Development

ABSTRACT Last year one of us (Mr. Willey) collected during the months of May, July, and August many hundreds of embryos and larvæ of Amphioxus in Sicily.

@article{doi101242jcss231123445,
    author = "Lankester, E. Ray and Willey, Arthur",
    title = "The Development of the Atrial Chamber of Amphioxus",
    year = "1890",
    journal = "Journal of Cell Science",
    abstract = "ABSTRACT Last year one of us (Mr. Willey) collected during the months of May, July, and August many hundreds of embryos and larvæ of Amphioxus in Sicily.",
    url = "https://doi.org/10.1242/jcs.s2-31.123.445",
    doi = "10.1242/jcs.s2-31.123.445",
    openalex = "W2485135052"
}

IN view of certain current discussions regarding the nature of embryological development, the cleavage of the ovum in Amphioxu.~ is of more than ordinary interest on account of its remarkably plastic character, which is shown in two directions.First, it normally exhibits a protean variability, and a study of its various forms yields new data bearing on the origin of cleavage-forms in general.Second, the development is capable in a very high degree of artificial modification through mechanical disturbances operating on the early stages.The descriptive,portion of this paper is accordingly divided into two parts, the first treating of the natural forms of cleavage, and the second of induced forms caused by the isolation or mechanical displacement of the blastomeres.In a third and a fourth part the bearing of these facts on the origin of cleavage-forms and on some of the problems of embryological dynamics is briefly discussed.In studying the natural forms of cleavage I have sought, especially, to find a basis, first, for the accurate comparison of the cleavage of the chordates with that of lower forms, and second, for the experimental studies described in Part 11.T o those who have followed recent inquiries into the significance of the first stages of cleavage I need not apologize for the description of many apparently trifling details, especially since my observations on the early development differ very materially from Hatschek's acc0unt.lThe material for this study was procured at Faro during the months of June and July, 1892, by the following method: The animals, on being removed from the sand of the Pantano, were placed in large shallow glass vessels filled with clean water; here they lie perfectly quiescent and, if mature, discharge the reproductive elements within a few minutes.The eggs (which are invariably passed out through the atrial opening) were drawn up, during or immediately after their discharge, into a pipette and transferred to a smaller vessel of clean water to 579

@article{doi101002jmor1050080306,
    author = "Wilson, Edmund",
    title = "Amphioxus, and the mosaic theory of development",
    year = "1893",
    journal = "Journal of Morphology",
    abstract = "IN view of certain current discussions regarding the nature of embryological development, the cleavage of the ovum in Amphioxu.\textasciitilde\ is of more than ordinary interest on account of its remarkably plastic character, which is shown in two directions.First, it normally exhibits a protean variability, and a study of its various forms yields new data bearing on the origin of cleavage-forms in general.Second, the development is capable in a very high degree of artificial modification through mechanical disturbances operating on the early stages.The descriptive,portion of this paper is accordingly divided into two parts, the first treating of the natural forms of cleavage, and the second of induced forms caused by the isolation or mechanical displacement of the blastomeres.In a third and a fourth part the bearing of these facts on the origin of cleavage-forms and on some of the problems of embryological dynamics is briefly discussed.In studying the natural forms of cleavage I have sought, especially, to find a basis, first, for the accurate comparison of the cleavage of the chordates with that of lower forms, and second, for the experimental studies described in Part 11.T o those who have followed recent inquiries into the significance of the first stages of cleavage I need not apologize for the description of many apparently trifling details, especially since my observations on the early development differ very materially from Hatschek's acc0unt.lThe material for this study was procured at Faro during the months of June and July, 1892, by the following method: The animals, on being removed from the sand of the Pantano, were placed in large shallow glass vessels filled with clean water; here they lie perfectly quiescent and, if mature, discharge the reproductive elements within a few minutes.The eggs (which are invariably passed out through the atrial opening) were drawn up, during or immediately after their discharge, into a pipette and transferred to a smaller vessel of clean water to 579",
    url = "https://doi.org/10.1002/jmor.1050080306",
    doi = "10.1002/jmor.1050080306",
    openalex = "W2030302791"
}

@misc{hatschek1893the,
    author = "Hatschek, Berthold and Tuckey, James.",
    title = "The Amphioxus and its development",
    year = "1893",
    url = "https://doi.org/10.5962/bhl.title.3749",
    doi = "10.5962/bhl.title.3749",
    openalex = "W2477803610"
}

@misc{hatschek1893the2,
    author = "Hatschek, B",
    title = "The amphioxus and its development",
    year = "1893",
    howpublished = "London, Sonnenschein; Translated and edited by J. Tuckey",
    note = "talkorigins\_source = {true}; raw\_reference = {Hatschek, B., 1893, The amphioxus and its development: London, Sonnenschein; Translated and edited by J. Tuckey.}"
}

The work which forms the subject of the present essay was carried out in the Cambridge Zoological Laboratory during the years 1895-7. The material on which my results are founded consisted of a collection of embryos and larvæ which had been obtained by Mr. Sedgwick and Dr. Willey during their visits to Faro in 1890-91, and I have to express my warmest thanks to Mr. Sedgwick for placing this valuable material at my disposal.

@article{macbride1898the,
    author = "MacBride, E. W.",
    title = "The Early Development of Amphioxus",
    year = "1898",
    journal = "Journal of Cell Science",
    abstract = "The work which forms the subject of the present essay was carried out in the Cambridge Zoological Laboratory during the years 1895-7. The material on which my results are founded consisted of a collection of embryos and larvæ which had been obtained by Mr. Sedgwick and Dr. Willey during their visits to Faro in 1890-91, and I have to express my warmest thanks to Mr. Sedgwick for placing this valuable material at my disposal.",
    url = "https://doi.org/10.1242/jcs.s2-40.160.589",
    doi = "10.1242/jcs.s2-40.160.589",
    number = "160",
    openalex = "W1521603453",
    pages = "589-612",
    volume = "S2-40",
    references = "doi101002jmor1050080306, doi101038044202a0, doi101242jcss22494208, doi101242jcss229116365, doi101242jcss231123445, openalexw564391913"
}

