Journal of Molecular Evolution

, Volume 35, Issue 2, pp 93–101 | Cite as

Relative importance of molecular, neontological, and paleontological data in understanding the biology of the vertebrate invasion of land

  • Charles Marshall
  • Hans-Peter Schultze
Article

Summary

Meyer and Wilson's (1990) 12S rRNA phylogeny unites lungfish and tetrapods to the exclusion of the coelacanth. These workers also provide a list of morphological features shared in common between modern lungfish and tetrapods, and they conclude that these traits were probably present in their last common ancestor. However, the exquisite fossil records of the abundant extinct lungfishes and rhipidistians show that at least 13 out of Meyer and Wilson's 14 supposed ancestral traits were not present in the last common ancestor of lungfishes and tetrapods. Using extant taxa to infer ancestral morphologies is fraught with difficulties; just like molecular sequences, ancestral character states of morphological traits may be severely overprinted by subsequent modifications. Modern lungfish are air-breathing nonmarine forms, yet their Devonian forebears were marine fish that did not breathe air. Fossils dating from the time of origin of tetrapods in the Devonian offer the only hope of understanding the morphological innovations that led to tetrapods; morphological analysis of the “living fossils,” the coelacanth and lungfish, only lends confusion.

Key words

Molecular phylogeny 12S rRNA Cytochrome b Fossil record Rhipidistians Tetrapods Lungfish Coelacanth Ray-finned fish Morphological parallelisms Living fossils Ancestor 

