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Ontogenetic and stratigraphic influence on observed phenotypic integration in the limb skeleton of a fossil tetrapod

Published online by Cambridge University Press:  08 April 2016

Erin E. Maxwell  and
T. Alexander Dececchi
Erin E. Maxwell
Affiliation:
Museum für Naturkunde Berlin and Staatliches Museum für Naturkunde, Rosenstein 1, 70191 Stuttgart, Germany. E-mail: [email protected]
T. Alexander Dececchi
Affiliation:
Redpath Museum, McGill University, 859 Sherbrooke Street West, Montreal, Quebec H3A 2K6, Canada. E-mail: [email protected]
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Abstract

Understanding morphological integration is one of the central goals of evolutionary developmental biology. Despite its applicability to questions of paleontological interest, there are few studies on integration in fossil vertebrates. In this study, we examine limb integration in the Lower Jurassic ichthyosaur Stenopterygius quadriscissus, with the aim of examining the effect of ontogeny and anagenetic changes over short geological time spans on metrics of limb integration. Both ontogenetic and stratigraphic effects had a significant influence on measured values of integration, the identity of strongly integrated elements, and some common ratio values such as the relative integration of the forelimb to the hind limb, or within-limb to between-limb integration. Ontogenetic effects were relatively greater, although this could be linked to sample size. Although adults showed the lowest levels of overall integration, they possessed high levels of integration between serially homologous elements, something that was unexpected due to strong divergence in limb size and perhaps functional differences in derived ichthyosaurs. Ontogenetic differences in the relative integration of the forelimb to the hind limb are probably related to early locomotor demands on the forelimb. We conclude that if samples are pooled, the resulting pattern of integration may not reflect any one subsample but will be a composite created through the superposition of several variables. Pooling data in paleontological studies of integration has a non-trivial effect on the results obtained.

Type
Articles
Information
Paleobiology , Volume 39 , Issue 1 , Winter 2013 , pp. 123 - 134
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Ackermann, R. R. 2005. Ontogenetic integration of the hominoid face. Journal of Human Evolution 48:175.—197.Google Scholar
Ackermann, R. R., and Cheverud, J. M. 2000. Phenotypic covariance structure in tamarins (genus Saguinus): a comparison of variation patterns using matrix correlation and common principal component analysis. American Journal of Physical Anthropology 111:489.—501.Google Scholar
Bell, E., Andres, B., and Goswami, A. 2011. Integration and dissociation of limb elements in flying vertebrates: a comparison of pterosaurs, birds and bats. Journal of Evolutionary Biology 24:2589.—2599.Google Scholar
Bennett, C. V., and Goswami, A. 2011. Does developmental strategy drive limb integration in marsupials and monotremes? Mammalian Biology 76:79.—83.Google Scholar
Böttcher, R. 1990. Neue Erkenntnisse über die Fortpflanzungsbiologie der Ichthyosaurier (Reptilia). Stuttgarter Beiträge zur Naturkunde, serie B 164:1.—52.Google Scholar
Buchholtz, E. A. 2001. Swimming styles in Jurassic ichthyosaurs. Journal of Vertebrate Paleontology 21:61.—73.Google Scholar
Caldwell, M. W. 1997. 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.Google Scholar
Cane, W. P. 1993. The ontogeny of postcranial integration in the Common Tern, Sterna hirundo. Evolution 47:1138.—1151.Google Scholar
Cheverud, J. M. 1996a. Developmental integration and the evolution of pleiotropy. American Zoologist 36:44.—50.Google Scholar
Cheverud, J. M. 1996b. Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins. Journal of Evolutionary Biology 9:5.—42.Google Scholar
