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The evolutionary origin of flatfish asymmetry

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.

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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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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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