An evolutionary and developmental perspective on the loss of regionalization in the limbs of derived ichthyosaurs

Geological Magazine

Volumn 151, Issue 1, 2014, Pages 29-40

  Maxwell, Erin E ^a   Scheyer, Torsten M ^a   Fowler, Donald A ^b  

^a PALÄONTOLOGISCHES INSTITUT UND MUSEUM   (Switzerland)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

bone histology; heterochrony; HoxD13; Ichthyosauria; intraspecific variation; limb evolution; Stenopterygius

Indexed keywords

HISTOLOGY;

HETEROCHRONY; HOXD13; ICHTHYOSAURIA; INTRASPECIFIC VARIATION; LIMB EVOLUTION; STENOPTERYGIUS;

MORPHOLOGY;

BONE; EVOLUTION; HISTOLOGY; INTRASPECIFIC VARIATION; LIMB; MICROSTRUCTURE; MORPHOLOGY; PALEONTOLOGY; REPTILE;

ICHTHYOSAURIA; REPTILIA; STENOPTERYGIUS; TETRAPODA;

EID: 84896958973     PISSN: 00167568     EISSN: 14695081     Source Type: Journal    
DOI: 10.1017/S0016756812001070     Document Type: Article

References (66)

1. ANAN, K., YOSHIDA, N., KATAOKA, Y., SATO, M., ICHISE, H., NASU, M. & UEDA, S. 2007. Morphological change caused by loss of the taxon-specific polyalanine tract in Hoxd-13. Molecular Biology and Evolution 24, 281-7.
2. ARCHER, C. W., DOWTHWAITE, G. P. & FRANCIS-WEST, P. 2007. Joint formation. In Fins into Limbs (ed. B. K. Hall), pp. 109-17. Chicago: University of Chicago Press.
3. BLANCO, M. J., MISOF, B. Y. & WAGNER, G. P. 1998. Heterochronic differences of Hoxa-11 expression in Xenopus fore- and hind limb development: evidence for lower limb identity of the anuran ankle bones. Development Genes and Evolution 208, 175-87.
4. BRUNEAU, S., JOHNSON, K. R., YAMAMOTO, M., KUROIWA, A. & DUBOULE, D. 2001. The mouse Hoxd13spdh mutation, a polyalanine expansion similar to human type II synpolydactyly (SPD), disrupts the function but not the expression of other Hoxd genes. Developmental Biology 237, 345-53.
5. BUCHHOLTZ, E. A. 2001. Swimming styles in Jurassic ichthyosaurs. Journal of Vertebrate Paleontology 21, 61-73.
6. BUCHHOLTZ, E. A. 2007. Modular evolution of the cetacean vertebral column. Evolution and Development 9, 278-89.
7. CALDWELL, M. W. 1997a. Limb ossification patterns of the ichthyosaur Stenopterygius, and a discussion of the proximal tarsal rowof ichthyosaurs and other neodiapsid reptiles. Zoological Journal of the Linnean Society 120, 1-25.
8. CALDWELL, M. W. 1997b. Modified perichondral ossification and the evolution of paddle-like limbs in ichthyosaurs and plesiosaurs. Journal of Vertebrate Paleontology 17, 534-47.
9. CALDWELL, M. W. 2002. From fins to limbs to fins: limb evolution in fossil marine reptiles. American Journal of Medical Genetics 112, 236-49.
10. CAMP, C. L. 1980. Large ichthyosaurs from the Upper Triassic of Nevada. Palaeontographica Abteilung A 170, 139-200.
11. CANOVILLE, A. & LAURIN, M. 2010. Evolution of humeral microanatomy and lifestyle in amniotes, and some comments on palaeobiological inferences. Biological Journal of the Linnean Society 100, 384-406.
12. CHINSAMY, A. & RAATH, M. A. 1992. Preparation of fossil bone for histological examination. Palaeontologia Africana 29, 39-44.
13. COCQUEMPOT, O., BRAULT, V., BABINET, C. & HERAULT, Y. 2009. Fork stalling and template switching as a mechanism for polyalanine tract expansion affecting the DYC mutant of HOXD13, a new murine model of synpolydactyly. Genetics 183, 23-30.
