Skip to main content

Lamprey Metamorphosis

  • Chapter
  • First Online:
Lampreys: Biology, Conservation and Control

Part of the book series: Fish & Fisheries Series ((FIFI,volume 37))

Abstract

Among vertebrates, true metamorphosis is restricted to amphibians, two groups of bony fishes, and lampreys. This chapter provides a comprehensive review of the ecology, morphology, physiology, and molecular biology of lamprey metamorphosis. The lamprey life cycle includes an embryonic period, a larval period ending with metamorphosis, a parasitic or non-parasitic juvenile period, and an adult reproductive period. Lamprey metamorphosis is influenced by endogenous and exogenous factors, most significantly a rise in spring water temperature, the accumulation of sufficient lipid reserves for the non-trophic metamorphic phase, and thyroid hormones. In lampreys, thyroid hormones appear to have a dual role, whereby high levels promote larval growth and a subsequent sharp decline is important for development and metamorphosis. As with other true metamorphoses, dramatic biochemical, cellular, and morphological changes occur during lamprey metamorphosis. The external changes are striking and include the development of an oral (suctorial) disc and eyes, restructuring of the branchial region, and changes in the fins and body coloration. Internal changes include major modifications to the digestive system (new esophagus, remodeled intestine, and loss of hepatic biliary tree and gall bladder). The larval kidneys regress while the definitive juvenile kidney develops de novo. Numerous changes are also observed in the respiratory and skeletal systems in preparation for the juvenile and spawning periods.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adinolfi M, Chieffi G (1958) Larval and adult haemoglobins of the cyclostome Petromyzon planeri. Nature 182:730

    CAS  PubMed  Google Scholar 

  • Ahima RS, Osei SY (2004) Leptin signaling. Physiol Behav 81:223–241

    CAS  PubMed  Google Scholar 

  • Ahima RS, Osei SY (2008) Adipokines in obesity. Obes Metab 36:182–197

    CAS  Google Scholar 

  • Antipova O, Orgel JPRO (2010) In situ D-periodic molecular structure of type II collagen. J Biol Chem 285:7087–7096

    CAS  PubMed Central  PubMed  Google Scholar 

  • Applegate VC (1950) Natural history of the sea lamprey, Petromyzon marinus, in Michigan. US Fish and Wildlife Service Special Scientific Report 55, Washington, DC

    Google Scholar 

  • Applegate VC, Thomas MLH (1965) Sex ratios and sexual dimorphism among recently transformed sea lampreys, Petromyzon marinus Linnaeus. J Fish Res Board Can 22:695–711

    Google Scholar 

  • Armstrong LA, Wright GM, Youson JH (1987) Transformation of mucocartilage to a definitive cartilage during metamorphosis in the sea lamprey, Petromyzon marinus. J Morphol 194:1–21

    Google Scholar 

  • Barrington EJW, Sage M (1963a) On the responses of iodine-binding regions of the endostyle of the larval lamprey to goitrogens and thyroxine. Gen Comp Endocrinol 3:669–679

    CAS  Google Scholar 

  • Barrington EJW, Sage M (1963b) On the responses of the glandular tracts and associated regions of the endostyle of the larval lamprey to goitrogens and thyroxine. Gen Comp Endocrinol 3:153–165

    CAS  Google Scholar 

  • Barrington EJW, Sage M (1972) The endosytle and thyroid gland. In: Hardisty MW, Potter IC (eds) The biology of lampreys, vol 2. Academic Press, New York, pp 105–134

    Google Scholar 

  • Bartels H, Potter IC (1991) Structural changes in the zonular occludentes of the chloride cells of young adult lampreys following acclimation to seawater. Cell Tissue Res 265:447–457

    Google Scholar 

  • Bartels H, Potter IC (1998) Membrane structure of the cells of the lamprey notochord. J Electron Microsc 47:627–636

    Google Scholar 

  • Bartels H, Potter IC (2004) Cellular composition and ultrastructure of the gill epithelium of larval and adult lampreys: implications for osmoregulation in fresh and seawater. J Exp Biol 207:3447–3462

    CAS  PubMed  Google Scholar 

  • Bartels H, Fazekas U, Youson JH, Potter IC (2011) Changes in the cellular composition of the gill epithelium during the life cycle of a nonparasitic lamprey: functional and evolutionary implications. Can J Zool 89:538–545

    Google Scholar 

  • Bartels H, Docker MF, Fazekas U, Potter IC (2012) Functional and evolutionary implications of the cellular composition of the gill epithelium of feeding adults of a freshwater parasitic species of lamprey, Ichthyomyzon unicuspis. Can J Zool 90:1278–1283

    CAS  Google Scholar 

  • Beamish FWH (1980) Osmoregulation in juvenile and adult lampreys. Can J Fish Aquat Sci 37:1735–1750

    Google Scholar 

  • Beamish FWH, Austin LS (1985) Growth of the mountain brook lamprey Ichthyomyzon greeleyi Hubbs and Trautman. Copeia 4:881–890

    Google Scholar 

  • Beamish FWH, Hanson LH (1987) Summary of evaluation methods and population studies of parasitic phase sea lamprey, Section B. In: Johnson BGH (ed) Workshop to evaluate sea lamprey populations “WESLP.” Great Lakes Fishery Commission, Special Publication 87-2, Ann Arbor

    Google Scholar 

  • Beamish FWH, Medland TE (1988) Metamorphosis of the mountain brook lamprey Ichthyomyzon greeleyi. Environ Biol Fish 23:45–54

    Google Scholar 

  • Beamish FWH, Thomas EJ (1984) Metamorphosis of the southern brook lamprey, Ichthyomyzon gagei. Copeia 1984:502–515

    Google Scholar 

  • Beamish FWH, Strachan PD, Thomas E (1978) Osmotic and ionic performance of the anadromous sea lamprey, Petromyzon marinus. Comp Biochem Physiol 60A:435–443

    Google Scholar 

  • Beamish RJ (1985) Freshwater parasitic lamprey on Vancouver island and a theory of the evolution of the freshwater parasitic and nonparasitic life histories. In: Foreman RE, Gorbman A, Dodd JM, Olsson R (eds) Evolutionary biology of primitive fishes. Plenum, New York, pp 123–140

    Google Scholar 

  • Beamish RJ (1987) Evidence that parasitic and nonparasitic life-history types are produced by one population of lamprey. Can J Fish Aquat Sci 44:1779–1782

    Google Scholar 

  • Beamish RJ, Youson JH (1987) Life history and abundance of young adult Lampetra ayresi in the Fraser River and their possible impact on salmon and herring stocks in the Strait of Georgia.Can J Fish Aquat Sci 44:525–537

    Google Scholar 

  • Becker KB, Stephens KC, Davey JC, Schneider MJ, Galton VA (1997) The type 2 and type 3 iodothyronine deiodinases play important roles in coordinating development in Rana catesbeiana tadpoles. Endocrinology 138:2989–2997

    CAS  PubMed  Google Scholar 

  • Berry DL, Rose CS, Remo BF, Brown DD (1998) The expression pattern of thyroid hormone response genes in remodeling tadpole tissues defines distinct growth and resorption gene expression programs. Dev Biol 203:24–35

    CAS  PubMed  Google Scholar 

  • Bianco PG (1986) Lethenteron zanandreai (Vladykov 1955). In: Holčík J (ed) The freshwater fishes of Europe, vol 1, part 1, Petromyzontiformes. AULA, Wiesbaden, pp 237–246

    Google Scholar 

  • Bianco AC, Kim BW (2006) Deiodinases: implications of the local control of thyroid hormone action. J Clin Invest 116:2571–2579

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR (2002) Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr Rev 23:38–89

    CAS  PubMed  Google Scholar 

  • Bird DJ, Potter IC (1979) Metamorphosis in the paired species of lampreys, Lampetra fluviatilis (L) and Lampetra planeri (Bloch). 1. Description of the timing and stages. Zool J Linn Soc 65:127–143

    Google Scholar 

  • Blanton ML, Specker JL (2007) The hypothalamic-pituitary-thyroid (HPT) axis in fish and its role in fish development and reproduction. Crit Rev Toxicol 37:97–115

    CAS  PubMed  Google Scholar 

  • Boenig H (1928) Studien zur Morphologie und Entsicklungsgeschichte des Pankreas beim Nachneunauge (Lampetra (Petromyzon) planeri). Teil II. Z Mikrosk-anat Forsch 12:537–594

    Google Scholar 

  • Boenig H (1929) Studien zur Morphologie und Entsicklungsgeschichte des Pankreas beim Bachneunauge (Lampetra [Petromyzon] planeri). Teil III. Die histologie und histogenese des pankreas. Z Mikrosk-anat Forsch 17:124–184

    Google Scholar 

  • Bonneville MA (1963) Fine structural changes in the intestinal epithelium of the bullfrog during metamorphosis. J Cell Biol 18:579–597

    CAS  PubMed Central  PubMed  Google Scholar 

  • Boomer LA, Bellister SA, Stephenson LL et al (2010) Cholangiocyte apoptosis is an early event during induced metamorphosis in the sea lamprey, Petromyzon marinus L. J Pediatr Surg 45:114–120

    PubMed  Google Scholar 

  • Brown DD (2005) The role of deiodinases in amphibian metamorphosis. Thyroid 15:815–821

    CAS  PubMed  Google Scholar 

  • Brown DD, Cai LQ (2007) Amphibian metamorphosis. Dev Biol 306:20–33

    CAS  PubMed Central  PubMed  Google Scholar 

  • Buchholz DR, Paul BD, Fu LZ, Shi YB (2006) Molecular and developmental analyses of thyroid hormone receptor function in Xenopus laevis, the African clawed frog. Gen Comp Endocrinol 145:1–19

    CAS  PubMed  Google Scholar 

  • Buchholz DR, Moskalik C, Kulkarni S, Hollar A, Ng A (2011) Hormone regulation and the evolution of frog metamorphic diversity. In: Flatt T, Heyland A (eds) Mechanisms of life history evolution: the genetics and physiology of life history traits and trade-offs. Oxford University, Oxford, pp 87–98

