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The evolution of lamprey (Petromyzontida) life history and the origin of metamorphosis

Abstract

Modern lampreys (Petromyzontiformes) are one of two lineages of surviving jawless fishes (agnathans), and are thus of critical importance to understanding the evolution of the vertebrates. Although their fossil record is meager, it appears they have remained morphologically conserved for at least 360 million years, but the origin of their multi-stage life history is unclear. Unlike hagfishes, the other extant group of jawless fishes, which exhibit direct development, all modern lampreys possess a complex life cycle which includes a long-lived freshwater larval (or ammocoete) period, followed by a true metamorphosis into a sexually-immature juvenile and then mature adult which differ dramatically in their morphology and ecology from the larva. Because of their basal position, it is critical to understand when the extant lamprey life history evolved, and if such a life history was present in the last common ancestor of agnathans and gnathostomes. Recent discoveries in paleontology, genomic analyses, and developmental biology are providing insights into this problem. The current review synthesizes these findings and concludes that the ancestral lamprey life cycle followed a direct development. We suggest that the larval period was short and relatively limited if present at all, but that the juvenile included modern larval traits; over the course of evolution, differential selection pressures throughout the lifetime produced distinct larval and juvenile/adult periods. Each period required the dramatically different morphologies seen in modern lampreys, ultimately requiring a true metamorphosis to accommodate the large changes in the body plan and to maximize the efficiency of each life period. As a result, modern lamprey life histories are a patchwork of ancestral and derived characters.

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Notes

  1. 1.

    Conodonts are an enigmatic “fish-like” group, which may or may not be vertebrates. They suffered prodigious extinctions at the end of the Permian (250 million years [Ma] ago), but persisted until the end of the Triassic (201 Ma ago) when the whole lineage became extinct. For the purposes of the present paper they are assumed not to belong to the vertebrate family tree (Nelson et al. 2016). However, conodonts may be vertebrates and possibly cyclostomes (Janvier 2015).

  2. 2.

    While the term “parasitic” is commonly used to describe feeding juvenile lampreys (Potter et al. 2015), juvenile lampreys actually display a range of feeding behaviors (Renaud et al. 2009) from predatory (consumption of multiple prey items) to fully parasitic (removal of a portion of prey item, without necessarily killing the host) which varies between species (Hardisty 2011) and across the juvenile stage (Bence et al. 2003; Madenjian et al. 2003). For instance, small landlocked sea lamprey (Petromyzon marinus) feed on the body fluids of hosts, and probably cause limited host mortality, but as they increase in size their feeding almost always ends in host death (Bence et al. 2003) even though only a portion of the host’s body is consumed (Bergstedt and Schneider 1988). In contrast, Carpathian lamprey (Eudontomyzon danfordi) consume varying portions of the prey, but often eat heart tissue and bones (Talabishka et al. 2012) suggesting a truly predatory relationship. Finally, Arctic lamprey (Lethenteron camtschaticum) stomach contents include fins, scales, vertebral columns, eggs, and internal organs of prey (Shink 2017) showing a range of possible feeding behaviors from parasitic to predatory. Regardless, the literature precedent is to describe lampreys as parasitic or non-parasitic, so the terms are adopted here.

References

  1. Bardack D, Zangerl R (1968) First fossil lamprey: a record from the Pennsylvanian of Illinois. Science 162:1265–1267. https://doi.org/10.1126/science.162.3859.1265

    CAS  Article  PubMed  Google Scholar 

  2. Beamish FWH (1980a) Biology of the North American anadromous sea lamprey, Petromyzon marinus. Can J Fish Aquat Sci 37:1924–1943. https://doi.org/10.1139/f80-233

    Article  Google Scholar 

  3. Beamish RJ (1980b) Adult biology of the River Lamprey (Lampetra ayresi) and the Pacific Lamprey (Lampetra tridentata) from the Pacific Coast of Canada. Can J Fish Aquat Sci 37:1906–1923. https://doi.org/10.1139/f80-232

    Article  Google Scholar 

  4. Beamish RJ, Levings CD (1991) Abundance and freshwater migrations of the anadromous parasitic lamprey, Lampetra tridentata, in a tributary of the Fraser River, British Co. Can J Fish Aquat Sci 48:1250–1263. https://doi.org/10.1139/f91-151