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References

  1. Ahlberg P (1991) Tetrapod or near-tetrapod fossils from the Upper Devonian of Scotland. Nature 354:298–301Google Scholar
  2. Arratia G, Schultze H-P (1991) Palatoquadrate and its ossifications: development and homology within osteichthyans. J Morphol 208:1–81Google Scholar
  3. Bemis WE (1987) Feeding systems of living Dipnoi: anatomy and function. J Morphol Suppl 1:249–275Google Scholar
  4. Bing R, Burckhardt R (1905) Das Zentralnervensystem von Ceratodus forsteri. In: Semon R (ed) Zoologische Forschungsreisen in Australien and dem Malayischen Archipel. Denkschr Med-Naturwiss Ges Jena 4, 1. Ceratodus, pp 511–584Google Scholar
  5. Burggren WW, Johansen K (1987) Circulation and respiration in lungfishes (Dipnoi). J Morphol Suppl 1:217–236Google Scholar
  6. Campbell KSW, Barwick RE (1982) The neurocranium of the primitive dipnoan Dipnorhynchus sussmilchi (Etheridge). J Vertebr Paleontol 2:286–327Google Scholar
  7. Campbell KSW, Barwick RE (1984) The choana, maxillae, premaxillae and anterior palatal bones of early dipnoans. Proc Linn Soc NSW 107:147–170Google Scholar
  8. Campbell KSW, Barwick RE (1987) Paleozoic lungfishes—a review. J Morphol Suppl 1:93–131Google Scholar
  9. Campbell KSW, Barwick RE (1988) Geological and palaeontological information and phylogenetic hypotheses. Geol Mag 125:207–277Google Scholar
  10. Chang M-M (1991) “Rhipidistians”, dipnoans, and tetrapods. In: Schultze H-P, Trueb L (eds) Origins of the higher groups of tetrapods. Controversy and consensus. Cornell University Press, Ithaca NY, pp 3–28Google Scholar
  11. Chang M-M, Yu X (1984) Structure and phylogenetic significance of Diabolichthys speratus gen. et sp. nov., a new Dipnoan-like form from the Lower Devonian of Eastern Yunnan, China. Proc Linn Soc NSW 107:171–184Google Scholar
  12. Cloutier R (1992) Phylogenetic status, basal taxa, and interrelationships of lower sarcopterygian groups. Zool J Linn Soc (in press)Google Scholar
  13. Coates MI, Clark JA (1991) Fish-like gills and breathing in the earliest known tetrapod. Nature 352:234–236Google Scholar
  14. Dorn E (1955) Der Saccus vasculosus. In: Möllendorf W, Bargmann W (eds) Handbuch der mikroskopischen Anatomie des Menschen 4(2):140–195Google Scholar
  15. Donoghue MJ, Doyle JA, Gauthier J, Kluge AG (1989) The importance of fossils in phylogeny reconstruction. Annu Rev Ecol Syst 20:431–460Google Scholar
  16. Forey PL (1980) Latimeria: a paradoxical fish. Proc R Soc Lond (Biol) 208:369–384Google Scholar
  17. Forey PL (1987) Relationships of lungfishes. J Morphol Suppl 1:75–91Google Scholar
  18. Forey PL (1991) Blood lines of the coelacanth. Nature 351: 347–348Google Scholar
  19. Forey PL, Gardiner GB, Patterson C (1991) The lungfish, the coelacanth, and the cow revisited. In: Schultze H-P, Trueb L (eds) Origins of the higher groups of tetrapods. Controversy and consensus. Cornell University Press, Ithaca NY, pp 145–172Google Scholar
  20. Fritsch B (1987) Inner ear of the coelacanth fish Latimeria has tetrapod affinities. Nature 327:153–154Google Scholar
  21. Gardiner BG (1980) Tetrapod ancestry: a reappraisal. In: Panchen AL (ed) The terrestrial environment and the origin of land vertebrates. Syst Assoc Spec Vol 15:177–185Google Scholar
  22. Gardiner BG (1984) The relationships of the palaeoniscid fishes, a review based on new specimens of Mimia and Moythomasia from the Upper Devonian of Western Australia. Bull Brit Mus (Nat Hist), Geol 37:173–428Google Scholar
  23. Gauthier J, Kluge AG, Rowe T (1988) Amniote phylogeny and the importance of fossils. Cladistics 4:105–208Google Scholar
  24. Gee H (1990) Fossil fishes and fashion. Nature 348:194–195Google Scholar
  25. Gorr T, Kleinschmidt T, Fricke H (1991) Close tetrapod relationships of the coelacanth Latimeria indicated by haemoglobin sequences. Nature 351:394–397Google Scholar
  26. Griffiths M (1938) Studies on the pituitary body. II. Observations on the pituitary in Dipnoi and speculations concerning the evolution of the pituitary. Proc Linn Soc NSW 63: 89–94Google Scholar
  27. Hennig W (1983) Stammesgeschichte der Chordaten. P. Parey, Hamburg, BerlinGoogle Scholar
  28. Holmes EB (1985) Are lungfishes the sister group of tetrapods? Biol J Linn Soc 25:379–397Google Scholar
  29. Holmgren N, van der Horst CJ (1925) Contribution to the morphology of the brain of Ceratodus. Acta Zool Stockholm 6:59–165Google Scholar
  30. Jarvik E (1942) On the structure of the snout of crossopterygians and lower gnathostomes in general. Zool Bidr Upps 21:235–675Google Scholar
  31. Jarvik E (1980) Basic structure and evolution of vertebrates, vol 1. Academic Press, LondonGoogle Scholar
  32. Lagios MD (1979) The coelacanth and the Chondrichthyes as sister groups: a review of shared apomorph characters and a cladistic analysis and reinterpretation. Occas Pap Calif Acad Sci 134:25–44Google Scholar
