Molecular determinants of marsupial limb integration and constraint

From Clone to Bone: The Synergy of Morphological and Molecular Tools in Palaeobiology

Volumn , Issue , 2009, Pages 257-278

  Sears, Karen E ^a   Doroba, Carolyn K ^a   Cao, Xiaoyi ^b   Xie, Dan ^c   Zhong, Sheng ^a  

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

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

^c University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84923538723     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1017/CBO9780511760174.010     Document Type: Chapter

References (90)

1. Alberch, P. (1982). Developmental constraints in evolutionary processes. In Evolution and Development, ed. J. T. Bonner. New York: Springer-Verlag, pp. 313–32.
2. Bénazet, J. D., Bischofberger, M., Tiecke, E., et al. (2009). A self-regulatory system of interlinked signaling feedback loops controls mouse limb patterning. Science, 323, 1050–3.
3. Bennett, V. and Goswami, A. (2011). Does developmental strategy drive limb integration in marsupials and monotremes? Mammalian Biology, 76, 79–83.
4. Bininda-Emonds, O. R. P., Jeffery, J. E. and Richardson, M. K. (2003a). Inverting the hourglass: quantitative evidence against the phylotypic stage in vertebrate development. Proceedings of the Royal Society B–Biological Sciences, 270, 341–6.
5. Bininda-Emonds, O. R. P., Jeffrey, J. E. and Richardson, M. K. (2003b). Is sequence heterochrony an important evolutionary mechanism in mammals. Journal of Mammalian Evolution, 10(4), 335–61.
6. Bininda-Emonds, O. R. P., Jeffery, J. E., Sánchez-Villagra, M. R., et al. (2007). Forelimb-hindlimb developmental timing changes across tetrapod phylogeny. BMC Evolutionary Biology, 7, 182–9.
7. Capdevila, J. and Belmonte, J. (2001). Patterning mechanisms controlling vertebrate limb development. Annual Review of Cellular and Developmental Biology, 17, 87–132.
8. Chen, C. H., Cretekos, C. J., Rasweiler, J. J. and Behringer, R. R. (2005). Hoxd13 expression in the developing limbs of the short-tailed fruit bat, Carollia perspicillata. Evolution and Development, 7(2), 130–41.
9. Cheng, C. (1955). The development of the shoulder region of the opossum, Didelpihis virginiana, with special reference to the musculature. Journal of Morphology, 97, 415–71.
10. Cohn, M. J. and Tickle, C. (1999). Developmental basis of limblessness and axial patterning in snakes. Nature, 399, 474–9.
11. Cooper, J. and Steppan, S. J. (2010). Developmental constraint on the evolution of marsupial forelimb morphology. Australian Journal of Zoology, 58, 1–15.
12. Cooper, L. N., Armfield, B. A. and Thewissen, J. G. M. (2011). Phenotypic variation and conserved FGF gene expression in the vertebrate limb ectoderm. In Epigenetics:Linking Genotype and Phenotype in Development and Evolution, ed. B. Hallgrímmson and B. K. Hall, pp. 238–55.
13. Doroba, C. K. and Sears, K. E. (2010). The divergent developmental of the apical ectodermal ridge in the marsupial Monodelphis domestica. Anatomical Record, 293(8), 1325–32.
14. Errick, J. E. and Saunders, J. W. (1974). Effects of an ‘inside-out’ limb-bud ectoderm on development of the avian limb. Developmental Biology, 41, 338–51.
15. Errick, J. E. and Saunders, J. W. (1976). Limb outgrowth in the chick embryo induced by dissociation and reaggregated cells of the apical ectodermal ridge. Developmental Biology, 50, 26–34.
16. Fallon, J. F., Lopez, A., Ros, M. A., et al. (1994). Fgf-2: apical ectodermal ridge growth signal for chick limb development. Science, 264, 104–7.
17. Fernandez-Teran, M. and Ros, M. A. (2008). The apical ectodermal ridge: morphological aspects and signaling pathways. International Journal of Developmental Biology, 52, 857–71.
18. Galis, F. and Metz, J. A. J. (2001). Testing the vulnerability of the phylotypic stage: on modularity and evolutionary conservation. Journal of Experimental Zoology–Molecular and Developmental Evolution, 291, 195–204.
19. Galis, F., van Alphen, J. J. M. and Metz, J. A. J. (2001). Why five fingers? Evolutionary constraints on digit numbers. Trends in Ecology and Evolution, 16(11), 637–46.