    Article  Google Scholar 

  5. Beamish FWH, Lowartz S (1996) Larval habitat of American brook lamprey. Can J Fish Aquat Sci 53:693–700. https://doi.org/10.1139/f95-232

    Article  Google Scholar 

  6. Belles X (2011) Origin and evolution of insect metamorphosis. Encyclopedia of life sciences. Wiley, Chichester

    Google Scholar 

  7. Bence JR, Bergstedt RA, Christie GC, Cochran PA, Ebener MP, Koonce JF, Rutter MA, Swink WD (2003) Sea lamprey (Petromyzon marinus) parasite-host interactions in the Great Lakes. J Gt Lakes Res 29(Supplement 1):253–282. https://doi.org/10.1016/S0380-1330(03)70493-6

    Article  Google Scholar 

  8. Bergstedt RA, Schneider CP (1988) Assessment of sea lamprey (Petromyzon marinus) predation by recovery of dead lake trout (Salvelinus namaycush) from Lake Ontario, 1982–1985. Can J Fish Aquat Sci 45:1406–1410. https://doi.org/10.1139/f88-164

    Article  Google Scholar 

  9. Bergstedt RA, Swink WD (1995) Seasonal growth and duration of the parasitic life stage of the landlocked sea lamprey (Petromyzon marinus). Can J Fish Aquat Sci 52:1257–1264. https://doi.org/10.1139/f95-122

    Article  Google Scholar 

  10. Bird DJ, Potter IC (1979) Metamorphosis in the paired species of lampreys, Lampetra fluviatilis (L.) and Lampetra planeri (Bloch): 2. Quantitative data for body proportions, weights, lengths and sex ratios. Zool J Linn Soc 65:145–160. https://doi.org/10.1111/j.1096-3642.1979.tb01087.x

    Article  Google Scholar 

  11. Bird DJ, Potter IC (1981) Proximate body composition of the larval, metamorphosing and downstream migrant stages in the life cycle of the Southern Hemisphere lamprey, Geotria australis. Environ Biol Fishes 6:285–297. https://doi.org/10.1007/BF00005758

    Article  Google Scholar 

  12. Bird DJ, Potter IC, Hardisty MW, Baker BI (1994) Morphology, body size and behavior of recently-metamorphosed sea lampreys, Petromyzon marinus, from the lower River Severn, and their relevance to the onset of parasitic feeding. J Fish Biol 44:67–74. https://doi.org/10.1111/j.1095-8649.1994.tb01586.x

    Article  Google Scholar 

  13. Callery EM, Hung F, Elinson RP (2001) Frogs without polliwogs: evolution of anuran direct development. BioEssays 23:233–241. https://doi.org/10.1002/1521-1878(200103)23:3%3c233:AID-BIES1033%3e3.0.CO;2-Q

    CAS  Article  PubMed  Google Scholar 

  14. Chang M, Zhang J, Miao D (2006) A lamprey from the Cretaceous Jehol biota of China. Nature 441:972–974. https://doi.org/10.1073/pnas.1415716111

    CAS  Article  PubMed  Google Scholar 

  15. Chang M, Wu F, Miao D, Zhang J (2014) Discovery of fossil lamprey larva from the Lower Cretaceous reveals its three-phased life cycle. Proc Natl Acad Sci 111:15486–15490

    CAS  Article  Google Scholar 

  16. Cochran PA (2014) Field and laboratory observations on the ecology and behavior of the chestnut lamprey Ichthyomyzon castaneus. J Freshw Ecol 29:491–505. https://doi.org/10.1080/02705060.2014.910477

    CAS  Article  Google Scholar 

  17. Dawson HA, Quintella BR, Almeida PR, Treble AJ, Jolley JC (2015) The ecology of larval and metamorphosing lampreys. In: Docker MF (ed) Lampreys: biology, conservation and control. Springer, New York, pp 75–138

    Google Scholar 

  18. Derosier A, Jones M, Scribner K (2007) Dispersal of sea lamprey larvae during early life: relevance for recruitment dynamics. Environ Biol Fishes 78:271–284. https://doi.org/10.1007/s10641-006-9095-3

    Article  Google Scholar 

  19. Docker MF (2009) A review of the evolution of nonparasitism in lampreys and an update of the paired species concept. In: Brown L, Chase S, Mesa M, Beamish R, Moyle PB (eds) Biology, management, and conservation of lampreys in North America. American Fisheries Society, Bethesda, pp 71–114