    Google Scholar 

  • Bujor MP (1891) Contribution à l’étude métamorphose de l’ammocoetes branchialis en Petromyzon planeri. Rev Biol N Fr 12:475–486

    Google Scholar 

  • Callery EM, Fang H, Elinson RP (2001) Frogs without polliwogs: evolution of anural direct development. Bioessays 23:233–241

    CAS  PubMed  Google Scholar 

  • Cetin I, Morpurgo PS, Radaelli T et al (2000) Fetal plasma leptin concentrations: relationship with different intrauterine growth patterns from 19 weeks to term. Pediatr Res 48:646–651

    CAS  PubMed  Google Scholar 

  • Cheung R, Plisetskaya EM, Youson JH (1990) Distribution of two forms of somatostatin in the brain, anterior intestine, and pancreas of adult lampreys (Petromyzon marinus). Cell Tissue Res 262:283–292

    CAS  PubMed  Google Scholar 

  • Cheung R, Andrews PC, Plisetskaya EM, Youson JH (1991a) Immunoreactivity to peptides belonging to the pancreatic polypeptide family (NPY, aPY, PP, PYY) and to glucagon-like peptide in the endocrine pancreas and anterior intestine of adult lampreys, Petromyzon marinus: an immunohistochemical study. Gen Comp Endocrinol 81:51–63

    CAS  Google Scholar 

  • Cheung R, Ferreira LCG, Youson JH (1991b) Distribution of two forms of somatostatin and peptides belonging to the pancreatic polypeptide family in tissues of larval lampreys, Petromyzon marinus L.: an immunohistochemical study. Gen Comp Endocrinol 82:93–102

    CAS  Google Scholar 

  • Clements-Merlini M (1962) Altered metabolism of I131 by the endostyle and notochord of ammocoetes larvae. II. Effects of treatment with thiourea or potassium thiocyanate. Gen Comp Endocrinol 2:361–368

    CAS  Google Scholar 

  • Cochran PA, Lyons J, Merino-Namob E (1996) Notes on the biology of the Mexican lampreys Lampetra spadicea and L. geminis (Agnatha: Petromyzontidae). Ichthyol Explor Freshw 7:173–180

    Google Scholar 

  • Cole WC, Youson JH (1981) The effect of pinealectomy, continuous light, and continuous darkness on metamorphosis of anadromous sea lampreys, Petromyzon marinus L. J Exp Zool 218:397–404

    CAS  PubMed  Google Scholar 

  • Copeland DL, Duff RJ, Liu Q, Prokop J, Londraville RL (2011) Leptin in teleost fishes: an argument for comparative study. Front Physiol 2:1–11

    Google Scholar 

  • Crespi EJ, Denver RJ (2006) Leptin (ob gene) of the South African clawed frog Xenopus laevis. Proc Natl Acad Sci U S A 103:10092–10097

    CAS  PubMed Central  PubMed  Google Scholar 

  • Damas H (1935) Contribution à l’étude de la métamorphose de la tête de la lamproie. Arch Biol Paris 46:171–227

    Google Scholar 

  • Damas H (1944) Recherches sur le développement de Lampetra fluviatilis L.: contribution à l’étude de la céphalogenèse des Vertebrés. Arch Biol Paris 55:1–284

    Google Scholar 

  • Danis MH, Filosa MF, Youson JH (2000) An albumin-like protein in the serum of non-parasitic brook lamprey (Lampetra appendix) is restricted to preadult phases of the life cycle in contrast to the parasitic species Petromyzon marinus. Comp Biochem Physiol B Biochem Mol Biol 127:251–260

    CAS  PubMed  Google Scholar 

  • De Groef B, Van derGS, Darras VM, Kuhn ER (2006) Role of corticotropin-releasing hormone as a thyrotropin-releasing factor in non-mammalian vertebrates. Gen Comp Endocrinol 146:62–68

    CAS  PubMed  Google Scholar 

  • Delarbre C, Gallut C, Barriel V, Janvier P, Gachelin G (2002) Complete mitochondrial DNA of the hagfish, Eptatretus burgeri: the comparative analysis of mitochondrial DNA sequences strongly supports the cyclostome monophyly. Mol Phylogenet Evol 22:184–192

    CAS  Google Scholar 

  • Denver RJ (1998) Hormonal correlates of environmentally induced metamorphosis in the western spadefoot toad, Scaphiopus hammondii. Gen Comp Endocrinol 110:326–336

    CAS  PubMed  Google Scholar 

  • Denver RJ, Glennemeier KA, Boorse GC (2002) Endocrinology of complex life cycles: amphibians. In: Pfaff D, Arnold A, Etgen A, Fahrbach S, Rubin R (eds) Hormones, brain and behavior, vol 2. Academic Press, San Diego, pp 469–513

    Google Scholar 

  • Docker MF (2009) A review of the evolution of nonparasitism in lampreys and an update of the paired species concept. In: Brown LR, Chase SD, Mesa MG, Beamish RJ, Moyle PB (eds) Biology, management, and conservation of lampreys in North America. American Fisheries Society Symposium 72, Bethesda, pp 71–114

    Google Scholar 

  • Docker MF, Potter IC (in press) Life history variation in lampreys: alternate feeding and migratory types. In: Docker MF (ed)  Lampreys: biology, conservation and control, vol 2. Springer, Dordrecht

    Google Scholar 

  • Eales JG (1985) The peripheral metabolism of thyroid hormones and regulation of thyroidal status in poikilotherms. Can J Zool 63:1217–1231

    CAS  Google Scholar 

  • Eales JG (1997) Iodine metabolism and thyroid-related functions in organisms lacking thyroid follicles: are thyroid hormones also vitamins? Proc Soc Exp Biol Med 214:302–317

    CAS  PubMed  Google Scholar 

  • Eales JG, Brown SB (1993) Measurement and regulation of thyroidal status in teleost fish. Rev Fish Biol Fish 3:299–347

    Google Scholar 

  • Eales JG, Holmes JA, McLeese JM, Youson JH (1997) Thyroid hormone deiodination in various tissues of larval and upstream-migrant sea lampreys, Petromyzon marinus. Gen Comp Endocrinol 106:202–210

    CAS  PubMed  Google Scholar 

  • Eales JG, McLeese JM, Holmes JA, Youson JH (2000) Changes in intestinal and hepatic thyroid hormone deiodination during spontaneous metamorphosis of the sea lamprey, Petromyzon marinus. J Exp Zool 286:305–312

    CAS  PubMed  Google Scholar 

  • Eddy JMP (1969) Metamorphosis and pineal complex in brook lamprey, Lampetra planeri. J Endocrinol 44:451–452

    CAS  PubMed  Google Scholar 

  • Eikenberry EF, Childs B, Sheren SB et al (1984) Crystalline fibril structure of type II collagen in lamprey notochord sheath. J Mol Biol 176:261–277

    CAS  PubMed  Google Scholar 

  • Elliott WM (1989) Development of the endocrine pancreas and related parts of the alimentary canal during metamorphosis in the lamprey, Petromyzon marinus L. PhD thesis, University of Toronto, Toronto

    Google Scholar 

  • Elliott WM, Youson JH (1986) Immunocytochemical localization of insulin and somatostatin in the endocrine pancreas of the sea lamprey, Petromyzon marinus L., at various stages of its life cycle. Cell Tissue Res 243:629–634

    CAS  Google Scholar 

  • Elliott WM, Youson JH (1987) Immunohistochemical observations of the endocrine pancreas during metamorphosis of the sea lamprey, Petromyzon marinus L. Cell Tissue Res 247:351–357

    CAS  Google Scholar 

  • Elliott WM, Youson JH (1988) Fine structure and immunocytochemistry of cells within the endocrine pancreas of larval and adult sea lampreys, Petromyzon marinus L. Am J Anat 182:73–83

    CAS  PubMed  Google Scholar 

  • Elliott WM, Youson JH (1991) Somatostatin concentrations in the pancreatic-intestinal tissues of the sea lamprey, Petromyzon marinus L., at various periods of its life cycle. Comp Biochem Physiol A Physiol 99:357–360

    CAS  Google Scholar 

  • Elliott WM, Youson JH (1993a) Development of the adult endocrine pancreas during metamorphosis in the sea lamprey, Petromyzon marinus L. I. Light microscopy and autoradiography. Anat Rec 237:259–270

    CAS  Google Scholar 

  • Elliott WM, Youson JH (1993b) Development of the adult endocrine pancreas during metamorphosis in the sea lamprey, Petromyzon marinus L. II. Electron microscopy and immunocytochemistry. Anat Rec 237:271–290

    CAS  Google Scholar 

  • Elliott WM, Youson JH (1994) Alterations to the subepithelial layers of the larval alimentary tract during metamorphosis in the sea lamprey Petromyzon marinus, with emphasis on tissue interactions. Cell Tissue Res 276:503–513

    Google Scholar 

  • Ellis LC (1993) An ultrastructural investigation of the pronephric kidney of the sea lamprey, Petromyzon marinus L., throughout the life cycle. PhD thesis, University of Toronto, Toronto

    Google Scholar 

  • Ellis LC, Youson JH (1990) Pronephric regression during larval life in the sea lamprey, Petromyzon marinus L.: a histochemical and ultrastructural study. Anat Embryol 182:41–52

    CAS  PubMed  Google Scholar 

  • Eng EWY (2004) Investigation of albumin-like serum proteins associated with lamprey life histories. MSc thesis, University of Toronto, Toronto

    Google Scholar 

  • Eng F, Youson JH (1992a) Morphology of the bile ducts of the brook lamprey, Lampetra lamottenii (Le Sueur) before and during infection with the nematode, Truttaedacnitis stelmioides (Vessichelli, 1910) (Nematoda, Cucullanidae). Anat Rec 234:201–214

    CAS  Google Scholar 

  • Eng F, Youson JH (1992b) Morphology of the liver of the brook lamprey, Lampetra lamottenii before and during infection with the nematode, Truttaedacnitis stelmioides, hepatocytes, sinusoids, and perisinusoidal cells. Tissue Cell 24:575–592

