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Eel Biology pp 31-48 | Cite as

Catadromous Eels of the North Atlantic: A Review of Molecular Genetic Findings Relevant to Natural History, Population Structure, Speciation, and Phylogeny

  • John C. Avise

Abstract

The North Atlantic is home to two recognized species of “freshwatereels” (Fig. 1): Anguilla Rostrata of the Americas, and A. anguilla of Europe and North Africa. Like the approximately 13 other named Anguilla species of the western Indo-Pacific region (Ege 1939; Jellyman 1987; Nelson 1994), Atlanticeels have a catadromous life cycle, spending most of their lives in estuarine or inland waters, but, on reaching sexual maturity, migrating far out to sea for a once-in-a-lifetime (semelparous) spawn (Bertin 1957; Tesch 1977; but see also Tsukamoto et al. 1998). This peculiar life history has raised a number of interesting ecological and evolutionary questions. Does spawning byeels in the open sea occur at random with respect to the coastal localities from which the adults had emigrated? Does the dispersal of larvae back to North America and Europe occur in ways that genetically homogenize continental populations across vast geographic areas? How does speciation occur within the context of this diadromous life cycle? Do different morphological forms of Atlanticeels hybridize? How and when dideels colonize the Atlantic from their probable ancestral homeland in the Indo-Pacific? This review examines how molecular genetic data from polymorphic markers have contributed to a current understanding of the natural history and evolution of Atlanticeels.