1. S. horsti occurs on the Hampshire coast of the Solent near the mouth of the Lymington River, in glutinous grey mud associated with Corophium volutator. 2. The species is distinguished by the following characters: coloration; dorsal and ventral grooves present on the proboscis throughout its length; collar forming a slight operculum posteriorly; ventral muscle bands of the trunk forming projecting ridges; rounded genital ridges present, the gonads beginning within 1 mm. of the collar; 100–140 pairs of gill slits; longitudinal muscle fibres of the proboscis arranged in nine or more concentric rings; ventral septum of the proboscis short; stomochord straight, with ventral diverticulum and wide lumen throughout; no dorsal glomerulus present; single proboscis pore on the left side; proboscis skeleton embracing half to two-thirds of the circumference of the buccal cavity and extending one-fourth to one-third of the length of the collar; four epidermal zones present in the collar; collar cavities completely separated; anterior extensions of the collar cavities extending into the neck of the proboscis; perihaemal cavities separate posteriorly but confluent in front of the level of the tips of the crura, and extending into the neck of the proboscis as far as the proboscis pore; neural keel well developed and in continuity with the epidermal nerve layer at intervals; no dorsal diverticulum of the buccal cavity; branchial epidermis characterized by the predominant intensely eosinophil glandular elements; tongues broader and projecting further into the lumen of the pharynx than the septa; epibranchial ridge formed by two convex ridges bounding a median groove; oesophagus divided into three regions; 4–8 intestinal pores; hepatic region of gut not sacculated and with an expanded lumen; gonads not lobed; oocytes attain a size of 0·23 × 0·17 mm.; yolk cells present in the ovaries. 3. The probable identity of the specimen of Saccoglossus from the French coast of the English Channel, recorded by Caullery & Mesnil (1916) as S. kowalevskyi, with this species is discussed.

@article{brambell1941saccoglossus,
    author = "Brambell, F. W. Rogers and Goodhart, C. B.",
    title = "Saccoglossus horsti sp.n., an Enteropneust occurring in the Solent",
    year = "1941",
    journal = "Journal of the Marine Biological Association of the United Kingdom",
    abstract = "1. S. horsti occurs on the Hampshire coast of the Solent near the mouth of the Lymington River, in glutinous grey mud associated with Corophium volutator. 2. The species is distinguished by the following characters: coloration; dorsal and ventral grooves present on the proboscis throughout its length; collar forming a slight operculum posteriorly; ventral muscle bands of the trunk forming projecting ridges; rounded genital ridges present, the gonads beginning within 1 mm. of the collar; 100–140 pairs of gill slits; longitudinal muscle fibres of the proboscis arranged in nine or more concentric rings; ventral septum of the proboscis short; stomochord straight, with ventral diverticulum and wide lumen throughout; no dorsal glomerulus present; single proboscis pore on the left side; proboscis skeleton embracing half to two-thirds of the circumference of the buccal cavity and extending one-fourth to one-third of the length of the collar; four epidermal zones present in the collar; collar cavities completely separated; anterior extensions of the collar cavities extending into the neck of the proboscis; perihaemal cavities separate posteriorly but confluent in front of the level of the tips of the crura, and extending into the neck of the proboscis as far as the proboscis pore; neural keel well developed and in continuity with the epidermal nerve layer at intervals; no dorsal diverticulum of the buccal cavity; branchial epidermis characterized by the predominant intensely eosinophil glandular elements; tongues broader and projecting further into the lumen of the pharynx than the septa; epibranchial ridge formed by two convex ridges bounding a median groove; oesophagus divided into three regions; 4–8 intestinal pores; hepatic region of gut not sacculated and with an expanded lumen; gonads not lobed; oocytes attain a size of 0·23 × 0·17 mm.; yolk cells present in the ovaries. 3. The probable identity of the specimen of Saccoglossus from the French coast of the English Channel, recorded by Caullery \& Mesnil (1916) as S. kowalevskyi, with this species is discussed.",
    url = "https://doi.org/10.1017/s0025315400054734",
    doi = "10.1017/s0025315400054734",
    number = "2",
    openalex = "W2004491645",
    pages = "283-301",
    volume = "25",
    references = "doi101111j109636421927tb00384x, doi101111j109636421939tb00712x, doi101111j109636421939tb00714x, openalexw3183166503"
}

The genital products of Saccoglossus horsti are discharged within the burrows and expelled after the tide has ebbed. They are not retained in the burrows for any length of time. Fertilization occurs mainly in the overlying surface water, or during the flood. An ‘epidemic’ spawning was observed on three occasions in the field. A rise of temperature to about 160° C. is regarded as the essential factor primarily responsible for initiating the spawning. The females were observed to spawn before the males. Some reciprocal inducement might have occurred. The breeding season in the Solent area is mainly confined to the months of May, June and July, and is seemingly dependent on climatic and tidal conditions during these months. The spawning behaviour of other species of the Enteropneusta is discussed.

@article{burdonjones1951observations,
    author = "Burdon-Jones, C.",
    title = "Observations on the spawning behaviour of Saccoglossus horsti Brambell \& Goodhart, and of other Enteropneusta",
    year = "1951",
    journal = "Journal of the Marine Biological Association of the United Kingdom",
    abstract = "The genital products of Saccoglossus horsti are discharged within the burrows and expelled after the tide has ebbed. They are not retained in the burrows for any length of time. Fertilization occurs mainly in the overlying surface water, or during the flood. An ‘epidemic’ spawning was observed on three occasions in the field. A rise of temperature to about 160° C. is regarded as the essential factor primarily responsible for initiating the spawning. The females were observed to spawn before the males. Some reciprocal inducement might have occurred. The breeding season in the Solent area is mainly confined to the months of May, June and July, and is seemingly dependent on climatic and tidal conditions during these months. The spawning behaviour of other species of the Enteropneusta is discussed.",
    url = "https://doi.org/10.1017/s0025315400052826",
    doi = "10.1017/s0025315400052826",
    number = "3",
    openalex = "W1984469469",
    pages = "625-638",
    volume = "29",
    references = "brambell1941saccoglossus, doi101002jez1401040102, doi101017s0025315400000102, doi101017s0025315400009267, doi101017s0025315400056022, doi101111j1469185x1950tb00585x, doi101242jcss226104511, doi1023071537736, doi1023071537806, doi1023071948665, doi10230725058009"
}