14. COOPER, L. N., BERTA, A., DAWSON, S. D. & REIDENBERG, J. S. 2007a. Evolution of hyperphalangy and digit reduction in the cetacean manus. Anatomical Record 290, 654-72.
15. COOPER, L. N., DAWSON, S. D., REIDENBERG, J. S. & BERTA, A. 2007b. Neuromuscular anatomy and evolution of the cetacean forelimb. Anatomical Record 290, 1121-37.
16. COOPER, L. N. & DAWSON, S. D. 2009. The trouble with flippers: a report on the prevalence of digital anomalies in Cetacea. Zoological Journal of the Linnean Society 155, 722-35.
17. DAL SASSO, C. & PINNA, G. 1996. Besanosaurus leptorhynchus n. gen. n. sp., a new shastasaurid ichthyosaur from the Middle Triassic of Besano (Lombardy, N. Italy). Paleontologia Lombarda, Nuova Serie 4, 1-23.
18. DAWSON, S. D. 2003. Patterns of ossification in the manus of the harbor porpoise (Phocoena phocoena): hyperphalangy and delta-shaped bones. Journal of Morphology 258, 200-6.
19. DE BUFFRÉNIL, V. & MAZIN, J.-M. 1990. Bone histology of the ichthyosaurs: comparative data and functional interpretation. Paleobiology 16, 435-47.
20. DE LA BECHE, H. T. & CONYBEARE, W. D. 1821. Notice of the discovery of a new fossil animal, forming a link between the Ichthyosaurus and crocodile, together with general remarks on the osteology of the Ichthyosaurus. Transactions of the Geological Society, London 5, 559-94.
21. EVANS, M. 2010. The roles played by museums, collections and collectors in the early history of reptile palaeontology. In Dinosaurs and Other Extinct Saurians: A Historical Perspective (eds R. T. J. Moody, E. Buffetaut, D. Naish&D. M. Martill), pp. 5-29. London: Geological Society.
22. FEDAK, T. J. & HALL, B. K. 2004. Perspectives on hyperphalangy: patterns and processes. Journal of Anatomy 204, 151-63.
23. FISCHER, V., MASURE, E., ARKHANGELSKY, M. S. & GODEFROIT, P. 2011. A new Barremian (Early Cretaceous) ichthyosaur from Western Russia. Journal of Vertebrate Paleontology 31, 1010-25.
24. FRAAS, E. 1891. Ichthyosaurier der süddeutschen Trias- und Jura- Ablagerungen. Tübingen: H. Laupp.
25. GOODMAN, F. R., MUNDLOS, S., MURAGAKI, Y., DONNAI, D., GIOVANNUCCI-UZIELLI, M. L., LAPI, E., MAJEWSKI, F., MCGAUGHRAN, J., MCKEOWN, C., REARDON, W., UPTON, J., WINTER, R. M., OLSEN, B. R. & SCAMBLER, P. J. 1997. Synpolydactyly phenotypes correlate with size of expansions in HOXD13 polyalanine tract. Proceedings of the National Academy of Sciences 94, 7458-63.
26. HORSNELL, K., ALI, M., MALIK, S., WILSON, L., HALL, C., DEBEER, P. & CROW, Y. 2006. Clinical phenotype associated with homozygosity for a HOXD13 7- residue polyalanine tract expansion. European Journal of Medical Genetics 49, 396-401.
27. VON HUENE, F. 1922. Die Ichthyosaurier des Lias und ihre Zusammenhänge. Berlin: Verlag von Gebrüder Borntraeger.
28. JOHNSON, R. 1977. Size independent criteria for estimating relative age and the relationship among growth parameters in a group of fossil reptiles (Reptilia: Ichthyosauria). Canadian Journal of Earth Sciences 14, 1916-24.
29. JOHNSON, R. 1979. The osteology of the pectoral complex of Stenopterygius Jaekel (Reptilia: Ichthyosauria). Neues Jahrbuch für Geologie und Paläontologie. Abhandlungen 159, 41-86.
30. KIPRIJANOFF, W. 1881. Studien über die fossilen Reptilien Russlands. Theil 1. Gattung Ichthyosaurus König aus dem Sewerischen Sandstein oder Osteolith der Kreide-Gruppe. Mémoires de lAcadémie Impériale des Sciences de Saint-Pétersbourg 28, 1-103.