    Google Scholar 

  20. 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. Environ Biol Fishes 41:191–205. https://doi.org/10.1007/BF02197844

    Article  Google Scholar 

  21. Docker MF, Hume JB, Clemens BJ (2015) Introduction: a surfeit of lampreys. In: Docker MF (ed) Lampreys: biology, conservation and control. Springer, New York, pp 1–34

    Google Scholar 

  22. Donoghue PCJ, Keating JN (2014) Early vertebrate evolution. Palaeontology 57:879–893. https://doi.org/10.1111/pala.12125

    Article  Google Scholar 

  23. Engel MS (2015) Insect evolution. Curr Biol 25:R868–R872. https://doi.org/10.1016/j.cub.2015.07.059

    CAS  Article  PubMed  Google Scholar 

  24. Evans TM (2017) Measuring the growth rate in three populations of larval lampreys with mark-recapture techniques. Trans Am Fish Soc 146:147–159. https://doi.org/10.1080/00028487.2016.1249292

    Article  Google Scholar 

  25. Evans TM, Bauer JE (2016a) Identification of the nutritional resources of larval Sea Lamprey in two Great Lakes tributaries using stable isotopes. J Gt Lakes Res 42:99–107. https://doi.org/10.1016/j.jglr.2015.11.010

    Article  Google Scholar 

  26. Evans TM, Bauer JE (2016b) Using stable isotopes and C:N ratios to examine the life-history strategies and nutritional sources of larval lampreys. J Fish Biol 88:638–654. https://doi.org/10.1111/jfb.12858

    CAS  Article  PubMed  Google Scholar 

  27. Fernholm B (1974) Diurnal variations in the behavior of the hagfish Eptatretus burger. Mar Biol 27:351–356. https://doi.org/10.1007/BF00394371

    Article  Google Scholar 

  28. Gabbott SE, Donoghue PCJ, Sansom RS, Vinther J, Dolocan A, Purnell MA (2016) Pigmented anatomy in Carboniferous cyclostomes and the evolution of the vertebrate eye. Proc R Soc B Biol 278:1150–1157. https://doi.org/10.1098/rspb.2016.1151

    Article  Google Scholar 

  29. Gess RW, Coates MI, Rubidge BS (2006) A lamprey from the Devonian period of South Africa. Nature 443:981–984. https://doi.org/10.1038/nature05150

    CAS  Article  PubMed  Google Scholar 

  30. Gill HS, Renaud CB, Chapleau F, Mayden RL, Potter IC (2003) Phylogeny of living parasitic lampreys (Petromyzontiformes) based on morphological data. Copeia 4:687–703. https://doi.org/10.1643/IA02-085.1

    Article  Google Scholar 

  31. Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, New York

    Google Scholar 

  32. Hall JD (1963) An ecological study of chestnut lamprey, Ichthyomyzon castaneus Girard, in the Manistee River, Michigan. Dissertation, University of Michigan

  33. Hardisty MW (2011) Lampreys: life without jaws, 2nd edn. Forrest Text, Ceredigion

    Google Scholar 

  34. Hardisty MW, Potter IC (1971) The general biology of adult lampreys. In: Hardisty MW, Potter IC (eds) The biology of lampreys, vol 1. Academic Press, New York, pp 127–206

    Google Scholar 

  35. Haug JT, Haug C (2013) An unusual fossil larva, the ontogeny of achelatan lobsters, and the evolution of metamorphosis. Bull Geosci 88:195–206. https://doi.org/10.3140/bull.geosci.1374

    Article  Google Scholar 

  36. Haug JT, Haug C, Garwood RJ (2016) Evolution of insect wings and development—new details from Palaeozoic nymphs. Biol Rev 91:53–69. https://doi.org/10.1111/brv.12159

    Article  PubMed  Google Scholar 

  37. 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 107:19379–19383. https://doi.org/10.1073/pnas.1010350107

    Article  PubMed  Google Scholar 

  38. Janvier P (1981) The phylogeny of the Craniata, with particular reference to the significance of fossil “agnathans”. J Vertebr Paleontol 1:121–159

    Article  Google Scholar 

  39. Janvier P (1996) The dawn of the vertebrates: characters versus common ascent in the rise of current vertebrate phylogenies. Palaeontology 39:259–287