Larvae of Saccoglossus horsti were reared in the laboratory, and their developmental history from the egg to the five gill-slit stage studied. The immature eggs varied from 0.23 to 0.30 mm in length and from 0.15 to 0.22 mm in breadth. They were irregular, opaque, finely granular and creamish grey in colour. They became spherical on maturing. Fertilization resulted in the rapid erection of a fertilization membrane, making the eggs buoyant. Two similar polar bodies were extruded shortly afterwards, marking the plane of the first cleavage which, with the second, was holoblastic and meridional. Subsequent cleavages were different in the animal and vegetative tiers. There was evidence of radial cleavage during the 16- to 32-cell stage. A hollow blastula was formed at the 9th to 10th cleavage stage, and gastrulation by invagination followed. The blastocoele was completely obliterated and a typical archigastrula resulted. This rapidly became uniformly ciliated and developed a telotroch around the closing blastopore. The component cilia of the telotroch imparted a slow rotatory movement to the embryo. Axial elongation and the growth of an apical tuft were accompanied by the formation of a faint annular groove. This groove marked off the definitive proboscis and the anterior part of the collar. Hatching followed 30 to 36 h after fertilization, and the larva became planktonic. During its lecithotrophic existence the larva developed a second annular groove anterior to the first, marking off the definitive proboscis from the anterior region of the collar. No definite phototaxis was detectable. Swimming movements were spasmodic. The larva rotated in a clockwise direction when viewed from the apical tuft. The spiral mode of propulsion and the propelling action of the telotroch is discussed. Settlement occurred some 2 days after hatching. A post-telotrochal adhesive patch was developed just prior to settlement, enabling the larva to adhere tenaciously to the substratum. After settlement further elongation of the main axis occurred, a well-defined proboscis, collar and trunk were rapidly differentiated. Of particular interest is the development of a long, muscular strongly ciliated post-anal tail. A dispersal period of about 612 to 7 days occurred prior to settlement. The existence of this phase prior to the animal adopting the adult mode of life demands that the mode of development of certain members of the family Harrimanidae be regarded as indirect and comparable in many respects to that known for some of the family Ptychoderidae. The mouth, anus and gill apertures became functional at much the same period, viz., at the onset of the burrowing phase. Remarkable growth movements initiated during the late planktonic phase were accelerated after settlement. This resulted in the translation of the telotroch to a latero-ventral position on the trunk and tail. The behaviour of the tail during the process of ciliary feeding, as well as during the coursing through the burrow, was observed. Ciliary reversal occurred on collar, trunk and tail. This phenomenon is discussed. Special tactile cilia have been described. They occurred on the dorsal and latero-dorsal surfaces of the trunk and tail. There was some evidence of gregariousness. The possibility of this larval habit is briefly considered in relation to the dispersal of the adults in the field. The homologies of the Enteropneusta and the Pterobranchia are discussed in some detail, with particular reference to the tail of the larval Saccoglossus horsti, and the stalk of the genus Cephalodiscus.

@article{burdonjones1952development,
    author = "Burdon-Jones, C.",
    title = "Development and Biology of the Larva of Saccoglossus Horsti (Enteropneusta)",
    year = "1952",
    journal = "Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences",
    abstract = "Larvae of Saccoglossus horsti were reared in the laboratory, and their developmental history from the egg to the five gill-slit stage studied. The immature eggs varied from 0.23 to 0.30 mm in length and from 0.15 to 0.22 mm in breadth. They were irregular, opaque, finely granular and creamish grey in colour. They became spherical on maturing. Fertilization resulted in the rapid erection of a fertilization membrane, making the eggs buoyant. Two similar polar bodies were extruded shortly afterwards, marking the plane of the first cleavage which, with the second, was holoblastic and meridional. Subsequent cleavages were different in the animal and vegetative tiers. There was evidence of radial cleavage during the 16- to 32-cell stage. A hollow blastula was formed at the 9th to 10th cleavage stage, and gastrulation by invagination followed. The blastocoele was completely obliterated and a typical archigastrula resulted. This rapidly became uniformly ciliated and developed a telotroch around the closing blastopore. The component cilia of the telotroch imparted a slow rotatory movement to the embryo. Axial elongation and the growth of an apical tuft were accompanied by the formation of a faint annular groove. This groove marked off the definitive proboscis and the anterior part of the collar. Hatching followed 30 to 36 h after fertilization, and the larva became planktonic. During its lecithotrophic existence the larva developed a second annular groove anterior to the first, marking off the definitive proboscis from the anterior region of the collar. No definite phototaxis was detectable. Swimming movements were spasmodic. The larva rotated in a clockwise direction when viewed from the apical tuft. The spiral mode of propulsion and the propelling action of the telotroch is discussed. Settlement occurred some 2 days after hatching. A post-telotrochal adhesive patch was developed just prior to settlement, enabling the larva to adhere tenaciously to the substratum. After settlement further elongation of the main axis occurred, a well-defined proboscis, collar and trunk were rapidly differentiated. Of particular interest is the development of a long, muscular strongly ciliated post-anal tail. A dispersal period of about 612 to 7 days occurred prior to settlement. The existence of this phase prior to the animal adopting the adult mode of life demands that the mode of development of certain members of the family Harrimanidae be regarded as indirect and comparable in many respects to that known for some of the family Ptychoderidae. The mouth, anus and gill apertures became functional at much the same period, viz., at the onset of the burrowing phase. Remarkable growth movements initiated during the late planktonic phase were accelerated after settlement. This resulted in the translation of the telotroch to a latero-ventral position on the trunk and tail. The behaviour of the tail during the process of ciliary feeding, as well as during the coursing through the burrow, was observed. Ciliary reversal occurred on collar, trunk and tail. This phenomenon is discussed. Special tactile cilia have been described. They occurred on the dorsal and latero-dorsal surfaces of the trunk and tail. There was some evidence of gregariousness. The possibility of this larval habit is briefly considered in relation to the dispersal of the adults in the field. The homologies of the Enteropneusta and the Pterobranchia are discussed in some detail, with particular reference to the tail of the larval Saccoglossus horsti, and the stalk of the genus Cephalodiscus.",
    url = "https://doi.org/10.1098/rstb.1952.0010",
    doi = "10.1098/rstb.1952.0010",
    number = "639",
    openalex = "W1994913686",
    pages = "553-589",
    volume = "236",
    references = "doi101242jcss282326227, openalexw605661459"
}