    CAS  Google Scholar 

  • Epple A, Brinn JE (1986) Pancreatic islets. In: Pang PKT, Schreibman M (eds) Vetebrate endocrinology: funadmentals and biochemical implications. Academic Press, New York, pp 279–317

    Google Scholar 

  • Escriva H, Manzon L, Youson J, Laudet V (2002) Analysis of lamprey and hagfish genes reveals a complex history of gene duplications during early vertebrate evolution. Mol Biol Evol 19:1440–1450

    CAS  PubMed  Google Scholar 

  • Etkin W (1935) The mechanism of anuran metamorphosis. I. Thyroxine concentrations and the metamorphic pattern. J Exp Zool 71:317–340

    Google Scholar 

  • Etkin W (1964) Metamorphosis. In: Moore JA (ed) Physiology of the amphibia. Academic, London, pp 371–410

    Google Scholar 

  • Etkin W (1968) Hormonal control of amphibian metamorphosis. In: Etkin W, Gilbert LI (eds) Metamorphosis: a problem in developmental biology. Meredith Corporation, New York, pp 313–348

    Google Scholar 

  • Falkmer S (1985) Comparative morphology of pancreatic islets in animals. In: Vok BW, Arquilla ER (eds) The diabetic pancreas. Plenum, New York, pp 17–52

    Google Scholar 

  • Fernandes RJ, Eyre DR (1999) The elastin-like protein matrix of lamprey branchial cartilage is cross-linked by lysyl pyridinoline. Biochem Biophys Res Commun 261:635–640

    CAS  PubMed  Google Scholar 

  • Ficele G, Heinig JA, Kawauchi H et al (1998) Spatial and temporal distribution of proopiomelanotropin and proopiocortin mRNA during the life cycle of the sea lamprey: a qualitative and quantitative in situ hybridization study. Gen Comp Endocrinol 110:212–225

    CAS  PubMed  Google Scholar 

  • Filosa MF, Sargent PA, Fisher MM, Youson JH (1982) An electrophoretic and immunoelectrophoretic characterization of the serum proteins of the adult lamprey, Petromyzon marinus L. Comp Biochem Physiol B Biochem Mol Biol 72:521–530

    CAS  Google Scholar 

  • Filosa MF, Sargent PA, Youson JH (1986) An electrophoretic and immunoelectrophoretic study of serum proteins during the life cycle of the lamprey, Petromyzon marinus L. Comp Biochem Physiol B Biochem Mol Biol 83:143–149

    CAS  Google Scholar 

  • Filosa MF, Ito MA, Youson JH (1992) Quantitative changes in a serum protein, AS, during the life cycle of the lamprey, Petromyzon marinus L. Fish Physiol Biochem 9:417–426

    CAS  PubMed  Google Scholar 

  • Filosa MF, Adam I, Robson P et al (1998) Partial clone of the gene for AS protein of the lamprey Petromyzon marinus, a member of the albumin supergene family whose expression is restricted to the larval and metamorphic phases of the life cycle. J Exp Zool 282:301–309

    CAS  PubMed  Google Scholar 

  • Forey P, Janvier P (1993) Agnathans and the origin of jawed vertebrates. Nature 361:129–134

    Google Scholar 

  • Forey P, Janvier P (1994) Evolution of the early vertebrates. Am Sci 82:554–565

    Google Scholar 

  • Fort DJ, Degitz S, Tietge J, Touart LW (2007) The hypothalamic-pituitary-thyroid (HPT) axis in frogs and its role in frog development and reproduction. Crit Rev Toxicol 37:117–161

    CAS  PubMed  Google Scholar 

  • Freamat M, Kawauchi H, Nozaki M, Sower SA (2006) Identification and cloning of a glycoprotein hormone receptor from sea lamprey, Petromyzon marinus. J Mol Endocrinol 37:135–146

    CAS  PubMed  Google Scholar 

  • Galloway R, Potter IC, Macey DJ, Hilliard RW (1987) Oxygen consumption and responses to hypoxia of ammocoetes of the southern hemisphere lamprey Geotria australis. Fish Physiol Biochem 4:63–72

    CAS  PubMed  Google Scholar 

  • Gess RW, Coates MI, Rubidge BS (2006) A lamprey from the Devonian period of South Africa. Nature 443:981–984

    CAS  PubMed  Google Scholar 

  • Glennemeier KA, Denver RJ (2002) Role for corticoids in mediating the response of Rana pipiens tadpoles to intraspecific competition. J Exp Zool 292:32–40

    CAS  PubMed  Google Scholar 

  • Gray JE, Doolittle RF (1992) Characterization, primary structure, and evolution of lamprey plasma albumin. Protein Sci 1:289–302

    CAS  PubMed Central  PubMed  Google Scholar 

  • Griffith RW, Beamish FWH, Morrison BJ, Barker LA (2001) Factors affecting larval sea lamprey growth and length at metamorphosis in lampricide-treated streams. Trans Am Fish Soc 130:289–306

    Google Scholar 

  • Gross TN, Manzon RG (2011) Sea lamprey (Petromyzon marinus) contain four developmentally regulated serum thyroid hormone distributor proteins. Gen Comp Endocrinol 170:640–649

    CAS  PubMed  Google Scholar 

  • Gudernatsch JF (1912) Feeding experiments on tadpoles. I. The influence of specific organs given as food on growth and differentiation. A contribution to the knowledge of organs with internal secretion. Arch Entwicklungsmech Org 35:457–483

    Google Scholar 

  • Hall BK (1999) The neural crest in development and evolution. Springer, New York

    Google Scholar 

  • Hardisty MW (1979) Biology of cyclostomes. Chapman and Hall, London

    Google Scholar 

  • Hardisty MW (1981) The skeleton. In: Hardisty MW, Potter IC (eds) The biology of lampreys, vol 3. Academic Press, London, pp 333–376

    Google Scholar 

  • Hardisty MW (1986a) Lampetra fluviatilis (Linnaeus, 1758). In: Holčík J (ed), The freshwater fishes of Europe, vol 1, part 1, Petromyzontiformes. AULA-Verlag, Wiesbaden, pp 249–278

    Google Scholar 

  • Hardisty MW (1986b) Lampetra planeri (Bloch, 1784). In: Holčík J (ed), The freshwater fishes of Europe, vol 1, part 1, Petromyzontiformes. AULA-Verlag, Wiesbaden, pp 279–304

    Google Scholar 

  • Hardisty MW (2006) Lampreys life without jaws. Forrest Text, Tresaith

    Google Scholar 

  • Hardisty MW, Potter IC (1971a) Paired species. In: Hardisty MW, Potter IC (eds) The biology of lampreys, vol 1. Academic Press, London, pp 249–277

    Google Scholar 

  • Hardisty MW, Potter IC (1971b) The behaviour, ecology and growth of larval lampreys. In: Hardisty MW, Potter IC (eds) The biology of lampreys, vol 1. Academic, London, pp 88–125

    Google Scholar 

  • Harris LR, Cake MH, Macey DJ, Potter IC (1990) An increase in the concentration of hepatic iron during the metamorphosis of the lamprey Geotria australis is accompanied by increased superoxide dismutase activity. Fish Physiol Biochem 8:451–457

    CAS  PubMed  Google Scholar 

  • Harris LR, Macey DJ, Potter IC, Cake MH (1995) Hepatic molecular conversion and detoxification of ferritin iron in adult lampreys (Geotria australis) following natural and induced iron loading. Biochem J 305:975–980

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hart JL (1973) Pacific fishes of Canada. Bulletin Fisheries Research Board of Canada 180, Ottawa

    Google Scholar 

  • Harvey J, Ashford MLJ (2003) Leptin in the CNS: much more than a satiety signal. Neuropharmacology 44:845–854

    CAS  PubMed  Google Scholar 

  • Heard WR (1966) Observations on lampreys in the Naknek River system of southwest Alaska. Copeia 1966:332–339

    Google Scholar 

  • Heimberg AM, Cowper-Sal·lari R, Sémon M, Donoghue PCJ, Peterson KJ (2010) microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate. Proc Natl Acad Sci U S A 107:19379–19383

    CAS  PubMed Central  PubMed  Google Scholar 

  • Heinig JA, Keeley FW, Robson P, Sower SA, Youson JH (1995) The appearance of proopiomelanocortin early in vertebrate evolution: cloning and sequencing of POMC from a lamprey pituitary cDNA library. Gen Comp Endocrinol 99:137–144

    CAS  PubMed  Google Scholar 

  • Heinig JA, Keeley FW, Kawauchi H, Youson JH (1999) Expression of proopiocortin and proopiomelanotropin during the life cycle of the sea lamprey (Petromyzon marinus). J Exp Zool 283:95–101

    CAS  Google Scholar 

  • Henson MP, Bergstedt RA, Adams JV (2003) Comparison of spring measures of length, weight, and condition factor for predicting metamorphosis in two populations of sea lamprey (Petromyzon marinus) larvae. J Great Lakes Res 29(Suppl 1):204–213

    Google Scholar 

  • Hilliard RW, Potter IC (1988) Morphology of the exocrine pancreas of the southern hemisphere lamprey, Geotria australis, and changes during metamorphosis. J Morphol 197:33–52

    CAS  PubMed  Google Scholar 

  • Hilliard RW, Epple A, Potter IC (1985) The morphology and histology of the endocrine pancreas of the Southern Hemisphere lamprey, Geotria australis Gray. J Morphol 184:253–261

    CAS  PubMed  Google Scholar 

  • Hoff JG (1988) Some aspects of the ecology of the American brook lamprey, Lampetra appendix, in the Mashpee River, Cape Cod, Massachusetts. Can Field-Nat 102:735–737

    Google Scholar 

  • Hoheisel G, Sterba G (1963) Uber die Wirkung von Kaliumperchlorat (KClO4) auf Ammocoeten von Lampetra Planeri Bloch. Z Mikroskop Anat Forsch 70:490–516

