Molecular determinants of marsupial limb integration and constraint

What are the intrinsic factors responsible for shaping mammalian biodiversity? This question is highly relevant to discussion of the two groups of therian mammals alive today, marsupials (kangaroos, possums, etc.) and placentals (humans, bats, whales, etc.). Despite arising at the same time, marsupials have never achieved the taxonomic or morphologic diversity of their sister group, the placentals (Lillegraven 1975; Kirsch 1977; Sears 2004; Cooper and Steppan 2010). To explain this phenomenon, scientists hypothesized that the evolution of marsupials had been constrained relative to that of placentals as a result of marsupials’ unique mode of reproduction (Lillegraven 1975; Klima 1987; Sanchez-Villagra and Maier 2003).

Subsequent research confirmed that marsupials are less morphologically diverse and specialized than placentals (Sears 2004; Cooper and Steppan 2010; Kelly and Sears 2011a). Sears (2004) found that the shoulder girdles of living and extinct adult marsupials are less diverse than those of adult placentals, and adult marsupial scapulae are less morphologically diverse than adult marsupial pelves, as predicted by the marsupial constraint. Cooper and Steppan (2010) and Kelly and Sears (2011a) found that this pattern extended to forelimb versus hind limb comparisons in living mammals. Sears (2004) also linked this reduction in morphological diversity to a reduction in morphologic variation during development as a result of the functional requirements on the marsupial newborn.

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Type: Chapter
Information: From Clone to Bone
The Synergy of Morphological and Molecular Tools in Palaeobiology
, pp. 257 - 278
DOI: https://doi.org/10.1017/CBO9780511760174.010 [Opens in a new window]
Publisher: Cambridge University Press
Print publication year: 2012

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References

Alberch, P. 1982 Developmental constraints in evolutionary processesEvolution and DevelopmentBonner, J. T.New YorkSpringer-Verlag313CrossRef Google Scholar

Bénazet, J. D.Bischofberger, M.Tiecke, E. 2009 A self-regulatory system of interlinked signaling feedback loops controls mouse limb patterningScience 323 1050CrossRef Google Scholar PubMed

Bennett, V.Goswami, A. 2011 Does developmental strategy drive limb integration in marsupials and monotremes?Mammalian Biology 76 79CrossRef Google Scholar

Bininda-Emonds, O. R. P.Jeffery, J. E.Richardson, M. K. 2003 Inverting the hourglass: quantitative evidence against the phylotypic stage in vertebrate developmentProceedings of the Royal Society B–Biological Sciences 270 341Google Scholar PubMed

Bininda-Emonds, O. R. P.Jeffrey, J. E.Richardson, M. K. 2003 Is sequence heterochrony an important evolutionary mechanism in mammalsJournal of Mammalian Evolution 10 335CrossRef Google Scholar

Bininda-Emonds, O. R. P.Jeffery, J. E.Sánchez-Villagra, M. R. 2007 Forelimb-hindlimb developmental timing changes across tetrapod phylogenyBMC Evolutionary Biology 7 182CrossRef Google Scholar PubMed

Capdevila, J.Belmonte, J. 2001 Patterning mechanisms controlling vertebrate limb developmentAnnual Review of Cellular and Developmental Biology 17 87CrossRef Google Scholar PubMed

Chen, C. H.Cretekos, C. J.Rasweiler, J. J.Behringer, R. R. 2005 Hoxd13 expression in the developing limbs of the short-tailed fruit bat, Evolution and Development 7 130CrossRef Google Scholar

Cheng, C. 1955 The development of the shoulder region of the opossum, , with special reference to the musculatureJournal of Morphology 97 415CrossRef Google Scholar

Cohn, M. J.Tickle, C. 1999 Developmental basis of limblessness and axial patterning in snakesNature 399 474CrossRef Google Scholar PubMed

Cooper, J.Steppan, S. J. 2010 Developmental constraint on the evolution of marsupial forelimb morphologyAustralian Journal of Zoology 58 1CrossRef Google Scholar