    Google Scholar 

  40. Janvier P (2008) Early jawless vertebrates and cyclostome origins. Zoolog Sci 25:1045–1056. https://doi.org/10.2108/zsj.25.1045

    Article  PubMed  Google Scholar 

  41. Janvier P (2015) Facts and fancies about early fossil chordates and vertebrates. Nature 520:483–489. https://doi.org/10.1038/nature14437

    CAS  Article  PubMed  Google Scholar 

  42. 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 29:143–216

    Google Scholar 

  43. Johnson CK, Voss SR (2013) Salamander paedomorphosis: linking thyroid hormone to life history and life cycle evolution. In: Yon-Bo S (ed) Animal metamorphosis. Academic Press, Burlington, pp 229–258

    Chapter  Google Scholar 

  44. Johnson NS, Buchinger TJ, Li W (2015) Reproductive ecology of lampreys. In: Docker MF (ed) Lampreys: biology, conservation, and control. Springer, New York, pp 265–303

    Google Scholar 

  45. Kearn GC (2004) Leeches, lice, and lampreys: a natural history of skin and gill parasites of fishes. Springer, Norwell

    Google Scholar 

  46. Keating JN, Donoghue PCJ (2016) Histology and affinity of anaspids and the early evolution of the vertebrate dermal skeleton. Proc R Soc B Bio. https://doi.org/10.1098/rspb.2015.2917

    Article  Google Scholar 

  47. Kucheryavyi AV, Savvaitova KA, Pavlov DS, Gruzdeva MA, Kuzishchin KV, Stanford JA (2007) Variations of life history strategy of the arctic lamprey Lethenteron camtschaticum from the Utkholok River (Western Kamchatka). J Ichthyol 47:37–52. https://doi.org/10.1134/S0032945207010055

    Article  Google Scholar 

  48. Kuraku S, Kuratani S (2006) Time scale for cyclostome evolution inferred with a phylogenetic diagnosis of hagfish and lamprey cDNA sequences. Zool Sci 23:1053–1064. https://doi.org/10.2108/zsj.23.1053

    CAS  Article  PubMed  Google Scholar 

  49. Lamb TD, Collin SP, Pugh EN Jr (2007) Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat Rev Neurosci 8:960–976. https://doi.org/10.1038/nrn2283

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. Lang NJ, Roe KJ, Renaud CB, Gill HS, Potter IC, Freyhof J, Naseka AM, Cochran P, Peréz HE, Habit EM, Kuhajda BR, Neely DA, Reshetnikov YS, Salnikov VB, Stoumboudi MT, Mayden RL (2009) Novel relationships among lampreys (Petromyzontiformes) revealed by a taxonomically comprehensive molecular data set. In: Brown LR, Chase SD, Mesa MG, Beamish RJ, Moyle PB (eds) Biology, management, and conservation of lampreys in North America. American Fisheries Society, Bethesda, pp 41–55

    Google Scholar 

  51. Løvtrup S (1977) The phylogeny of the Vertebrata. Wiley, New York

    Google Scholar 

  52. Lowe DR, Beamish FWH, Potter IC (1973) Changes in the proximate body composition of the landlocked sea lamprey Petromyzon marinus (L.) during larval life and metamorphosis. J Fish Biol 5:673–682. https://doi.org/10.1111/j.1095-8649.1973.tb04503.x

    Article  Google Scholar 

  53. Lund R, Janvier P (1986) A second lamprey from the Lower Carboniferous (Namurian) of Bear Gulch, Montana (U.S.A.). Geobios 19:647–652. https://doi.org/10.1016/S0016-6995(86)80061-4

    Article  Google Scholar 

  54. Macey DJ, Potter IC (1978) Lethal temperatures of ammocoetes of the Southern Hemisphere lamprey, Geotria australis Gray. Environ Biol Fishes 3:241–243. https://doi.org/10.1007/BF00691950

    Article  Google Scholar 

  55. MacLeod N (2015) The great extinctions: What causes them and how they shape life. Firefly Books, New York

    Google Scholar 

  56. Madenjian CP, Cochran PA, Bergstedt RA (2003) Seasonal patterns in growth, blood consumption, and effects on hosts by parasitic-phase sea lampreys in the Great Lakes: an individual-based model approach. J Gt Lakes Res 29(Supplement 1):332–346. https://doi.org/10.1016/S0380-1330(03)70498-5