@article{burdonjones1953development1,
    author = "Burdon-Jones, C",
    title = "Development and biology of the larva of Saccoglossus horsti (Enteropnuesta)",
    year = "1953",
    journal = "Philosophical Transactions of the Royal Society, London B, v. 236, p. 553-589",
    note = "talkorigins\_source = {true}; raw\_reference = {Burdon-Jones, C., 1953, Development and biology of the larva of Saccoglossus horsti (Enteropnuesta): Philosophical Transactions of the Royal Society, London B, v. 236, p. 553-589.}"
}

@article{barrington1963comparative,
    author = "Barrington, E.J.W. and Thorpe, A.",
    title = "Comparative observations on lodine binding by Saccoglossus horsti brambell and goodhart, and by the tunic of Ciona intestinalis (L)",
    year = "1963",
    journal = "General and Comparative Endocrinology",
    url = "https://doi.org/10.1016/0016-6480(63)90036-4",
    doi = "10.1016/0016-6480(63)90036-4",
    number = "2",
    openalex = "W1970750225",
    pages = "166-175",
    volume = "3",
    references = "doi101002jez1400250108, doi101002jez1400250109, doi101002jez1401270105, doi101007bf02148301, doi1010160006300261904851, doi101016000630026290570x, doi101017s0025315400017021, doi101152physrev1955352336, doi1023071792682, doi105694j132653771960tb62641x"
}

@article{dilly1969the,
    author = "Dilly, P. N.",
    title = "The nerve fibres in the basement membrane and related structures in Saccoglossus horsti (Enteropneusta)",
    year = "1969",
    journal = "Zeitschrift f�r Zellforschung und Mikroskopische Anatomie",
    url = "https://doi.org/10.1007/bf00331872",
    doi = "10.1007/bf00331872",
    number = "1",
    openalex = "W2005058069",
    pages = "69-83",
    volume = "97",
    references = "brambell1941saccoglossus, dilly1969the, doi101083jcb113571, doi101083jcb72297, doi101083jcb74717, doi101098rstb19520004, doi101111j146363951950tb01028x, doi101242jcss226104511, openalexw2421517847"
}

The gastrulae of amphioxus were investigated by means of scanning and transmission electron microscopy (SEM and TEM) during 7 arbitrary stages that were seen about 4 to 10 hr after fertilization. Throughout gastrulation, SEM revealed subtle differences in cells of the blastoporal lip. In fractured specimens at early and middle stages, two opposing zones different in shape, size, and connection of the component cells were found: one which consists of columnar smaller cells in close contact in animal region and the other which is composed of round or polygonal larger cells in looser association in vegetal region. The polar body was found unexpectedly on the concave vegetal surface of the early gastrula in about 25% of cases. This might be the result of migration of the polar body. A short cilium that later elongated was recognized on each cell at mid-gastrula stage. The cilia on the dorsal surface (the neural ectoderm) of the final-stage gastrula became shorter than those on the epidermal ectoderm. TEM of thin sections demonstrated that the cytoplasmic components of gastrula cells are essentially the same as those of cleavage cells. But, the homogeneous nucleus seen during cleavage changed into a heterogeneous structure in which a nucleolus and dense particles were seen. Until the late stage, regional characteristics of the gastrulae indicating definitively the anterior-posterior and dorso-ventral polarity were not detected in the present SEM and TEM study.

@article{doi101002jmor1052070106,
    author = "Hirakow, Reiji and Kajita, N.",
    title = "Electron microscopic study of the development of amphioxus, Branchiostoma belcheri tsingtauense: The gastrula",
    year = "1991",
    journal = "Journal of Morphology",
    abstract = "The gastrulae of amphioxus were investigated by means of scanning and transmission electron microscopy (SEM and TEM) during 7 arbitrary stages that were seen about 4 to 10 hr after fertilization. Throughout gastrulation, SEM revealed subtle differences in cells of the blastoporal lip. In fractured specimens at early and middle stages, two opposing zones different in shape, size, and connection of the component cells were found: one which consists of columnar smaller cells in close contact in animal region and the other which is composed of round or polygonal larger cells in looser association in vegetal region. The polar body was found unexpectedly on the concave vegetal surface of the early gastrula in about 25\% of cases. This might be the result of migration of the polar body. A short cilium that later elongated was recognized on each cell at mid-gastrula stage. The cilia on the dorsal surface (the neural ectoderm) of the final-stage gastrula became shorter than those on the epidermal ectoderm. TEM of thin sections demonstrated that the cytoplasmic components of gastrula cells are essentially the same as those of cleavage cells. But, the homogeneous nucleus seen during cleavage changed into a heterogeneous structure in which a nucleolus and dense particles were seen. Until the late stage, regional characteristics of the gastrulae indicating definitively the anterior-posterior and dorso-ventral polarity were not detected in the present SEM and TEM study.",
    url = "https://doi.org/10.1002/jmor.1052070106",
    doi = "10.1002/jmor.1052070106",
    openalex = "W2140415852",
    references = "doi105962bhltitle140340, macbride1898the"
}