Cheverud, J. M., Wagner, G. P., and Dow, M. M. 1989. Methods for the comparative analysis of variation patterns. Systematic Zoology 38:201.—213.Google Scholar
de Buffrénil, V., and Mazin, J.-M. 1990. Bone histology of the ichthyosaurs: comparative data and functional interpretation. Paleobiology 16:435.—447.Google Scholar
de Oliveira, F. B., Porto, A., and Marroig, G. 2009. Covariance structure in the skull of Catarrhini: a case of pattern stasis and magnitude evolution. Journal of Human Evolution 56:417.—430.Google Scholar
Duboc, V., and Logan, M. P. O. 2011. Regulation of limb bud initiation and limb-type morphology. Developmental Dynamics 240:1017.—1027.Google Scholar
Erickson, G. M., Rogers, K. C., Varricchio, D. J., Norell, M. A., and Xu, X. 2007. Growth patterns in brooding dinosaurs reveal the timing of sexual maturity in non-avian dinosaurs and genesis of the avian condition. Biology Letters 3:558.—561.Google Scholar
Farnum, C. E. 2007. Postnatal growth of fins and limbs through endochondral ossification. Pp. 118.—151inHall, B. K., ed. Fins into limbs: evolution, development, and transformation. University of Chicago Press, Chicago.Google Scholar
Fernández, M. S. 1994. A new long-snouted ichthyosaur from the Early Bajocian of Neuquén Basin (Argentina). Ameghiniana 31:291.—297.Google Scholar
Fernández, M. S. 2007. Ichthyosauria. Pp. 271.—291inGasparini, Z., Salgado, L., and Coria, R. A., eds. Patagonian Mesozoic reptiles. Indiana University Press, Bloomington.Google Scholar
Fischer-Rousseau, L., Cloutier, R., and Zelditch, M. L. 2009. Morphological integration and developmental progress during fish ontogeny in two contrasting habitats. Evolution and Development 11:740.—753.Google Scholar
Game, E. T., and Caley, M. J. 2006. The stability of P in coral reef fishes. Evolution 60:814.—823.Google Scholar
Goswami, A., and Polly, P. D. 2010. Methods for studying morphological integration and modularity. InAlroy, J. and Hunt, G., eds. Quantitative methods in paleobiology. Paleontological Society Papers 16:213.—243CrossRefGoogle Scholar
Hallgrímsson, B., Jamniczky, H., Young, N. M., Rolian, C., Parsons, T. E., Boughner, J. C., and Marcucio, R. S. 2009. Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evolutionary Biology 36:355.—376.Google Scholar
Hammer, Ø., Harper, D. A. T., and Ryan, P. D. 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4 (1):9pp.Google Scholar
Hendrikse, J. L., Parsons, T. E., and Hallgrímsson, B. 2007. Evolvability as the proper focus of evolutionary developmental biology. Evolution and Development 9:393.—401.Google Scholar
Hunt, G. 2004. Phenotypic variance inflation in fossil samples: an empirical assessment. Paleobiology 30:487.—506.Google Scholar
Hunt, G., Bell, M. A., and Travis, M. P. 2008. Evolution toward a new adaptive optimum: phenotypic evolution in a fossil stickleback lineage. Evolution 62:700.—710.Google Scholar
Ivanović, A., Kalezić, M. L., and Aleksić, I. 2005. Morphological integration of cranium and postcranial skeleton during ontogeny of facultative paedomorphic European newts (Triturus vulgaris and T. alpestris). Amphibia-Reptilia 26:485.—495.Google Scholar
Kardong, K. V. 1998. Vertebrates: comparative anatomy, function, evolution. WCB McGraw Hill, Boston.Google Scholar
Keller, T. 1976. Magen- und Darminhalte von Ichthyosauriern des süddeutschen Posidonienshiefers. Neues Jahrbuch für Geologie und Paläontologie Monatshefte 1976:253.—320.Google Scholar
Keller, T. 1992. “Weichteil-Erhaltung” bei großen Vertebraten (Ichthyosauriern) des Posidonienschiefers Holzmadens (Oberer Lias, Mesozoikum Süddeutschlands). Kaupia: Darmstädter Beiträge zur Naturgeschichte 1:23.—62.Google Scholar
Kelly, E. M., and Sears, K. E. 2011. Reduced phenotypic covariation in marsupial limbs and the implications for mammalian evolution. Biological Journal of the Linnean Society 102:22.—36.Google Scholar
