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Evolutionary, molecular and comparative zoology
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RESEARCH ARTICLE
Contents Vol 58(1)

Developmental constraint on the evolution of marsupial forelimb morphology

W. James Cooper A B C and Scott J. Steppan A
+ Author Affiliations
- Author Affiliations

A Department of Biological Science, The Florida State University, Tallahassee, FL 32306-4295, USA.

B Present address: Department of Biology, Syracuse University, 107 College Place, Life Sciences Complex, Syracuse, NY 13244, USA.

C Corresponding author. Email: wjcooper@syr.edu

Australian Journal of Zoology 58(1) 1-15 https://doi.org/10.1071/ZO09102
Submitted: 7 October 2009  Accepted: 19 January 2010   Published: 7 April 2010

Abstract

Compared with the placental mammals, marsupials are born at an almost embryonic stage, but nearly all of these neonates immediately climb or crawl to one of their mother’s teats using precociously developed forelimbs. Marsupial adults also exhibit limited forelimb shape diversity relative to the members of their sister group. That the functional requirements of this natal climb have imposed a developmental constraint on marsupial forelimb evolution represents a compelling and widely accepted hypothesis, yet its resulting predictions for the comparative patterns of mammal limb shape diversity have never been tested. In order to perform such tests we conducted extensive taxonomic sampling of mammal limb morphology (including fossil specimens), and then examined these data using morphometric methods, non-parametric analyses of anatomical disparity, and phylogenetic comparative analyses of evolutionary rates. Our results strongly support the constraint hypothesis, and indicate that the highly significant differences between marsupial and placental forelimb shape diversity has been strongly influenced by different rates of morphological evolution among the distal forelimb elements in these two important mammal lineages.

Additional keywords: comparative method, developmental constraint, eutheria, forelimb, hindlimb, marsupial, metatheria, morphological evolution, morphometrics, placental mammal.


Acknowledgements

We thank Mike LaBarbera, Bill Parker, William Herrnkind, Mark Westneat, Barry Chernoff, Miriam Zelditch, Don Swiderski, Brian O’Meara, Craig Albertson and Geeta Sawh for valuable support and assistance. We also thank the staff of the following museums and universities for access to specimens: AMNH, FLIN, FLMNH, FMNH, MVZ, SAMA, and USNM. This work was supported by a grant from Sigma Xi and by the Department of Biological Science at The Florida State University.


References

Alroy, J. (1999). The fossil record of North American mammals: evidence for a Paleocene evolutionary radiation. Systematic Biology 48, 107–118.
| Crossref | GoogleScholarGoogle Scholar | Brooks D. R. , and McLennan D. H. (1993). ‘Phylogeny, Ecology, and Behavior: a Research Program in Comparative Biology.’ (University of Chicago Press: Chicago, IL.)

Burnaby, T. P. (1966). Growth-invariant discriminant functions and generalized distances. Biometrics 22, 96–110.
| Crossref | GoogleScholarGoogle Scholar | Hughes R. L. , and Hall L. S. (1988). Structural adaptations of the newborn marsupial. In ‘The Developing Marsupial’. (Eds C. H. Tyndale-Biscoe and P. A. Janssens.) pp. 8–27. (Springer-Verlag: Berlin.)

Jansa, S. A. , and Voss, R. (2005). Phylogenetic relationships of the marsupial genus Hyladelphys based on nuclear gene sequences and morphology. Journal of Mammalogy 86, 853–865.
| Crossref | GoogleScholarGoogle Scholar | Janssens P. A. , Hulbert A. J. , and Baudinette R. V. (1997). Development of the pouch young from birth to pouch vacation. In ‘Marsupial Biology’. (Eds N. R. Saunders and L. A. Hinds.) pp. 71–89. (University of New South Wales Press: Sydney.)

Jeffery, J. E. , Richardson, M. K. , Coates, M. I. , and Bininda-Emonds, O. R. P. (2002). Analyzing developmental sequences within a phylogenetic framework. Systematic Biology 51, 478–491.
| Crossref | GoogleScholarGoogle Scholar | LaBarbera M. (2002). Permutation resampling program for HiQ. Available at http://pondside.uchicago.edu/oba/faculty/labarbera_m.html [Verified February 2010]

Lee A. K. , and Cockburn A. (1985). ‘Evolutionary Ecology of Marsupials.’ (Cambridge University Press: Cambridge.)

Lentle, R. G. , Kruger, M. C. , Mellor, D. J. , Birtles, M. , and Moughan, P. J. (2006). Limb development in pouch young of the brushtail possum (Trichosurus vulpecula) and tammar wallaby (Macropus eugenii). Journal of Zoology 270, 122–131.
Maddison W. P. , and Maddison D. R. (2008). Mesquite: a modular system for evolutionary analysis. Version 2.5. Available at http://mesquiteproject.org [Verified January 2010]

Marshall, L. G. (1974). Why kangaroos hop. Nature 248, 174–176.
| Crossref | GoogleScholarGoogle Scholar | Nowak R. M. (1999). ‘Walker’s Mammals of the World.’ 6th edn. (The Johns Hopkins University Press: Baltimore.)

