Skip to main content Accessibility help
Hostname: page-component-77c89778f8-gq7q9 Total loading time: 0 Render date: 2024-07-24T16:01:07.425Z Has data issue: false hasContentIssue false

2 - Comparative Development of Cyclostomes

Published online by Cambridge University Press:  31 December 2018

Zerina Johanson
Natural History Museum, London
Charlie Underwood
Birkbeck, University of London
Martha Richter
Natural History Museum, London
Get access


We present a concise summary of embryonic development in hagfish and lampreys. With the rise of evolutionary developmental approaches, the rapidly advancing frontier of research on these jawless vertebrates has revealed a number of developmental traits common among cyclostomes (e.g., distribution of trigeminal neural crest cells) and even vertebrates (e.g., brain regionalization), as well as an array of lineage-specific features (e.g., sclerotome differentiations, shift of branchial pouches). In addition to the wealth of data on gene expression patterns, techniques such as reporter expression assay, cell labeling, and functional analysis using morpholino and CRISPR are beginning to identify patterns and mechanisms of tissue inductions and interactions underlying the cyclostome body plan. However, it remains challenging to trace developmental traits to a common ancestry because each of the three living vertebrate lineages (hagfish, lampreys, gnathostomes) and their invertebrate outgroups sits atop a long branch. Fossils and embryos can complement each other to reinforce inferences about stem conditions and, with recent advances, such a reciprocal approach may be within our reach.

Publisher: Cambridge University Press
Print publication year: 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


Abitua, PB, Gainous, TB, Kaczmarczyk, AN, Winchell, CJ, Hudson, C, Kamata, K, Nakagawa, M, Tsuda, M, Kusakabe, TG, Levine, M. 2015. The pre-vertebrate origins of neurogenic placodes. Nature 524:462465.CrossRefGoogle ScholarPubMed
Ahlborn, F. 1883. Untersuchungen über das Gehirn der Petromyzonten. Z Für Wiss Zool 39:191294.Google Scholar
Ahlborn, F. 1884. Über den Ursprung und Austritt der Hirnnerven von Petromyzon. Z Für Wiss Zool 40:286308.Google Scholar
Alcock, R. 1898. The peripheral distribution of the cranial nerves of ammocoetes. J Anat Physiol 33:131.Google ScholarPubMed
Allen, WF. 1916. Studies on the spinal cord and medulla of cyclostomes with special reference to the formation and expansion of the roof plate and the flattening of the spinal cord. J Comp Neurol 26:977.Google Scholar
Ayers, H, Worthington, J. 1908. The finer anatomy of the brain of Bdellostoma dombeyi. I. The acustico-lateral system. Am J Anat 8:116.Google Scholar
Calberla, E. 1877. Zur Entwicklung des Medullarrohres und der Chorda dorsalis der Teleostier und der Petromyzonten. Morphol Jahrb Leipz 3:227270.Google Scholar
Cattell, M, Lai, S, Cerny, R, Medeiros, DM. 2011. A new mechanistic scenario for the origin and evolution of vertebrate cartilage. PLoS ONE 6:e22474.Google Scholar
Cerny, R, Cattell, M, Sauka-Spengler, T, Bronner-Fraser, M, Yu, F, Medeiros, DM. 2010. Evidence for the prepattern/cooption model of vertebrate jaw evolution. Proc Natl Acad Sci 107:1726217267.CrossRefGoogle ScholarPubMed
Clark, AJ, Summers, AP. 2007. Morphology and kinematics of feeding in hagfish: Possible functional advantages of jaws. J Exp Biol 210:38973909.Google Scholar
Clements, T, Dolocan, A, Martin, P, Purnell, MA, Vinther, J, Gabbott, SE. 2016. The eyes of Tullimonstrum reveal a vertebrate affinity. Nature 532:500503.Google Scholar
Cohn, MJ. 2002. Lamprey Hox genes and the origin of jaws. Nature 416:386387.CrossRefGoogle ScholarPubMed
Cole, FJ. 1905. A monograph on the general morphology of the myxinoid fishes, based on a study of Myxine. I. The anatomy of the skeleton. Transactions of the Royal Society of Edinburgh 41, 749791.Google Scholar
Cole, AG, Hall, BK. 2004. The nature and significance of invertebrate cartilages revisited: Distribution and histology of cartilage and cartilage-like tissues within the Metazoa. Zoology 107:261273.CrossRefGoogle ScholarPubMed
Conel, JL. 1929. The development of the brain of Bdellostoma stouti. I. External growth changes. J Comp Neurol 47:343403.Google Scholar
Conel, JL. 1931. The development of the brain of Bdellostoma stouti. II. Internal growth changes. J Comp Neurol 52:365499.Google Scholar
Conel, JL. 1942. The origin of the neural crest. J Comp Neurol 76:191215.Google Scholar
Conway Morris, S, Caron, J-B. 2014. A primitive fish from the Cambrian of North America. Nature 512:419422.Google Scholar
Cori, CI. 1906. Das Blutgefäßsystem des jungen Ammocoetes. Arb Aus Den Zool Instituten Univ Wien 16:217312.Google Scholar
Damas, H. 1935. Contribution à l’étude de la metamorphose de la tête de la lamproie. Arch Biol Paris 46:171227.Google Scholar
Damas, H. 1942. Le développement de la tête de la lamproie (Lampetra fluviatilis L.). Ann Société R Zool Belg 73:201211.Google Scholar
Damas, H. 1944. Recherches sur le dévelopment de Lampetra fluviatilis L. Contribution à l’étude de la cephalogénèse des vertébrés. Arch Biol Paris 55:1289.Google Scholar
Damas, H. 1948. L’influence de la lumière sur la segmentation et la gastrulation chez Lampetra fluviatilis. Bull Société R Sci Liège 7–10:286292.Google Scholar
Damas, H. 1951. Observations sur le développement des ganglions crâniens chez Lampetra fluviatillis (L.). Arch Biol Paris 62:6595.Google Scholar