Cooper, L. N.Armfield, B. A.Thewissen, J. G. M. 2011

Doroba, C. K.Sears, K. E. 2010 The divergent developmental of the apical ectodermal ridge in the marsupial Anatomical Record 293 1325CrossRef Google Scholar

Errick, J. E.Saunders, J. W. 1974 Effects of an ‘inside-out’ limb-bud ectoderm on development of the avian limbDevelopmental Biology 41 338CrossRef Google Scholar PubMed

Errick, J. E.Saunders, J. W. 1976 Limb outgrowth in the chick embryo induced by dissociation and reaggregated cells of the apical ectodermal ridgeDevelopmental Biology 50 26CrossRef Google Scholar

Fallon, J. F.Lopez, A.Ros, M. A. 1994 Fgf-2: apical ectodermal ridge growth signal for chick limb developmentScience 264 104CrossRef Google Scholar PubMed

Fernandez-Teran, M.Ros, M. A. 2008 The apical ectodermal ridge: morphological aspects and signaling pathwaysInternational Journal of Developmental Biology 52 857CrossRef Google Scholar PubMed

Galis, F.Metz, J. A. J. 2001 Testing the vulnerability of the phylotypic stage: on modularity and evolutionary conservationJournal of Experimental Zoology–Molecular and Developmental Evolution 291 195CrossRef Google Scholar PubMed

Galis, F.van Alphen, J. J. M.Metz, J. A. J. 2001 Why five fingers? Evolutionary constraints on digit numbersTrends in Ecology and Evolution 16 637CrossRef Google Scholar

Galis, F.van Alphen, J. J. MMetz, J. A. J. 2002 Digit reduction: via repatterning or developmental arrestEvolution and Development 4 249CrossRef Google Scholar PubMed

Gemmell, R. T.Veitch, C.Nelson, J. 1999 Birth in the northern brown bandicoot, (Marsupialia: Peramelidae)Australian Journal of Zoology 47 517CrossRef Google Scholar

Gemmell, R. T.Veitch, C.Nelson, J. 2002 Birth in marsupialsComparative Biochemistry and Physiology Part B 131 621CrossRef Google Scholar PubMed

Goswami, A.Polly, P. D. 2010 The influence of modularity on cranial morphological disparity in Carnivora and Primates (Mammalia)PLOS One 5CrossRef Google Scholar

Goswami, A.Weisbecker, V.Sánchez-Villagra, M. R. 2009 Developmental modularity and the marsupial-placental dichotomyJournal of Experimental Zoology B 312B 186CrossRef Google Scholar PubMed

Hallgrímmson, B.Willmore, K. E.Hall, B. K. 2002 Canalization, developmental stability, and morphological integration in primate limbsYearbook of Physical Anthropology 45 131CrossRef Google Scholar

Hamrick, M. W. 2002 Developmental mechanisms of digit reductionEvolution and Development 4 247CrossRef Google Scholar PubMed

Harrison, L. B.Larsson, H. C. E. 2008 Estimating evolution of temporal sequence changes: a practical approach inferring ancestral developmental sequences and sequences heterochronySystematic Biology 57 378CrossRef Google Scholar PubMed

Hockman, D.Cretekos, C. J.Mason, M. K. 2008 A second wave of sonic hedgehog expression during the development of the bat limbProceedings of the National Academy of Sciences of the United States of America 105 16 982CrossRef Google Scholar PubMed

Hübler, M.Niswander, L.Peters, J.Sears, K. E. 2010 The developmental reduction of the marsupial coracoid: a case study in Journal of Morphology 271 769Google Scholar PubMed

Hughes, R. L.Hall, L. S. 1988 Structural adaptations of the newborn marsupialThe Developing Marsupial: Models for Biomedical ResearchTyndale-Biscoe, C. H.Janssens, P. A.BerlinSpringer8CrossRef Google Scholar

