Limb specialization in living marsupial and eutherian mammals: Constraints on mammalian limb evolution

Journal of Mammalogy

Volumn 92, Issue 5, 2011, Pages 1038-1049

  Kelly, E McKenna ^a   Sears, Karen E ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

development; functional constraints; limb; macroevolution; mammalian evolution; marsupials; morphological evolution; morphometrics; reproductive strategies; specialization

Indexed keywords

EVOLUTIONARILY STABLE STRATEGY; FUNCTIONAL GROUP; HYPOTHESIS TESTING; LIMB; MAMMAL; MORPHOMETRY; REPRODUCTIVE STRATEGY; SPECIALIZATION;

EUTHERIA; MAMMALIA; METATHERIA;

EID: 80054741802     PISSN: 00222372     EISSN: 15451542     Source Type: Journal    
DOI: 10.1644/10-MAMM-A-425.1     Document Type: Article

References (53)

1. ALBERCH, P. 1982. Developmental constraints in evolutionary processes. Pp. 313-332 in Evolution and development (J. T. Bonner, ed.). Springer-Verlag, New York.
2. ARTHUR, W. 2001. Developmental drive: An important determinant of the direction of phenotypic evolution. Evolution and Development 3:271-278. (Pubitemid 32665254)
3. BELDADE, P., AND P. M. BRAKEFIELD. 2003. The difficulty of agreeing about constraints. Evolution and Development 5:119-120. (Pubitemid 37123879)
4. BELDADE, P., K. KOOPS, AND P. M. BRAKEFIELD. 2002. Developmental constraints versus flexibility in morphological evolution. Nature 416:844-847. (Pubitemid 34453739)
5. BENNETT, V., AND A. GOSWAMI. 2010. Does developmental strategy drive limb integration in marsupials and monotremes? Mammalian Biology 76:79-83.
6. BININDA-EMONDS, O. R. P., ET AL. 2007. Forelimb-hindlimb developmental timing changes across tetrapod phylogeny. BMC Evolutionary Biology 7:182-189.
7. BLOB, R. W., AND A. A. BIEWENER. 1999. In vivo locomotor strain in the hindlimb bones of Alligator mississippiensis and Iguana iguana: Implications for the evolution of limb bone safety factor and non-sprawling limb posture. Journal of Experimental Biology 202:1023-1046. (Pubitemid 29253001)
8. BRAKEFIELD, P. M. 2006. Evo-devo and constraints on selection. Trends in Ecology & Evolution 21:362-368. (Pubitemid 43947343)
9. BREUKER, C. J., V. DEBAT, AND C. P. KLINGENBERG. 2006. Functional evo-devo. Trends in Ecology & Evolution 21:488-492. (Pubitemid 44233955)
10. CHENG, C. 1955. The development of the shoulder region of the opossum, Didelphys virginiana, with special reference to the musculature. Journal of Morpholology 97:415-471.
11. CIAMPAGLIO, C. N. 2002. Determining the role that ecological and developmental constraints play in controlling disparity: Examples from the crinoid and blastozoan fossil record. Evolution and Development 4:170-188. (Pubitemid 34544124)
12. COOPER, J., AND S. J. STEPPAN. 2010. Developmental constraint on the evolution of marsupial forelimb morphology. Australian Journal of Zoology 58:1-15.
13. DOMAZET-LOSO, T., AND D. TAUTZ. 2010. A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 468:815-818.
14. FOOTE, M. 1994. Morphological disparity in Ordovician-Devonian crinoids and the early saturation of morphological space. Paleobiology 20:320-344.
15. FOOTE, M. 1995. Morphological diversification of Paleozoic crinoids. Paleobiology 21:273-299. (Pubitemid 26458331)
16. FRANKINO, W. A., B. J. ZWAAN, D. L. STERN, AND P. M. BRAKEFIELD. 2005. Natural selection and developmental constraints in the evolution of allometries. Science 307:718-720. (Pubitemid 40194640)
17. GALIS, F., J. M. JACQUES, AND J. A. J. METZ. 2001. Why five fingers? Evolutionary constraints on digit numbers. Trends in Ecology & Evolution 16:637-646. (Pubitemid 32947024)
18. GEMMELL, R. T., C. VEITCH, AND J. NELSON. 2002. Birth in marsupials. Comparative Biochemistry and Physiology, B. Comparative Biochemistry 131:621-630. (Pubitemid 34266815)
19. GOSWAMI, A., AND P. D. POLLY. 2010. The influence of modularity on cranial morphological disparity in Carnivora and Primates (Mammalia). PLoS ONE 5:e9517.
20. GOSWAMI, A., V. WEISBECKER, AND M. R. SÁNCHEZ-VILLAGRA. 2009. Developmental modularity and the marsupial-placental dichotomy. Journal of Experimental Zoology, B. Molecular and Developmental Evolution 312:186-195.
21. HUGHES, R. L., AND L. S. HALL. 1988. Structural adaptations of the newborn marsupial. Pp. 8-27 in The developing marsupial: Models for biomedical research (C. H. Tyndale-Biscoe and P. A. Janssens, eds.). Springer, Berlin, Germany.
22. JI, Q., Z.X. LUO, AND S. A. JI. 1999. A Chinese triconodont mammal and mosaic evolution of the mammalian skeleton. Nature 398:326-330. (Pubitemid 29161685)
23. KALINKA, A. T., ET AL. 2010. Gene expression divergence recapitulates the developmental hourglass model. Nature 468:811-814.