20. Galis, F., van Alphen, J. J. M and Metz, J. A. J. (2002). Digit reduction: via repatterning or developmental arrest. Evolution and Development, 4(4), 249–51.
21. Gemmell, R. T., Veitch, C. and Nelson, J. (1999). Birth in the northern brown bandicoot, Isoodon macrourus (Marsupialia: Peramelidae). Australian Journal of Zoology, 47, 517–28.
22. Gemmell, R. T., Veitch, C. and Nelson, J. (2002). Birth in marsupials. Comparative Biochemistry and Physiology Part B, 131, 621–30.
23. Goswami, A. and Polly, P. D. (2010). The influence of modularity on cranial morphological disparity in Carnivora and Primates (Mammalia). PLOS One, 5(3), e9517.
24. Goswami, A., Weisbecker, V. and Sánchez-Villagra, M. R. (2009). Developmental modularity and the marsupial-placental dichotomy. Journal of Experimental Zoology B, 312B, 186–95.
25. Hallgrímmson, B., Willmore, K. E. and Hall, B. K. (2002). Canalization, developmental stability, and morphological integration in primate limbs. Yearbook of Physical Anthropology, 45, 131–58.
26. Hamrick, M. W. (2002). Developmental mechanisms of digit reduction. Evolution and Development, 4(4), 247–8.
27. Harrison, L. B. and Larsson, H. C. E. (2008). Estimating evolution of temporal sequence changes: a practical approach inferring ancestral developmental sequences and sequences heterochrony. Systematic Biology, 57(3), 378–87.
28. Hockman, D., Cretekos, C. J., Mason, M. K., et al. (2008). A second wave of sonic hedgehog expression during the development of the bat limb. Proceedings of the National Academy of Sciences of the United States of America, 105(44), 16 982–7.
29. Hübler, M., Niswander, L., Peters, J. and Sears, K. E. (2010). The developmental reduction of the marsupial coracoid: a case study in Monodelphis domestica. Journal of Morphology, 271(7), 769–76.
30. Hughes, R. L. and Hall, L. S. (1988). Structural adaptations of the newborn marsupial. In The Developing Marsupial: Models for Biomedical Research, ed. C. H. Tyndale-Biscoe and P. A. Janssens. Berlin: Springer, pp. 8–27.
31. Hutson, G. D. (1976). Grooming behaviour and birth in the dasyurid marsupial Dasyuroides byrnei. Australian Journal of Zoology, 24, 277–82.
32. Kalinka, A. T., Varga, K. M., Gerrard, D. T., et al. (2010). Gene expression divergence recapitulates the developmental hourglass model. Nature, 468(7325), 811–14.
33. Kelly, E. M. and Sears, K. E. (2011a). Limb specialization in living marsupial and eutherian mammals: an investigation of constraints on mammalian limb evolution. Journal of Mammalogy, 92(5), 1038–49.
34. Kelly, M. and Sears, K. E. (2011b). Limb integration in New World marsupials. Biological Journal of the Linnean Society, 102, 22–36.
35. Keyte, A. L. and Smith, K. K. (2010). Developmental origins of precocial forelimbs in marsupial neonates. Development, 137, 4283–94.
36. Kirsch, J. A. W. (1977). The six-percent solution: second thoughts on the adaptedness of the marsupialia. American Scientist, 65, 276–88.
37. Klima, M. (1987). Early development of the shoulder girdle and sternum in marsupials (Mammalia: Metatheria). Advances in Anatomy Embryology and Cell Biology, 47(2), 1–80.
38. Lai, D. M., Tu, Y. K., Hsieh, Y. H., et al. (2007). Angiopoietin-like protein I expression is related to intermuscular connective tissue and cartilage development. Developmental Dynamics, 236, 2643–52.
39. Lanctot, C., Moreau, A., Chamberland, M., et al. (1999). Hindlimb patterning and mandible development require the PtxI gene. Development, 126, 1805–10.
40. Lee, K. K. H., Tang, M. K., Yew, D. T. W., et al. (1999). gas2 is a multifunctional gene involved in the regulation of apoptosis and chondrogenesis in the developing mouse limb. Developmental Biology, 207, 14–25.
41. Lillegraven, J. A. (1975). Biological considerations of the marsupial-placental dichotomy. Evolution, 29, 707–22.
42. Lu, Y., Huggins, P. and Bar-Joseph, Z. (2009). Cross species analysis of microarray expression data. Bioinformatics, 25(12), 1476–83.