Keywords

Allozyme Locus Vertebral Number Vertebral Count Molecular Genetic Finding Atlantic Clade 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Aoyama J, Tsukamoto K (1997) Evolution of freshwatereels. Naturwissenschaften 84:17–21PubMedCrossRefGoogle Scholar
  2. Aoyama J, Kobayashi T, Tsukamoto K (1996) Phylogeny ofeels suggested by mitochondrial DNA sequences. Nippon Suisan Gakkaishi 62:370–375CrossRefGoogle Scholar
  3. Aoyama J, Watanabe S, Nishida M, Tsukamoto K (2000) Discrimination of catadromouseels of the genus Anguilla using polymerase chain reaction-restriction fragment length polymorphism analysis of the mitochondrial 16S ribosomal RNA domain. Trans Am Fish Soc 129:873–878CrossRefGoogle Scholar
  4. Aoyama J, Nishida M, Tsukamoto K (2001) Molecular phylogeny and evolution of the freshwatereel, genus Anguilla. Mol Phylogenet Evol 20:450–459PubMedCrossRefGoogle Scholar
  5. Avise JC (1976) Genetic differentiation during speciation. In: Ayala FJ (ed) Molecular evolution. Sinauer, Sunderland, MA, pp 106–112Google Scholar
  6. Avise JC (1992) Molecular population structure and the biogeographic history of a regional fauna: a case history with lessons for conservation biology. Oikos 63:62–76CrossRefGoogle Scholar
  7. Avise JC (1994) Molecular markers, natural history and evolution. Chapman Hall, New YorkCrossRefGoogle Scholar
  8. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  9. Avise JC, Helfman GS, Saunders NC, Hales LS (1986) Mitochondrial DNA differentiation in North Atlanticeels: population genetic consequences of an unusual life history pattern. Proc Natl Acad Sci USA 83:4350–4354PubMedCrossRefGoogle Scholar
  10. Avise JC, Ball RM, Arnold J (1988) Current versus historical population sizes in vertebrate species with high gene flow: a comparison based on mitochondrial DNA lineages and inbreeding theory for neutral mutations. Mol Biol Evol 5:331–344PubMedGoogle Scholar
  11. Avise JC, Nelson WS, Arnold J, Koehn RK, Williams GC, Thorsteinsson V (1990) The evolutionary genetic status of Icelandiceels. Evolution 44:1254–1262CrossRefGoogle Scholar
  12. Bastrop R, Strehlow B, Jüirss K, Sturmbauer C (2000) A new molecular phylogenetic hypothesis for the evolution of freshwatereels. Mol Phylogenet Evol 14:250–258PubMedCrossRefGoogle Scholar
  13. Bertin L (1957)eels: a biological study. Philosophical Library, New YorkGoogle Scholar
  14. Boëtius J (1980) Atlantic Anguilla. A presentation of old and new data of total numbers of vertebrae with special reference to the occurrence of Anguilla Rostrata in Europe. Dana 1:93–112Google Scholar
  15. Boëtius J, Harding EF (1985a) A re-examination of Johannes Schmidt’s Atlanticeel investigations. Dana 4:129–162Google Scholar
  16. Boëtius J, Harding EF (1985b) List of Atlantic and Mediterranean Anguilla leptocephali: Danish material up to 1966. Dana 4:163–249Google Scholar
  17. Brown WM, George M Jr, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967–1971PubMedCrossRefGoogle Scholar
  18. Bruun AF (1963) The breeding of the north Atlantic freshwater-eels. Adv Mar Biol 1:137–169CrossRefGoogle Scholar
  19. Carson RL (1941) Under the sea wind: a naturalist’s picture of ocean life. Simon Schuster, New YorkGoogle Scholar
  20. Comparini A, Rodino E (1980) Electrophoretic evidence for two species of Anguilla leptocephali in the Sargasso Sea. Nature (Lond) 287:435–437CrossRefGoogle Scholar
  21. Comparini A, Schoth M (1982) Comparison of electrophoretic and meristic characters of 0groupeel larvae from the Sargasso Sea. Helgol Meeresunters 35:289–299CrossRefGoogle Scholar
  22. Comparini A, Rizzotti M, Nardella M, Rodino E (1975) Ricerche elettroforetiche sulla variabilita’ genetica di Anguilla anguilla. Boll Zool 42:283–288CrossRefGoogle Scholar
  23. Comparini A, Rizzotti M, Rodino E (1977) Genetic control and variability of phosphoglucose isomerase (PGI) ineels from the Atlantic Ocean and the Mediterranean Sea. Mar Biol 43:109–116CrossRefGoogle Scholar
  24. Daemen E, Volckaert F, Cross T, Ollevier F (1997) Four polymorphic microsatellite markers in the Europeaneel Anguilla anguilla (L). Anim Genet 28:58–71CrossRefGoogle Scholar
  25. D’Ancona U, Tucker DW (1959) Old and new solutions to theeel problem. Nature (Lond). 183:1405–1406CrossRefGoogle Scholar