Daniel, JF. 1934. The circulation of blood in ammocoetes. Univ Calif Publ Zool 39:311340.Google Scholar
Dean, B. 1898. On the development of the Californian hagfish, Bdellostoma stouti. Q J Microsc Sci 40:269279.Google Scholar
Dean, B. 1899. On the embryology of Bdellostoma stouti. A general account of myxinoid development from the egg and segmentation to hatching. In: Festschrift zum 70ten Geburststag Carl von Kupffer. Jena: Gustav Fischer Verlag. pp. 220276.Google Scholar
Docker, MF, Beamish, FWH. 1994. Age, growth, and sex ratio among populations of least brook lamprey, Lampetra aepyptera, larvae: An argument for environmental sex determination. In: Balon, EK, Bruton, MN, Noakes, DLG, editors. Women in Ichthyology: An Anthology in Honour of ET. Ro and Genie Springer Netherlands. pp. 191205.Google Scholar
Doflein, F. 1898. Bericht über eine wissenschaftliche Reise nach Californien. Sitzungsber Gesellsch Morph Physiol Münch 14:105118.Google Scholar
Dohrn, A. 1886. Studien zur Urgeschichte des Wirbelthierkorpers. VII. Entstehung und differenzirung des zungenbein – und kiefer – apparates de Selachier. VIII. Die thyroidea bei Petromyzon, Amphioxus und Tunicaten. Mitth Aus Zool Stn Zu Naepel 6:192.Google Scholar
Dudgeon, CL, Coulton, L, Bone, R, Ovenden, JR, Thomas, S. 2017. Switch from sexual to parthenogenetic reproduction in a zebra shark. Sci Rep 7:40537.Google Scholar
Feldheim, KA, Clews, A, Henningsen, A, Todorov, L, McDermott, C, Meyers, M, Bradley, J, Pulver, A, Anderson, E, Marshall, A. 2017. Multiple births by a captive swellshark Cephaloscyllium ventriosum via facultative parthenogenesis. J Fish Biol 90:10471053.Google Scholar
Fernholm, B. 1969. A third embryo of Myxine: Considerations on hypophysial ontogeny and phylogeny. Acta Zool 50:169177.Google Scholar
Freud, S. 1877. Über den Ursprung der hinteren Nervenwurzeln im Rückenmarke von Ammocötes (Petromyzon planeri). Akad Wiss Wien Sitzungsberichte Math-Naturwissenschaftliche Kl 3 Abt 75:1527.Google Scholar
Freud, S. 1878. Über Spinalganglien und Rückenmark des Petromyzon. Akad Wiss Wien Sitzungsberichte Math-Naturwissenschaftliche Kl 3 Abt 78:81167.Google Scholar
Fujimoto, S, Oisi, Y, Kuraku, S, Ota, KG, Kuratani, S. 2013. Non-parsimonious evolution of hagfish Dlx genes. BMC Evol Biol 13:15.CrossRefGoogle ScholarPubMed
Gans, C, Northcutt, RG. 1983. Neural crest and the origin of vertebrates: A new head. Science 220:268273.Google Scholar
Glaesner, L. 1910. Studien zur Entwicklungsgeschichte von Petromyzon fluviatilis. Zool Jahrb Anat 24:139190.Google Scholar
Goette, A. 1890. Entwicklungsgeschichte des Flussneunauges, Petromyzon fluviatilis. Leipzig: L Voss.Google Scholar
Gorbman, A. 1983. Early development of the hagfish pituitary gland: Evidence for the endodermal origin of the adenohypophysis. Am Zool 23:639654.Google Scholar
Gorbman, A, Tamarin, A. 1985. Early development of oral, olfactory and adenohypophyseal structures of agnathans and its evolutionary implications. In: Foreman, RE, Gorbman, A, Dodd, JM, Olsson, R, editors. Evolutionary Biology of Primitive Fishes. Springer. pp. 165185.Google Scholar
Green, SA, Simoes-Costa, M, Bronner, ME. 2015. Evolution of vertebrates as viewed from the crest. Nature 520:474482.Google Scholar
Green, SA, Uy, BR, Bronner, ME. 2017. Ancient evolutionary origin of vertebrate enteric neurons from trunk-derived neural crest. Nature 544:8891.Google Scholar
Griffith, RW, Thomson, KS. 1973. Latimeria chalumnae: Reproduction and conservation. Nature 242:617618.Google Scholar
Häming, D, Simoes-Costa, M, Uy, B, Valencia, J, Sauka-Spengler, T, Bronner-Fraser, M. 2011. Expression of sympathetic nervous system genes in lamprey suggests their recruitment for specification of a new vertebrate feature. PLOS ONE 6:e26543.Google Scholar
Hammond, KL, Baxendale, S, McCauley, DW, Ingham, PW, Whitfield, TT. 2009. Expression of patched, prdm1 and engrailed in the lamprey somite reveals conserved responses to Hedgehog signaling. Evol Dev 11:2740.Google Scholar
Hammond, KL, Whitfield, TT. 2006. The developing lamprey ear closely resembles the zebrafish otic vesicle: otx1 expression can account for all major patterning differences. Development 133:13471357.Google Scholar
Hardisty, MW. 1981. The skeleton. In: Hardisty, MW, Potter, IC, editors. The Biology of Lampreys. New York: Academic Press. pp. 118124.Google Scholar
Hasse, C. 1893. Die Entwicklung der wirbelsäule der cyclostomen. Z Für Wiss Zool 57:290305.Google Scholar
Hatta, S. 1897. Contributions to the morphology of Cyclostomata. I. On the formation of the heart in Petromyzon. J Coll Sci Imp Univ Tokyo 10:225237.Google Scholar
Hatta, S. 1900. Contributions to the morphology of Cyclostomata. II. The development of pronephros and segmental duct in Petromyzon. J Coll Sci Imp Univ Tokyo 13:311425.Google Scholar
Hatta, S. 1907. On the gastrulation in Petromyzon. J Coll Sci Imp Univ Tokyo 21:144.Google Scholar
Hatta, S. 1915. The fate of the peristomal mesoderm and the tail in Petromyzon. Annot Zool Jpn 9:4962.Google Scholar
Hatta, S. 1923. Über die entwicklung des gefäßsytems des neunauges, Lampetra mitsukurii Hatta. Zool Jahrb Anat 44:1264.Google Scholar
Higashiyama, H, Hirasawa, T, Oisi, Y, Sugahara, F, Hyodo, S, Kanai, Y, Kuratani, S. 2016. On the vagal cardiac nerves, with special reference to the early evolution of the head–trunk interface. J Morphol 277:11461158.Google Scholar
Hirasawa, T, Oisi, Y, Kuratani, S. 2016. Palaeospondylus as a primitive hagfish. Zool Lett 2:20.Google Scholar