    Article  Google Scholar 

  57. Mallatt J (1984) Feeding ecology of the earliest vertebrates. Zool J Linn Soc 82:261–272. https://doi.org/10.1111/j.1096-3642.1984.tb00643.x

    Article  Google Scholar 

  58. Manzon RG, Youson JH, Holmes JA (2015) Lamprey metamorphosis. In: Docker MF (ed) Lampreys: biology, conservation and control. Springer, New York, pp 139–214

    Google Scholar 

  59. Martini FH (1998) The ecology of hagfishes. In: Jørgensen JM, Lomholt JP, Weber RE, Malte H (eds) The biology of hagfishes. Springer, New York, pp 57–77

    Chapter  Google Scholar 

  60. McMahon DP, Hayward A (2016) Why grow up? A perspective on insect strategies to avoid metamorphosis. Ecolog Entomol 41:505–515. https://doi.org/10.1111/een.12313

    Article  Google Scholar 

  61. 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. https://doi.org/10.1111/j.1095-8649.1987.tb05743.x

    Article  Google Scholar 

  62. Moser ML, Almeida PR, Kemp PS, Sorensen PW (2015) Lamprey spawning migration. In: Docker MF (ed) Lampreys: biology, conservation and control. Springer, New York, pp 215–264

    Google Scholar 

  63. Moyle PB, Cech JJ Jr (2011) Fishes: an introduction to ichthyology, 5th edn. Prentice Hall, Upper Saddle River

    Google Scholar 

  64. Murauskas JG, Orlov AM, Siwicke KA (2013) Relationships between the abundance of Pacific lamprey in the Columbia River and their common hosts in the marine environment. Trans Am Fish Soc 142:143–155. https://doi.org/10.1080/00028487.2012.730113

    Article  Google Scholar 

  65. 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. https://doi.org/10.1139/z92-027

    Article  Google Scholar 

  66. Nelson JS, Grande TC, Wilson MVH (2016) Fishes of the world, 5th edn. Wiley, New York

    Book  Google Scholar 

  67. Nichols OC, Tscherter UT (2011) Feeding of sea lampreys Petromyzon marinus on minke whales Balaenoptera acutorostrata in the St Lawrence Estuary, Canada. J Fish Biol 78:338–343. https://doi.org/10.1111/j.1095-8649.2010.02842.x

    CAS  Article  PubMed  Google Scholar 

  68. O’Boyle R, Beamish FWH (1977) Growth and intermediary metabolism of larval and metamorphosing stages of the landlocked sea lamprey, Petromyzon marinus L. Environ Biol Fishes 2:103–120. https://doi.org/10.1007/BF00005366

    Article  Google Scholar 

  69. Orlov A, Beamish R (2016) Jawless fishes of the world, vol 1. Cambridge Scholars Publishing, New Castle

    Google Scholar 

  70. 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 2:1–6. https://doi.org/10.1038/ncomms1355

    CAS  Article  Google Scholar 

  71. Ota KG, Fujimoto S, Oisi Y, Kuratani S (2013) Late development of hagfish vertebral elements. J Exp Zool B Mol Dev Evol 320:129–139. https://doi.org/10.1002/jez.b.22489

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  72. Penney D, Jepson JE (2014) Fossil insects: an introduction to palaeoentomology. Siri Scientific Press, Manchester

    Google Scholar 

  73. Potter IC (1980a) Ecology of larval and metamorphosing lampreys. Can J Fish Aquat Sci 37:1641–1657. https://doi.org/10.1139/f80-212

    Article  Google Scholar 

  74. Potter IC (1980b) The Petromyzoniformes with particular reference to paired species. Can J Fish Aquat Sci 37:1595–1615. https://doi.org/10.1139/f80-207

    Article  Google Scholar 

  75. Potter IC, Beamish FWH (1975) Lethal temperatures in ammocoetes of four species of lampreys. Acta Zoologica 56:85–91. https://doi.org/10.1111/j.1463-6395.1975.tb00084.x

    Article  Google Scholar 

  76. Potter IC, Hilliard RW (1987) A proposal for the functional and phylogenetic significance of differences in the dentition of lampreys (Agnatha: Petromyzontiformes). J Zool 212:713–737. https://doi.org/10.1111/j.1469-7998.1987.tb05966.x