31. KOLB, C., SÁNCHEZ-VILLAGRA, M. R. & SCHEYER, T. M. 2011. The paleohistology of the basal ichthyosaur Mixosaurus Baur, 1887 (Ichthyopterygia, Mixosauridae) from the Middle Triassic: palaeobiological implications. Comptes Rendus Palevol 10, 403-11.
32. LOPUCHOWYCZ, V. B. & MASSARE, J. A. 2002. Bone microstructure of a Cretaceous ichthyosaur. Paludicola 3, 139-47.
33. MAISCH, M. W. & MATZKE, A. T. 1998. Observations on Triassic ichthyosaurs. Part IV: on the forelimb of Mixosaurus Baur, 1887. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 209, 247-72.
34. MAXWELL, E. E. 2012. Unraveling the influences of softtissue flipper development on skeletal variation using an extinct taxon. Journal of Experimental Zoology (Molecular and Developmental Evolution) 318, 545-54.
35. MAXWELL, E. E. & DECECCHI, T. A. 2012. Ontogenetic and stratigraphic influence on observed phenotypic integration in the limb skeleton of a fossil tetrapod. Paleobiology 39, 123-34.
36. MAXWELL, E. E., FERNÁNDEZ, M. S. & SCHOCH, R. R. 2012. First diagnostic marine reptile remains from the Aalenian (Middle Jurassic): a new ichthyosaur from southwestern Germany. PLoS ONE 7, e41692.
37. MCGOWAN, C. 1973. Differential growth in three ichthyosaurs: Ichthyosaurus communis, I. breviceps, and Stenopterygius quadriscissus (Reptilia, Ichthyosauria). Life Sciences Contributions, Royal OntarioMuseum 93, 1-21.
38. MCGOWAN, C. 1974. A revision of the latipinnate ichthyosaurs of the Lower Jurassic of England (Reptilia: Ichthyosauria). Life Sciences Contributions, Royal Ontario Museum 100, 1-30.
39. MCGOWAN, C. & MOTANI, R. 2003. Ichthyopterygia. Handbook of Paleoherpetology (ed. H.-D. Sues). München: Verlag Dr. Friedrich Pfeil.
40. MELLOR, L., COOPER, L. N., TORRE, J. & BROWNELL, R. L. J. 2009. Paedomorphic ossification in porpoises with an emphasis on the vaquita (Phocoena sinus). Aquatic Mammals 35, 193-202.
41. MONTAVON, T., SOSHNIKOVA, N., MASCREZ, B., JOYE, E., THEVENET, L., SPLINTER, E., DE LAAT, W., SPITZ, F. & DUBOULE, D. 2011. A regulatory archipelago controls Hox genes transcription in digits. Cell 147, 1132-45.
42. MOTANI, R. 1997. New information of the forefin of Utatsusaurus hataii (Ichthyosauria). Journal of Paleontology 71, 475-9.
43. MOTANI, R. 1998. First complete forefin of the ichthyosaur Grippia longirostris from the Triassic of Spitsbergen. Palaeontology 41, 591-9.
44. MOTANI, R. 1999a. On the evolution and homologies of ichthyopterygian forefins. Journal of Vertebrate Paleontology 19, 28-41.
45. MOTANI, R. 1999b. Phylogeny of the Ichthyopterygia. Journal of Vertebrate Paleontology 19, 472-95.
46. MÜLLER, J., SCHEYER, T. M., HEAD, J. J., BARRETT, P. M., WERNEBURG, I., ERICSON, P. G. E., POL, D. & SÁNCHEZ-VILLAGRA, M. R. 2010. Homeotic effects, somitogenesis and the evolution of vertebral numbers in recent and fossil amniotes. Proceedings of the National Academy of Sciences of the United States of America 107, 2118-23.
47. MURAGAKI, Y., MUNDLOS, S., UPTON, J. & OLSEN, B. R. 1996. Altered growth and branching patterns in synpolydactyly caused by mutations in HOXD13. Science 272, 548-51.