Holland, ND, Holland, LZ, Honma, Y, Fujii, T. 1993. Engrailed expression during development of a lamprey, Lampetra japonica: A possible clue to homologies between agnathan and gnathostome muscles of the mandibular arch. Dev Growth Differ 35:153160.Google Scholar
Holland, PWH. 2015. Did homeobox gene duplications contribute to the Cambrian explosion? Zool Lett 1:1.Google Scholar
Holmgren, N. 1946. On two embryos of Myxine glutinosa. Acta Zool 27:190.Google Scholar
Horigome, N, Myojin, M, Ueki, T, Hirano, S, Aizawa, S, Kuratani, S. 1999. Development of cephalic neural crest cells in embryos of Lampetra japonica, with special reference to the evolution of the jaw. Dev Biol 207:287308.Google Scholar
Jandzik, D, Garnett, AT, Square, TA, Cattell, MV, Yu, J-K, Medeiros, DM. 2015. Evolution of the new vertebrate head by co-option of an ancient chordate skeletal tissue. Nature 518:534537.Google Scholar
Jandzik, D, Hawkins, MB, Cattell, MV, Cerny, R, Square, TA, Medeiros, DM. 2014. Roles for FGF in lamprey pharyngeal pouch formation and skeletogenesis highlight ancestral functions in the vertebrate head. Development 141:629638.Google Scholar
Janvier, P. 1996. Early Vertebrates. Oxford: Clarendon Press.CrossRefGoogle Scholar
Janvier, P, Arsenault, M. 2007. The anatomy of Euphanerops longaevus Woodward, 1900, an anaspid-like jawless vertebrate from the Upper Devonian of Miguasha, Quebec, Canada. Geodiversitas 29:143216.Google Scholar
Johanson, Z, Kearsley, A, den Blaauwen, J, Newman, M, Smith, MM. 2010. No bones about it: An enigmatic Devonian fossil reveals a new skeletal framework – A potential role of loss of gene regulation. Semin Cell Dev Biol 21:414423.Google Scholar
Johanson, Z, Kearsley, A, den Blaauwen, J, Newman, M, Smith, MM. 2012. Ontogenetic development of an exceptionally preserved Devonian cartilaginous skeleton. J Exp Zool B Mol Dev Evol 318B:5058.Google Scholar
Johanson, Z, Smith, M, Sanchez, S, Senden, T, Trinajstic, K, Pfaff, C. 2017. Questioning hagfish affinities of the enigmatic Devonian vertebrate Palaeospondylus. Royal Society Open Science, 4(7):170214.Google Scholar
Johnels, AG. 1948. On the development and morphology of the skeleton of the head of Petromyzon. Acta Zool 29:139279.Google Scholar
Johnston, JB. 1905. The cranial nerve components of Petromyzon. Morphol Jahrb Leipz 34:149203.Google Scholar
Julin, C. 1887. Des origines de l’aorta et des carotides chez les poissons Cyclostomes. Anat Anz 1887:228238.Google Scholar
Kano, S, Xiao, J-H, Osório, J, Ekker, M, Hadzhiev, Y, Müller, F, Casane, D, Magdelenat, G, Rétaux, S. 2010. Two lamprey hedgehog genes share non-coding regulatory sequences and expression patterns with gnathostome hedgehogs. PLOS ONE 5:e13332.Google Scholar
Keibel, F. 1906. Die entwickelung der äusseren körperform der wirbeltierembryonen, insbesondere der menschlichen embryonen aus den ersten 2 monaten. Jena: Gustav Fischer.Google Scholar
Keibel, F. 1928. Beiträge zur anatomie, zur entwicklungsgeschichte und zur stammesgeschichte der sehorgane der Cyklostomen. Z Mikrosk Anat Forsch 12:391456.Google Scholar
Keiser, W. 1914. Untersuchungen über die erste anlage des herzens, der beiden längsgefäßstämme und des blutes bei embryonen von Petromyzon planeri. Vierteljahrsschr Naturforschenden Ges Zür 58:269275.Google Scholar
Kieckebusch, H-H. 1928. Bau und entwicklung der schildrüse bei neunaugenlarven (Lampetra fluviatilis L. und Lampetra planeri Bl.). Z Für Morphol Ökol Tiere 11:247360.Google Scholar
Kimmel, CB, Miller, T. C, Keynes, J. R. 2001. Neural crest patterning and the evolution of the jaw. J Anat 199:105119.Google Scholar
Kohrs, DG. 2013. Hopkins Seaside Laboratory of Natural History. Pacific Grove: Hopkins Marine Station.Google Scholar
Kokubo, N, Matsuura, M, Onimaru, K, Tiecke, E, Kuraku, S, Kuratani, S, Tanaka, M. 2010. Mechanisms of heart development in the Japanese lamprey, Lethenteron japonicum. Evol Dev 12:3444.Google Scholar
Koltzoff, NK. 1901. Entwicklungsgeschichte des kopfes von Petromyzon planeri. Bull Société Nat Mosc 15:259589.Google Scholar
Kuraku, S. 2013. Impact of asymmetric gene repertoire between cyclostomes and gnathostomes. Semin Cell Dev Biol 24:119127.Google Scholar
Kuraku, S, Meyer, A, Kuratani, S. 2009. Timing of genome duplications relative to the origin of the vertebrates: Did cyclostomes diverge before or after? Mol Biol Evol 26:4759.Google Scholar
Kuraku, S, Takio, Y, Sugahara, F, Takechi, M, Kuratani, S. 2010. Evolution of oropharyngeal patterning mechanisms involving Dlx and endothelins in vertebrates. Dev Biol 341:315323.Google Scholar
Kuratani, S, Adachi, N, Wada, N, Oisi, Y, Sugahara, F. 2013. Developmental and evolutionary significance of the mandibular arch and prechordal/premandibular cranium in vertebrates: Revising the heterotopy scenario of gnathostome jaw evolution. J Anat 222:4155.Google Scholar
Kuratani, S, Horigome, N, Hirano, S. 1999. Developmental morphology of the head mesoderm and reevaluation of segmental theories of the vertebrate head: Evidence from embryos of an agnathan vertebrate, Lampetra japonica. Dev Biol 210:381400.Google Scholar
Kuratani, S, Murakami, Y, Nobusada, Y, Kusakabe, R, Hirano, S. 2004. Developmental fate of the mandibular mesoderm in the lamprey, Lethenteron japonicum: Comparative morphology and development of the gnathostome jaw with special reference to the nature of the trabecula cranii. J Exp Zool B Mol Dev Evol 302B:458468.Google Scholar