    CAS  Google Scholar 

  • Holčík J (1986a) Lethenteron japonicum (Martens, 1868). In: Holčík J (ed) The freshwater fishes of Europe, vol 1, part 1, Petromyzontiformes. AULA, Wiesbaden, pp 198–219

    Google Scholar 

  • Holčík J (1986b) Caspiomyzon wagneri (Kessler, 1870). In: Holčík J (ed) The freshwater fishes of Europe, vol 1, part 1, Petromyzontiformes. AULA, Wiesbaden, pp 119–142

    Google Scholar 

  • Holčík J, Renaud CB (1986) Eudontomyzon mariae (Berg, 1931). In: Holčík J (ed) The freshwater fishes of Europe, vol 1, part 1: Petromyzontiformes. AULA, Wiesbaden, pp 165–185

    Google Scholar 

  • Holland LZ, Holland ND, Gilland E (2008) Amphioxus and the evolution of head segmentation. Integr Comp Biol 48:630–646

    PubMed  Google Scholar 

  • Hollett AK (1998) Condition factor and statolith aging in assessment of metamorphosis in sea lampreys (Petromymzon marinus), in the Great Lakes. MSc thesis, University of Toronto, Toronto

    Google Scholar 

  • Holmes JA, Lin P (1994) Thermal niche of larval sea lamprey, Petromyzon marinus. Can J Fish Aquat Sci 51:253–262

    Google Scholar 

  • Holmes JA, Youson JH (1993) Induction of metamorphosis in landlocked sea lampreys, Petromyzon marinus. J Exp Zool 267:598–604

    Google Scholar 

  • Holmes JA, Youson JH (1994) Fall condition factor and temperature influence the incidence of metamorphosis in sea lampreys, Petromyzon marinus. Can J Zool 72:1134–1140

    Google Scholar 

  • Holmes JA, Youson JH (1997) Laboratory study of the effects of spring warming and larval density on the metamorphosis of sea lampreys. Trans Am Fish Soc 126:647–657

    Google Scholar 

  • Holmes JA, Youson JH (1998) Extreme and optimal temperatures for metamorphosis in sea lampreys. Trans Am Fish Soc 127:206–211

    Google Scholar 

  • Holmes JA, Beamish FWH, Seelye JG, Sower SA, Youson JH (1994) Long-term influence of water temperature, photoperiod, and food deprivation on metamorphosis of sea lamprey, Petromyzon marinus. Can J Fish Aquat Sci 51:2045–2051

    Google Scholar 

  • Holmes JA, Chu H, Khanam SA, Manzon RG, Youson JH (1999) Spontaneous and induced metamorphosis in the American brook lamprey, Lampetra appendix. Can J Zool 77:959–971

    Google Scholar 

  • Horton FM (1934) On the relation of the thyroid gland to metamorphosis in the lamprey. J Exp Biol 11:257–261

    CAS  Google Scholar 

  • Hubbs CL, Potter IC (1971) Distribution, phylogeny and taxonomy. In: Hardisty MW, Potter IC (eds) The biology of lampreys, vol 1. Academic Press, London, pp 1–65

    Google Scholar 

  • Ito MA, Filosa MF, Youson JH (1988) In vitro study of serum protein synthesis in the livers of larvae and adults of the lamprey, Petromyzon marinus L. J Exp Zool 245:256–263

    CAS  Google Scholar 

  • Janvier P (2010) microRNAs revive old views about jawless vertebrate divergence and evolution. Proc Natl Acad Sci U S A 107:19137–19138

    CAS  PubMed Central  PubMed  Google Scholar 

  • Johnels AG (1948) On the development and morphology of the skeleton of the head of Petromyzon. Acta Zool 29:139–279

    Google Scholar 

  • Johnson CK, Voss SR (2013) Salamander paedomorphosis: linking thyroid hormone to life history and life cycle evolution. Curr Top Dev Biol 103:229–258

    CAS  PubMed  Google Scholar 

  • Jones RP (1947) Effect of thiourea on the endostyle of ammocoetes. Nature 160:638–639

    CAS  PubMed  Google Scholar 

  • Joss JMP (1985) Pituitary control of metamorphosis in the southern hemisphere lamprey, Geotria australis. Gen Comp Endocrinol 60:58–62

    CAS  PubMed  Google Scholar 

  • Kao YH, Youson JH, Holmes JA, Sheridan MA (1997a) Changes in lipolysis and lipogenesis in selected tissues of the landlocked lamprey, Petromyzon marinus, during metamorphosis. J Exp Zool 277:301–312

    CAS  Google Scholar 

  • Kao YH, Youson JH, Sheridan MA (1997b) Differences in the total lipid and lipid class composition of larvae and metamorphosing sea lampreys, Petromyzon marinus. Fish Physiol Biochem 16:281–290

    CAS  Google Scholar 

  • Kao YH, Youson JH, Holmes JA, Sheridan MA (1998) Effects of somatostatin on lipid metabolism of larvae and metamorphosing landlocked sea lamprey, Petromyzon marinus. Gen Comp Endocrinol 111:177–185

    CAS  PubMed  Google Scholar 

  • Kao Y, Youson JH, Holmes JA, Al-Mahrouki A, Sheridan MA (1999a) Effects of insulin on lipid metabolism of larvae and metamorphosing landlocked sea lamprey, Petromyzon marinus. Gen Comp Endocrinol 114:405–414

    CAS  Google Scholar 

  • Kao YH, Manzon RG, Sheridan MA, Youson JH (1999b) Study of the relationship between thyroid hormones and lipid metabolism during KClO4-induced metamorphosis of landlocked lamprey Petromyzon marinus. Comp Biochem Physiol C Toxicol Pharmacol 122:363–373

    CAS  Google Scholar 

  • Kavanaugh SI, Nozaki M, Sower SA (2008) Origins of gonadotropin-releasing hormone (GnRH) in vertebrates: identification of a novel GnRH in a basal vertebrate, the sea lamprey. Endocrinology 149:3860–3869

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kawauchi H, Sower SA (2006) The dawn and evolution of hormones in the adenohypophysis. Gen Comp Endocrinol 148:3–14

    CAS  PubMed  Google Scholar 

  • Keibel F (1927) Zur Entwicklungsgeschichte des Vorderdarmes und das Pankreas beim Bachneunauge (Lampetra (Petromyzon) planeri) und beim Flussneunauge (Lampetra (Petromyzon) fluviatilis). Z Mikrosk Anat Forsch 8:408–476

    Google Scholar 

  • Kimura S, Kamimura T (1982) The characterization of lamprey notochord collagen with special reference to its skin collagen. Comp Biochem Physiol B Biochem Mol Biol 73:335–339

    Google Scholar 

  • Klenner JJ, Schipper AL (1954) The response of the endostyle of Lampetra lamottenii to itrumil, thiouracil, thiourea, thiocyanate and thyroxin. Anat Rec 120:790

    Google Scholar 

  • Knowles FGW (1941) Duration of larval life in ammocoetes. Proc Zool Soc Lond 111:101–109

    Google Scholar 

  • Koob TJ, Long JH (2000) The vertebrate body axis: evolution and mechanical function. Am Zool 40:1–18

    Google Scholar 

  • Kusakabe R, Kuratani S (2007) Evolutionary perspectives from development of mesodermal components in the lamprey. Dev Dynam 236:2410–2420

    CAS  Google Scholar 

  • Lanfranchi G, Pallavicini A, Laveder P, Valle G (1994) Ancestral hemoglobin switching in lampreys. Dev Biol 164:402–408

    CAS  PubMed  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 102:301–310

    Google Scholar 

  • Langille RM, Hall BK (1993) Calcification of cartilage from the lamprey Petromyzon marinus (L) in vitro. Acta Zool 74:31–41

    Google Scholar 

  • Laudet V (2011) The origins and evolution of vertebrate metamorphosis. Curr Biol 21:R726–R737

    CAS  PubMed  Google Scholar 

  • Leach WJ (1940) Occurrence and life history of the northern brook lamprey, Ichthyomyzon fossor, in Indiana. Copeia 1940:21–34

    Google Scholar 

  • Leach WJ (1946) Oxygen consumption of lampreys, with special reference to metamorphosis and phylogenetic position. Physiol Zool 19:365–374

    CAS  PubMed  Google Scholar 

  • Leatherland JF (1994) Reflections on the thyroidology of fishes: from molecules to humankind. Guelph Ichthyol Rev 2:1–67

    Google Scholar 

  • Leatherland JF, Hilliard RW, Macey DJ, Potter IC (1990) Changes in serum thyroxine and triiodothyronine concentrations during metamorphosis of the southern hemisphere lamprey Geotria australis, and the effect of propylthiouracil, triiodothyronine and environmental temperature on serum thyroid hormone concentrations of ammocoetes. Fish Physiol Biochem 8:167–177

    CAS  PubMed  Google Scholar 

  • Lee M-J, McCauley DW (in press) Lampreys as model vertebrates in evolutionary developmental biology. In: Docker MF (ed) Lampreys: biology, conservation and control, vol 2. Springer, Dordrecht

    Google Scholar 

  • Lepercq J, Challier JC, Guerre-Millo M et al (2001) Prenatal leptin production: evidence that fetal adipose tissue produces leptin. J Clin Endocrinol Metab 86:2409–2413

    CAS  PubMed  Google Scholar 

  • Lewis SV (1980) Respiration of lampreys. Can J Fish Aquat Sci 37:1711–1722

    Google Scholar 

  • Lewis SV, Potter IC (1977) Oxygen consumption during metamorphosis of parasitic lamprey, Lampetra fluviatilis (L) and its non-parasitic derivative, Lampetra planeri (Bloch). J Exp Biol 69:187–198

    Google Scholar 

  • Lintlop SP, Youson JH (1983a) Binding of triiodothyronine to hepatocyte nuclei from sea lampreys, Petromyzon marinus L, at various stages of the life cycle. Gen Comp Endocrinol 49:428–436