43. Lyne, A. G. (1974). Gestation period and birth in the marsupial Isoodon macrourus. Australian Journal of Zoology, 22, 303–9.
44. Lyne, A. G. and Hollis, D. E. (1977). The early development of marsupials, with special references to bandicoots. In Reproduction and Evolution, ed. J. H. Calaby and C. H. Tyndale-Biscoe. Canberra, Australia: Australian Academy of Science, pp. 293–302.
45. Lyne, A. G., Pilton, P. E. and Sharman, G. B. (1959). Oestrous cycle, gestation period and parturition in the marsupial Trichosurusvulpecula. Nature, 183(4661), 622–3.
46. Mardis, E. R. (2008). Next-generation DNA sequencing methods. Annual Review of Genomics and Human Genetics, 9, 328–402.
47. Margulies, E. H., Kardia, S. L. R. and Innia, J. W. (2001). A comparative molecular analysis of developing mouse forelimbs and hindlimbs using serial analysis of gene expression (SAGE). Genome Research, II, 1686–98.
48. Mate, K. E., Robinson, E. S., VandeBerg, J. L. and Pederson, R. A. (1994). Timetable of in vivo embryonic development in the gray short-tailed opossum (Monodelphis domestica). Molecular Reproduction and Development, 39, 365–74.
49. Maynard Smith, J., Burian, R., Kauffman, S., et al. (1985). Developmental constraints and evolution: a perspective from the Mountain Lake Conference on Development and Evolution. Quarterly Review of Biology, 60(3), 265–87.
50. McCrady, E. (1938). The Embryology of the Opossum. Philadelphia, PA: Wistar Institute of Anatomy and Biology, 233 pp.
51. Motomura, H., Niimi, H., Sugimori, K., Ohtsuka, T., Kimura, T. and Kitajima, I. (2007). Gas6, a new regulator of chondrogenic differentiation from mesenchymal cells. Biochemical and Biophysical Research Communications, 15(4), 997–1003.
52. Nelson, J. E. and Gemmell, R T. (2003). Birth in the northern quoll, Dasyurus hallucatus (Marsupialia: Dasyuridae). Australian Journal of Zoology, 51(2), 187–98.
53. Niswander, L. (2003). Pattern formation: old models out on a limb. Nature Reviews Genetics, 4(2), 133–43.
54. Niswander, L., Tickle, C., Vogel, A., Booth, I. and Martin, G. R. (1993). FGF4 replaces the apical ectodermal ridgge and directs outgrowth and patterning of the limb. Cell, 75, 579–87.
55. Parker, P. (1977). The evolutionary comparison of placental and marsupial patterns of reproduction. In The Biology of Marsupials, ed. B. Stonehouse and D. Gilmore. London: Macmillan Press, pp. 273–86.
56. Poole, W. E. (1975). Reproduction in two species of grey kangaroos, Macropus giganteus Shaw and Macropus fuliginosus (Desmarest). 2. Gestation, parturition and pouch life. Australian Journal of Zoology, 23(3), 333–53.
57. Renfree, M., Fletcher, T. P. and Lewis, D. R. (1989). Physiological and behavioral events around the time of birth in macropodid marsupials. In Kangaroos, Wallabies and Rat-Kangaroos, ed. P. Jarman, I. Hume and G. Grigg. Sydney, Australia: Surrey Beatty, pp. 323–7.
58. Reynolds, H. C. (1952). Studies on reproduction in the opossum (Didelphis virginiana). University of California Publications in Zoological Sciences, 52, 223–84.
59. Rodriguez-Esteban, C., Tsukui, T., Yonei, S., et al. (1999). The T-box genes Tbx4 and Tbx5 regulate limb outgrowth and identity. Nature, 398, 814–18.
60. Sánchez-Villagra, M. R. (2002). Comparative patterns of postcranial ontogeny in therian mammals: an analysis of relative timing of ossification events. Journal of Experimental Zoology, 294, 264–73.
61. Sánchez-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 therian scapula. Journal of Morphology, 258, 115–29.
62. Saunders, J. W. J. (1948). The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm. Journal of Experimental Zoology, 108, 363–403.
63. Schluter, D. (1996). Adaptive radiation along genetic lines of least resistance. Evolution, 50(5), 1766–74.
64. Schmidt, M. and Fischer, M. S. (2009). Morphological integration in mammalian limb proportions: dissociation between function and development. Evolution, 63, 749–66.
65. Sears, K. E. (2004). Constraints on the morphological evolution of marsupial shoulder girdles. Evolution, 58(10), 2353–70.