Kuratani, S, Nobusada, Y, Horigome, N, Shigetani, Y. 2001. Embryology of the lamprey and evolution of the vertebrate jaw: Insights from molecular and developmental perspectives. Philos Trans R Soc Lond Ser B 356:16151632.Google Scholar
Kuratani, S, Oisi, Y, Ota, KG. 2016. Evolution of the vertebrate cranium: Viewed from hagfish developmental studies. Zool Sci 33:229238.Google Scholar
Kuratani, S, Ueki, T, Aizawa, S, Hirano, S. 1997. Peripheral development of cranial nerves in a cyclostome, Lampetra japonica: Morphological distribution of nerve branches and the vertebrate body plan. J Comp Neurol 384:483500.Google Scholar
Kusakabe, R, Kuraku, S, Kuratani, S. 2011. Expression and interaction of muscle-related genes in the lamprey imply the evolutionary scenario for vertebrate skeletal muscle, in association with the acquisition of the neck and fins. Dev Biol 350:217227.Google Scholar
Kusakabe, R, Kuratani, S. 2005. Evolution and developmental patterning of the vertebrate skeletal muscles: Perspectives from the lamprey. Dev Dyn 234:824834.Google Scholar
Kusakabe, R, Kuratani, S. 2007. Evolutionary perspectives from development of mesodermal components in the lamprey. Dev Dyn 236:24102420.Google Scholar
Kusakabe, R, Takechi, M, Tochinai, S, Kuratani, S. 2004. Lamprey contractile protein genes mark different populations of skeletal muscles during development. J Exp Zool B Mol Dev Evol 302B:121133.Google Scholar
Kusakabe, R, Tochinai, S, Kuratani, S. 2003. Expression of foreign genes in lamprey embryos: An approach to study evolutionary changes in gene regulation. J Exp Zool B Mol Dev Evol 296B:8797.Google Scholar
Lakiza, O, Miller, S, Bunce, A, Lee, EM-J, McCauley, DW. 2011. SoxE gene duplication and development of the lamprey branchial skeleton: Insights into development and evolution of the neural crest. Dev Biol 359:149161.Google Scholar
Langille, RM, Hall, BK. 1988. Role of the neural crest in development of the trabeculae and branchial arches in embryonic sea lamprey, Petromyzon marinus (L). Development 102:301310.Google Scholar
Lavett Smith, C, Rand, CS, Schaeffer, B, Atz, JW. 1975. Latimeria, the living coelacanth, is ovoviviparous. Science 190:11051106.Google Scholar
Lee, EM, Yuan, T, Ballim, RD, Nguyen, K, Kelsh, RN, Medeiros, DM, McCauley, DW. 2016. Functional constraints on SoxE proteins in neural crest development: The importance of differential expression for evolution of protein activity. Dev Biol 418:166178.Google Scholar
Lee, S-H, Bédard, O, Buchtová, M, Fu, K, Richman, JM. 2004. A new origin for the maxillary jaw. Dev Biol 276:207224.Google Scholar
Lee, S-H, Fu, KK, Hui, JN, Richman, JM. 2001. Noggin and retinoic acid transform the identity of avian facial prominences. Nature 414:909912.Google Scholar
Lindström, T. 1949. On the cranial nerves of the cyclostomes with special reference to n. trigeminus. Acta Zool 30:315458.Google Scholar
Marinelli, W, Strenger, A. 1954. Vergleichende Anatomie und Morphologie der Wirbeltiere. I Lieferung. Petromyzon marinus (L). Vienna: Franz Deuticke Wien.Google Scholar
Martin, WM, Bumm, LA, McCauley, DW. 2009. Development of the viscerocranial skeleton during embryogenesis of the sea lamprey, Petromyzon marinus. Dev Dyn 238:31263138.Google Scholar
Martini, F, Heiser, JB, Lesser, MP. 1998. A population profile for Atlantic hagfish, Myxine glutinosa (L.), in the Gulf of Maine. I: Morphometrics and reproductive state. Oceanogr Lit Rev 1:148.Google Scholar
Martini, FH, Beulig, A. 2013. Morphometics and gonadal development of the hagfish Eptatretus cirrhatus in New Zealand. PLOS ONE 8:e78740.Google Scholar
Matsuura, M, Nishihara, H, Onimaru, K, Kokubo, N, Kuraku, S, Kusakabe, R, Okada, N, Kuratani, S, Tanaka, M. 2008. Identification of four Engrailed genes in the Japanese lamprey, Lethenteron japonicum. Dev Dyn 237:15811589.Google Scholar
McCauley, DW. 2008. SoxE, Type II collagen, and evolution of the chondrogenic neural crest. Zoological Science 25: 982989.Google Scholar
McCauley, DW, Bronner-Fraser, M. 2002. Conservation of Pax gene expression in ectodermal placodes of the lamprey. Gene 287:129139.Google Scholar
McCauley, DW, Bronner-Fraser, M. 2003. Neural crest contributions to the lamprey head. Development 130:23172327.Google Scholar
McCauley, DW, Bronner-Fraser, M. 2004. Conservation and divergence of BMP2/4 genes in the lamprey: Expression and phylogenetic analysis suggest a single ancestral vertebrate gene. Evol Dev 6:411422.Google Scholar
McCauley, DW, Bronner-Fraser, M. 2006. Importance of SoxE in neural crest development and the evolution of the pharynx. Nature 441:750752.Google Scholar
McCoy, VE, Saupe, EE, Lamsdell, JC, Tarhan, LG, McMahon, S, Lidgard, S, Mayer, P, Whalen, CD, Soriano, C, Finney, L, Vogt, S, Clark, EG, Anderson, RP, Petermann, H, Locatelli, ER, Briggs, DEG. 2016. The ‘Tully monster’ is a vertebrate. Nature 532:496499.Google Scholar
Medeiros, DM, Crump, JG. 2012. New perspectives on pharyngeal dorsoventral patterning in development and evolution of the vertebrate jaw. Dev Biol 371:121135.CrossRefGoogle ScholarPubMed
Meulemans, D, Bronner-Fraser, M. 2002. Amphioxus and lamprey AP-2 genes: Implications for neural crest evolution and migration patterns. Development 129:49534962.Google Scholar
Meulemans, D, McCauley, D, Bronner-Fraser, M. 2003. Id expression in amphioxus and lamprey highlights the role of gene cooption during neural crest evolution. Dev Biol 264:430442.Google Scholar