ABSTRACT The embryology of amphioxus has much in common with vertebrate embryology, reflecting a close phylogenetic relationship between the two groups. Amphioxus embryology is simpler in several key respects, however, including a lack of pronounced craniofacial morphogenesis. To gain an insight into the molecular changes that accompanied the evolution of vertebrate embryology, and into the relationship between the amphioxus and vertebrate body plans, we have undertaken the first molecular level investigation of amphioxus embryonic development. We report the cloning, complete DNA sequence determination, sequence analysis and expression analysis of an amphioxus homeobox gene, AmphiHox3, evolutionarily homologous to the thirdmost 3′ paralogous group of mammalian Hox genes. Sequence comparison to a mammalian homologue, mouse Hox-2.7 (HoxB3), reveals several stretches of amino acid conservation within the deduced protein sequences. Whole mount in situ hybridization reveals localized expression of AmphiHox3 in the posterior mesoderm (but not in the somites), and region-specific expression in the dorsal nerve cord, of amphioxus neurulae, later embryos and larvae. The anterior limit to expression in the nerve cord is at the level of the four/five somite boundary at the neurula stage, and stabilises to just anterior to the first nerve cord pigment spot to form. Comparison to the anterior expression boundary of mouse Hox-2.7 (HoxB3) and related genes suggests that the vertebrate brain is homologous to an extensive region of the amphioxus nerve cord that contains the cerebral vesicle (a region at the extreme rostral tip) and extends posterior to somite four. This proposed homology implies that the vertebrate brain probably did not evolve solely from the cerebral vesicle of an amphioxus-like ancestor, nor did it arise entirely de novo anterior to the cerebral vesicle.

@article{doi101242dev1163653,
    author = "Holland, Peter W. H. and Holland, Linda Z. and Williams, Nicola A. and Holland, Nicholas D.",
    title = "An amphioxus homeobox gene: sequence conservation, spatial expression during development and insights into vertebrate evolution",
    year = "1992",
    journal = "Development",
    abstract = "ABSTRACT The embryology of amphioxus has much in common with vertebrate embryology, reflecting a close phylogenetic relationship between the two groups. Amphioxus embryology is simpler in several key respects, however, including a lack of pronounced craniofacial morphogenesis. To gain an insight into the molecular changes that accompanied the evolution of vertebrate embryology, and into the relationship between the amphioxus and vertebrate body plans, we have undertaken the first molecular level investigation of amphioxus embryonic development. We report the cloning, complete DNA sequence determination, sequence analysis and expression analysis of an amphioxus homeobox gene, AmphiHox3, evolutionarily homologous to the thirdmost 3′ paralogous group of mammalian Hox genes. Sequence comparison to a mammalian homologue, mouse Hox-2.7 (HoxB3), reveals several stretches of amino acid conservation within the deduced protein sequences. Whole mount in situ hybridization reveals localized expression of AmphiHox3 in the posterior mesoderm (but not in the somites), and region-specific expression in the dorsal nerve cord, of amphioxus neurulae, later embryos and larvae. The anterior limit to expression in the nerve cord is at the level of the four/five somite boundary at the neurula stage, and stabilises to just anterior to the first nerve cord pigment spot to form. Comparison to the anterior expression boundary of mouse Hox-2.7 (HoxB3) and related genes suggests that the vertebrate brain is homologous to an extensive region of the amphioxus nerve cord that contains the cerebral vesicle (a region at the extreme rostral tip) and extends posterior to somite four. This proposed homology implies that the vertebrate brain probably did not evolve solely from the cerebral vesicle of an amphioxus-like ancestor, nor did it arise entirely de novo anterior to the cerebral vesicle.",
    url = "https://doi.org/10.1242/dev.116.3.653",
    doi = "10.1242/dev.116.3.653",
    openalex = "W2097360425",
    references = "doi101002j146020751989tb03534x, doi101007bf00291041, doi1010160020711x9390093t, doi1010160092867489909124, doi101016009286749290471n, doi1010160378111988903307, doi101016s0091679x08603076, doi101038313545a0, doi101038353861a0, doi101086413055, doi101242jcss231123445, doi1023071541578, doi105962bhltitle55924"
}

@misc{crossref2010menkia,
    title = "Menkia horsti: Gómez, B.",
    year = "2010",
    booktitle = "IUCN Red List of Threatened Species",
    url = "https://doi.org/10.2305/iucn.uk.2011-1.rlts.t156631a4976000.en",
    doi = "10.2305/iucn.uk.2011-1.rlts.t156631a4976000.en",
    openalex = "W4254104109"
}

Homeobox genes encode a large superclass of transcription factors with widespread roles in animal development. Within chordates there are over 100 homeobox genes in the invertebrate cephalochordate amphioxus and over 200 in humans. Set against this general trend of increasing gene number in vertebrate evolution, some ancient homeobox genes that were present in the last common ancestor of chordates have been lost from vertebrates. Here, we describe the embryonic expression of four amphioxus descendants of these genes--AmphiNedxa, AmphiNedxb, AmphiMsxlx and AmphiNKx7. All four genes are expressed with a striking asymmetry about the left-right axis in the pharyngeal region of neurula embryos, mirroring the pronounced asymmetry of amphioxus embryogenesis. AmphiMsxlx and AmphiNKx7 are also transiently expressed in an anterior neural tube region destined to become the cerebral vesicle. These findings suggest significant rewiring of developmental gene regulatory networks occurred during chordate evolution, coincident with homeobox gene loss. We propose that loss of otherwise widely conserved genes is possible when these genes function in a confined role in development that is subsequently lost or significantly modified during evolution. In the case of these homeobox genes, we propose that this has occurred in relation to the evolution of the chordate pharynx and brain.