24. KELLY, M., AND K. E. SEARS. 2011. Limb integration in New World marsupials. Biological Journal of the Linnean Society 102:22-36.
25. 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.
26. KLINGENBERG, C. P. 2003. Developmental constraints, modules and evolvability. Pp. 219-249 in Variation: A central concept in biology (B. Hallgrimmson and B. K. Hall, eds.). Elsevier, Oxford, United Kingdom.
27. KOWALESKI, M., AND P. NOVACK-GOTTSHALL. 2010. Resampling methods in paleontology. Pp. 19-54 in Quantitative methods in paleobiology (J. Alroy and G. Hunt, eds.). The Paleontological Society Papers, The Paleotological Society, Chicago, Illinois.
28. LEE, A. K., AND A. COCKBURN. 1985. Evolutionary ecology of marsupials. Cambridge University Press, Cambridge, United Kingdom.
29. LILLEGRAVEN, J. A. 1975. Biological considerations of the marsupial- placental dichotomy. Evolution 29:707-722.
30. MARRIOG, G., AND J. M. CHEVERUD. 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 55:2576-2600. (Pubitemid 34115687)
31. MAYNARD SMITH, J., ET AL. 1985. Developmental constraints and evolution: A perspective from the Mountain Lake conference on development and evolution. Quarterly Review of Biology 60: 265-287.
32. OXNARD, C. E. 1963. Locomotor adaptations in the primate forelimb. Symposia of the Zoological Society of London 10:165-182.
33. NOWAK, R. M. 1999. Walker's mammals of the world. 6th ed. Johns Hopkins University Press, Baltimore, Maryland.
34. POLLY, P. D. 1998. Variability, selection, and constraints: Development and evolution in viverravid (Carnivora, Mammalia) molar morphology. Paleobiology 24:409-429.
35. POLLY, P. D. 2007. Limbs in mammalian evolution. Pp. 245-268 in Fins into limbs: Evolution, development, and transformation (B. K. Hall, ed.). University of Chicago Press, Chicago, Illinois.
36. RESNICK, D. 1995. Developmental constraints and patterns: Some pertinent distinctions. Journal of Theoretical Biology 173:231-240.
37. RICHARDSON, M. K., AND A. D. CHIPMAN. 2003. Developmental constraints in a comparative framework: A test case using variations in phalanx number during amniote evolution. Journal of Experimental Zoology, B. Molecular and Developmental Evolution 296:8-22. (Pubitemid 37529148)
38. SALAZAR-CIUDAD, I. 2006. Developmental constraints versus variational properties: How pattern formation can help to understand evolution and development. Journal of Experimental Zoology, B. Molecular and Developmental Evolution 306:107-125.
39. SCHMIDT, M., AND M. S. FISCHER. 2009. Morphological integration in mammalian limb proportions: Dissociation between function and development. Evolution 63:749-766.
40. SCHWENK, K. 1995. A utilitarian approach to evolutionary constraint. Zoology 98:251-262.
41. SEARS, K. E. 2004. Constraints on the morphological evolution of marsupial shoulder girdles. Evolution 58:2353-2370. (Pubitemid 39448283)
42. SEARS, K. E. 2009a. Differences in the timing of prechondrogenic limb development in mammals: The marsupial-placental dichotomy resolved. Evolution 63:2193-2200.
43. SEARS, K. E. 2009b. Molecular determinants of marsupial modularity and constraint. Journal of Vertebrate Paleontology 29:31A.
44. SEARS, K. E., R. R. BEHRINGER, J. J. RASWEILER, AND L. A. NISWANDER. 2007. The evolutionary and developmental basis of parallel reduction in mammalian zeugopod elements. American Naturalist 169:105-117. (Pubitemid 46095017)
45. SHARMAN, G. B. 1973. Adaptations of marsupial pouch young for extra-uterine existence. Pp. 67-90 in The mammalian fetus in vitro (C. R. Austin, ed.). Chapman and Hall, London, United Kingdom.
46. SOKAL, R. R., AND F. J. ROHLF. 1995. Biometry. 3rd ed. W. H. Freeman & Company, New York.
47. 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. (Pubitemid 128059915)
48. TARDIEU, C. 2010. Development of the human hind limb and its importance for the evolution of bipedalism. Evolutionary Anthropology 19:174-186.
49. WAGNER, P. J. 1995. Testing evolutionary constraint hypotheses with early Paleozoic gastropods. Paleobiology 21:248-272. (Pubitemid 26458246)
50. WAYNE, R. K. 1986. Limb morphology of domestic and wild canids: The influence of development on morphologic change. Journal of Morphology 187:301-319. (Pubitemid 16126134)
51. WEISBECKER, V., A. GOSWAMI, S. WROE, AND M. R. SANCHEZ-VILLAGRA. 2008. Ossification heterochrony in the therian postcranial skeleton and the marsupial-placental dichotomy. Evolution 62:2027-2041. (Pubitemid 352037069)
52. WILSON, D. E., AND D. M. REEDER (EDS.). 2005. Mammal species of the world: A taxonomic and geographic reference. 3rd ed. Johns Hopkins University Press, Baltimore, Maryland.
53. ZELDITCH, M. L., F. L. BOOKSTEIN, AND B. LUNDRIGAN. 1993. The ontogenetic complexity of developmental constraints. Journal of Evolutionary Biology 6:621-641.