Miyashita, T. 2012. Comparative Analysis of the Anatomy of the Myxinoidea and the Ancestry of Early Vertebrate Lineages. Unpublished M.Sc. thesis. Edmonton: University of Alberta.Google Scholar
Miyashita, T, Coates, MI. 2016. The embryology of hagfishes and the evolution and development of vertebrates. In: Edwards, SL, Goss, GG, editors. Hagfish Biology. Boca Raton: CRC Press. pp. 95127.Google Scholar
Modrell, MS, Hockman, D, Uy, B, Buckley, D, Sauka-Spengler, T, Bronner, ME, Baker, CVH. 2014. A fate-map for cranial sensory ganglia in the sea lamprey. Dev Biol 385:405416.Google Scholar
Müller, A. 1856. Über die entwicklung der neunaugen. Arch Für Anat Physiol Wiss Med. 18: 298–301.Google Scholar
Murakami, Y, Ogasawara, M, Satoh, N, Sugahara, F, Myojin, M, Hirano, S, Kuratani, S. 2002. Compartments in the lamprey embryonic brain as revealed by regulatory gene expression and the distribution of reticulospinal neurons. Brain Res Bull 57:271275.Google Scholar
Murakami, Y, Ogasawara, M, Sugahara, F, Hirano, S, Satoh, N, Kuratani, S. 2001. Identification and expression of the lamprey Pax6 gene: Evolutionary origin of the segmented brain of vertebrates. Development 128:35213531.Google Scholar
Murakami, Y, Pasqualetti, M, Takio, Y, Hirano, S, Rijli, FM, Kuratani, S. 2004. Segmental development of reticulospinal and branchiomotor neurons in lamprey: Insights into the evolution of the vertebrate hindbrain. Development 131:983995.Google Scholar
Murakami, Y, Uchida, K, Rijli, FM, Kuratani, S. 2005. Evolution of the brain developmental plan: Insights from agnathans. Dev Biol 280:249259.Google Scholar
Myojin, M, Ueki, T, Sugahara, F, Murakami, Y, Shigetani, Y, Aizawa, S, Hirano, S, Kuratani, S. 2001. Isolation of Dlx and Emx gene cognates in an agnathan species, Lampetra japonica, and their expression patterns during embryonic and larval development: Conserved and diversified regulatory patterns of homeobox genes in vertebrate head evolution. J Exp Zool 291:6884.Google Scholar
Neidert, AH, Virupannavar, V, Hooker, GW, Langeland, JA. 2001. Lamprey Dlx genes and early vertebrate evolution. Proc Natl Acad Sci 98:16651670.Google Scholar
Nelson, JS, Grande, TC, Wilson, MVH. 2016. Fishes of the World. 5th edition. New York: Wiley.Google Scholar
Nestler, K. 1890. Anatomie und entwicklungsgeschichte von Petromyzon planeri. Arch Für Naturgeschichte 56:81112.Google Scholar
Neumayr, L. 1938. Die entwicklung des kopskelettes von Bdellostoma St. L. Arch Ital Anat E Embriologia 40:1222.Google Scholar
Newth, DR. 1950. Fate of the neural crest in lampreys. Nature 165:284284.Google Scholar
Newth, DR. 1951. Experiments on the neural crest of the lamprey embryo. J Exp Biol 28:247260.Google Scholar
Newth, DR. 1956. On the neural crest of the lamprey embryo. Development 4:358375.Google Scholar
Nuel, P. 1881. Quelques phases du développement du Petromyzon planeri. Arch Biol (Liege) 2:403454.Google Scholar
Ogasawara, M, Shigetani, Y, Hirano, S, Satoh, N, Kuratani, S. 2000. Pax1/Pax9-related genes in an agnathan vertebrate, Lampetra japonica: Expression pattern of LjPax9 implies sequential evolutionary events toward the gnathostome body plan. Dev Biol 223:399410.Google Scholar
Ogasawara, M, Shigetani, Y, Suzuki, S, Kuratani, S, Satoh, N. 2001. Expression of thyroid transcription factor-1 (TTF-1) gene in the ventral forebrain and endostyle of the agnathan vertebrate, Lampetra japonica. genesis 30:5158.Google Scholar
Ohtani, K, Yao, T, Kobayashi, M, Kusakabe, R, Kuratani, S, Wada, H. 2008. Expression of Sox and fibrillar collagen genes in lamprey larval chondrogenesis with implications for the evolution of vertebrate cartilage. J Exp Zool B Mol Dev Evol 310B:596607.Google Scholar
Oisi, Y, Fujimoto, S, Ota, KG, Kuratani, S. 2015. On the peculiar morphology and development of the hypoglossal, glossopharyngeal and vagus nerves and hypobranchial muscles in the hagfish. Zool Lett 1:6.Google Scholar
Oisi, Y, Ota, KG, Fujimoto, S, Kuratani, S. 2013a. Development of the chondrocranium in hagfishes, with special reference to the early evolution of vertebrates. Zool Sci 30:944961.Google Scholar
Oisi, Y, Ota, KG, Kuraku, S, Fujimoto, S, Kuratani, S. 2013b. Craniofacial development of hagfishes and the evolution of vertebrates. Nature 493:175180.Google Scholar
Okkelberg, P. 1921. The early history of the germ cells in the brook lamprey, Entosphenus wilderi (GAGE), up to and including the period of sex differentiation. J Morphol 35:1151.Google Scholar
Onimaru, K, Shoguchi, E, Kuratani, S, Tanaka, M. 2011. Development and evolution of the lateral plate mesoderm: Comparative analysis of amphioxus and lamprey with implications for the acquisition of paired fins. Dev Biol 359:124136.Google Scholar
Ota, KG, Fujimoto, S, Oisi, Y, Kuratani, S. 2011. Identification of vertebra-like elements and their possible differentiation from sclerotomes in the hagfish. Nat Commun 2:373.Google Scholar
Ota, KG, Fujimoto, S, Oisi, Y, Kuratani, S. 2013. Late development of hagfish vertebral elements. J Exp Zool B Mol Dev Evol 320:129139.Google Scholar
Ota, KG, Kuraku, S, Kuratani, S. 2007. Hagfish embryology with reference to the evolution of the neural crest. Nature 446:672675.Google Scholar
Ota, KG, Kuratani, S. 2006. The history of scientific endeavors towards understanding hagfish embryology. Zool Sci 23:403418.Google Scholar
Ota, KG, Kuratani, S. 2007. Cyclostome embryology and early evolutionary history of vertebrates. Integr Comp Biol 47:329337.Google Scholar
