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The evolutionary origin of flatfish asymmetry

Nature volume 454, pages 209–212 (2008)Cite this article

Abstract

All adult flatfishes (Pleuronectiformes), including the gastronomically familiar plaice, sole, turbot and halibut, have highly asymmetrical skulls, with both eyes placed on one side of the head. This arrangement, one of the most extraordinary anatomical specializations among vertebrates, arises through migration of one eye during late larval development. Although the transformation of symmetrical larvae into asymmetrical juveniles is well documented1,2,3,4,5,6,7, the evolutionary origins of flatfish asymmetry are uncertain1,2 because there are no transitional forms linking flatfishes with their symmetrical relatives8,9. The supposed inviability of such intermediates gave pleuronectiforms a prominent role in evolutionary debates10,11,12,13,14,15,16, leading to attacks on natural selection11 and arguments for saltatory change14,15. Here I show that Amphistium and the new genus Heteronectes, both extinct spiny-finned fishes from the Eocene epoch of Europe, are the most primitive pleuronectiforms known. The orbital region of the skull in both taxa is strongly asymmetrical, as in living flatfishes, but these genera retain many primitive characters unknown in extant forms. Most remarkably, orbital migration was incomplete in Amphistium and Heteronectes, with eyes remaining on opposite sides of the head in post-metamorphic individuals. This condition is intermediate between that in living pleuronectiforms and the arrangement found in other fishes. Amphistium and Heteronectes indicate that the evolution of the profound cranial asymmetry of extant flatfishes was gradual in nature.

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Figure 1: Skulls of primitive pleuronectiforms showing incomplete orbital migration intermediate between generalized fishes and living flatfishes.
Figure 2: Phylogenetic placement of Heteronectes and Amphistium and implications for the origin of cranial asymmetry in flatfishes.

References

  1. Kyle, H. M. The asymmetry, metamorphosis, and origin of flat-fishes. Phil. Trans. R. Soc. Lond. B 211, 75–129 (1923)

    Article  ADS  Google Scholar 

  2. Norman, J. R. A Systematic Monograph of the Flatfishes (Heterosomata). Vol. 1. Psettotidae, Bothidae, Pleuronectidae (British Museum (Natural History), London, 1934)

    Book  Google Scholar 

  3. Ahlstrom, E. H., Amaoka, K., Hensley, D. A., Moser, H. G. & Sumida, B. Y. in Ontogeny and Systematics of Fishes (eds Moser, H. G. et al.) 640–670 (Allen, Lawrence, Kansas, 1984)

    Google Scholar 

  4. Okada, N., Takagi, Y., Seikai, T., Tanaka, M. & Tagawa, M. Asymmetrical development of bones and soft tissues during eye migration of metamorphosing Japanese flounder, Paralichthys olivaceus. Cell Tissue Res. 304, 59–66 (2001)

    Article  CAS  Google Scholar 

  5. Wagemans, F. & Vandewalle, P. Development of the bony skull in common sole: brief survey of morpho-functional aspects of ossification sequence. J. Fish Biol. 59, 1350–1369 (2001)

    Article  Google Scholar 

  6. Hoshino, K. Fixing the confused term “pseudomesial bar” and homologies of pleuronectiform cranial elements, with proposals of new terms. Ichthyol. Res. 53, 435–440 (2006)

    Article  Google Scholar 

  7. Schreiber, A. M. Asymmetric craniofacial remodeling and lateralized behavior in larval flatfish. J. Exp. Biol. 209, 610–621 (2006)

    Article  Google Scholar 

  8. Chanet, B. A cladistic reappraisal of the fossil flatfishes record consequences on the phylogeny of the Pleuronectiformes (Osteichthyes: Teleostei). Ann. Sci. Nat. Zool. 18, 105–117 (1997)

    Google Scholar 

  9. Chanet, B. Supposed and true flatfishes [Teleostei: Pleuronectiformes] from the Eocene of Monte Bolca, Italy. Stud. Ric. Giacim. Terz. Bolca 8, 220–243 (1999)