O’Meara, B. C. , Ane, C. , Sanderson, M. J. , and Wainwright, P. C. (2006). Testing for different rates of continuous trait evolution using likelihood. Evolution 60, 922–933.
Polly P. D. (2007). Limbs in mammalian evolution. In ‘Fins into Limbs: Evolution, Development and Transformation’. (Ed. B. K. Hall.) pp. 245–268. (University of Chicago Press: Chicago.)

Pujos, F. , and De Iuliis, G. (2007). Late oligocene Megatherioidea fauna (Mammalia: Xenarthra) from Salla-Luribay (Bolivia): new data on basal sloth radiation and Cingulata–Tardigrada split. Journal of Vertebrate Paleontology 27, 132–144.
| Crossref | GoogleScholarGoogle Scholar | Renfree M. (1993). Ontogeny, genetic control and phylogeny of female reproduction in monotreme and therian mammals. In ‘Mammalian Phylogeny: Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians and Marsupials’. (Eds F. S. Szalay, M. J. Novacek and M. C. McKenna.) pp. 4–20. (Springer-Verlag: New York.)

Reyes, A. , Gissi, C. , Catzeflis, F. , Nevo, E. , Pesole, G. , and Saccone, C. (2004). Congruent mammalian trees from mitochondrial and nuclear genes using Bayesian methods. Molecular Biology and Evolution 21, 397–403.
| Crossref | GoogleScholarGoogle Scholar | Romer A. S. (1966). ‘Vertebrate Paleontology.’ 3rd edn. (The University of Chicago Press: Chicago)

Sanchez-Villagra, M. R. , and Maier, W. (2003). Ontogenesis of the scapula in marsupial mammals, with special emphasis on perinatal stages of Didelphis and remarks on the origin of the scapula. Journal of Morphology 258, 115–129.
| Crossref | GoogleScholarGoogle Scholar | Szalay F. S. (1994). ‘Evolutionary History of Marsupials and an Analysis of Osteological Characters.’ (Cambridge University Press: Cambridge.)

Tyndale-Biscoe H. (2005). ‘Life of Marsupials.’ (CSIRO Publishing: Melbourne.)

Vaughan T. A. , Ryan J. M. , and Czaplewski N. J. (1999). ‘Mammalogy.’ 4th edn. (Brooks Cole: Pacific Grove.)

Waddell, P. J. , and Shelley, S. (2003). Evaluating placental inter-ordinal phylogenies with novel sequences including RAG1, gamma-fibrinogen, ND6, and mt-tRNA, plus MCMC-driven nucleotide, amino acid, and codon models. Molecular Phylogenetics and Evolution 28, 197–224.
| Crossref | GoogleScholarGoogle Scholar | Wilson D. E. , and Reeder D. M. (1993). ‘Mammal Species of the World: a Taxonomic and Geographic Reference.’ 2nd edn. (Smithsonian Institution Press: Washington, DC.)

Wilson D. E. , and Reeder D. M. (Eds) (2005). ‘Mammal Species of the World: a Taxonomic and Geographic Reference.’ 3rd edn. (The Johns Hopkins University Press: Baltimore, MD.)

Windsor, D. E. , and Dagg, A. L. (1971). The gaits of the Macropodidae (Marsupialia). Journal of Zoology 163, 165–175.


Withers, P. C. , Thompson, G. G. , and Seymour, R. S. (2000). Metabolic physiology of the north-western marsupial mole, Notoryctes caurinus (Marsupialia: Notoryctidae). Australian Journal of Zoology 48, 241–258.
| Crossref | GoogleScholarGoogle Scholar |

Wroe, S. , and Milne, N. (2007). Convergence and remarkably consistent constraint in the evolution of carnivore skull shape. Evolution 61, 1251–1260.
| Crossref | GoogleScholarGoogle Scholar |

Yu, L. , and Zhang, Y. P. (2006). Phylogeny of the caniform Carnivora: evidence from multiple genes. Genetica 127, 65–79.
| Crossref | GoogleScholarGoogle Scholar |

Zelditch, M. L. , Fink, W. L. , Swiderski, D. L. , and Lundrigan, B. L. (1998). On applications of geometric morphometrics to studies of ontogeny and phylogeny: a reply to Rohlf. Systematic Biology 47, 159–167.
| Crossref | GoogleScholarGoogle Scholar |





Appendix 1.  Taxonomic list of the species examined
An asterisk denotes fossil specimens
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Appendix 2.  Alphabetical list of specimens with museum identification numbers
AMNH, American Museum of Natural History; FLIN, Flinders University; FLMNH, Florida Museum of Natural History; FMNH, Field Museum of Natural History; MVZ, Museum of Vertebrate Zoology, University of California, Berkeley; SAMA, South Australian Museum; USNM, United States National Museum of Natural History
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Appendix 3.  Limb measurements collected
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