Ota, KG, Kuratani, S. 2008. Developmental biology of hagfishes, with a report on newly obtained embryos of the Japanese inshore hagfish, Eptatretus burgeri. Zool Sci 25:9991011.Google Scholar
Ota, KG, Kuratani, S. 2010. Expression pattern of two collagen type 2 α1 genes in the Japanese inshore hagfish (Eptatretus burgeri) with special reference to the evolution of cartilaginous tissue. J Exp Zool B Mol Dev Evol 314B:157165.Google Scholar
Owsjannikow, P. 1893. On the embryology of the river-lamprey. Ann Mag Nat Hist 11:3043.Google Scholar
Pani, AM, Mullarkey, EE, Aronowicz, J, Assimacopoulos, S, Grove, EA, Lowe, CJ. 2012. Ancient deuterostome origins of vertebrate brain signalling centres. Nature 483:289294.Google Scholar
Parker, HJ, Bronner, ME, Krumlauf, R. 2014. A Hox regulatory network of hindbrain segmentation is conserved to the base of vertebrates. Nature 514:490493.Google Scholar
Parker, HJ, Piccinelli, P, Sauka-Spengler, T, Bronner, M, Elgar, G. 2011. Ancient Pbx-Hox signatures define hundreds of vertebrate developmental enhancers. BMC Genomics 12:637.Google Scholar
Parker, HJ, Sauka-Spengler, T, Bronner, M, Elgar, G. 2014. A reporter assay in lamprey embryos reveals both functional conservation and elaboration of vertebrate enhancers. PLoS ONE 9:e85492.Google Scholar
Pascual-Anaya, J, Sato, I, Sugahara, F, Higuchi, S, Paps, J, Ren, Y, Takagi, W, Ruiz-Villalba, A, Ota, KG, Wang, W, Kuratani, S. 2018. Hagfish and lamprey Hox genes reveal conservation of temporal colinearity in vertebrates. Nature Ecology and Evolution, 2(5):859866.Google Scholar
Patzner, RA. 1998. Gonads and reproduction in hagfishes. In: Jørgensen, JM, Lomholt, JP, Weber, RE, Malte, H, editors. The Biology of Hagfishes London: Chapman. pp. 378395.Google Scholar
Piavis, GW. 1971. Embryology. In: Hardisty, MW, Potter, IC, editors. The Biology of Lampreys. Volume 1. New York: Academic Press. pp. 361400.Google Scholar
Price, G. 1896a. Zur ontogenie eines myxinoiden (Bdellostoma stouti Lockington). Sitzungsberichte Math Cl KB Akad Wiss Zu Münch 36:167174.Google Scholar
Price, G. 1896b. Some points in the development of a myxinoid (Bdellostoma stouti Lockington). Anat Anz 12:8186.Google Scholar
Price, G. 1896c. Development of the excretory organs of a myxinoid, Bdellostoma stoutii Lockington. Zool Jahrb Anat 10:205226.Google Scholar
Price, G. 1904. A further study of the development of the excretory organs in Bdellostoma stouti. Am J Anat 4:117138.Google Scholar
Renaud, CB. 2011. Lampreys of the World. An annotated and illustrated catalogue of lamprey species known to date. Rome: Food and Agriculture Organization of the United Nations.Google Scholar
Richman, JM, Lee, S-H. 2003. About face: Signals and genes controlling jaw patterning and identity in vertebrates. BioEssays 25:554568.Google Scholar
Ritchie, A. 1967. Ateleaspis tessellata Traquair, a non-cornuate cephalaspid from the Upper Silurian of Scotland. Zool J Linn Soc 47:6981.Google Scholar
Robson, P, Wright, GM, Keeley, FW. 2000. Distinct non-collagen based cartilages comprising the endoskeleton of the Atlantic hagfish, Myxine glutinosa. Anat Embryol (Berl) 202:281290.Google Scholar
Sallan, L, Giles, S, Sansom, RS, Clarke, JT, Johanson, Z, Sansom, IJ, Janvier, P. 2017. The ‘Tully Monster’ is not a vertebrate: Characters, convergence and taphonomy in Palaeozoic problematic animals. Palaeontology 60:149157.Google Scholar
Sasselli, V, Pachnis, V, Burns, AJ. 2012. The enteric nervous system. Dev Biol, Neural Crest 366:6473.Google Scholar
Sauka-Spengler, T, Le Mentec, C, Lepage, M, Mazan, S. 2002. Embryonic expression of Tbx1, a DiGeorge syndrome candidate gene, in the lamprey Lampetra fluviatilis. Gene Expr Patterns 2:99103.Google Scholar
Sauka-Spengler, T, Meulemans, D, Jones, M, Bronner-Fraser, M. 2007. Ancient evolutionary origin of the neural crest gene regulatory network. Dev Cell 13:405420.Google Scholar
Sauka-Spengler, T, Bronner-Fraser, M. 2008. A gene regulatory network orchestrates neural crest formation. Nature Reviews Molecular Cell Biology 9(7), 557568.Google Scholar
Schaffer, J. 1896. Über das knorpelige skelett van ammocoetes branchialis nebst bemerkungen über das knorpelgewebe im allgemeinen. Z Für Wiss Zool 61:606659.Google Scholar
Schalk, A. 1913. Die entwicklung des cranial-und visceralskeletts von Petromyzon fluviatilis. Arch Für Mikrosk Anat 83.Google Scholar
Schultze, MS. 1856. Die Entwickelungs-Geschichte von Petromyzon planeri. Haarlem: Loosjes.Google Scholar
Scott, WB. 1880. Vorläufige mittheilung über die entwickelungsgeschichte der Petromyzonten. Zool Anz 1880:443449.Google Scholar
Scott, WB. 1881. Preliminary account of the development of the lampreys. Q J Microsc Sci s2–21:146153.Google Scholar
Scott, WB. 1882. Beiträge zur entwicklungsgeschichte der Petromyzonten. Morphol Jahrb Leipz 7:101172.Google Scholar
Scott, WB. 1883. On the development of the pituitary body in Petromyzon, and the significance of that organ in other types. Science 2:184186.Google Scholar
Scott, WB. 1887. Notes on the development of Petromyzon. J Morphol 1:253310.Google Scholar
Sewertzoff, AN. 1913. Das visceralskelet der Cyclostomen. Anat Anz 82:280283.Google Scholar
Sewertzoff, AN. 1916. Études sur l’évolution des vertébrés inférieurs. I. Morphologie du squelette et de la musculature de le tête des Cyclostomes. Arch Russ Anat Histol Embryol 1:1104.Google Scholar