    CAS  Google Scholar 

  • Lintlop SP, Youson JH (1983b) Concentration of triiodothyronine in the sera of the sea lamprey, Petromyzon marinus, and the brook lamprey, Lampetra lamottenii, at various phases of the life cycle. Gen Comp Endocrinol 49:187–194

    CAS  Google Scholar 

  • Lowe DR, Beamish FWH, Potter IC (1973) Changes in proximate body composition of landlocked sea lamprey Petromyzon marinus (L) during larval life and metamorphosis. J Fish Biol 5:673–682

    Google Scholar 

  • Macey DJ, Potter IC (1986) Concentrations of non-heme iron in ammocoetes of species representing the three extant lamprey families. Comp Biochem Physiol A Physiol 84:77–79

    Google Scholar 

  • Macey DJ, Youson JH (1990) Occurrence and structure of iron inclusions in adipocytes of larval lampreys. Acta Zool 71:69–76

    Google Scholar 

  • Macey DJ, Webb J, Potter IC (1982) Iron levels and major iron-binding proteins in the plasma of ammocoetes and adults of the southern hemisphere lamprey Geotria australis Gray. Comp Biochem Physiol A Physiol 72:307–312

    CAS  Google Scholar 

  • Macey DJ, Cake MH, Potter IC (1988) Exceptional iron concentrations in larval lampreys (Geotria australis) and the activities of superoxide radical detoxifying enzymes. Biochem J 252:167–172

    CAS  PubMed Central  PubMed  Google Scholar 

  • Maitland PS (1980) Review of the ecology of lampreys in northern Europe. Can J Fish Aquat Sci 37:1944–1952

    Google Scholar 

  • Mallatt J (1983) Laboratory growth of larval lampreys (Lampetra (Entosphenus) tridentata Richardson) at different food concentrations and animal densities. J Fish Biol 22:293–301

    Google Scholar 

  • Malmqvist B (1983) Growth, dynamics, and distribution of a population of the brook lamprey Lampetra planeri in a south Swedish stream. Holarct Ecol 6:404–412

    Google Scholar 

  • Manion PJ, Stauffer TM (1970) Metamorphosis of the landlocked sea lamprey, Petromyzon marinus. J Fish Res Board Can 27:1735–1746

    Google Scholar 

  • Manzon LA (2006) Cloning and developmental expression of sea lamprey (Petromyzon marinus) thyroid hormone and retinoid X receptors. PhD thesis, University of Toronto, Toronto

    Google Scholar 

  • Manzon LA, Youson JH, Holzer G, Staiano L, Laudet V, Manzon RG (2014) Thyroid hormone and retinoid X receptor function and expression during sea lamprey (Petromyzon marinus) metamorphosis. Gen Comp Endocrinol 204:211–222

    Google Scholar 

  • Manzon RG (2011) Thyroidal regulation of life history transitions in fish. In: Flatt T, Heyland A (eds) Mechanisms of life history evolution: the genetics and physiology of life history traits and trade-offs. Oxford University, Oxford, pp 72–86

    Google Scholar 

  • Manzon RG, Youson JH (1997) The effects of exogenous thyroxine (T4) or triiodothyronine (T3), in the presence and absence of potassium perchlorate, on the incidence of metamorphosis and on serum T4 and T3 concentrations in larval sea lamrpey (Petromyzon marinus). Gen Comp Endocrinol 106:211–220

    CAS  PubMed  Google Scholar 

  • Manzon RG, Youson JH (2002) KClO4 inhibits thyroidal activity in the larval endostyle in vitro. Gen Comp Endocrinol 128:214–223

    CAS  PubMed  Google Scholar 

  • Manzon RG, Eales JG, Youson JH (1998) Blocking of KClO4-induced metamorphosis in premetamorphic sea lampreys by exogenous thyroid hormones (TH): effects of KClO4 and TH on serum TH concentrations and intestinal thyroxine outer-ring deiodination. Gen Comp Endocrinol 112:54–62

    CAS  PubMed  Google Scholar 

  • Manzon RG, Holmes JA, Youson JH (2001) Variable effects of goitrogens in inducing precocious metamorphosis in sea lampreys (Petromyzon marinus). J Exp Zool 289:290–303

    CAS  PubMed  Google Scholar 

  • Manzon RG, Neuls TM, Manzon LA (2007) Molecular cloning, tissue distribution, and developmental expression of lamprey transthyretins. Gen Comp Endocrinol 151:55–65

    CAS  PubMed  Google Scholar 

  • Marsden JE, Siefkes MJ (in press) Sea lamprey control in the Great Lakes, Finger Lakes, and Lake Champlain. In: Docker MF (ed) Lampreys: biology, conservation and control, vol 2. Springer, Dordrecht

    Google Scholar 

  • Martin WM, Bumm LA, McCauley DW (2009) Development of the viscerocranial skeleton during embryogenesis of the sea lamprey, Petromyzon marinus. Dev Dynam 238:3126–3138

    Google Scholar 

  • Maskell FG (1931) On the New Zealand lamprey, Geotria australis Gray. Part 3. The loss of the mid-gut diverticula of the ammocoetes stage at metamorphosis. Trans Proc N Z Inst 62:120–128

    Google Scholar 

  • Mathers JS, Beamish FWH (1974) Changes in serum osmotic and ionic concentration in landlocked Petromyzon marinus. Comp Biochem Physiol 49:677–688

    CAS  Google Scholar 

  • McBurney KM, Wright GM (1996) Chondrogenesis of a non-collagen-based cartilage in the sea lamprey, Petromyzon marinus. Can J Zool 74:2118–2130

    Google Scholar 

  • McBurney KM, Keeley FW, Kibenge FSB, Wright GM (1996) Spatial and temporal distribution of lamprin mRNA during chondrogenesis of trabecular cartilage in the sea lamprey. Anat Embryol 193:419–426

    CAS  PubMed  Google Scholar 

  • McCauley DW, Bronner-Fraser M (2003) Neural crest contributions to the lamprey head. Development 130:2317–2327

    CAS  PubMed  Google Scholar 

  • McCauley DW, Bronner-Fraser M (2006) Importance of SoxE in neural crest development and the evolution of the pharynx. Nature 441:750–752

    CAS  PubMed  Google Scholar 

  • McGree M, Whitesel TA, Stone J (2008) Larval metamorphosis of individual Pacific lampreys reared in captivity. Trans Am Fish Soc 137:1866–1878

    Google Scholar 

  • McNabb FMA (2007) The hypothalamic-pituitary-thyroid (HPT) axis in birds and its role in bird development and reproduction. Crit Rev Toxicol 37:163–193

    CAS  PubMed  Google Scholar 

  • Moore JW, Beamish FWH (1973) Food of larval sea lamprey (Petromyzon marinus) and American brook lamprey (Lampetra lamottei). J Fish Res Board Can 30:7–15

    Google Scholar 

  • Moore JW, Mallatt J (1980) Feeding of larval lamprey. Can J Fish Aquat Sci 37:1658–1664

    Google Scholar 

  • Morgado I, Santos CRA, Jacinto R, Power DM (2007) Regulation of transthyretin by thyroid hormones in fish. Gen Comp Endocrinol 152:189–197

    CAS  PubMed  Google Scholar 

  • Morii M, Mezaki Y, Yamaguchi N et al (2010) Onset of apoptosis in the cystic duct during metamorphosis of a Japanese lamprey, Lethenteron reissneri. Anat Rec 293:1155–1166

    Google Scholar 

  • Morii M, Mezaki Y, Yoshikawa K et al (2012) How do lampreys avoid cholestasis after bile duct degeneration? In: Tripodi V (ed) Cholestasis. InTech, Shanghai, pp 81–98

    Google Scholar 

  • Morkert SB, Swink WD, Seelye JG (1998) Evidence for early metamorphosis of sea lampreys in the Chippewa River, Michigan. N Am J Fish Manag 18:966–971

    Google Scholar 

  • Morman RH (1987) Relationship of density to growth and metamorphosis of caged larval sea lampreys, Petromyzon marinus Linnaeus, in Michigan streams. J Fish Biol 30:173–181

    Google Scholar 

  • Morris R (1972) Osmoregulation. In: Hardisty MW, Potter IC (eds) Biology of lampreys, vol 2. Academic Press, London, pp 193–239

    Google Scholar 

  • Morris R (1980) Blood composition and osmoregulation in ammocoete larvae. Can J Fish Aquat Sci 37:1665–1679

    CAS  Google Scholar 

  • Morrison SL, Campbell CK, Wright GM (2000) Chondrogenesis of the branchial skeleton in embryonic sea lamprey, Petromyzon marinus. Anat Rec 260:252–267

    CAS  PubMed  Google Scholar 

  • Murdoch SP, Docker MF, Beamish FWH (1992) Effect of density and individual variation on growth of sea lamprey (Petromyzon marinus) larvae in the laboratory. Can J Zool 70:184–188

    Google Scholar 

  • Nakabayashi K, Matsumi H, Bhalla A et al (2002) Thyrostimulin, a heterodimer of two new human glycoprotein hormone subunits, activates the thyroid-stimulating hormone receptor. J Clin Invest 109:1445–1452

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nelson JS (2006) Fishes of the world, 4th edn. Wiley, Hoboken

    Google Scholar 

  • Nikitina N, Sauka-Spengler T, Bronner-Fraser M (2008) Dissecting early regulatory relationships in the lamprey neural crest gene network. Proc Natl Acad Sci U S A 105:20083–20088

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nozaki M, Takahashi A, Amemiya Y, Kawauchi H, Sower SA (1995) Distribution of lamprey adrenocorticotropin and melanotropins in the pituitary of the adult sea lamprey, Petromyzon marinus. Gen Comp Endocrinol 98:147–156

    CAS  PubMed  Google Scholar 

  • Nozaki M, Ominato K, Shimotani T et al (2008) Identity and distribution of immunoreactive adenohypophysial cells in the pituitary during the life cycle of sea lampreys, Petromyzon marinus. Gen Comp Endocrinol 155:403–412