66. Sears, K. E. (2009). Differences in the timing of prechondrogenic limb development in mammals: the marsupial-placental dichotomy resolved. Evolution, 63(8), 2193–200.
67. Sears, K. E. (2011). Novel insights into the regulation of limb development from ‘natural’ mammalian mutants. BioEssays, 33(5), 327–31.
68. Sears, K. E., Behringer, R. R., Rasweiler, J. J. and Niswander, L. A. (2006). Development of bat flight: morphologic and molecular evolution of bat wing digits. Proceedings of the National Academy of Sciences of the United States of America, 103(17), 6581–6.
69. Sharman, G. B. (1973). Adaptations of marsupial pouch young for extra-uterine existence. In The Mammalian Fetus in Vitro, ed. C. R. Austin. London: Chapman and Hall, pp. 67–90.
70. Sharman, G. B., Calaby, J. H. and Poole, W. E. (1965). Patterns of reproduction in female diprotodont marsupials. Journal of Reproduction and Fertility, 9(3), 375–6.
71. Shaw, G. and Renfree, M. B. (2006). Parturition and perfect prematurity: birth in marsupials. Australian Journal of Zoology, 54, 139–49.
72. Shendure, J. (2008). The beginning of the end for microarrays? Nature Methods, 5(7), 585–87.
73. Shou, S., Scott, V., Reed, C., Hitzemann, R. and Stadler, H. S. (2005). Transcriptome analysis of the murine forelimb and hindlimb autopod. Developmental Dynamics, 234, 74–89.
74. Stopper, G. F. and Wagner, G. P. (2005). Of chicken wings and frog legs: a smorgasbord of evolutionary variation in mechanisms of tetrapod limb development. Developmental Biology, 288, 21–39.
75. Summerbell, D. A. (1974). A quantitative analysis of the effect of excision of the AER from the chick limb-bud. Journal of Embryology and Experimental Morphology, 32, 651–60.
76. Sun, X., Mariani, F. V. and Martin, G. R. (2002). Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature, 418, 501–8.
77. Takeuchi, J., Koshiba-Takeuchi, K., Suzuki, T., et al. (2003). Tbx5 and Tbx4 trigger limb initiation through activation of the Wnt/Fgf signaling cascade. Development, 130(12), 2729–39.
78. Thewissen, J. G. M., Cohn, M. J., Stevens, M. E., et al. (2006). Developmental basis for hind-limb loss in dolphins and origin of the cetacean bodyplan. Proceedings of the National Academy of Sciences of the United States of America, 103(22), 8414–18.
79. Towers, M. and Tickle, C. (2009a). Generation of pattern and form in the developing limb. International Journal of Developmental Biology, 53, 805–12.
80. Towers, M. and Tickle, C. (2009b). Growing models of vertebrate limb development. Development, 136, 179–90.
81. Tyndale-Biscoe, C. H. (1973). Life of Marsupials. London: Edward Arnold, 254 pp.
82. Tyndale-Biscoe, C. H. and Renfree, M. (1987). Reproductive Physiology of Marsupials. Cambridge, UK: Cambridge University Press.
83. Veitch, C., Nelson, C. E. and Gemmell, R. T. (2000). Birth in the brushtail possum, Trichosurus vulpecula (Marsupialia: Phalangeridae). Australian Journal of Zoology, 48, 691–700.
84. Wagner, G. P. (1996). Homologues, natural kinds and the evolution of modularity. American Zoologist, 36(1), 36–43.
85. Wanek, N., Muneoka, K., Holler-Dinsmore, G., Burton, R. and Bryant, S. V. (1989). A staging system for mouse limb development. Journal of Experimental Zoology, 249, 41–9.
86. Weisbecker, V., Goswami, A., Wroe, S. and Sánchez-Villagra, M. R. (2008). Ossification heterochrony in the therian postcranial skeleton and the marsupial-placental dichotomy. Evolution, 62(8), 2027–41.
87. Wilmore, K. E., Leamy, L. J. and Hallgrímsson, B. (2006). Effects of develpmental and functional interactions on mouse cranial variability through late ontogeny. Evolution and Development, 8(6), 550–67.
88. Yampolsky, L. Y. and Stoltzfus, A. (2001). Bias in the introduction of variation as an orienting factor in evolution. Evolution and Development, 3(2), 73–83.
89. Young, N. M. and Hallgrímsson, B. (2005).Serial homology and the evolution of mammalian limb covariance structure. Evolution, 59(12), 2691–704.
90. Zeller, R., Lopez-Rios, J. and Zuniga, A. (2009). Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nature Reviews Genetics, 10, 845–58.