48. NICHOLLS, E. L. & BRINKMAN, D. B. 1995. A new ichthyosaur from the Triassic Sulphur Mountain Formation of British Columbia. In Vertebrate Fossils and the Evolution of Scientific Concepts (ed. W. A. S. Sarjeant), pp. 521-35. Amsterdam: Gordon and Breach.
49. QUINN, G. P. & KEOUGH, M. J. 2002. Experimental Design and Data Analysis for Biologists. Cambridge: Cambridge University Press.
50. R DEVELOPMENT CORE TEAM. 2011. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
51. REISZ, R. R. 1981. A diapsid reptile from the Pennsylvanian of Kansas. Special Publication of the Museum of Natural History, University of Kansas 7, 1-74.
52. RENO, P. L., MCCOLLUM, M. A., COHN, M. J., MEINDL, R. S., HAMRICK, M. & LOVEJOY, C. O. 2008. Patterns of correlation and covariation of anthropoid distal forelimb segments correspond to Hoxd expression territories. Journal of Experimental Zoology (Molecular and Developmental Evolution) 310B, 240-58.
53. SANDER, P. M., CHEN, X., CHENG, L. & WANG, X. 2011. Short-snouted toothless ichthyosaur from China suggests Late Triassic diversification of suction feeding ichthyosaurs. PLoS ONE 6, e19480.
54. SWALLA, B. J. 2006. Building divergent body plans with similar genetic pathways. Heredity 97, 235-43.
55. TABIN, C. & WOLPERT, L. 2007. Rethinking the proximodistal axis of the vertebrate limb in the molecular era. Genes and Development 21, 1433-42.
56. THEWISSEN, J. G. M. & TAYLOR, M. A. 2007. Aquatic adaptations in the limbs of amniotes. In Fins into Limbs (ed. B. K. Hall), pp. 310-22. Chicago: University of Chicago Press.
57. THORNE, P. M., RUTA, M. & BENTON, M. J. 2011. Resetting the evolution of marine reptiles at the Triassic-Jurassic boundary. Proceedings of the National Academy of Sciences of the United States of America 108, 8339-44.
58. TOWERS, M. & TICKLE, C. 2009. Growing models of vertebrate limb development. Development 136, 179-90.
59. URLICHS, M., WILD, R. & ZIEGLER, B. 1979. Fossilien aus Holzmaden. Stuttgarter Beiträge zur Naturkunde Serie C 11, 1-34.
60. VILLAVICENCIO-LORINI, P., KUSS, P., FRIEDRICH, J., HAUPT, J., FAROOQ, M., TÜRKMEN, S., DUBOULE, D., HECHT, J. & MUNDLOS, S. 2010. Homeobox genes d11-d13 and a13 control mouse autopod cortical bone and joint formation. Journal of Clinical Investigation 120, 1994- 2004.
61. WAGNER, G. P. & CHIU, C.-H. 2001. The tetrapod limb: a hypothesis of its origin. Journal of Experimental Zoology (Molecular and Developmental Evolution) 291B, 226-40.
62. WANG, Z., YUAN, L., ROSSITER, S. J., ZUO, X., RU, B., ZHONG, H., HAN, N., JONES, G., JEPSON, P. D. & ZHANG, S. 2008. Adaptive evolution of 5′ HoxD genes in the origin and diversification of the cetacean flipper. Molecular Biology and Evolution 26, 613-22.
63. WOLTERING, J. M. &DUBOULE, D. 2010. The origin of digits: expression patterns versus regulatory mechanisms. Developmental Cell 18, 526-32.
64. YOUNG, R. L., BEVER, G. S., WANG, Z. & WAGNER, G. P. 2011. Identity of the avian wing digits: problems resolved and unsolved. Developmental Dynamics 240, 1042-53.
65. ZELLER, R., LPEZ-RÍOS, J. & ZUNIGA, A. 2009. Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nature Reviews Genetics 10, 845-58.
66. ZHU, J., ZHANG, Y.-T., ALBER, M. S. &NEWMAN, S. A. 2010. Bare bones pattern formation: a core regulatory network in varying geometries reproduces major features of vertebrate limb development and evolution. PLoS ONE 5, e10892.