Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-22T02:47:10.206Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  03 May 2013

ERIN E. MAXWELL ,
TORSTEN M. SCHEYER  and
DONALD A. FOWLER
ERIN E. MAXWELL*
Affiliation:
Paläontologisches Institut und Museum der Universität Zürich, Karl Schmid-Strasse 4, 8006 Zürich, Switzerland
TORSTEN M. SCHEYER
Affiliation:
Paläontologisches Institut und Museum der Universität Zürich, Karl Schmid-Strasse 4, 8006 Zürich, Switzerland
DONALD A. FOWLER
Affiliation:
Redpath Museum, McGill University, 859 Sherbrooke St West, Montreal QC Canada H3A 2K6
*
†Author for correspondence: emaxwell@ualberta.ca
Get access Rights & Permissions [Opens in a new window]

Abstract

Ichthyosaurs, a lineage of extinct Mesozoic marine reptiles, have garnered attention in both the palaeontological and developmental literature for the unique limb morphology seen in derived genera. These morphologies include an increase in the number of phalanges per digit (hyperphalangy) and in the number of digits (hyperdactyly), but most interestingly also a shift in element identity. Elements distal to the stylopodium acquire characteristics of mesopodial elements, such as a rounded, nodular shape and a loss of perichondral bone on the anterior and posterior surfaces. Here, we examine numerous aspects of the loss of proximodistal identity in ichthyosaur limbs including phylogenetic progression of the loss of perichondral bone, histology and microstructure of the elements retaining perichondral bone in derived taxa, and correlates of intraspecific variation in degree of perichondral bone reduction in a derived ichthyosaur, Stenopterygius quadriscissus. Results show that loss of limb element identity occurred progressively over ichthyosaurian evolution, and the notches seen on the anterior surface of limb elements in derived ichthyosaurs are homologous to the long bone shafts in terrestrial tetrapods. Variation in the number of notches in S. quadriscissus can best be explained through delayed ossification of the anterior perichondrium, indicating a heterochronic component to the loss of identity. We propose a developmental mechanism – gradual expansion of the polyalanine region of HoxD13 over ichthyosaurian evolution – to explain the progressive loss of limb regionalization as well as the heterochronic delay in perichondral ossification.