@article{doi101098rspb20100647,
    author = "Butts, Thomas and Holland, Peter W. H. and Ferrier, David",
    title = "Ancient homeobox gene loss and the evolution of chordate brain and pharynx development: deductions from amphioxus gene expression",
    year = "2010",
    journal = "Proceedings of the Royal Society B Biological Sciences",
    abstract = "Homeobox genes encode a large superclass of transcription factors with widespread roles in animal development. Within chordates there are over 100 homeobox genes in the invertebrate cephalochordate amphioxus and over 200 in humans. Set against this general trend of increasing gene number in vertebrate evolution, some ancient homeobox genes that were present in the last common ancestor of chordates have been lost from vertebrates. Here, we describe the embryonic expression of four amphioxus descendants of these genes--AmphiNedxa, AmphiNedxb, AmphiMsxlx and AmphiNKx7. All four genes are expressed with a striking asymmetry about the left-right axis in the pharyngeal region of neurula embryos, mirroring the pronounced asymmetry of amphioxus embryogenesis. AmphiMsxlx and AmphiNKx7 are also transiently expressed in an anterior neural tube region destined to become the cerebral vesicle. These findings suggest significant rewiring of developmental gene regulatory networks occurred during chordate evolution, coincident with homeobox gene loss. We propose that loss of otherwise widely conserved genes is possible when these genes function in a confined role in development that is subsequently lost or significantly modified during evolution. In the case of these homeobox genes, we propose that this has occurred in relation to the evolution of the chordate pharynx and brain.",
    url = "https://doi.org/10.1098/rspb.2010.0647",
    doi = "10.1098/rspb.2010.0647",
    openalex = "W2103332964",
    references = "hatschek1893the"
}

The phylogenetic position of amphioxus, together with its relatively simple and evolutionarily conserved morphology and genome structure, has led to its use as a model for studies of vertebrate evolution. In particular, the recent development of technical approaches, as well as access to the complete amphioxus genome sequence, has provided the community with tools with which to study the invertebrate-chordate to vertebrate transition. Here, we present this animal model, discussing its life cycle, the model species studied and the experimental techniques that it is amenable to. We also summarize the major findings made using amphioxus that have informed us about the evolution of vertebrate traits.

@article{bertrand2011evolutionary,
    author = "Bertrand, Stephanie and Escriva, Hector",
    title = "Evolutionary crossroads in developmental biology: amphioxus",
    year = "2011",
    journal = "Development",
    abstract = "The phylogenetic position of amphioxus, together with its relatively simple and evolutionarily conserved morphology and genome structure, has led to its use as a model for studies of vertebrate evolution. In particular, the recent development of technical approaches, as well as access to the complete amphioxus genome sequence, has provided the community with tools with which to study the invertebrate-chordate to vertebrate transition. Here, we present this animal model, discussing its life cycle, the model species studied and the experimental techniques that it is amenable to. We also summarize the major findings made using amphioxus that have informed us about the evolution of vertebrate traits.",
    url = "https://doi.org/10.1242/dev.066720",
    doi = "10.1242/dev.066720",
    number = "22",
    openalex = "W1981337585",
    pages = "4819-4830",
    volume = "138",
    references = "doi1010079783642866593, doi101016jydbio201005016, doi101038370563a0, doi101038nature04336, doi101038nature05241, doi101038nature06967, doi101038nrm2428, doi101086413055, doi101098rstb19580007, doi101126science2204594268, doi101371journalpbio0030007, doi101371journalpbio0030314"
}

Currently, most developmental biologists work on one or more of a relatively small number of experimental systems, such as Arabidopsis thaliana, Drosophila melanogaster (fruit fly), Xenopus laevis (frog), Caenorhabditis elegans (nematode), Danio rerio (zebrafish) and Mus musculus (mouse), and their research is largely focused on understanding developmental mechanisms at the genetic, biochemical and molecular levels. This bias toward certain species is easily understood – analyses in these organisms is greatly facilitated by the availability of an array of genetic, molecular and genomic resources that have been generated over the years by large communities of scientists. However, the field of developmental biology has a long and colourful history of experimentation with a remarkably varied assemblage of creatures, and many crucial discoveries were first made in species that are now relatively understudied. Furthermore, some species possess certain remarkable attributes that have generated interest for a very long time. For example, the axolotl (Ambystoma mexicanum, a Mexican salamander) is considered to be the champion of regeneration among vertebrates, and although the number of people working with axolotls is relatively small, they remain a species of great interest because of the potential breakthroughs that might come from them.Another important reason that some developmental biologists have maintained interests in animals, plants and fungi outside of the main experimental systems comes from a desire to understand the evolution of development. Most of our model species are evolutionarily distant from one another, and in some cases certain aspects of their development are derived with respect to other closely related species. For example, the study of segmentation in Drosophila melanogaster has produced a multitude of remarkable insights into basic developmental mechanisms, but many of the well-understood steps in early patterning are atypical of the process of segmentation in arthropods as a whole. For this reason, developmental biologists have studied other arthropods, such as mosquitoes, beetles, crickets, grasshoppers, centipedes and spiders, to understand the diversity of developmental mechanisms at work in the process of segmentation. When placed into a phylogenetic framework, such comparative studies can also provide us with hypotheses as to how the process of segmentation has evolved within the arthropods and give us better insight into how segmentation is related between phyla.The interest in such comparative studies and their implications stretches back through the entire history of developmental biology. The important evolutionary insight that they provide has long been recognised; Charles Darwin even devotes an entire chapter of The Origin of Species to a discussion of how development can help unravel the pattern and process of evolution. In more recent decades, genetics has proven to be a key bridge between developmental and evolutionary biologists. Although developmental and evolutionary geneticists often seem to speak very different languages, there is an increasing awareness of what one can contribute to the other, and a synthesis between the two has begun to yield remarkable insights in many cases. Furthermore, the ability to work with an increasing diversity of species has received a major boost owing to several technical breakthroughs. These include the genomic tools that allow us to quickly compare the genes that are shared and not shared between species, techniques such as in situ hybridisation, microarrays and transcriptome sequencing that facilitate comparative studies of the timing and pattern of gene expression and, finally, new tools for functional analyses that take advantage of breakthroughs in RNAi and transgenic technology.For these reasons, research into the development of many species outside of the major experimental systems has flourished in recent years. Some, such as sea urchins, have indeed been studied for a very long time and can arguably now be placed in the pantheon of major ‘model’ systems. Their phylogenetic position as a sister group to the chordates provides insights into deuterostome origins, but at the same time they have made many direct contributions to our understanding of developmental mechanisms outside of any evolutionary context. Others, such as the cnidarian Nematostella, have risen to prominence relatively recently.Starting about two years ago, Development began to publish a series of Primer articles under the banner ‘Evolutionary crossroads in developmental biology’, which aimed to review advances that have come from particular organisms, or closely related groups of organisms, that lie outside of the major experimental systems. Ten of these Primers have been published so far, and the organisms covered include Dictyostelium discoideum [slime mold (Schaap, 2011)], Cnidaria [including both Hydra and Nematostella (Technau and Steele, 2011)], cyclostomes [lamprey and hagfish (Shimeld and Donoghue, 2012)], tunicates (Lemaire, 2011), sea urchins (McClay, 2011), Physcomitrella patens [moss (Prigge and Bezanilla, 2010)], amphioxus (Bertrand and Escriva, 2011), annelids [including Platynereis, leech and Capitella (Ferrier, 2012)], spiders (Hilbrant et al., 2012) and hemichordates [including the acorn worm Saccoglossus kowalevskii (Röttinger and Lowe, 2012)]. Each Primer provides an overview of the phylogenetic position of the species, the experimental tools and techniques that are available for studying these organisms, and the evolutionary questions that can be addressed using this organism. It is important to remember that none of these are living ancestors, although some are thought to retain particularly striking ancestral features. For example, present day amphioxus is not the ancestor to all chordates, but it can be well argued that its genome has retained many ancestral features. Nevertheless, when placed into a phylogenetic context, each of the species discussed in these Primers can be used to make deductions about various common ancestors that did once exist. In so doing, this gives us insights into macroevolutionary processes that have shaped animal, plant and fungal diversity. Each article also highlights the usefulness of each species from a purely developmental perspective, and illustrates the impressive progress that can be made by relatively small communities of researchers applying modern tools.Our world depends on maintaining biodiversity for its survival and, in a similar vein, the field of developmental biology is also strengthened by maintaining a wide diversity of experimental systems, each with its own unique and fascinating biology and place within the tree of life. This set of Primer articles is likely to expand as other non-model organisms are studied and developed, and will hopefully prove useful to those with a broad perspective on what it means to be a developmental biologist.