Shigetani, Y, Sugahara, F, Kawakami, Y, Murakami, Y, Hirano, S, Kuratani, S. 2002. Heterotopic shift of epithelial-mesenchymal interactions in vertebrate jaw evolution. Science 296:13161319.Google Scholar
Shipley, AE. 1885. On the formation of the mesoblast, and the persistence of the blastopore in the lamprey. Proc R Soc Lond 39:244248.Google Scholar
Shipley, AE. 1887. On some points in the development of Petromyzon fluviatilis. Q J Microsc Sci s2–27:325377.Google Scholar
Shu, D-G, Luo, H-L, Conway Morris, S, Zhang, X-L, Hu, S-X, Chen, L, Han, J, Zhu, M, Li, Y, Chen, L-Z. 1999. Lower Cambrian vertebrates from south China. Nature 402:4246.Google Scholar
Smith, JJ, Kuraku, S, Holt, C, Sauka-Spengler, T, Jiang, N, Campbell, MS, Yandell, MD, Manousaki, T, Meyer, A, Bloom, OE, Morgan, JR, Buxbaum, JD, Sachidanandam, R, Sims, C, Garruss, AS, Cook, M, Krumlauf, R, Wiedemann, LM, Sower, SA, Decatur, WA, Hall, JA, Amemiya, CT, Saha, NR, Buckley, KM, Rast, JP, Das, S, Hirano, M, McCurley, N, Guo, P, Rohner, N, Tabin, CJ, Piccinelli, P, Elgar, G, Ruffier, M, Aken, BL, Searle, SMJ, Muffato, M, Pignatelli, M, Herrero, J, Jones, M, Brown, CT, Chung-Davidson, Y-W, Nanlohy, KG, Libants, SV, Yeh, C-Y, McCauley, DW, Langeland, JA, Pancer, Z, Fritzsch, B, de Jong, PJ, Zhu, B, Fulton, LL, Theising, B, Flicek, P, Bronner, ME, Warren, WC, Clifton, SW, Wilson, RK, Li, W. 2013. Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat Genet 45:415421.Google Scholar
Smith, JJ, Timoshevskaya, N, Ye, C, Holt, C, Keinath, MC, Parker, HJ, Cook, ME, Hess, JE, Narum, SR, Lamanna, F, Kaessmann, H, Timoshevskiy, VA, Waterbury, CKM, Saraceno, C, Wiedemann, LM, Robb, SMC, Baker, C, Eichler, EE, Hockman, D, Sauka-Spengler, T, Yandell, M, Krumlauf, R, Elgar, G, Amemiya, CT. 2018. The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution. Nature Genetics 50:270277.Google Scholar
Sollas, WJ, Sollas, IBJ. 1904. An account of the Devonian fish, Palæospondylus gunni, Traquair. Philos Trans R Soc Lond Ser B Contain Pap Biol Character 196:267294.Google Scholar
Square, T, Jandzik, D, Cattell, M, Coe, A, Doherty, J, Meulemans Medeiros, D. 2015. A gene expression map of the larval Xenopus laevis head reveals developmental changes underlying the evolution of new skeletal elements. Developmental Biology 397: 293304.Google Scholar
Square, T, Jandzik, D, Cattell, M, Hansen, A, Medeiros, DM. 2016. Embryonic expression of endothelins and their receptors in lamprey and frog reveals stem vertebrate origins of complex Endothelin signaling. Sci Rep 6:34282.Google Scholar
Square, T, Jandzik, D, Romášek, M, Cerny, R, Medeiros, DM. 2017. The origin and diversification of the developmental mechanisms that pattern the vertebrate head skeleton. Dev Biol. 427:219–229.Google Scholar
Stockard, CR. 1906a. The development of the mouth and gills in Bdellostoma stouti. Am J Anat 5:481517.Google Scholar
Stockard, CR. 1906b. The development of the thyroid gland in Bdellostoma stoutii. Anat Anz 29:9199.Google Scholar
Stolfi, A, Ryan, K, Meinertzhagen, IA, Christiaen, L. 2015. Migratory neuronal progenitors arise from the neural plate borders in tunicates. Nature 527:371374.Google Scholar
Strahan, R. 1958. The velum and the respiratory current of Myxine. Acta Zool 39:227240.Google Scholar
Sugahara, F, Aota, S, Kuraku, S, Murakami, Y, Takio-Ogawa, Y, Hirano, S, Kuratani, S. 2011. Involvement of Hedgehog and FGF signalling in the lamprey telencephalon: Evolution of regionalization and dorsoventral patterning of the vertebrate forebrain. Development 138:12171226.Google Scholar
Sugahara, F, Murakami, Y, Adachi, N, Kuratani, S. 2013. Evolution of the regionalization and patterning of the vertebrate telencephalon: what can we learn from cyclostomes? Current Opinion in Genetics & Development 23(4), 475483.Google Scholar
Sugahara, F, Pascual-Anaya, J, Oisi, Y, Kuraku, S, Aota, S, Adachi, N, Takagi, W, Hirai, T, Sato, N, Murakami, Y, Kuratani, S. 2016. Evidence from cyclostomes for complex regionalization of the ancestral vertebrate brain. Nature 531:97100.Google Scholar
Suzuki, DG, Fukumoto, Y, Yoshimura, M, Yamazaki, Y, Kosaka, J, Kuratani, S, Wada, H. 2016. Comparative morphology and development of extra-ocular muscles in the lamprey and gnathostomes reveal the ancestral state and developmental patterns of the vertebrate head. Zool Lett 2:10.Google Scholar
Tahara, Y. 1988. Normal stages of development in the lamprey, Lampetra reissneri (Dybowski). Zool Sci 5:109118.Google Scholar
Takechi, M, Adachi, N, Hirai, T, Kuratani, S, Kuraku, S. 2013. The Dlx genes as clues to vertebrate genomics and craniofacial evolution. Semin Cell Dev Biol 24:110118.Google Scholar
Takechi, M, Takeuchi, M, Ota, KG, Nishimura, O, Mochii, M, Itomi, K, Adachi, N, Takahashi, M, Fujimoto, S, Tarui, H, Okabe, M, Aizawa, S, Kuratani, S. 2011. Overview of the transcriptome profiles identified in hagfish, shark, and bichir: Current issues arising from some nonmodel vertebrate taxa. J Exp Zool B Mol Dev Evol 316B:526546.Google Scholar
Takio, Y, Kuraku, S, Murakami, Y, Pasqualetti, M, Rijli, FM, Narita, Y, Kuratani, S, Kusakabe, R. 2007. Hox gene expression patterns in Lethenteron japonicum embryos – Insights into the evolution of the vertebrate Hox code. Dev Biol 308:606620.Google Scholar
Takio, Y, Pasqualetti, M, Kuraku, S, Hirano, S, Rijli, FM, Kuratani, S. 2004. Lamprey Hox genes and the evolution of jaws. Nature 429.Google Scholar
Tiecke, E, Matsuura, M, Kokubo, N, Kuraku, S, Kusakabe, R, Kuratani, S, Tanaka, M. 2007. Identification and developmental expression of two Tbx1/10-related genes in the agnathan Lethenteron japonicum. Dev Genes Evol 217:691697.Google Scholar