    Article  Google Scholar 

  77. Potter IC, Gill HS, Renaud CB, Hanoucher D (2015) The taxonomy, phylogeny, distribution, of lampreys. In: Docker MF (ed) Lampreys: biology, conservation and control. Springer, New York, pp 35–73

    Google Scholar 

  78. Quintella BR, Andrade NO, Espanhol R, Almeida PR (2005) The use of PIT telemetry to study movements of ammocoetes and metamorphosing sea lampreys in river beds. J Fish Biol 66:97–106. https://doi.org/10.1111/j.0022-1112.2005.00584.x

    Article  Google Scholar 

  79. Rainford JL, Hofreiter M, Nicholson DB, Mayhew PJ (2014) Phylogenetic distribution of extant richness suggests metamorphosis is a key innovation driving diversification in insects. PLoS ONE 9:e109085. https://doi.org/10.1371/journal.pone.0109085

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  80. Renaud C (2011) Lampreys of the world: an annotated and illustrated catalogue of lamprey species known to date. Food and Agriculture Organization, Rome

    Google Scholar 

  81. Renaud CB, Gill HS, Potter IC (2009) Relationships between the diets and characteristics of the dentition, buccal glands and velar tentacles of the adults of the parasitic species of lamprey. J Zool 278:231–242. https://doi.org/10.1111/j.1469-7998.2009.00571.x

    Article  Google Scholar 

  82. Rohlfing K, Stuhlmann F, Docker MF, Burmester T (2016) Convergent evolution of hemoglobin switching in jawed and jawless vertebrates. BMC Evol Biol 16:1–9. https://doi.org/10.1186/s12862-016-0597-0

    CAS  Article  Google Scholar 

  83. Rose CS (2014) The importance of cartilage to amphibian development and evolution. Int J Dev Biol 58:917–927. https://doi.org/10.1387/ijdb.150053cr

    Article  PubMed  Google Scholar 

  84. Schoch RP (2009a) Evolution of life cycles in early amphibians. Annu Rev Earth Planet Sci 37:135–162. https://doi.org/10.1146/annurev.earth.031208.100113

    CAS  Article  Google Scholar 

  85. Schoch RP (2009b) Life-cycle evolution as response to diverse lake habitats in Paleozoic amphibians. Evolution 63:2738–2749. https://doi.org/10.1111/j.l558-5646.2009.0076.x

    Article  PubMed  Google Scholar 

  86. Schoch RP (2014) Life history evolution. In: Schoch RR (ed) Amphibian evolution: the life of early land vertebrates. Wiley, New York, pp 208–221

    Chapter  Google Scholar 

  87. Schoch RP, Fröbisch NB (2006) Metamorphosis and neoteny: alternative pathways in an extinct amphibian clade. Evolution 60:1467–1475. https://doi.org/10.1554/05-632.1

    Article  PubMed  Google Scholar 

  88. Schwarze K, Campbell KL, Hankeln R, Storz JF, Hoffmann FG, Burmester T (2014) The globin gene repertoire of lampreys: convergent evolution of hemoglobin and myoglobin in jawed and jawless vertebrates. Mol Biol Evol 31:2708–2721. https://doi.org/10.1093/molbev/msu216

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  89. Shimeld SM, Donoghue PCJ (2012) Evolutionary crossroads in developmental biology: cyclostomes (lamprey and hagfish). Development 139:2091–2099. https://doi.org/10.1242/dev.074716

    CAS  Article  PubMed  Google Scholar 

  90. Shink KG (2017) Characterizing the diet and population structure of lampreys Lethenteron spp. using molecular techniques. Master’s thesis, University of Alaska Fairbanks

  91. Shu DG, Luo HL, Morris SC, Zhang XL, Hu SX, Chen L, Han J, Zhu M, Li Y, Chen LZ (1999) Lower Cambrian vertebrates from south China. Nature 402:42–46. https://doi.org/10.1038/46965

    CAS  Article  Google Scholar 

  92. Shu DG, Conway Morris S, Han J, Zhang ZF, Yasui K, Janvier P, Chen L, Zhang XL, Liu JN, Li Y, Liu HQ (2003) Head and backbone of the early Cambrian vertebrate Haikouichthys. Nature 421:526–529. https://doi.org/10.1038/nature01264