    CAS  PubMed  Google Scholar 

  • O’Boyle RN, Beamish FWH (1977) Growth and intermediary metabolism of larval and metamorphosing stages of the landlocked sea lamprey, Petromyzon marinus L. Environ Biol Fish 2:103–120

    Google Scholar 

  • Ogasawara M, Di Lauro R, Satoh N (1999) Ascidian homologs of mammalian thyroid peroxidase genes are expressed in the thyroid-equivalent region of the endostyle. J Exp Zool 285:158–169

    CAS  PubMed  Google Scholar 

  • Ohtani K, Yao TY, Kobayashi M et al (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 E 310:596–607

    Google Scholar 

  • Ooi EC, Youson JH (1979) Regression of larval opisthonephros during metamorphosis of sea lamprey, Petromyzon marinus L. Am J Anat 154:57–79

    CAS  PubMed  Google Scholar 

  • Orozco A, Valverde R (2005) Thyroid hormone deiodination in fish. Thyroid 15:799–813

    CAS  PubMed  Google Scholar 

  • Osório J, Rétaux S (2008) The lamprey in evolutionary studies. Dev Genes Evol 218:221–235

    PubMed  Google Scholar 

  • Paris M, Escriva H, Schubert M et al (2008) Amphioxus postembryonic development reveals the homology of chordate metamorphosis. Curr Biol 18:825–830

    CAS  PubMed  Google Scholar 

  • Parker PS, Lennon RE (1956) Biology of the sea lamprey in its parasitic phase. US Fish Wildl Serv Res Rep 44:1–32

    Google Scholar 

  • Peek WD, Youson JH (1979a) Transformation of the interlamellar epithelium of the gills of the anadromous sea lamprey, Petromyzon marinus L, during metamorphosis. Can J Zool 57:1318–1332

    Google Scholar 

  • Peek WD, Youson JH (1979b) Ultrastructure of chloride cells in young adults of the anadromous sea lamprey, Petromyzon marinus L, in fresh water and during adaptation to sea water. J Morphol 160:143–163

    CAS  Google Scholar 

  • Piavis GW (1961) Embryological stages in the sea lamprey and effects of temperature on development. US Fish Wildl Serv Fish Bull 61:111–143

    Google Scholar 

  • Potter IC (1970) Life cycles and ecology of Australian lampreys of genus Mordacia. J Zool 161:487–511

    Google Scholar 

  • Potter IC (1980) Ecology of larval and metamorphosing lampreys. Can J Fish Aquat Sci 37:1641–1657

    Google Scholar 

  • Potter IC, Beamish FWH (1975) Lethal temperatures in ammocoetes of four species of lampreys. Acta Zool 56:85–91

    Google Scholar 

  • Potter IC, Brown ID (1975) Changes in haemoglobin electorpherograms during the life cycle of two closely related lampreys. Comp Biochem Physiol 51B:517–519

    Google Scholar 

  • Potter IC, Gill HS (2003) Adaptive radiation of lampreys. J Great Lakes Res 29:95–112

    Google Scholar 

  • Potter IC, Welsch U (1992) Arrangement, histochemistry and fine structure of the connective tissue architecture of lampreys. J Zool 226:1–30

    Google Scholar 

  • Potter IC, Wright GM, Youson JH (1978) Metamorphosis in the anadromous sea lamprey, Petromyzon marinus L. Can J Zool 56:561–570

    CAS  PubMed  Google Scholar 

  • Potter IC, Hilliard RW, Bird DJ (1980) Metamorphosis in the southern hemisphere lamprey, Geotria australis. J Zool 190:405–430

    Google Scholar 

  • Potter IC, Hilliard RW, Bird DJ (1982) Stages in metamorphosis. In: Hardisty MW, Potter IC (eds) Biology of lampreys, vol 4b. Academic Press, London, pp 137–164

    Google Scholar 

  • Pough FH, Janis CM, Heiser JB (2013) Vertebrate Life, 9th edn. Pearson, Boston

    Google Scholar 

  • Power DM, Einarsdottir IE, Pittman K et al (2008) The molecular and endocrine basis of flatfish metamorphosis. Rev Fish Sci 16:95–111

    CAS  Google Scholar 

  • Purvis HA (1970) Growth, age at metamorphosis, and sex ratio of northern brook lamprey in a tributary of southern Lake Superior. Copeia 1970:326–332

    Google Scholar 

  • Purvis HA (1979) Variations in growth age at transformation and sex ratio of sea lampreys Petromyzon marinus reestablished in chemically treated tributaries of the Upper Great Lakes USA. Great Lakes Fish Comm Tech Rep 35:1–36

    Google Scholar 

  • Purvis HA (1980) Effects of temperature on metamorphosis and the age and length at metamorphosis in sea lamprey (Petromyzon marinus) in the Great Lakes. Can J Fish Aquat Sci 37:1827–1834

    Google Scholar 

  • Reis-Santos P, McCormick SD, Wilson JM (2008) Ionoregulatory changes during metamorphosis and salinity exposure of juvenile sea lamprey (Petromyzon marinus L.). J Exp Biol 211:978–988

    CAS  PubMed  Google Scholar 

  • Rémy C, Bounhiol JJ (1971) Normalized metamorphosis achieved by adrenocorticotropic hormone in hypophysectomized and thyroxined Alytes tadpoles. C R Acad Sci Hebd Seances Acad Sci D 272:455–458

    PubMed  Google Scholar 

  • Renaud CB (1986) Eudontomyzon hellenicus Vladykov, Renaud, Kott, and Economidis, 1982. In: Holčík J (ed) The freshwater fishes of Europe, vol 1, part 1, Petromyzontiformes. AULA, Wiesbaden, pp 186–195

    Google Scholar 

  • Renaud CB, Cochran PA (in press) Post-metamorphic feeding in lampreys. In: Docker MF (ed) Lampreys: biology, conservation and control, vol 2. Springer, Dordrecht

    Google Scholar 

  • Renaud CB, Holčík J (1986) Eudontomyzon danfordi Regan, 1911. In: J Holčík (ed) The freshwater fishes of Europe, vol 1, part 1, Petromyzontiformes. AULA-Verlag, Wiesbaden, Germany, pp 146–164

    Google Scholar 

  • Renaud CB, Docker MF, Mandrak NE (2009) Taxonomy, distribution, and conservation of lampreys in Canada. In: Brown LR, Chase SD, Mesa MG, Beamish RJ, Moyle PB (eds) Biology, management, and conservation of lampreys in North America. American Fisheries Society Symposium 72, Bethesda, pp 293–309

    Google Scholar 

  • Richards JE, Beamish FWH (1981) Initiation of feeding and salinity tolerance in the Pacific lamprey Lampetra tridentata. Mar Biol 63:73–77

    Google Scholar 

  • Richardson SJ (2008) Marsupial models for understanding evolution of thyroid hormone distributor proteins. Mol Cell Endocrinol 293:32–42

    CAS  PubMed  Google Scholar 

  • Richardson SJ, Monk JA, Shepherdley CA et al (2005) Developmentally regulated thyroid hormone distributor proteins in marsupials, a reptile, and fish. Am J Physiol Regul Integr Comp Physiol 288:R1264–R1272

    Google Scholar 

  • Richardson MK, Admiraal J, Wright GM (2010) Developmental anatomy of lampreys. Biol Rev 85:1–33

    PubMed  Google Scholar 

  • Ricker WE (1975) Computation and interpretation of biological statistics of fish populations. Bulletin Fisheries Research Board of Canada 191, Ottawa

    Google Scholar 

  • Robson P (1998) Biochemical and molecular studies of the cartilaginous endoskeleton of adult lampreys and hagfish. PhD thesis, University of Toronto, Toronto

    Google Scholar 

  • Robson P, Wright GM, Sitarz E et al (1993) Characterization of lamprin, an unusual matrix protein from lamprey cartilage. Implications for evolution, structure, and assembly of elastin and other fibrillar proteins. J Biol Chem 268:1440–1447

    CAS  PubMed  Google Scholar 

  • Robson P, Wright GM, Youson JH, Keeley FW (1997) A family of non-collagen-based cartilages in the skeleton of the sea lamprey, Petromyzon marinus. Comp Biochem Physiol B Biochem Mol Biol 118:71–78

    Google Scholar 

  • Robson P, Wright GM, Youson JH, Keeley FW (2000) The structure and organization of lamprin genes: multiple-copy genes with alternative splicing and convergent evolution with insect structural proteins. Mol Biol Evol 17:1739–1752

    CAS  PubMed  Google Scholar 

  • Rodríguez-Muñoz R, Nicieza AG, Braña F (2003) Density-dependent growth of sea lamprey larave: evidence for chemical interference. Funct Ecol 17:403–408

    Google Scholar 

  • Root AR, Nucci NV, Sanford JD et al (2005) In situ characterization of gonadotropin-releasing hormone-I, -III, and glutamic acid decarboxylase expression in the brain of the sea lamprey, Petromyzon marinus. Brain Behav Evol 65:60–70

    PubMed  Google Scholar 

  • Sargent PA, Youson JH (1986) Quantification of iron deposits in several body tissues of lampreys (Petromyzon marinus L.) throughout the life cycle. Comp Biochem Physiol A Physiol 83:573–577

    Google Scholar 

  • Sauka-Spengler T, Bronner-Fraser M (2008) Insights from a sea lamprey into the evolution of neural crest gene regulatory network. Biol Bull 214:303–314

    PubMed  Google Scholar 

  • Schinko I, Potter IC, Welsch U, Debbage P (1992) Structure and development of the notochord elastica externa and nearby components of the elastic fiber system of agnathans. Acta Zool 73:57–66

    Google Scholar 

  • Sheren SB, Eikenberry EF, Broek DL et al (1986) Type-II collagen of lamprey. Comp Biochem Physiol B Biochem Mol Biol 85:5–14

    CAS  Google Scholar 

  • Shi YB (2000) Amphibian metamorphosis: from morphology to molecular biology. Wiley, New York