Tomsa, JM, Langeland, JA. 1999. Otx expression during lamprey embryogenesis provides insights into the evolution of the vertebrate head and jaw. Dev Biol 207:2637.Google Scholar
Tretjakoff, D. 1909a. Das nervensystem von Ammocoetes. I. Das rückenmark. Arch Für Mikrosk Anat 73:607680.Google Scholar
Tretjakoff, D. 1909b. Das nervensystem von Ammocoetes. II. Gehirn. Arch Für Mikrosk Anat 74:636779.Google Scholar
Tretjakoff, D. 1909c. Nervus mesencephalicus bei Ammocoetes. Anat Anz 34:151157.Google Scholar
Tretjakoff, D. 1913. Die zentralen Sinnesorgane bei Petromyzon. Arch Für Mikrosk Anat 83:A68A117.Google Scholar
Tretjakoff, D. 1926a. Das skelett und die muskulatur im kopfe des flüssneunauges. Z Für Wiss Zool 128:267304.Google Scholar
Tretjakoff, D. 1926b. Die Wirbelsäule des neunauges. Anat Anz 61:387396.Google Scholar
Tretjakoff, D. 1927. Das periphere nervensystem de flussneunauges. Z Für Wiss Zool 129:359452.Google Scholar
Tretjakoff, D. 1929. Die schleimknorpeligen bestandteile in kopfskelett von Ammocoetes. Z Für Wiss Zool 133:470516.Google Scholar
Tsuneki, K, Ouji, M, Saito, H. 1983. Seasonal migration and gonadal changes in the hagfish Eptatretus burgeri. Jpn J Ichthyol 29:429440.Google Scholar
Tulenko, FJ, McCauley, DW, MacKenzie, EL, Mazan, S, Kuratani, S, Sugahara, F, Kusakabe, R, Burke, AC. 2013. Body wall development in lamprey and a new perspective on the origin of vertebrate paired fins. Proc Natl Acad Sci 110:1189911904.Google Scholar
Uchida, K, Murakami, Y, Kuraku, S, Hirano, S, Kuratani, S. 2003. Development of the adenohypophysis in the lamprey: Evolution of epigenetic patterning programs in organogenesis. J Exp Zool B Mol Dev Evol 300B:3247.Google Scholar
Ueki, T, Kuratani, S, Hirano, S, Aizawa, S. 1998. Otx cognates in a lamprey, Lampetra japonica. Dev Genes Evol 208:223228.Google Scholar
Uy, BR, Simoes-Costa, M, Koo, DES, Sauka-Spengler, T, Bronner, ME. 2015. Evolutionarily conserved role for SoxC genes in neural crest specification and neuronal differentiation. Dev Biol 397:282292.Google Scholar
Uy, BR, Simoes-Costa, M, Sauka-Spengler, T, Bronner, ME. 2012. Expression of Sox family genes in early lamprey development. Int J Dev Biol 56:377383.Google Scholar
Van Otterloo, E, Li, W, Garnett, A, Cattell, M, Medeiros, DM, Cornell, RA. 2012. Novel Tfap2-mediated control of soxE expression facilitated the evolutionary emergence of the neural crest. Development 139(4):720730.Google Scholar
Veit, O. 1939. Beiträge zur kenntnis des kopfes der wirbelthiere. Morphol Jahrb Leipz 84:86107.Google Scholar
von Kupffer, C. 1890. Entwicklung von Petromyzon planeri. Arch Für Mik Anat 35:469558.Google Scholar
von Kupffer, C. 1899. Zur kopfentwicklung von Bdellostoma. Sitzungsberichte Geselleschaft Morpholigie Physioligie 15:2135.Google Scholar
von Kupffer, C. 1900. Studien zur vergleichenden entwicklungsgeschichte des kopfes der kranioten, Heft 4: Zur Kopfentwicklung von Bdellostoma. München: Verlag von J. F. Lehmann.Google Scholar
von Kupffer, C. 1906. Die morphogenie des centralnervensystems. Handb Ver- Gleichenden Exp Entwicklungslehre Wirbeltiere 2 (Part 3):1–272.Google Scholar
Wedin, AB. 1949. The anterior mesoblast in some lower vertebrates. In: A Comparative Study of the Ontogenetic Development of the Anterior Mesoblast in Petromyzon, Etmopterus, Torpedo, et al. Lund: Håkan Ohlssons Boktryckeri.Google Scholar
Wheeler, WM. 1900. The development of the urogenital organs of the lamprey. Zool Jahrb Anat 13:188.Google Scholar
Wicht, H, Northcutt, RG. 1995. Ontogeny of the head of the Pacific hagfish (Eptatretus stouti, Myxinoidea): Development of the lateral line system. Philos Trans R Soc Lond B Biol Sci 349:119134.Google Scholar
Wiedersheim, R. 1880. Das gehirn von ammocoetes und Petromyzon planeri. Morph Stud Jenaische Zeitschr 14:138.Google Scholar
Wright, GM, Keeley, FW, Robson, P. 2001. The unusual cartilaginous tissues of jawless craniates, cephalochordates and invertebrates. Cell Tissue Res 304:165174.Google Scholar
Yalden, DW. 1985. Feeding mechanisms as evidence for cyclostome monophyly. Zool J Linn Soc 84:291300.Google Scholar
Yao, T, Ohtani, K, Kuratani, S, Wada, H. 2011. Development of lamprey mucocartilage and its dorsal–ventral patterning by endothelin signaling, with insight into vertebrate jaw evolution. J Exp Zool B Mol Dev Evol 316B:339346.Google Scholar
York, JR, Yuan, T, Zehnder, K, McCauley, DW. 2017. Lamprey neural crest migration is Snail-dependent and occurs without a differential shift in cadherin expression. Developmental Biology 428(1):176187.Google Scholar
York, JR, Yuan, T, Lakiza, O, McCauley, DW. 2018 (online publication ahed of print). An ancestral role for Semaphorin3F-Neuropilin signalling in patterning neural crest within the new vertebrate head. Development DOI: dev-164780.Google Scholar
Yuan, T, York, JR, McCauley, DW. 2018. Gliogenesis in lampreys shares gene regulatory interactions with oligodendrocyte development in jawed vertebrates. Developmental Biology 441:176190.Google Scholar
Zhang, G, Miyamoto, MM, Cohn, MJ. 2006. Lamprey type II collagen and Sox9 reveal an ancient origin of the vertebrate collagenous skeleton. Proc Natl Acad Sci U S A 103:31803185.Google Scholar
Zhu, M, Ahlberg, PE, Pan, Z, Zhu, Y, Qiao, T, Zhao, W, Jia, L, Lu, J. 2016. A Silurian maxillate placoderm illuminates jaw evolution. Science 354:334336.Google Scholar