@article{doi101242dev085464,
    author = "Patel, Nipam H.",
    title = "Evolutionary crossroads in developmental biology",
    year = "2012",
    journal = "Development",
    abstract = "Currently, most developmental biologists work on one or more of a relatively small number of experimental systems, such as Arabidopsis thaliana, Drosophila melanogaster (fruit fly), Xenopus laevis (frog), Caenorhabditis elegans (nematode), Danio rerio (zebrafish) and Mus musculus (mouse), and their research is largely focused on understanding developmental mechanisms at the genetic, biochemical and molecular levels. This bias toward certain species is easily understood – analyses in these organisms is greatly facilitated by the availability of an array of genetic, molecular and genomic resources that have been generated over the years by large communities of scientists. However, the field of developmental biology has a long and colourful history of experimentation with a remarkably varied assemblage of creatures, and many crucial discoveries were first made in species that are now relatively understudied. Furthermore, some species possess certain remarkable attributes that have generated interest for a very long time. For example, the axolotl (Ambystoma mexicanum, a Mexican salamander) is considered to be the champion of regeneration among vertebrates, and although the number of people working with axolotls is relatively small, they remain a species of great interest because of the potential breakthroughs that might come from them.Another important reason that some developmental biologists have maintained interests in animals, plants and fungi outside of the main experimental systems comes from a desire to understand the evolution of development. Most of our model species are evolutionarily distant from one another, and in some cases certain aspects of their development are derived with respect to other closely related species. For example, the study of segmentation in Drosophila melanogaster has produced a multitude of remarkable insights into basic developmental mechanisms, but many of the well-understood steps in early patterning are atypical of the process of segmentation in arthropods as a whole. For this reason, developmental biologists have studied other arthropods, such as mosquitoes, beetles, crickets, grasshoppers, centipedes and spiders, to understand the diversity of developmental mechanisms at work in the process of segmentation. When placed into a phylogenetic framework, such comparative studies can also provide us with hypotheses as to how the process of segmentation has evolved within the arthropods and give us better insight into how segmentation is related between phyla.The interest in such comparative studies and their implications stretches back through the entire history of developmental biology. The important evolutionary insight that they provide has long been recognised; Charles Darwin even devotes an entire chapter of The Origin of Species to a discussion of how development can help unravel the pattern and process of evolution. In more recent decades, genetics has proven to be a key bridge between developmental and evolutionary biologists. Although developmental and evolutionary geneticists often seem to speak very different languages, there is an increasing awareness of what one can contribute to the other, and a synthesis between the two has begun to yield remarkable insights in many cases. Furthermore, the ability to work with an increasing diversity of species has received a major boost owing to several technical breakthroughs. These include the genomic tools that allow us to quickly compare the genes that are shared and not shared between species, techniques such as in situ hybridisation, microarrays and transcriptome sequencing that facilitate comparative studies of the timing and pattern of gene expression and, finally, new tools for functional analyses that take advantage of breakthroughs in RNAi and transgenic technology.For these reasons, research into the development of many species outside of the major experimental systems has flourished in recent years. Some, such as sea urchins, have indeed been studied for a very long time and can arguably now be placed in the pantheon of major ‘model’ systems. Their phylogenetic position as a sister group to the chordates provides insights into deuterostome origins, but at the same time they have made many direct contributions to our understanding of developmental mechanisms outside of any evolutionary context. Others, such as the cnidarian Nematostella, have risen to prominence relatively recently.Starting about two years ago, Development began to publish a series of Primer articles under the banner ‘Evolutionary crossroads in developmental biology’, which aimed to review advances that have come from particular organisms, or closely related groups of organisms, that lie outside of the major experimental systems. Ten of these Primers have been published so far, and the organisms covered include Dictyostelium discoideum [slime mold (Schaap, 2011)], Cnidaria [including both Hydra and Nematostella (Technau and Steele, 2011)], cyclostomes [lamprey and hagfish (Shimeld and Donoghue, 2012)], tunicates (Lemaire, 2011), sea urchins (McClay, 2011), Physcomitrella patens [moss (Prigge and Bezanilla, 2010)], amphioxus (Bertrand and Escriva, 2011), annelids [including Platynereis, leech and Capitella (Ferrier, 2012)], spiders (Hilbrant et al., 2012) and hemichordates [including the acorn worm Saccoglossus kowalevskii (Röttinger and Lowe, 2012)]. Each Primer provides an overview of the phylogenetic position of the species, the experimental tools and techniques that are available for studying these organisms, and the evolutionary questions that can be addressed using this organism. It is important to remember that none of these are living ancestors, although some are thought to retain particularly striking ancestral features. For example, present day amphioxus is not the ancestor to all chordates, but it can be well argued that its genome has retained many ancestral features. Nevertheless, when placed into a phylogenetic context, each of the species discussed in these Primers can be used to make deductions about various common ancestors that did once exist. In so doing, this gives us insights into macroevolutionary processes that have shaped animal, plant and fungal diversity. Each article also highlights the usefulness of each species from a purely developmental perspective, and illustrates the impressive progress that can be made by relatively small communities of researchers applying modern tools.Our world depends on maintaining biodiversity for its survival and, in a similar vein, the field of developmental biology is also strengthened by maintaining a wide diversity of experimental systems, each with its own unique and fascinating biology and place within the tree of life. This set of Primer articles is likely to expand as other non-model organisms are studied and developed, and will hopefully prove useful to those with a broad perspective on what it means to be a developmental biologist.",
    url = "https://doi.org/10.1242/dev.085464",
    doi = "10.1242/dev.085464",
    openalex = "W2011026922",
    references = "dilly1973the, doi101002dvg20395, doi101002jezb21172, doi101002jmor10533, doi101002jmor10868, doi1010079783642866593, doi101007bf00289234, doi101016jydbio200407010, doi101016jydbio201005016, doi101016s0091679x04740091, doi10103835049541, doi101038nature04336, doi101038nature05874, doi101038nature06614, doi101038nature06967, doi101093bioinformaticsbtg180, doi101093molbevmsj055, doi101098rstb19580007, doi101111j146363951988tb00906x, doi101126science1080049, doi101126science1150646, doi101139z04190, doi101186147121487127, doi101242dev066712, doi101371journalpone0000206, doi1023071541578, doi1023073227024, gonzalez2009the, openalexw564391913"
}