  26. Deelder Cl, Tucker DW (1960) The Atlanticeel problem. Nature (Lond) 185:589–592CrossRefGoogle Scholar
  27. de Ligny W, Pantelouris EM (1973) Origin of the Europeaneel. Nature (Lond) 246:518–519CrossRefGoogle Scholar
  28. Ege V (1939) A revision of the genus Anguilla Shaw: a systematic, phylogenetic and geographical study. Dana Rep 16:1–256Google Scholar
  29. Hadrys H, Balick M, Schierwater B (1992) Applications of random amplified polymorphic DNA (RAPD) in molecular ecology. Mol Ecol 1:55–63PubMedCrossRefGoogle Scholar
  30. Hare MP, Avise JC (1996) Molecular genetic analysis of a stepped multilocus cline in the American oyster (Crassostrea virginica). Evolution 50:2305–2315CrossRefGoogle Scholar
  31. Jellyman DJ (1987) Review of the marine life history of A ustralasian temperate species of Anguilla. Am Fish Soc Symp 1:276–285Google Scholar
  32. Jones JW, Tucker DW (1959)eel migration. Nature (Lond) 184:1281–1283CrossRefGoogle Scholar
  33. Karl SA, Avise JC (1992) Balancing selection at allozyme loci in oysters: implications from nuclear RFLPs. Science 256:100–102PubMedCrossRefGoogle Scholar
  34. Kleckner RC, McCleave JD (1988) The northern limit of spawning by Atlanticeels (Anguilla spp.) in the Sargasso Sea in relation to thermal fronts and surface water masses. J Mar Res 46:647–667CrossRefGoogle Scholar
  35. Koehn RK (1972) Genetic variation in theeel: a critique. Mar Biol 14:179–181CrossRefGoogle Scholar
  36. Koehn RK, Williams GC (1978) Genetic differentiation without isolation in the Americaneel, Anguilla Rostrata. II. Temporal stability of geographic patterns. Evolution 32:624–637CrossRefGoogle Scholar
  37. Lecomte-Finiger R (1994) The early life of the Europeaneel. Nature (Lond) 370:424CrossRefGoogle Scholar
  38. Lehmann D, Hettwer H, Taraschewski H (2000) RAPD-PCR investigations of systematic relationships among four species ofeels (Teleostei: Anguillidae), particularly Anguilla anguilla and A. rostrata. Mar Biol 137:195–204CrossRefGoogle Scholar
  39. Lin YS, Poh YP, Tzeng CS (2001) A phylogeny of freshwatereels inferred from mitochondrial genes. Mol Phylogenet Evol 20:252–261 Lintas C, Hirano J, Archer S (1998) Genetic variation of the Europeaneel (Anguilla anguilla). Mol Mar Biol Biotechnol 7:263–269 McCleave JD, Kleckner RC, Castonguay M (1987) Reproductive sympatry of American and Europeaneels and implications for migration and taxonomy. Am Fish Soc Symp 1:286–297Google Scholar
  40. Meyer A (1993) Evolution of mitochondrial DNA in fishes. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes, vol 2. Elsevier, Amsterdam, pp 1–38Google Scholar
  41. Mindell DP, Honeycutt RL (1990) Ribosomal RNA in vertebrates: evolution and phylogenetic applications. Annu Rev Ecol Syst 21:541–566CrossRefGoogle Scholar
  42. Nelson JS (1994) Fishes of the world, 3rd edn Wiley, New YorkGoogle Scholar
  43. Nieddu M, Pichiri G, Coni P, Salvadori S, Deiana AM, Mezzanotte R (1998) A comparative analysis of European and Americaneel (Anguilla anguilla and Anguilla Rostrata) genomic DNA: 55 rDNA polymorphism permits the distinction between the two populations. Genome 41:728–732Google Scholar
  44. Palumbi SR (1996) Nucleic acids. II: The polymerase chain reaction. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics, 2nd edn. Sinauer, Sunderland, MA, pp 205–247Google Scholar
  45. Pantelouris EM (1976) Aspartate aminotransferase variation in the Atlanticeel. J Exp Mar Biol Ecol 22:123–130CrossRefGoogle Scholar
  46. Post A, Tesch F-W (1982) Midwater trawl catches of adolescent and adult anguilliform fishes during the Sargasso Seaeel expedition 1979. Helgol Meeresunters 35:341–356CrossRefGoogle Scholar
  47. Rodino E, Comparini A (1978) Genetic variability in the Europeaneel, Anguilla anguilla L. In: Battaglia B, Beardmore JA (eds) Marine organisms: genetics, ecology and evolution. Plenum, New York, pp 389–424Google Scholar
  48. Salvadori S, Cau A, Deiana AM, Coluccia E, Milia A, Cannas R, Nieddu M, Pichiri G, Mezzanotte R (1997) Cytogenetic and molecular characteristics of Atlanticeels (Anguilla anguilla and A. rostrata) genome. Ital J Zool 65(suppl):61–64CrossRefGoogle Scholar