    Google Scholar 

  • Shi YB, Ishizuya-Oka A (1996) Biphasic intestinal development in amphibians: embryogenesis and remodeling during metamorphosis. Curr Top Dev Biol 32:205–235

    CAS  PubMed  Google Scholar 

  • Smalley SR, Macey DJ, Potter IC (1986) Changes in the amount of non-heme iron in the plasma, whole body, and selected organs during the postlarval life of the lamprey Geotria australis. J Exp Zool 237:149–157

    CAS  PubMed  Google Scholar 

  • Smith AI, Funder JW (1988) Proopiomelanocortin processing in the pituitary, central nervous system, and peripheral tissues. Endocr Rev 9:159–179

    CAS  PubMed  Google Scholar 

  • Smith BR, Tibbles JJ (1980) Sea lamprey (Petromyzon marinus) in Lakes Huron, Michigan, and Superior: history of invasion and control, 1936-78. Can J Fish Aquat Sci 37:1780–1801

    Google Scholar 

  • Sower SA (1998) Brain and pituitary hormones of lampreys, recent findings and their evolutionary significance. Am Zool 38:15–38

    CAS  Google Scholar 

  • Sower SA, Plisetskaya E, Gorbman A (1985) Steroid and thyroid hormone profiles following a single injection of partly purified salmon gonadotropin or GnRH analogs in male and female sea lamprey. J Exp Zool 235:403–408

    CAS  PubMed  Google Scholar 

  • Sower SA, Freamat M, Kavanaugh SI (2009) The origins of the vertebrate hypothalamic-pituitary-gonadal (HPG) and hypothalamic-pituitary-thyroid (HPT) endocrine systems: new insights from lampreys. Gen Comp Endocrinol 161:20–29

    CAS  PubMed  Google Scholar 

  • Stilborn SSM, Manzon LA, Schauenberg JD, Manzon RG (2009) Expression of sea lamprey, Petromyzon marinus, deiodinase type II throughout metamorphosis and following a thyroid challenge. Integr Comp Biol 49:E163

    Google Scholar 

  • Sudo S, Kuwabara Y, Park JI, Hsu SY, Hsueh AJW (2005) Heterodimeric fly glycoprotein hormone-α2 (GPA2) and glycoprotein hormone-β5 (GPB5) activate fly leucine-rich repeat-containing G protein-coupled receptor-1 (DLGR1) and stimulation of human thyrotropin receptors by chimeric fly GPA2 and human GPB5. Endocrinology 146:3596–3604

    CAS  PubMed  Google Scholar 

  • Suzuki S (1986) Induction of metamorphosis and thyroid function in the larval lamprey. Front Thyroidol 1:667–670

    Google Scholar 

  • Suzuki S (1987) Induction of metamorphosis and thyroid function in the larval lamprey. In: Ohnishi E, Nagahama Y, Ishizaki H (eds) Proceedings of the 1st Congress of the Asia Oceania Society for Comparative Endocrinology, Nagoya University Press, Nagoya, Japan, pp 220–221

    Google Scholar 

  • Suzuki S (1989) Why goitrogens are chemical triggers of metamorphosis in the lamprey relationship between thyroid-function and metamorphosis. Gen Comp Endocrinol 74:277

    Google Scholar 

  • Swink WD (1995) Growth and survival of newly parasitic sea lampreys at representative winter temperatures. Trans Am Fish Soc 124:380–386

    Google Scholar 

  • Swink WD, Johnson NS (2014) Growth and survival of sea lampreys from metamorphosis to spawning in Lake Huron. Trans Am Fish Soc 143:380–386

    Google Scholar 

  • Takahashi A, Amemiya Y, Sarashi M, Sower SA, Kawauchi H (1995) Melanotropin and corticotropin are encoded on two distinct genes in the lamprey, the earliest evolved extant vertebrate. Biochem Biophys Res Commun 213:490–498

    CAS  PubMed  Google Scholar 

  • Tata JR (2006) Amphibian metamorphosis as a model for the developmental actions of thyroid hormone. Mol Cell Endocrinol 246:10–20

    CAS  PubMed  Google Scholar 

  • Tata JR, Baker BS, Machuca I, Rabelo EML, Yamauchi K (1993) Autoinduction of nuclear receptor genes and its significance. J Steroid Biochem Mol Biol 46:105–119

    CAS  PubMed  Google Scholar 

  • Tobet SA, Nozaki M, Youson JH, Sower SA (1995) Distribution of lamprey gonadotropin-releasing hormone-III (GnRH-III) in brains of larval lampreys (Petromyzon marinus). Cell Tissue Res 279:261–270

    CAS  Google Scholar 

  • Tobet SA, Chickering TW, Sower SA (1996) Relationship of gonadotropin-releasing hormone (GnRH) neurons to the olfactory system in developing lamprey (Petromyzon marinus). J Comp Neurol 376:97–111

    CAS  PubMed  Google Scholar 

  • Tobet SA, Sower SA, Schwarting GA (1997) Gonadotropin-releasing hormone containing neurons and olfactory fibers during development: from lamprey to mammals. Brain Res Bull 44:479–486

    CAS  PubMed  Google Scholar 

  • Treble AJ, Jones ML, Steeves TB (2008) Development and evaluation of a new predictive model for metamorphosis of Great Lakes larval sea lamprey (Petromyzon marinus) populations. J Great Lakes Res 34:404–417

    Google Scholar 

  • Tsuneki K, Ouji M (1984) Morphometric changes during growth of the brook lamprey Lampetra reissneri. Jpn J Ichthyol 31:38–46

    Google Scholar 

  • Vladykov VD (1985) Does neoteny occur in holarctic lampreys (Petromyzontidae)? Syllogeus 57:1–13

    Google Scholar 

  • Walsh SR, Burr BM (1981) Distribution, morphology and life history of the least brook lamprey, Lampetra aepyptera (Pisces: Petromyzontidae) in Kentucky. Brimleyana 6:83–100

    Google Scholar 

  • Welsch U, Erlinger R, Potter IC (1991) Proteoglycans in the notochord sheath of lampreys. Acta Histochem 91:59–65

    CAS  PubMed  Google Scholar 

  • White B, Nicoll CS (1981) Hormonal control of amphibian metamorphosis. In: Gilbert LA, Frieden E (eds) Metamorphosis: a problem in developmental biology. Plenum, New York, pp 263–396

    Google Scholar 

  • Wright GM, Youson JH (1976) Transformation of the endostyle of anadromous sea lamprey, Petromyzon marinus L, during metamorphosis. 1. Light microscopy and autoradiography with 125I. Gen Comp Endocrinol 30:243–257

    CAS  PubMed  Google Scholar 

  • Wright GM, Youson JH (1977) Serum thyroxine concentrations in larval and metamorphosing anadromous sea lamprey, Petromyzon marinus L. J Exp Zool 202:27–32

    CAS  PubMed  Google Scholar 

  • Wright GM, Youson JH (1980) Transformation of the endostyle of the anadromous sea lamprey, Petromyzon marinus L, during metamorphosis. 2. Electron microscopy. J Morphol 166:231–257

    Google Scholar 

  • Wright GM, Youson JH (1982) Ultrastructure of mucocartilage in the larval anadromous sea lamprey, Petromyzon marinus L. Am J Anat 165:39–51

    CAS  PubMed  Google Scholar 

  • Wright GM, Youson JH (1983) Ultrastructure of cartilage from young adult sea lamprey, Petromyzon marinus L: a new type of vertebrate cartilage. Am J Anat 167:59–70

    CAS  PubMed  Google Scholar 

  • Wright GM, Filosa MF, Youson JH (1978) Immunocytochemical localization of thyroglobulin in endostyle of anadromous sea lamprey, Petromyzon marinus L. Am J Anat 152:263–268

    CAS  PubMed  Google Scholar 

  • Wright GM, Filosa MF, Youson JH (1980) Immunocytochemical localization of thyroglobulin in the transforming endostyle of anadromous sea lampreys, Petromyzon marinus L, during metamorphosis. Gen Comp Endocrinol 42:187–194

    CAS  PubMed  Google Scholar 

  • Wright GM, Armstrong LA, Jacques AM, Youson JH (1988) Trabecular, nasal, branchial, and pericardial cartilages in the sea lamprey, Petromyzon marinus: fine structure and immunohistochemical detection of elastin. Am J Anat 182:1–15

    CAS  PubMed  Google Scholar 

  • Wright GM, Mcburney KM, Youson JH, Sower SA (1994) Distribution of lamprey gonadotropin-releasing-hormone in the brain and pituitary gland of larval, metamorphic, and adult sea lampreys, Petromyzon marinus. Can J Zool 72:48–53

    CAS  Google Scholar 

  • Yaghoubian S, Filosa MF, Youson JH (2001) Proteins immunoreactive with antibody against a human leptin fragment are found in serum and tissues of the sea lamprey, Petromyzon marinus L. Comp Biochem Physiol B Biochem Mol Biol 129:777–785

    CAS  PubMed  Google Scholar 

  • Yamano K (2005) The role of thyroid hormone in fish development with reference to aquaculture. Jpn Agric Res Q 39:161–168

    CAS  Google Scholar 

  • Yamano K, Miwa S (1998) Differential gene expression of thyroid hormone receptor α and β in fish development. Gen Comp Endocrinol 109:75–85

    CAS  PubMed  Google Scholar 

  • Yamauchi K, Kasahara T, Hayashi H, Horiuchi R (1993) Purification and characterization of a 3,5,3ʹ-L-triiodothyronine-specific binding protein from bullfrog tadpole plasma: a homolog of mammalian transthyretin. Endocrinology 132:2254–2261

    CAS  PubMed  Google Scholar 

  • Yao T, Ohtani K, Wada H (2008) Whole mount observation of pharyngeal and trabecular cartilage development in lampreys. Zool Sci 25:976–981

    PubMed  Google Scholar 

  • Young JZ, Bellerby CW (1935) The response of the lamprey to injection of anterior lobe pituitary extract. J Exp Biol 12:246–253