Hutson, G. D. 1976 Grooming behaviour and birth in the dasyurid marsupial Australian Journal of Zoology 24 277CrossRef Google Scholar

Kalinka, A. T.Varga, K. M.Gerrard, D. T. 2010 Gene expression divergence recapitulates the developmental hourglass modelNature 468 811CrossRef Google Scholar PubMed

Kelly, E. M.Sears, K. E. 2011 Limb specialization in living marsupial and eutherian mammals: an investigation of constraints on mammalian limb evolutionJournal of Mammalogy 92 1038CrossRef Google Scholar

Kelly, M.Sears, K. E. 2011 Limb integration in New World marsupialsBiological Journal of the Linnean Society 102 22CrossRef Google Scholar

Keyte, A. L.Smith, K. K. 2010 Developmental origins of precocial forelimbs in marsupial neonatesDevelopment 137 4283CrossRef Google Scholar PubMed

Kirsch, J. A. W. 1977 The six-percent solution: second thoughts on the adaptedness of the marsupialiaAmerican Scientist 65 276Google Scholar PubMed

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

Lai, D. M.Tu, Y. K.Hsieh, Y. H. 2007 Angiopoietin-like protein 1 expression is related to intermuscular connective tissue and cartilage developmentDevelopmental Dynamics 236 2643CrossRef Google Scholar PubMed

Lanctot, C.Moreau, A.Chamberland, M. 1999 Hindlimb patterning and mandible development require the geneDevelopment 126 1805Google Scholar PubMed

Lee, K. K. H.Tang, M. K.Yew, D. T. W. 1999 gas2 is a multifunctional gene involved in the regulation of apoptosis and chondrogenesis in the developing mouse limbDevelopmental Biology 207 14CrossRef Google Scholar PubMed

Lillegraven, J. A. 1975 Biological considerations of the marsupial-placental dichotomyEvolution 29 707CrossRef Google Scholar PubMed

Lu, Y.Huggins, P.Bar-Joseph, Z. 2009 Cross species analysis of microarray expression dataBioinformatics 25 1476CrossRef Google Scholar PubMed

Lyne, A. G. 1974 Gestation period and birth in the marsupial Australian Journal of Zoology 22 303CrossRef Google Scholar

Lyne, A. G.Hollis, D. E. 1977 The early development of marsupials, with special references to bandicootsReproduction and EvolutionCalaby, J. H.Tyndale-Biscoe, C. H.Canberra, AustraliaAustralian Academy of Science293Google Scholar

Lyne, A. G.Pilton, P. E.Sharman, G. B. 1959 Oestrous cycle, gestation period and parturition in the marsupial Nature 183 622CrossRef Google Scholar

Mardis, E. R. 2008 Next-generation DNA sequencing methodsAnnual Review of Genomics and Human Genetics 9 328CrossRef Google Scholar PubMed

Margulies, E. H.Kardia, S. L. R.Innia, J. W. 2001 A comparative molecular analysis of developing mouse forelimbs and hindlimbs using serial analysis of gene expression (SAGE)Genome Research 11 1686CrossRef Google Scholar

Mate, K. E.Robinson, E. S.VandeBerg, J. L.Pederson, R. A. 1994 Timetable of in vivo embryonic development in the gray short-tailed opossum ()Molecular Reproduction and Development 39 365CrossRef Google Scholar

Maynard Smith, J.Burian, R.Kauffman, S. 1985 Developmental constraints and evolution: a perspective from the Mountain Lake Conference on Development and EvolutionQuarterly Review of Biology 60 265CrossRef Google Scholar

McCrady, E. 1938 The Embryology of the OpossumPhiladelphia, PAWistar Institute of Anatomy and BiologyGoogle Scholar

Motomura, H.Niimi, H.Sugimori, K.Ohtsuka, T.Kimura, T.Kitajima, I. 2007 Gas6, a new regulator of chondrogenic differentiation from mesenchymal cellsBiochemical and Biophysical Research Communications 15 997CrossRef Google Scholar