  49. Schmidt J (1915) Second report oneel investigations. Conseil Internationale pour l’Exploration de la Mer, Rapp et Proces-Verben des Reunions, CopenhagenGoogle Scholar
  50. Schmidt J (1922) The breeding places of theeel. Philos Trans R Soc Lond B 211:179–208CrossRefGoogle Scholar
  51. Schmidt J (1923) Breeding places and migrations of theeel. Nature (Lond) 111:51–54CrossRefGoogle Scholar
  52. Schmidt J (1925) The breeding places of theeel. Smithson Inst Annu Rep 1924:279–316Google Scholar
  53. Schoth M (1982) Taxonomic studies on the 0-groupeel larvae (Anguilla sp.) caught in the Sargasso Sea in 1979. Helgol Meeresunters 35:279–287CrossRefGoogle Scholar
  54. Schoth M, Tesch F-W (1982) Spatial distribution of 0-groupeel larvae (Anguilla sp.) in the Sargasso Sea. Helgol Meeresunters 35:309–320CrossRefGoogle Scholar
  55. Sick K,Westergarrd M, Frydenberg O (1962) Haemoglobin patterns and chromosome number of American, European and Japaneseeels (Anguilla). Nature (Lond) 193:1001–1002CrossRefGoogle Scholar
  56. Sick K, Bahn E, Frydenberg O, Nielsin JT, von Wettstein D (1967) Haemoglobin polymorphism of the American freshwatereel Anguilla. Nature (Lond) 214:1141–1142CrossRefGoogle Scholar
  57. Smith DG (1968) The occurrence of larvae of the Americaneel, Anguilla Rostrata, in the straits of Florida and nearby areas. Bull Mar Sci 18:280–293Google Scholar
  58. Tagliavini J, Gandolfi G, Cau A, Salvadori S, Deiana AM (1995a) Mitochondrial DNA variability in Anguilla anguilla and phylogenetic relationships with congeneric species. Ital J Zool 62:147–151Google Scholar
  59. Tagliavini J, Harrison IJ, Gandolfi G (1995b) Discrimination between Anguilla anguilla and A. rostrata by polymerase chain reaction-restriction fragment length polymorphism analysis. J Fish Biol 47:741–743Google Scholar
  60. Tagliavini J, Gandolfi G, Deiana AM, Salvadori S (1996) Phylogenetic relationships among two Atlantic and three Indo-Pacific Anguilla species (Osteichthyes, Anguillidae). Ital J Zool 63:271–276CrossRefGoogle Scholar
  61. Tesch FW (1977) Theeel: biology and management of anquillideels. Chapman Hall, LondonGoogle Scholar
  62. Tesch FW (1978) Telemetric observations on the spawning migration of theeel (Anguilla anguilla) west of the European continental shelf. Environ Biol Fish 3:203–209CrossRefGoogle Scholar
  63. Tsukamoto K, Aoyama J (1998) Evolution of freshwatereels of the genus Anguilla: a probable scenario. Environ Biol Fish 52:139–148CrossRefGoogle Scholar
  64. Tsukamoto K, Nakai I, Tesch W-V (1998) Do all freshwatereels migrate? Nature (Lond) 396:635–636CrossRefGoogle Scholar
  65. Tucker DW (1959) A new solution to the Atlanticeel problem. Nature (Lond) 183:495–501CrossRefGoogle Scholar
  66. Vladykov VD (1964) Quest for the true breeding area of the Americaneel (Anguilla Rostrata LeSueur). J Fish Res Board Can 21:1523–1530CrossRefGoogle Scholar
  67. Welsh J, Petersen C, McClelland M (1991) Polymorphisms generated by arbitrarily primed PCR in the mouse: application to strain identification and genetic mapping. Nucleic Acids Res 19:303–306PubMedCrossRefGoogle Scholar
  68. Wenner CA (1972) Aspects of the biology and systematics of the Americaneel, Anguilla Rostrata (LeSueur). MA thesis, College of William and Mary, VirginiaGoogle Scholar
  69. Williams GC, Koehn RK (1984) Population genetics of North Atlantic catadromouseels (Anguilla). In: Turner BJ (ed) Evolutionary genetics of fishes. Plenum, New York, pp 529–560CrossRefGoogle Scholar
  70. Williams GC, Koehn RK, Mitton JB (1973) Genetic differentiation without isolation in the Americaneel, Anguilla Rostrata. Evolution 27:192–204CrossRefGoogle Scholar
  71. Williams GC, Koehn RK, Thorsteinsson V (1984) Icelandiceels: evidence for a single species of Anguilla in the North Atlantic. Copeia 1984:221–223CrossRefGoogle Scholar
  72. Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res 18:6531–6535PubMedCrossRefGoogle Scholar
  73. Wirth T, Bernatchez L (2001) Genetic evidence against panmixia in the Europeaneel. Nature (Lond) 409:1037–1040CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Tokyo 2003

Authors and Affiliations

  • John C. Avise
    • 1
  1. 1.Department of GeneticsUniversity of GeorgiaAthensUSA

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