Klima, M. 1992. Schwimmbewegungen und Auftauchmodus bei Walen und bei Ichthyosauriern I. Anatomische Grundlagen der Schwimmbewegungen. Natur und Museum 122:1.—17.Google Scholar
Kolarov, N. T., Ivanović, A., and Kalezić, M. L. 2011. Morphological integration and ontogenetic niche shift: a study of crested newt limbs. Journal of Experimental Zoology B 316:296.—305.Google Scholar
Kolbe, J. J., Revell, L. J., Szekely, B., Brodie, E. D. III, and Losos, J. B. 2011. Convergent evolution of phenotypic integration and its alignment with morphological diversification in Caribbean Anolis ecomorphs. Evolution 65:3608.—3624.Google Scholar
Lawler, R. R. 2008. Morphological integration and natural selection in the postcranium of wild Verreaux's sifaka (Propithecus verreauxi verreauxi). American Journal of Physical Anthropology 136:204.—213.Google Scholar
Littke, R., Baker, D. R., Leythaeuser, D., and Rullkötter, J. 1991. Keys to the depositional history of the Posidonia Shale (Toarcian) in the Hils Syncline, northern Germany. InTyson, R. V. and Pearson, T. H., eds. Modern and ancient continental shelf anoxia. Geological Society Special Publication 58:311.—333.Google Scholar
Lockwood, C. A. 2007. Adaptation and functional integration in primate phylogenetics. Journal of Human Evolution 52:490.—503.Google Scholar
Lovejoy, C. O., Cohn, M. J., and White, T. D. 1999. Morphological analysis of the mammalian postcranium: a developmental perspective. Proceedings of the National Academy of Sciences 96:13247.—13252.Google Scholar
Magwene, P. M. 2001. New tools for studying integration and modularity. Evolution 55:1734.—1745.Google Scholar
Maisch, M. W. 2008. Revision der Gattung Stenopterygius Jaekel, 1904 emend. von Huene, 1922 (Reptilia: Ichthyosauria) aus dem unteren Jura Westeuropas. Paleodiversity 1:227.—271.Google Scholar
Marroig, G., and Cheverud, J. M. 2001. A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of New World monkeys. Evolution 55 (12):2576.—2600.Google Scholar
Maxwell, E. E. 2012. New metrics to differentiate species of Stenopterygius (Reptilia: Ichthyosauria) from the Lower Jurassic of southwestern Germany. Journal of Paleontology 86:105.—115.Google Scholar
Maxwell, E. E.In press. Unraveling the influences of soft-tissue flipper development on skeletal variation using an extinct taxon. Journal of Experimental Zoology B (Molecular and Developmental Evolution). doi: 10.1002/jez.b.22459.Google Scholar
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. 1979. A revision of the Lower Jurassic ichthyosaurs of Germany with descriptions of two new species. Palaeontographica Abt. A 166 (4–6):93.—135.Google Scholar
McGowan, C., and Motani, R. 2003. Ichthyopterygia. Friedrich Pfeil, Munich.Google Scholar
Mitteroecker, P., and Bookstein, F. 2009. The ontogenetic trajectory of the phenotypic covariance matrix, with examples from craniofacial shape in rats and humans. Evolution 63:727.—737.Google Scholar
Motani, R. 1999. On the evolution and homologies of ichthyopterygian forefins. Journal of Vertebrate Paleontology 19:28.—41.Google Scholar
Motani, R. 2002. Swimming speed estimation of extinct marine reptiles: energetic approach revisited. Paleobiology 28:251.—262.Google Scholar
Motani, R. 2005. Evolution of fish-shaped reptiles (Reptilia: Ichthyopterygia) in their physical environments and constraints. Annual Review of Earth and Planetary Sciences 33:395.—420.Google Scholar
Olson, E. C., and Miller, R. L. 1958. Morphological integration. University of Chicago Press, Chicago.Google Scholar
Pavlicev, M., Cheverud, J. M., and Wagner, G. P. 2009. Measuring morphological integration using eigenvalue variance. Evolutionary Biology 36:157.—170.Google Scholar
R Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Rolian, C. 2009. Integration and evolvability in primate hands and feet. Evolutionary Biology 36:100.—117.Google Scholar