Keywords

IchthyosauriaStenopterygiuslimb evolutionbone histologyheterochronyHoxD13intraspecific variation
Type
Original Articles
Information
Geological Magazine , Volume 151 , Issue 1 , January 2014 , pp. 29 - 40
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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.CrossRefGoogle ScholarPubMed
Archer, C. W., Dowthwaite, G. P. & Francis-West, P. 2007. Joint formation. In Fins into Limbs (ed. Hall, B. K.), pp. 109–17. Chicago: University of Chicago Press.Google Scholar
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.CrossRefGoogle ScholarPubMed
Bruneau, S., Johnson, K. R., Yamamoto, M., Kuroiwa, A. & Duboule, D. 2001. The mouse Hoxd13 spdh 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.CrossRefGoogle Scholar
Buchholtz, E. A. 2001. Swimming styles in Jurassic ichthyosaurs. Journal of Vertebrate Paleontology 21, 61–73.CrossRefGoogle Scholar
Buchholtz, E. A. 2007. Modular evolution of the cetacean vertebral column. Evolution and Development 9, 278–89.CrossRefGoogle ScholarPubMed
Caldwell, M. W. 1997 a. Limb ossification patterns of the ichthyosaur Stenopterygius, and a discussion of the proximal tarsal row of ichthyosaurs and other neodiapsid reptiles. Zoological Journal of the Linnean Society 120, 1–25.CrossRefGoogle Scholar
Caldwell, M. W. 1997 b. Modified perichondral ossification and the evolution of paddle-like limbs in ichthyosaurs and plesiosaurs. Journal of Vertebrate Paleontology 17, 534–47.CrossRefGoogle Scholar
Caldwell, M. W. 2002. From fins to limbs to fins: limb evolution in fossil marine reptiles. American Journal of Medical Genetics 112, 236–49.CrossRefGoogle ScholarPubMed
Camp, C. L. 1980. Large ichthyosaurs from the Upper Triassic of Nevada. Palaeontographica Abteilung A 170, 139–200.Google Scholar
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.CrossRefGoogle Scholar
Chinsamy, A. & Raath, M. A. 1992. Preparation of fossil bone for histological examination. Palaeontologia Africana 29, 39–44.Google Scholar
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.CrossRefGoogle ScholarPubMed
Cooper, L. N., Berta, A., Dawson, S. D. & Reidenberg, J. S. 2007 a. Evolution of hyperphalangy and digit reduction in the cetacean manus. Anatomical Record 290, 654–72.CrossRefGoogle ScholarPubMed
Cooper, L. N., Dawson, S. D., Reidenberg, J. S. & Berta, A. 2007 b. Neuromuscular anatomy and evolution of the cetacean forelimb. Anatomical Record 290, 1121–37.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
de Buffrénil, V. & Mazin, J.-M. 1990. Bone histology of the ichthyosaurs: comparative data and functional interpretation. Paleobiology 16, 435–47.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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 Moody, R. T. J., Buffetaut, E., Naish, D. & Martill, D. M.), pp. 5–29. London: Geological Society.Google Scholar
Fedak, T. J. & Hall, B. K. 2004. Perspectives on hyperphalangy: patterns and processes. Journal of Anatomy 204, 151–63.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Fraas, E. 1891. Ichthyosaurier der süddeutschen Trias- und Jura- Ablagerungen. Tübingen: H. Laupp.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
von Huene, F. 1922. Die Ichthyosaurier des Lias und ihre Zusammenhänge. Berlin: Verlag von Gebrüder Borntraeger.Google Scholar
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.CrossRefGoogle Scholar
Johnson, R. 1979. The osteology of the pectoral complex of Stenopterygius Jaekel (Reptilia: Ichthyosauria). Neues Jahrbuch für Geologie und Paläontologie. Abhandlungen 159, 41–86.Google Scholar
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 l'Académie Impériale des Sciences de Saint-Pétersbourg 28, 1–103.Google Scholar
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.CrossRefGoogle Scholar
Lopuchowycz, V. B. & Massare, J. A. 2002. Bone microstructure of a Cretaceous ichthyosaur. Paludicola 3, 139–47.Google Scholar
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.CrossRefGoogle Scholar
Maxwell, E. E. 2012. Unraveling the influences of soft-tissue flipper development on skeletal variation using an extinct taxon. Journal of Experimental Zoology (Molecular and Developmental Evolution) 318, 545–54.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
McGowan, C. 1973. Differential growth in three ichthyosaurs: Ichthyosaurus communis, I. breviceps, and Stenopterygius quadriscissus (Reptilia, Ichthyosauria). Life Sciences Contributions, Royal Ontario Museum 93, 1–21.Google Scholar
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.Google Scholar
McGowan, C. & Motani, R. 2003. Ichthyopterygia. Handbook of Paleoherpetology (ed. Sues, H.-D.). München: Verlag Dr. Friedrich Pfeil.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Motani, R. 1997. New information of the forefin of Utatsusaurus hataii (Ichthyosauria). Journal of Paleontology 71, 475–9.CrossRefGoogle Scholar
Motani, R. 1998. First complete forefin of the ichthyosaur Grippia longirostris from the Triassic of Spitsbergen. Palaeontology 41, 591–9.Google Scholar
Motani, R. 1999 a. On the evolution and homologies of ichthyopterygian forefins. Journal of Vertebrate Paleontology 19, 28–41.CrossRefGoogle Scholar
Motani, R. 1999 b. Phylogeny of the Ichthyopterygia. Journal of Vertebrate Paleontology 19, 472–95.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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. Sarjeant, W. A. S.), pp. 521–35. Amsterdam: Gordon and Breach.Google Scholar
Quinn, G. P. & Keough, M. J. 2002. Experimental Design and Data Analysis for Biologists. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
R Development Core Team. 2011. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Swalla, B. J. 2006. Building divergent body plans with similar genetic pathways. Heredity 97, 235–43.CrossRefGoogle ScholarPubMed
Tabin, C. & Wolpert, L. 2007. Rethinking the proximodistal axis of the vertebrate limb in the molecular era. Genes and Development 21, 1433–42.CrossRefGoogle ScholarPubMed
Thewissen, J. G. M. & Taylor, M. A. 2007. Aquatic adaptations in the limbs of amniotes. In Fins into Limbs (ed. Hall, B. K.), pp. 310–22. Chicago: University of Chicago Press.Google Scholar
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.CrossRefGoogle ScholarPubMed
Towers, M. & Tickle, C. 2009. Growing models of vertebrate limb development. Development 136, 179–90.CrossRefGoogle ScholarPubMed
Urlichs, M., Wild, R. & Ziegler, B. 1979. Fossilien aus Holzmaden. Stuttgarter Beiträge zur Naturkunde Serie C 11, 1–34.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Woltering, J. M. & Duboule, D. 2010. The origin of digits: expression patterns versus regulatory mechanisms. Developmental Cell 18, 526–32.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Zeller, R., López-Ríos, J. & Zuniga, A. 2009. Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nature Reviews Genetics 10, 845–58.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Supplementary material: File

Maxwell Supplementary Material

Tables S1-S2

Download Maxwell Supplementary Material(File)
File 76.3 KB