Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

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 |

Anker, A. , Ahyong, S. T. , Noel, P. Y. , and Palmer, A. R. (2006). Morphological phylogeny of alpheid shrimps: parallel preadaptation and the origin of a key morphological innovation, the snapping claw. Evolution 60, 2507–2528.


Asher, R. J. , Horovitz, I. , and Sanchez-Villagra, M. R. (2004). First combined cladistic analysis of marsupial mammal interrelationships. Molecular Phylogenetics and Evolution 33, 240–250.
CrossRef |

Baudinette, R. V. , Gannon, B. J. , Runciman, W. B. , Wells, S. , and Love, J. B. (1987). Do cardio-respiratory frequencies show entrainment with hopping in the tammar wallaby? The Journal of Experimental Biology 129, 251–263.


Beck, R. M. D. (2008). A dated phylogeny of marsupials using a molecular supermatrix and multiple fossil constraints. Journal of Mammalogy 89, 175–189.
CrossRef |

Bennett, M. B. (2000). Unifying principles in terrestrial locomotion: do hopping Australian marsupials fit in? Physiological and Biochemical Zoology 73, 726–735.
CrossRef |

Bininda-Emonds, O. R. P. , Jeffery, J. E. , and Richardson, M. K. (2003). Is sequence heterochrony an important evolutionary mechanism in mammals? Journal of Mammalian Evolution 10, 335–361.
CrossRef |

Bininda-Emonds, O. R. P. , Cardillo, M. , Jones, K. E. , MacPhee, R. D. E. , Beck, R. M. D. , Grenyer, R. , Price, S. A. , Vos, R. A. , Gittleman, J. L. , and Purvis, A. (2007). The delayed rise of present-day mammals. Nature 446, 507–512.
CrossRef |

Bond, J. E. , and Opell, B. D. (1998). Testing adaptive radiation and key innovation hypotheses in spiders. Evolution 52, 403–414.
CrossRef |

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 |

Cockburn, A. (1989). Adaptive patterns in marsupial reproduction. Trends in Ecology & Evolution 4, 126–130.
CrossRef |

Croft, D. A. (2006). Do marsupials make good predators? Insights from predator–prey diversity ratios. Evolutionary Ecology Research 8, 1193–1214.


de Muizon, C. (1999). Marsupial skulls from the Deseadan (Late Oligocene) of Bolivia and phylogenetic analysis of the Borhyaenoidea (Marsupialia, Mammalia). Geobios 32, 483–509.
CrossRef |

Delsuc, F. , Scally, M. , Madsen, O. , Stanhope, M. J. , de Jong, W. W. , Catzeflis, F. M. , Springer, M. S. , and Douzery, E. J. P. (2002). Molecular phylogeny of living xenarthrans and the impact of character and taxon sampling on the placental tree rooting. Molecular Biology and Evolution 19, 1656–1671.


Fernandez, M. H. , and Vrba, E. S. (2005). A complete estimate of the phylogenetic relationships in Ruminantia: a dated species-level supertree of the extant ruminants. Biological Reviews of the Cambridge Philosophical Society 80, 269–302.
CrossRef |

Foote, M. (1997). The evolution of morphological diversity. Annual Review of Ecology and Systematics 28, 129–152.
CrossRef |

Fulton, T. L. , and Strobeck, C. (2006). Molecular phylogeny of the Arctoidea (Carnivora): effect of missing data on supertree and supermatrix analyses of multiple gene data sets. Molecular Phylogenetics and Evolution 41, 165–181.
CrossRef |

Gaudin, T. J. (2004). Phylogenetic relationships among sloths (Mammalia, Xenarthra, Tardigrada): the craniodental evidence. Zoological Journal of the Linnean Society 140, 255–305.
CrossRef |

Gemmell, R. T. , Veitch, C. , and Nelson, J. (2002). Birth in marsupials. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 131, 621–630.
CrossRef |

Givnish, T. J. , Millam, K. C. , Mast, A. R. , Paterson, T. B. , Theim, T. J. , Hipp, A. L. , Henss, J. M. , Smith, J. F. , Wood, K. R. , and Sytsma, K. J. (2008). Origin, adaptive radiation and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae). Proceedings of the Royal Society B: Biological Sciences 276, 407–416.
CrossRef |

Graves, J. A. M. , and Westerman, M. (2002). Marsupial genetics and genomics. Trends in Genetics 18, 517–521.
CrossRef |

Hamrick, M. W. (2001). Development and evolution of the mammalian limb: adaptive diversification of nails, hooves, and claws. Evolution & Development 3, 355–363.
CrossRef |

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 |

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 |

Kirsch, J. A. W. (1977). The six-percent solution: second thoughts on the adaptedness of the Marsupialia. American Scientist 65, 276–288.


Klima, M. (1987). Early development of the shoulder girdle and sternum in marsupials (Mammalia: Metatheria). Advances in Anatomy, Embryology, and Cell Biology 47, 1–80.


Konow, N. , Bellwood, D. R. , Wainwright, P. C. , and Kerr, A. M. (2008). Evolution of novel jaw joints promote trophic diversity in coral reef fishes. Biological Journal of the Linnean Society 93, 545–555.
CrossRef |

Krajewski, C. , Wroe, S. , and Westerman, M. (2000). Molecular evidence for the pattern and timing of cladogenesis in dasyurid marsupials. Zoological Journal of the Linnean Society 130, 375–404.
CrossRef |

Kullberg, M. , Hallstrom, B. M. , Arnason, U. , and Janke, A. (2008). Phylogenetic analysis of 1.5 Mbp and platypus EST data refute the Marsupionta hypothesis and unequivocally support Monotremata as sister group to Marsupialia/Placentalia. Zoologica Scripta 37, 115–127.
CrossRef |

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.