    CAS  Article  PubMed  Google Scholar 

  93. Silva S, Araújo MJ, Bao M, Mucientes G, Cobo F (2014) The haematophagous feeding stage of anadromous populations of sea lamprey Petromyzon marinus: low host selectivity and wide range of habitats. Hydrobiologia 734:187–199. https://doi.org/10.1007/s1075

    CAS  Article  Google Scholar 

  94. Smith JJ, Kuraku S, Holt C, Sauka-Spengler T, Jiang N, Campbell MS, Yandell MD, Manousaki T, Meyer A, Bloom OE, Morgan JR et al (2013) Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat Genet 45:415–421. https://doi.org/10.1038/ng.2568

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  95. 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. https://doi.org/10.1016/j.ydbio.2016.11.014

    CAS  Article  PubMed  Google Scholar 

  96. Sugiyama H, Goto A (2002) Habitat selection by larvae of a fluvial lamprey, Lethenteron reissneri, in a small stream and an experimental aquarium. Ichthyol Res 49:62–68. https://doi.org/10.1007/s102280200

    Article  Google Scholar 

  97. Sutton TM, Bowen SH (1994) Significance of organic detritus in the diet of larval lampreys in the Great Lakes basin. Can J Fish Aquat Sci 51:2380–2387. https://doi.org/10.1139/f94-239

    Article  Google Scholar 

  98. Suzuki DG, Grillner S (2018) The stepwise development of the lamprey visual system and its evolutionary implications. Biol Rev. https://doi.org/10.1111/brv.12403

    Article  PubMed  Google Scholar 

  99. Talabishka EM, Bogutskaya NG, Naseka AM (2012) Local migration and feeding habitats of Carpathian lamprey Eudontomyzon danfordi (Petromyzontes: Petromyzontidae) in Tisza River system (Danube drainage, Ukraine). Proc Zool Inst RAS 316:361–368. https://doi.org/10.1134/S0032

    Article  Google Scholar 

  100. Truman JW, Riddiford LM (1999) The origins of insect metamorphosis. Nature 401:447–452. https://doi.org/10.1038/46737

    CAS  Article  PubMed  Google Scholar 

  101. Wallace MW, AvS Hood, Shuster A, Greig A, Planavsky NJ, Reed CP (2017) Oxygenation history of the Neoproterozoic to early Phanerozoic and the rise of land plants. Earth Planet Sci Lett 466(12):19. https://doi.org/10.1016/j.epsi.2017.02.046

    Article  Google Scholar 

  102. Young RJ, Kelso JRM, Weise JG (1990) Occurrence, relative abundance, and size of landlocked sea lamprey (Petromyzon marinus) ammocoetes in relation to stream characteristics in the Great Lakes. Can J Fish Aquat Sci 47:1773–1778. https://doi.org/10.1139/f90-201

    Article  Google Scholar 

  103. 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: towards a synthesis. Massachusetts Institute of Technology Press, Cambridge, pp 239–278

    Google Scholar 

  104. 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. https://doi.org/10.1016/S1546-5098(07)26008-X

    Chapter  Google Scholar 

  105. 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. https://doi.org/10.1016/S1096-4959(01)00341-4

    CAS  Article  PubMed  Google Scholar 

  106. Zintzen V, Roberts CD, Anderson MJ, Stewart AL, Struthers CD, Harvey ES (2011) Hagfish predatory behavior and slime defense mechanism. Sci Rep. https://doi.org/10.1038/srep00131

    Article  PubMed  PubMed Central  Google Scholar 

  107. Zintzen V, Rogers KM, Roberts CD, Stewart AL, Anderson MJ (2013) Hagfish feeding habits along a depth gradient inferred from stable isotopes. Mar Ecol Prog Ser 485:223–234. https://doi.org/10.3354/meps10341

    Article  Google Scholar 

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Acknowledgements

We thank the editor and two reviewers for helpful comments on an earlier draft which improved the manuscript.

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Correspondence to Thomas M. Evans.

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Evans, T.M., Janvier, P. & Docker, M.F. The evolution of lamprey (Petromyzontida) life history and the origin of metamorphosis. Rev Fish Biol Fisheries 28, 825–838 (2018). https://doi.org/10.1007/s11160-018-9536-z

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Keywords

  • Basal vertebrate
  • Heterochrony
  • Life history
  • Metamorphosis