  33. Long JA (1990) Heterochrony and the origin of tetrapods. Lethaia 23:157–166Google Scholar
  34. Maisey JG (1986) Heads and tails: a chordate phylogeny. Cladistics 2:201–256Google Scholar
  35. Marshall CR (1987a) A list of fossil and extant dipnoans. J Morphol Suppl 1:15–23Google Scholar
  36. Marshall CR (1987b) Lungfish: phylogeny and parsimony. J Morphol Suppl 1:151–162Google Scholar
  37. Matty AJ (1985) Fish endocrinology. Croom Helm, LondonGoogle Scholar
  38. Meyer A, Dolven SI (1992) Molecules, fossils, and the origin of tetrapods. J Mol Evol 35:102–113Google Scholar
  39. Meyer A, Wilson AC (1990) Origin of tetrapods inferred from their mitochondrial DNA affiliation to lungfish. J Mol Evol 31:359–364Google Scholar
  40. Meyer A, Wilson AC (1991) Coelacanth's relationships. Nature 353:19Google Scholar
  41. Miles RS (1975) The relationships of the Dipnoi. Colloq Int CNRS 218:133–148Google Scholar
  42. Miles RS (1977) Dipnoan (lungfish) skulls and the relationships of the group: a study based on new species from the Devonian of Australia. Zool J Linn Soc 61:1–328Google Scholar
  43. Normark BB, McCune AR, Harrison RG (1991) Phylogenetic relationships of neopterygian fishes, inferred from mitochondrial DNA sequences. Mol Biol Evol 8:819–834Google Scholar
  44. Northcutt RG (1987) Lungfish neural characters and their bearing on sarcopterygian phylogeny. J Morphol Suppl 1:277–297Google Scholar
  45. Panchen AL, Smithson TR (1987) Character diagnosis, fossils and the origin of tetrapods. Biol Rev 62:341–438Google Scholar
  46. Rosen DE, Forey PL, Gardiner BG, Patterson C (1981) Lungfishes, tetrapods, paleontology, and plesiomorphy. Bull Am Mus Nat Hist 167:159–276Google Scholar
  47. Säve-Söderbergh G (1952) On the skull of Chirodipterus wildungensis Gross, an Upper Devonian dipnoan from Wildungen. K Sven Vetenskaps akad Handl(4)3:1–29Google Scholar
  48. Schultze H-P (1969) Die Faltenzähne der rhipidistiiden Crossopterygier, der Tetrapoden und der Actinopterygier-Gattung Lepisosteus. Palaeontogr Ital 65:63–136Google Scholar
  49. Schultze H-P (1970) Folded teeth and the monophyletic origin of tetrapods. Am Mus Novit 2408:1–10Google Scholar
  50. Schultze H-P (1977) The origin of the tetrapod limb within the rhipidistian fishes. In: Hecht MK, Goody PC, Hecht BM (ed) Major patterns in vertebrate evolution. NATO Adv Stud Inst Ser 14:541–544Google Scholar
  51. Schultze H-P (1981) HENNIG and der Ursprung der Tetrapoda. Palaeontol Z 55:71–86Google Scholar
  52. Schultze H-P (1987) Dipnoans as Sarcopterygians. J Morphol Suppl 1:39–74Google Scholar
  53. Schultze H-P (1991) Der Ursprung der Tetrapoden-ein lebhaft diskutiertes altes Problem. Verh Dtsch Zool Ges 84:135–151Google Scholar
  54. Schultze H-P (1992) The origin of tetrapods—a hotly debated old problem. Syst Biol (in press)Google Scholar
  55. Schultze H-P, Arsenault M (1985) The panderichthyid fish Elpistostege: a close relative of tetrapods? Palaeontology 28: 293–309Google Scholar
  56. Schultze H-P, Campbell KSW (1987) Characterization of the Dipnoi, a monophyletic group. J Morphol Suppl 1(1986):2537Google Scholar
  57. Sharp PM, Loyd AT, Higgins DG (1991) Coelacanth's relationships. Nature 353:218–219Google Scholar
  58. Smith MM, Chang M-M (1990) The dentition of Diabolepis speratus Chang and Yu, with further consideration of its relationships and the primitive dipnoan dentition. J Vertebr Paleontol 10: 420–433Google Scholar
  59. Stock DW, Swofford DL (1991) Coelacanth's relationships. Nature 353:217–218Google Scholar
  60. Thomson KS, Campbell KSW (1971) The structure and relationships of the primitive dipnoan lungfish Dipnorhynchus sussmilchi (Etheridge). Bull Peabody Nat Hist 38:1–VI + 1109Google Scholar
  61. Waehneldt TV, Malotka J (1989) Presence of proteolipid protein in coelacanth brain myelin demonstrates tetrapod affinities and questions a chondrichthyan association. J Neurochem 52:1941–1943Google Scholar
  62. Wahlert G von (1968) Latimeria and die Geschichte der Wirbeltiere. Fischer, StuttgartGoogle Scholar
  63. Wake MH (1987) Urogenital morphology of dipnoans, with comparisons to other fishes and to amphibians. J Morphol Suppl 1:199–216Google Scholar
  64. Wiedersheim R (1904) Ueber das Vorkommen eines Kehlkopfes bei Ganoiden und Dipnoern Bowie fiber die Phylogenie der Lunge. Zool Jahrb Suppl 7:1–66Google Scholar
  65. Young GC, Barwick RE, Campbell KSW (1989) Pelvic girdles of lungfishes (Dipnoi). In: LaMaitre RW (ed) Pathways in geology essays in honour of Edwin Sherbon Hills. Blackwell Scientific Publishers, Melbourne, pp 59–75Google Scholar

Copyright information

© Springer-Verlag New York Inc 1992

Authors and Affiliations

  • Charles Marshall
    • 1
  • Hans-Peter Schultze
    • 2
  1. 1.Department of BiologyIndiana UniversityBloomingtonUSA
  2. 2.Museum of Natural HistoryUniversity of KansasLawrenceUSA

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