The Phylum Chordata includes three groups—Vertebrata, Tunicata, and Cephalochordata. In cephalochordates, commonly called amphioxus or lancelets, which are basal in the Chordata, the eggs are small and relatively non‐yolky. As in vertebrates, cleavage is indeterminate with cell fates determined gradually as development proceeds. The oocytes are attached to the ovarian follicle at the animal pole, where the oocyte nucleus is located. The cytoplasm at the opposite side of the egg, the vegetal pole, contains the future germ plasm or pole plasm, which includes determinants of the germline. After fertilization, additional asymmetries are established by movements of the egg and sperm nuclei, resulting in a concentration of mitochondria at one side of the animal hemisphere. This may be related to establishment of the dorsal/ventral axis. Patterning along the embryonic axes is mediated by secreted signaling proteins. Dorsal identity is specified by Nodal/Vg1 signaling, while during the gastrula stage, opposition between Nodal/Vg1 and BMP signaling establishes dorsal/anterior (i.e., head) and ventral/posterior (i.e., trunk/tail) identities, respectively. Wnt/ β ‐catenin signaling specifies posterior identity while retinoic acid signaling specifies positions along the anterior/posterior axis. These signals are further modulated by a number of secreted antagonists. This fundamental patterning mechanism is conserved, with some modifications, in vertebrates. WIREs Dev Biol 2012, 1:167–183. doi: 10.1002/wdev.11 This article is categorized under: Signaling Pathways > Global Signaling Mechanisms Early Embryonic Development > Fertilization to Gastrulation Early Embryonic Development > Gastrulation and Neurulation Comparative Development and Evolution > Body Plan Evolution

@article{holland2012early,
    author = "Holland, Linda Z. and Onai, Takayuki",
    title = "Early development of cephalochordates (amphioxus)",
    year = "2012",
    journal = "WIREs Developmental Biology",
    abstract = "The Phylum Chordata includes three groups—Vertebrata, Tunicata, and Cephalochordata. In cephalochordates, commonly called amphioxus or lancelets, which are basal in the Chordata, the eggs are small and relatively non‐yolky. As in vertebrates, cleavage is indeterminate with cell fates determined gradually as development proceeds. The oocytes are attached to the ovarian follicle at the animal pole, where the oocyte nucleus is located. The cytoplasm at the opposite side of the egg, the vegetal pole, contains the future germ plasm or pole plasm, which includes determinants of the germline. After fertilization, additional asymmetries are established by movements of the egg and sperm nuclei, resulting in a concentration of mitochondria at one side of the animal hemisphere. This may be related to establishment of the dorsal/ventral axis. Patterning along the embryonic axes is mediated by secreted signaling proteins. Dorsal identity is specified by Nodal/Vg1 signaling, while during the gastrula stage, opposition between Nodal/Vg1 and BMP signaling establishes dorsal/anterior (i.e., head) and ventral/posterior (i.e., trunk/tail) identities, respectively. Wnt/ β ‐catenin signaling specifies posterior identity while retinoic acid signaling specifies positions along the anterior/posterior axis. These signals are further modulated by a number of secreted antagonists. This fundamental patterning mechanism is conserved, with some modifications, in vertebrates. WIREs Dev Biol 2012, 1:167–183. doi: 10.1002/wdev.11 This article is categorized under: Signaling Pathways > Global Signaling Mechanisms Early Embryonic Development > Fertilization to Gastrulation Early Embryonic Development > Gastrulation and Neurulation Comparative Development and Evolution > Body Plan Evolution",
    url = "https://doi.org/10.1002/wdev.11",
    doi = "10.1002/wdev.11",
    number = "2",
    openalex = "W1997675270",
    pages = "167-183",
    volume = "1",
    references = "doi101007s000180100268z, doi101016jdevcel200906016, doi10103811932, doi10103817820, doi101038nature02006, doi101038nrc2780, doi101038nrm2654, doi101093cvrcvq086, doi101093jbmvq121, doi101111j14636395200800379x, doi101161circresaha110219840, holland1991the"
}