugeng and Turano, Helen and Alegado, Rosanna A. and Hadfield, Michael G.‏",
    title = "Bacterial lipopolysaccharide induces settlement and metamorphosis in a marine larva",
    year = "2022",
    journal = "Proceedings of the National Academy of Sciences",
    abstract = "How larvae of the many phyla of marine invertebrates find places appropriate for settlement, metamorphosis, growth, and reproduction is an enduring question in marine science. Biofilm-induced metamorphosis has been observed in marine invertebrate larvae from nearly every major marine phylum. Despite the widespread nature of this phenomenon, the mechanism of induction remains poorly understood. The serpulid polychaete Hydroides elegans is a well established model for investigating bacteria-induced larval development. A broad range of biofilm bacterial species elicit larval metamorphosis in H. elegans via at least two mechanisms, including outer membrane vesicles (OMVs) and complexes of phage-tail bacteriocins. We investigated the interaction between larvae of H. elegans and the inductive bacterium Cellulophaga lytica, which produces an abundance of OMVs but not phage-tail bacteriocins. We asked whether the OMVs of C. lytica induce larval settlement due to cell membrane components or through delivery of specific cargo. Employing a biochemical structure–function approach with a strong ecological focus, the cells and OMVs produced by C. lytica were interrogated to determine the class of the inductive compounds. Here, we report that larvae of H. elegans are induced to metamorphose by lipopolysaccharide produced by C. lytica. The widespread prevalence of lipopolysaccharide and its associated taxonomic and structural variability suggest it may be a broadly employed cue for bacterially induced larval settlement of marine invertebrates.",
    url = "https://doi.org/10.1073/pnas.2200795119",
    doi = "10.1073/pnas.2200795119",
    openalex = "W4226354589",
    references = "doi101007s0042700701570"
}

larvae which precisely follows the progression of neural signals of the central pattern generator necessary for the control of the movements of the larva towards the substrate. This highly dynamic localization profile perfectly matches with the central role played by NO from the first phase of settlement induction to the next control of swimming behavior, adhesion to substrate and progressive tissue resorption and reorganization of metamorphosis itself.

@article{doi103390ijms23073505,
    author = "Locascio, Annamaria and Vassalli, Quirino Attilio and Castellano, Immacolata and Palumbo, Anna",
    title = "Novel Insights on Nitric Oxide Synthase and NO Signaling in Ascidian Metamorphosis",
    year = "2022",
    journal = "International Journal of Molecular Sciences",
    abstract = "larvae which precisely follows the progression of neural signals of the central pattern generator necessary for the control of the movements of the larva towards the substrate. This highly dynamic localization profile perfectly matches with the central role played by NO from the first phase of settlement induction to the next control of swimming behavior, adhesion to substrate and progressive tissue resorption and reorganization of metamorphosis itself.",
    url = "https://doi.org/10.3390/ijms23073505",
    doi = "10.3390/ijms23073505",
    openalex = "W4220801090",
    references = "doi101242jeb167478"
}

Thyroid hormones (THs) are essential for development, growth, and metabolism in animals. Although TH synthesis is well described in vertebrates, it remains elusive in invertebrates due to the lack of identified thyroglobulin (TG) orthologs, the protein precursor for TH synthesis. Here, we identified a functional TG-like protein in ascidian Styela clava via immunoprecipitation-mass spectrometry combined with phylogenetic and expression analyses. In vitro iodination demonstrated that ScTG-like provides hormonogenic sites for TH synthesis. In vivo ScTg-like knockdown significantly reduced THs and inhibited larval metamorphosis. An invaginated follicle-like structure in the larval trunk, deposited with ScTG-like, was identified as the location for THs synthesis and storage. Furthermore, structural analysis of ScTG-like and predicted TG-like proteins across bilaterian phyla suggests that endogenous TH synthesis may be an ancestral and synapomorphic bilaterian trait. This study reports the identification of a TH precursor outside vertebrates, shedding lights on the evolution of the TH synthesis.

@article{doi101038s41467026692907,
    author = "Zhang, Jin and Yang, Likun and Beinsteiner, Brice and Ma, Yun and Wei, Jiankai and Yu, Haiyan and Laudet, Vincent and Dong, Bo",
    title = "Identification of protein precursor for thyroid hormone synthesis in basal chordate ascidian Styela clava.",
    year = "2026",
    journal = "Nature communications",
    abstract = "Thyroid hormones (THs) are essential for development, growth, and metabolism in animals. Although TH synthesis is well described in vertebrates, it remains elusive in invertebrates due to the lack of identified thyroglobulin (TG) orthologs, the protein precursor for TH synthesis. Here, we identified a functional TG-like protein in ascidian Styela clava via immunoprecipitation-mass spectrometry combined with phylogenetic and expression analyses. In vitro iodination demonstrated that ScTG-like provides hormonogenic sites for TH synthesis. In vivo ScTg-like knockdown significantly reduced THs and inhibited larval metamorphosis. An invaginated follicle-like structure in the larval trunk, deposited with ScTG-like, was identified as the location for THs synthesis and storage. Furthermore, structural analysis of ScTG-like and predicted TG-like proteins across bilaterian phyla suggests that endogenous TH synthesis may be an ancestral and synapomorphic bilaterian trait. This study reports the identification of a TH precursor outside vertebrates, shedding lights on the evolution of the TH synthesis.",
    url = "https://pmc.ncbi.nlm.nih.gov/articles/PMC12992692/",
    doi = "10.1038/s41467-026-69290-7",
    openalex = "W7128299211",
    pmcid = "PMC12992692",
    pmid = "41654703",
    references = "doi101016jcub201107030, doi101038ng2568, doi101038s4157401901848, doi101093molbevmsab120, doi101093nar22224673, doi101093nargky448, doi101186s1291501804992, doi101210er20151090, doi101242dev129153751, doi101242dev145615"
}