    Google Scholar 

  10. Lamarck, J. B. Philosophie Zoologique (Dentu, Paris, 1809)

    Google Scholar 

  11. Mivart, G. J. On the Genesis of Species (MacMillan, London, 1871)

    Book  Google Scholar 

  12. Darwin, C. On the Origin of Species by Means of Natural Selection 6th edn (Murray, London, 1872)

    Google Scholar 

  13. Wallace, A. R. Darwinism (MacMillan and Co., London, 1889)

    Google Scholar 

  14. Goldschmidt, R. Some aspects of evolution. Science 78, 539–547 (1933)

    Article  ADS  CAS  Google Scholar 

  15. Goldschmidt, R. The Material Basis of Evolution (Yale Univ. Press, New Haven, 1940)

    Google Scholar 

  16. von Wahlert, G. The role of ecological factors in the origin of higher levels of organization. Syst. Zool. 14, 288–300 (1965)

    Article  CAS  Google Scholar 

  17. Chanet, B. Eubuglossus eocenicus (Woodward 1910) from the Upper Lutetian of Egypt, one of the oldest soleids (Teleostei, Pleuronectiformes). Neues Jahrb. Geol. Paläntol. Monatsh. 1994, 391–398 (1994)

    Google Scholar 

  18. Trevisani, E., Papazzoni, C. A., Ragazzi, E. & Roghi, G. Early Eocene amber from the “Pesciara di Bolca” (Lessini Mountains, Northern Italy). Palaeogeogr. Palaeoclimatol. Palaeoecol. 223, 260–274 (2005)

    Article  Google Scholar 

  19. Chapleau, F. Pleuronectiform relationships: a cladistic reassessment. Bull. Mar. Sci. 52, 516–540 (1993)

    Google Scholar 

  20. Blot, J. Les poissons fossiles du Monte Bolca. Classés jusqu’ici dans les familles des Carangidae, Menidae, Ephippidae, Scatophagidae. Mem. Mus. Civ. Stor. Nat. Verona 1, 1–525 (1969)

    Google Scholar 

  21. Gaudant, J. Sur un Amphistium (poisson téléostéen, Percoidei) de l’Éocène Parisien. Bull. Inf. Géol. Bass. Paris 16, 11–14 (1979)

    Google Scholar 

  22. Liew, H.-C., Milward, N. E. & Hartwick, R. F. Descriptions of larval fishes of the genera Psettodes (Psettotidae) and Pseuorhombus (Paralichthyidae) from the Great Barrier Reef, Australia. Aust. J. Mar. Freshwat. Res. 39, 51–70 (1988)

    Article  Google Scholar 

  23. Gosline, W. A. The perciform caudal skeleton. Copeia 1961, 265–270 (1961)

    Article  Google Scholar 

  24. Patterson, C. An overview of the early fossil record of acanthomorphs. Bull. Mar. Sci. 52, 29–59 (1993)

    Google Scholar 

  25. Johnson, G. D. & Patterson, C. Percomorph phylogeny: a survey of acanthomorphs and a new proposal. Bull. Mar. Sci. 52, 554–626 (1993)

    Google Scholar 

  26. Hubbs, C. L. & Hubbs, L. C. Bilateral asymmetry and bilateral variation in fishes. Pap. Mich. Acad. Sci. Arts Lett. 30, 229–310 (1944)

    Google Scholar 

  27. Palmer, A. R. From symmetry to asymmetry: phylogenetic patterns of asymmetry variation in animals and their evolutionary significance. Proc. Natl Acad. Sci. USA 93, 14279–14286 (1996)

    Article  ADS  CAS  Google Scholar 

  28. Stickney, R. R., White, D. B. & Miller, D. Observations of fin use in relation to feeding and resting behavior in flatfishes (Pleuronectiformes). Copeia 1973, 154–156 (1973)