Nelson, J. E.Gemmell, R T. 2003 Birth in the northern quoll, (Marsupialia: Dasyuridae)Australian Journal of Zoology 51 187CrossRef Google Scholar

Niswander, L. 2003 Pattern formation: old models out on a limbNature Reviews Genetics 4 133CrossRef Google Scholar PubMed

Niswander, L.Tickle, C.Vogel, A.Booth, I.Martin, G. R. 1993 FGF4 replaces the apical ectodermal ridgge and directs outgrowth and patterning of the limbCell 75 579CrossRef Google Scholar

Parker, P. 1977 The evolutionary comparison of placental and marsupial patterns of reproductionThe Biology of MarsupialsStonehouse, B.Gilmore, D.LondonMacmillan Press273CrossRef Google Scholar

Poole, W. E. 1975 Reproduction in two species of grey kangaroos, Shaw and (Desmarest). 2. Gestation, parturition and pouch lifeAustralian Journal of Zoology 23 333CrossRef Google Scholar

Renfree, M.Fletcher, T. P.Lewis, D. R. 1989 Physiological and behavioral events around the time of birth in macropodid marsupialsKangaroos, Wallabies and Rat-KangaroosJarman, P.Hume, I.Grigg, G.Sydney, AustraliaSurrey Beatty323Google Scholar

Reynolds, H. C. 1952 Studies on reproduction in the opossum ()University of California Publications in Zoological Sciences 52 223Google Scholar

Rodriguez-Esteban, C.Tsukui, T.Yonei, S. 1999 The T-box genes Tbx4 and Tbx5 regulate limb outgrowth and identityNature 398 814CrossRef Google Scholar PubMed

Sánchez-Villagra, M. R. 2002 Comparative patterns of postcranial ontogeny in therian mammals: an analysis of relative timing of ossification eventsJournal of Experimental Zoology 294 264CrossRef Google Scholar PubMed

Sánchez-Villagra, M. R.Maier, W. 2003 Ontogenesis of the scapula in marsupial mammals, with special emphasis on perinatal stages of and remarks on the origin of the therian scapulaJournal of Morphology 258 115CrossRef Google Scholar PubMed

Saunders, J. W. J. 1948 The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectodermJournal of Experimental Zoology 108 363CrossRef Google Scholar PubMed

Schluter, D. 1996 Adaptive radiation along genetic lines of least resistanceEvolution 50 1766CrossRef Google Scholar PubMed

Schmidt, M.Fischer, M. S. 2009 Morphological integration in mammalian limb proportions: dissociation between function and developmentEvolution 63 749CrossRef Google Scholar PubMed

Sears, K. E. 2004 Constraints on the morphological evolution of marsupial shoulder girdlesEvolution 58 2353Google Scholar PubMed

Sears, K. E. 2009 Differences in the timing of prechondrogenic limb development in mammals: the marsupial-placental dichotomy resolvedEvolution 63 2193CrossRef Google Scholar PubMed

Sears, K. E. 2011 Novel insights into the regulation of limb development from ‘natural’ mammalian mutantsBioEssays 33 327CrossRef Google Scholar PubMed

Sears, K. E.Behringer, R. R.Rasweiler, J. J.Niswander, L. A. 2006 Development of bat flight: morphologic and molecular evolution of bat wing digitsProceedings of the National Academy of Sciences of the United States of America 103 6581CrossRef Google Scholar PubMed

Sharman, G. B. 1973 Adaptations of marsupial pouch young for extra-uterine existenceThe Mammalian Fetus in VitroAustin, C. R.LondonChapman and Hall67CrossRef Google Scholar

Sharman, G. B.Calaby, J. H.Poole, W. E. 1965 Patterns of reproduction in female diprotodont marsupialsJournal of Reproduction and Fertility 9 375Google Scholar