Ruvinsky, I., and Gibson-Brown, J. J. 2000. Genetic and developmental bases of serial homology in vertebrate limb evolution. Development 127:5233.—5244.Google Scholar
Sander, P. M. 2000. Ichthyosauria: their diversity, distribution and phylogeny. Paläontologische Zeitschrift 74 (1/2):1.—35.Google Scholar
Schmidt, M., and Fischer, M. S. 2009. Morphological integration in mammalian limb proportions: dissociation between function and development. Evolution 63:749.—766.Google Scholar
Steppan, S. J. 1997. Phylogenetic analysis of phenotypic covariance structure. I. Contrasting results from matrix correlation and common principal component analysis. Evolution 51:571.—586.Google Scholar
Steppan, S. J., Phillips, P. C., and Houle, D. 2002. Comparative quantitative genetics: evolution of the G matrix. Trends in Ecology and Evolution 17:320.—327.Google Scholar
Thewissen, J. G. M., and Taylor, M. A. 2007. Aquatic adaptations in the limbs of amniotes. Pp. 310.—322inHall, B. K., ed. Fins into limbs. University of Chicago Press, Chicago.Google Scholar
Ubukata, T., Kitamura, A., Hiramoto, M., and Kase, T. 2009. A 5000-year fossil record of larval shell morphology of submarine cave microshells. Evolution 63:295.—300.Google Scholar
Urlichs, M., Wild, R., and Ziegler, B. 1979. Fossilien aus Holzmaden. Stuttgarter Beiträge zur Naturkunde, serie C 11:1.—34.Google Scholar
Villmoare, B., Fish, J., and Jungers, W. 2011. Selection, morphological integration, and strepsirrhine locomotor adaptations. Evolutionary Biology 38:88.—99.Google Scholar
Wagner, G. P. 1984. On the eigenvalue distribution of genetic and phenotypic dispersion matrices: evidence for a nonrandom organization of quantitative character variation. Journal of Mathematical Biology 21:77.—95.Google Scholar
Weisbecker, V., and Nilsson, M. 2008. Integration, heterochrony and adaptation in pedal digits of syndactylous marsupials. BMC Evolutionary Biology 8 (160). doi:10.1186/1471-2148-8-160.Google Scholar
Williams, S. A. 2010. Morphological integration and the evolution of knuckle-walking. Journal of Human Evolution 58:432.—440.Google Scholar
Willmore, K. E., Leamy, L., and Hallgrímsson, B. 2006. Effects of developmental and functional interactions on mouse cranial variability through late ontogeny. Evolution and Development 8:550.—567.Google Scholar
Wilson, L. A. B.In press. The contribution of developmental palaeontology to extensions of evolutionary theory. Acta Zoologica. doi:10.1111/j.1463–6395.2011.00539.x.Google Scholar
Young, N. M., and Hallgrímsson, B. 2005. Serial homology and the evolution of mammalian limb covariation structure. Evolution 59:2691.—2704.Google Scholar
Young, N. M., Hallgrímsson, B., and Garland, T. Jr. 2009. Epigenetic effects on integration of limb lengths in a mouse model: selective breeding for high voluntary locomotor activity. Evolutionary Biology 36:88.—99.Google Scholar
Young, N. M., Wagner, G. P., and Hallgrímsson, B. 2010. Development and the evolvability of human limbs. Proceedings of the National Academy of Sciences 107:3400.—3405.Google Scholar
Zelditch, M. L. 1988. Ontogenetic variation in patterns of phenotypic integration in the laboratory rat. Evolution 42:28.—41.Google Scholar
Zelditch, M. L. 2005. Developmental regulation of variability. Pp. 249.—276inHallgrímsson, B. and Hall, B. K., eds. Variation: a central concept in biology. Academic Press, New York.Google Scholar
Zelditch, M. L., and Carmichael, A. C. 1989. Ontogenetic variation in patterns of developmental and functional integration in skulls of Sigmodon fulviventer. Evolution 43:814.—824.Google Scholar
Zelditch, M. L., Bookstein, F. L., and Lundrigan, B. L. 1992. Ontogeny of integrated skull growth in the cotton rat Sigmodon fulviventer. Evolution 46:1164.—1180.Google Scholar
Zelditch, M. L., Mezey, J., Sheets, H. D., Lundrigan, B. L., and Garland, T. Jr. 2006. Developmental regulation of skull morphology II: ontogenetic dynamics of covariance. Evolution and Development 8:46.—60.Google Scholar