Lillegraven, J. A. (1975). Biological considerations of the marsupial–placental dichotomy. Evolution 29, 707–722.
CrossRef |

Lyne, A. G. (1974). Gestation period and birth in the marsupial Isoodon macrourus. Australian Journal of Zoology 22, 303–309.
CrossRef |

Mabuchi, K. , Miya, M. , Azuma, Y. , and Nishida, M. (2007). Independent evolution of the specialized pharyngeal jaw apparatus in cichlid and labrid fishes. BMC Evolutionary Biology 7,
CrossRef |

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 |

Martin, K. E. A. , and Mackay, S. (2003). Postnatal development of the fore- and hindlimbs in the grey short-tailed opossum, Monodelphis domestica. Journal of Anatomy 202, 143–152.
CrossRef |

Meredith, R. W. , Westerman, M. , Case, J. A. , and Springer, M. S. (2008). A phylogeny and timescale for marsupial evolution based on sequences for five nuclear genes. Journal of Mammalian Evolution 15, 1–36.
CrossRef |

Monteiro, L. R. (2000). Why morphometrics is special: the problem with using partial warps as characters for phylogenetic inference. Systematic Biology 49, 796–800.
CrossRef |

Murphy, W. J. , Eizirik, E. , O’Brien, S. J. , Madsen, O. , and Scally, M. , et al. (2001). Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294, 2348–2351.
CrossRef |

Murphy, W. J. , Pringle, T. H. , Crider, T. A. , Springer, M. S. , and Miller, W. (2007). Using genomic data to unravel the root of the placental mammal phylogeny. Genome Research 17, 413–421.
CrossRef |

Nelson, J. E. , and Gemmell, R. T. (2003). Birth in the northern quoll, Dasyurus hallucatus (Marsupialia: Dasyuridae). Australian Journal of Zoology 51, 187–198.
CrossRef |

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.


Oldham, S. , Bohni, R. , Stocker, H. , Brogiolo, W. , and Hafen, E. (2000). Genetic control of size in Drosophila. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 945–952.
CrossRef |

Pflieger, J.-F. , Cassidy, G. , and Cabana, T. (1996). Development of spontaneous locomotor behaviors in the opossum, Monodelphis domestica. Behavioural Brain Research 80, 137–143.
CrossRef |

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 |

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 |

Richardson, M. K. , and Chipman, A. D. (2003). Developmental constraints in a comparative framework: a test case using variations in phalanx number during amniote evolution. Journal of Experimental Zoology. Part B. Molecular and Developmental Evolution 296B, 8–22.
CrossRef |

Rohland, N. , Malaspinas, A. S. , Pollack, J. L. , Slatkin, M. , Matheus, P. , and Hofreiter, M. (2007). Proboscidean mitogenomics: chronology and mode of elephant evolution using mastodon as outgroup. PLoS Biology 5, e207.
CrossRef |

Rohlf, F. J. (1998). On applications of geometric morphometrics to studies of ontogeny and phylogeny. Systematic Biology 47, 147–158.
CrossRef |

Rohlf, F. J. , and Bookstein, F. L. (1987). A comment on shearing as a method for size correction. Systematic Zoology 36, 356–367.
CrossRef |

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 |

Sears, K. E. (2004). Constraints on the morphological evolution of marsupial shoulder girdles. Evolution 58, 2353–2370.


Sharman, G. B. (1970). Reproductive physiology of marsupials. Science 167, 1221–1228.
CrossRef |

Smith, J. M. , Burian, R. , Kauffman, S. , Alberch, P. , Campbell, J. , Goodwin, B. , Lande, R. , Raup, D. , and Wolpert, L. (1985). Developmental constraints and evolution. The Quarterly Review of Biology 60, 265–287.
CrossRef |

Smith, K. K. (1997). Comparative patterns of craniofacial development in eutherian and metatherian mammals. Evolution 51, 1663–1678.
CrossRef |

Smith, K. K. (2001). Heterochrony revisited: the evolution of developmental sequences. Biological Journal of the Linnean Society 73, 169–186.
CrossRef |

Springer, M. S. (1997). Molecular clocks and the timing of the placental and marsupial radiations in relation to the Cretaceous–Tertiary boundary. Journal of Mammalian Evolution 4, 285–302.
CrossRef |

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 |

Warheit, K. I. , Forman, J. D. , Losos, J. B. , and Miles, D. B. (1999). Morphological diversification and adaptive radiation: a comparison of two diverse lizard clades. Evolution 53, 1226–1234.
CrossRef |

Weisbecker, V. , and Archer, M. (2008). Parallel evolution of hand anatomy in kangaroos and vombatiform marsupials: functional and evolutionary implications. Palaeontology 51, 321–338.
CrossRef |

Weisbecker, V. , and Warton, D. I. (2006). Evidence at hand: diversity, functional implications, and locomotor prediction in intrinsic hand proportions of diprotodontian marsupials. Journal of Morphology 267, 1469–1485.
CrossRef |

Weisbecker, V. , Goswami, A. , Wroe, S. , and Sanchez-Villagra, M. R. (2008). Ossification heterochrony in the therian postcranial skeleton and the marsupial–placental dichotomy. Evolution 62, 2027–2041.
CrossRef |

Wells, R. T. , and Tedford, R. H. (1995). Sthenurus (Macropodidae, Marsupialia) from the Pleistocene of Lake Callabonna, South Australia. Bulletin of the American Museum of Natural History 225, 1–111.


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 |

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

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

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 |





Appendix 1.  Taxonomic list of the species examined
An asterisk denotes fossil specimens
Click to zoom



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
Click to zoom



Appendix 3.  Limb measurements collected
Click to zoom



Rent Article (via Deepdyve) Export Citation Cited By (17)