Shaw, G.Renfree, M. B. 2006 Parturition and perfect prematurity: birth in marsupialsAustralian Journal of Zoology 54 139CrossRef Google Scholar

Shendure, J. 2008 The beginning of the end for microarrays?Nature Methods 5 585CrossRef Google Scholar PubMed

Shou, S.Scott, V.Reed, C.Hitzemann, R.Stadler, H. S. 2005 Transcriptome analysis of the murine forelimb and hindlimb autopodDevelopmental Dynamics 234 74CrossRef Google Scholar PubMed

Stopper, G. F.Wagner, G. P. 2005 Of chicken wings and frog legs: a smorgasbord of evolutionary variation in mechanisms of tetrapod limb developmentDevelopmental Biology 288 21CrossRef Google Scholar PubMed

Summerbell, D. A. 1974 A quantitative analysis of the effect of excision of the AER from the chick limb-budJournal of Embryology and Experimental Morphology 32 651Google Scholar PubMed

Sun, X.Mariani, F. V.Martin, G. R. 2002 Functions of FGF signalling from the apical ectodermal ridge in limb developmentNature 418 501CrossRef Google Scholar PubMed

Takeuchi, J.Koshiba-Takeuchi, K.Suzuki, T. 2003 Tbx5 and Tbx4 trigger limb initiation through activation of the Wnt/Fgf signaling cascadeDevelopment 130 2729CrossRef Google Scholar

Thewissen, J. G. M.Cohn, M. J.Stevens, M. E. 2006 Developmental basis for hind-limb loss in dolphins and origin of the cetacean bodyplanProceedings of the National Academy of Sciences of the United States of America 103 8414CrossRef Google Scholar PubMed

Towers, M.Tickle, C. 2009 Generation of pattern and form in the developing limbInternational Journal of Developmental Biology 53 805CrossRef Google Scholar PubMed

Towers, M.Tickle, C. 2009 Growing models of vertebrate limb developmentDevelopment 136 179CrossRef Google Scholar PubMed

Tyndale-Biscoe, C. H. 1973 Life of MarsupialsLondonEdward ArnoldGoogle Scholar

Tyndale-Biscoe, C. H.Renfree, M. 1987 Reproductive Physiology of MarsupialsCambridge, UKCambridge University PressCrossRef Google Scholar

Veitch, C.Nelson, C. E.Gemmell, R. T. 2000 Birth in the brushtail possum, (Marsupialia: Phalangeridae)Australian Journal of Zoology 48 691CrossRef Google Scholar

Wagner, G. P. 1996 Homologues, natural kinds and the evolution of modularityAmerican Zoologist 36 36CrossRef Google Scholar

Wanek, N.Muneoka, K.Holler-Dinsmore, G.Burton, R.Bryant, S. V. 1989 A staging system for mouse limb developmentJournal of Experimental Zoology 249 41CrossRef Google Scholar PubMed

Weisbecker, V.Goswami, A.Wroe, S.Sánchez-Villagra, M. R. 2008 Ossification heterochrony in the therian postcranial skeleton and the marsupial-placental dichotomyEvolution 62 2027CrossRef Google Scholar PubMed

Wilmore, K. E.Leamy, L. J.Hallgrímsson, B. 2006 Effects of develpmental and functional interactions on mouse cranial variability through late ontogenyEvolution and Development 8 550CrossRef Google Scholar

Yampolsky, L. Y.Stoltzfus, A. 2001 Bias in the introduction of variation as an orienting factor in evolutionEvolution and Development 3 73CrossRef Google Scholar

Young, N. M.Hallgrímsson, B. 2005 Serial homology and the evolution of mammalian limb covariance structureEvolution 59 2691CrossRef Google Scholar

Zeller, R.Lopez-Rios, J.Zuniga, A. 2009 Vertebrate limb bud development: moving towards integrative analysis of organogenesisNature Reviews Genetics 10 845CrossRef Google Scholar PubMed

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