    Article  Google Scholar 

  29. Patterson, C. in The Fossil Record 2 (ed. Benton, M. J.) 621–656 (Chapman & Hall, London, 1993)

    Google Scholar 

  30. Stiassny, M. L. J., Wiley, E. O., Johnson, G. D. & de Carvalho, M. R. in Assembling the Tree of Life (eds Cracraft, J. & Donoghue, M. J.) 410–429 (Oxford Univ. Press, New York, 2004)

    Google Scholar 

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Acknowledgements

I thank G. Clément, P. Forey, D. Goujet, M. Richter, O. Schultz, A. Vaccari and M. Véran for loaning or providing access to fossil specimens; R. Arrindell, B. Brown, D. Johnson, S. Raredon, M. Rogers and M. Westneat for arranging the loan or study of recent material; E. Hilton for checking gill-arch characters in carangids; M. Colbert and A. Gosselin-Ildari for compiling the computed tomography renderings, K. Claeson for providing specimen transport; L. Herzog, A. Shinya, D. Wagner and J. Holstein for helping in fossil preparation; and A. Bannikov, M. Coates, M. LaBarbera and N. Smith for discussion. This work was supported by a grant from the Lerner-Grey Fund for Marine Research, a Hinds Fund Grant, an Evolving Earth Grant, a National Science Foundation Graduate Research Fellowship (award number DGE-0228235), and an Environmental Protection Agency STAR Fellowship (award number FP916730).

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Authors and Affiliations

  1. Committee on Evolutionary Biology, University of Chicago, 1025 East 57th Street, Chicago, Illinois 60637, USA,

    Matt Friedman

  2. Department of Geology, The Field Museum, 1400 South Lake Shore Drive, Chicago, Illinois 60605, USA,

    Matt Friedman

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Correspondence to Matt Friedman.

Supplementary information

Supplementary information

The file contains Supplementary Information which includes the following sections: I. Institutional abbreviations; II. Supplementary morphological data: †Heteronectes chaneti; III. Details of computed tomography (CT); IV. Supplementary morphological data: †Amphistium; V. Legends for CT rendering movies; VI. Characters used in cladistic analysis; VII. Comparative materials used to code characters: fossil taxa; VIII. Comparative materials used to code characters: Recent taxa; IX. Taxon-by-character matrix; X. Systematic methodology; XI. Character optimisations; XII. additional references.. The file also includes Supplementary Figures 1-20 with Legends. (PDF 38916 kb)

Supplementary information

The file contains Supplementary Movie 1 showing CT rendering of neurocranium of †Amphistium paradoxum (BMNH P.16138; dextral morph). Animation begins with neurocranium in right-lateral view (damaged side with unmigrated orbit; the skull was fractured when the slab containing the fish was split), then rotates the skull 360 degrees about a vertical axis. Upon returning to start position, the skull rotates the skull 360 degrees about its long axis, showing ventral, left-lateral (side with migrated orbit), and dorsal views. Specimen missing ethmoid region and parasphenoid (broken off block). A still image of the CT rendering and interpretive line drawing are given in Supplementary figure 10. A photograph of the complete specimen is shown in Supplementary figure 8, and a close-up of the skull in Supplementary figure 9. (MOV 1619 kb)

Supplementary information

The file contains Supplementary Movie 2 showing CT rendering of neurocranium of †Amphistium paradoxum (BMNH P.1982; dextral morph). Animation begins with neurocranium in right-lateral view (damaged side with unmigrated orbit; the skull was fractured when the slab containing the fish was split), then rotates the skull 360 degrees about a vertical axis. Upon returning to start position, the skull rotates the skull 360 degrees about its long axis showing ventral, left-lateral (side with migrated orbit), and dorsal views. The latter clearly shows medial extent of migrated orbit. A still image of the CT rendering and interpretive line drawing are given in Supplementary figure (MOV 1359 kb)

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Friedman, M. The evolutionary origin of flatfish asymmetry. Nature 454, 209–212 (2008). https://doi.org/10.1038/nature07108

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