    Google Scholar 

  • Youson JH (1980) Morphology and physiology of lamprey metamorphosis. Can J Fish Aquat Sci 37:1687–1710

    Google Scholar 

  • Youson JH (1981a) The alimentary canal. In: Hardisty MW, Potter IC (eds) The biology of lampreys, vol 3. Academic Press, London, pp 95–189

    Google Scholar 

  • Youson JH (1981b) The kidneys. In: Hardisty MW, Potter IC (eds) The biology of lampreys, vol 3. Academic Press, London, pp 192–261

    Google Scholar 

  • Youson JH (1981c) The liver. In: Hardisty MW, Potter IC (eds) The biology of lampreys, vol 3. Academic Press, New York, pp 262–332

    Google Scholar 

  • Youson JH (1982) Replication of basal bodies and ciliogenesis in a ciliated epithelium of the lamprey. Cell Tissue Res 223:255–266

    CAS  PubMed  Google Scholar 

  • Youson JH (1984) Differentiation of the segmented tubular nephron and excretory duct during lamprey metamorphosis. Anat Embryol 169:275–292

    CAS  PubMed  Google Scholar 

  • Youson J (1985) Organ development and specialization in lamprey species. In: Foreman RE, Gorbman A, Dodd JM, Olsson R (eds) The evolutionary biology of primitive fishes. Plenum, New York, pp 141–156

    Google Scholar 

  • Youson JH (1988) First metamorphosis. In: Hoar WS, Randall DJ (eds) Fish physiology: the physiology of developing fish, vol 11A. Academic Press, New York, pp 135–196

    Google Scholar 

  • Youson JH (1993) Biliary atresia in lampreys. In: Cornelius CE (ed) Advances in veterinary science and comparative medicine, vol 37, animal models in liver research. Academic Press, San Diego, pp 197–255

    Google Scholar 

  • Youson (1994) Environmental and hormonal cues and endocrine glands during lamprey metamorphosis. In: Davey KG, Peter RE, Tobe SS (eds) Perspectives in comparative endocrinology. National Research Council of Canada, Ottawa, pp 400–408

    Google Scholar 

  • Youson JH (1997) Is lamprey metamorphosis regulated by thyroid hormones? Am Zool 37:441–460

    CAS  Google Scholar 

  • Youson JH (2000) The agnathan enteropancreatic endocrine system: phylogenetic and ontogenetic histories, structure, and function. Am Zool 40:179–199

    Google Scholar 

  • Youson JH (2003) The biology of metamorphosis in sea lampreys: endocrine, environmental, and physiological cues and events, and their potential application to lamprey control. J Great Lakes Res 29(Suppl 1):26–49

    Google Scholar 

  • Youson JH (2004) The impact of environmental and hormonal cues on the evolution of fish metamorphosis. In: Hall BK, Pearson RD, Muller GB (eds) Environment, development, and evolution: toward a synthesis. Massachusetts Institute of Technology Press, Cambridge, pp 239–278

    Google Scholar 

  • Youson JH (2007) Peripheral endocrine glands. I. The gastroenteropancreatic endocrine system and the thyroid gland. In: McKenzie DJ, Farrell AP, Brauner CJ (eds) Primitive fishes. Academic Press, New York, pp 381–455

    Google Scholar 

  • Youson JH, Al-Mahrouki AA (1999) Ontogenetic and phylogenetic development of the endocrine pancreas (islet organ) in fishes. Gen Comp Endocrinol 116:303–335

    CAS  PubMed  Google Scholar 

  • Youson JH, Beamish RJ (1991) Comparison of the internal morphology of adults of a population of lampreys that contains a nonparasitic life-history type, Lampetra richardsoni, and a potentially parasitic form, L. richardsoni var. marifuga. Can J Zool 69:628–637

    Google Scholar 

  • Youson JH, Cheung R (1990) Morphogenesis of somatostatin- and insulin-secreting cells in the lamprey endocrine pancreas. Fish Physiol Biochem 8:389–397

    CAS  PubMed  Google Scholar 

  • Youson JH, Connelly KL (1978) Development of longitudinal mucosal folds in intestine of the anadromous sea lamprey, Petromyzon marinus L, during metamorphosis. Can J Zool 56:2364–2371

    Google Scholar 

  • Youson JH, Elliott WM (1989) Morphogenesis and distribution of the endocrine pancreas in adult lampreys. Fish Physiol Biochem 7:125–131

    CAS  PubMed  Google Scholar 

  • Youson JH, Horbert WR (1982) Transformation of the intestinal epithelium of the larval anadromous sea lamprey, Petromyzon marinus L., during metamorphosis. J Morphol 171:89–117

    Google Scholar 

  • Youson JH, Manzon RG (2012) Lamprey metamorphosis. In: Dufour S, Rousseau K, Kapoor BG (eds) Metamorphosis in fish. Science Publishers, Enfield, pp 12–75

    Google Scholar 

  • Youson JH, Potter IC (1979) Description of the stages in the metamorphosis of the anadromous sea lamprey, Petromyzon marinus L. Can J Zool 57:1808–1817

    Google Scholar 

  • Youson JH, Potter IC (1993a) An immunohistochemical study of enteropancreatic endocrine cells in larvae and juveniles of the southern-hemisphere lampreys Geotria australis and Mordacia mordax. Gen Comp Endocrinol 92:151–167

    CAS  Google Scholar 

  • Youson JH, Potter IC (1993b) An immunohistochemical study of enteropancreatic endocrine cells in larvae and juveniles of the Southern-Hemisphere lampreys Geotria australis and Mordacia mordax. Gen Comp Endocrinol 92:151–167

    CAS  Google Scholar 

  • Youson JH, Sower SA (1991) Concentration of gonadotropin-releasing-hormone in the brain during metamorphosis in the lamprey, Petromyzon marinus. J Exp Zool 259:399–404

    CAS  Google Scholar 

  • Youson JH, Sower SA (2001) Theory on the evolutionary history of lamprey metamorphosis: role of reproductive and thyroid axes. Comp Biochem Physiol B Biochem Mol Biol 129:337–345

    CAS  PubMed  Google Scholar 

  • Youson JH, Lee J, Potter IC (1979) Distribution of fat in larval, metamorphosing, and young adult anadromous sea lampreys, Petromyzon marinus L. Can J Zool 57:237–246

    Google Scholar 

  • Youson JH, Sargent PA, Sidon EW (1983) Iron loading in the livers of metamorphosing lampreys, Petromyzon marinus L. Cell Tissue Res 234:109–124

    CAS  PubMed  Google Scholar 

  • Youson JH, Sargent PA, Barrett A (1987) Serum iron concentration and other blood parameters during the life cycle of the sea lamprey, Petromyzon marinus L. Comp Biochem Physiol A Physiol 88:325–330

    Google Scholar 

  • Youson JH, Elliott WM, Beamish RJ, Wang DW (1988) A comparison of endocrine pancreatic tissue in adults of four species of lampreys in British Columbia: a morphological and immunohistochemical study. Gen Comp Endocrinol 70:247–261

    CAS  PubMed  Google Scholar 

  • Youson JH, Holmes JA, Guchardi JA et al (1993) Importance of condition factor and the influence of water temperature and photoperiod on metamorphosis of sea lamprey, Petromyzon marinus. Can J Fish Aquat Sci 50:2448–2456

    Google Scholar 

  • Youson JH, Plisetskaya EM, Leatherland JF (1994) Concentrations of insulin and thyroid hormones in the serum of landlocked sea lampreys (Petromyzon marinus) of three larval year classes, in larvae exposed to two temperature regimes, and in individuals during and after metamorphosis. Gen Comp Endocrinol 94:294–304

    CAS  PubMed  Google Scholar 

  • Youson JH, Docker M, Sower SA (1995a) Concentration of gonadotropin-releasing hormones in brain of larval and metamorphosing lampreys of two species with different adult life histories. In: Goetz FW, Thomas P (eds) Proceedings of the 5th Internatinal Symposium Reproductive Physiology of Fish. University of Texas Press, Austin, p 83

    Google Scholar 

  • Youson JH, Holmes JA, Leatherland JF (1995b) Serum concentrations of thyroid hormones in KClO4-treated larval sea lampreys (Petromyzon marinus L). Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 111:265–270

    Google Scholar 

  • Youson JH, Manzon RG, Peck BJ, Holmes JA (1997) Effects of exogenous thyroxine (T4) and triiodothyronine (T3) on spontaneous metamorphosis and serum T4 and T3 levels in immediately premetamorphic sea lampreys, Petromyzon marinus. J Exp Zool 279:145–155

    CAS  PubMed  Google Scholar 

  • Youson JH, Heinig JA, Khanam SF et al (2006) Patterns of proopiomelanotropin and prooplocortin gene expression and of immunohistochemistry for gonadotropin-releasing hormones (GnRH-I and III) during the life cycle of a nonparasitic lamprey: relationship to this adult life history type. Gen Comp Endocrinol 148:54–71

    CAS  PubMed  Google Scholar 

  • Zanandrea G (1957) Neoteny in a lamprey. Nature 179:925–926

    CAS  PubMed  Google Scholar 

  • Zerrenner A, Marsden JE (2005) Influence of larval sea lamprey density on transformer life history characteristics in Lewis Creek, Vermont. Trans Am Fish Soc 134:687–696

    Google Scholar 

  • Zerrenner A, Marsden JE (2006) Comparison of larval sea lamprey life history characteristics in a lampricide-treated tributary and untreated tributary system of Lake Champlain. Trans Am Fish Soc 134:1301–1311

    Google Scholar 

  • Zhang G (2009) An evo-devo view on the origin of the backbone: evolutionary development of the vertebrae. Integr Comp Biol 49:178–186

    CAS  PubMed  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 103:3180–3185

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard G. Manzon .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Manzon, R., Youson, J., Holmes, J. (2015). Lamprey Metamorphosis. In: Docker, M. (eds) Lampreys: Biology, Conservation and Control. Fish & Fisheries Series, vol 37. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9306-3_4

Download citation

Publish with us

Policies and ethics