Repeated modification of early limb morphogenesis programmes underlies the convergence of relative limb length in Anolis lizards

T.J. Sanger; L.J. Revell; J.J. Gibson-Brown; J.B. Losos

doi:10.1098/rspb.2011.0840

Repeated modification of early limb morphogenesis programmes underlies the convergence of relative limb length in Anolis lizards

T.J. Sanger, L.J. Revell, J.J. Gibson-Brown, J.B. Losos

Research output: Contribution to journal › Article › peer-review

52 Scopus citations

Abstract

The independent evolution of similar morphologies has long been a subject of considerable interest to biologists. Does phenotypic convergence reflect the primacy of natural selection, or does development set the course of evolution by channelling variation in certain directions? Here, we examine the ontogenetic origins of relative limb length variation among Anolis lizard habitat specialists to address whether convergent phenotypes have arisen through convergent developmental trajectories. Despite the numerous developmental processes that could potentially contribute to variation in adult limb length, our analyses reveal that, in Anolis lizards, such variation is repeatedly the result of changes occurring very early in development, prior to formation of the cartilaginous long bone anlagen. © 2011 The Royal Society.

Original language	English (US)
Pages (from-to)	739-748
Number of pages	10
Journal	Proceedings of the Royal Society B: Biological Sciences
Volume	279
Issue number	1729
DOIs	https://doi.org/10.1098/rspb.2011.0840
State	Published - 2012

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10.1098/rspb.2011.0840

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@article{c99f7ee8f7f04b29bbe09e39b18a6555,

title = "Repeated modification of early limb morphogenesis programmes underlies the convergence of relative limb length in Anolis lizards",

abstract = "The independent evolution of similar morphologies has long been a subject of considerable interest to biologists. Does phenotypic convergence reflect the primacy of natural selection, or does development set the course of evolution by channelling variation in certain directions? Here, we examine the ontogenetic origins of relative limb length variation among Anolis lizard habitat specialists to address whether convergent phenotypes have arisen through convergent developmental trajectories. Despite the numerous developmental processes that could potentially contribute to variation in adult limb length, our analyses reveal that, in Anolis lizards, such variation is repeatedly the result of changes occurring very early in development, prior to formation of the cartilaginous long bone anlagen. {\textcopyright} 2011 The Royal Society.",

author = "T.J. Sanger and L.J. Revell and J.J. Gibson-Brown and J.B. Losos",

note = "Cited By :27 Export Date: 17 April 2018 CODEN: PRLBA Correspondence Address: Sanger, T. J.; Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, United States; email: tsanger@oeb.harvard.edu References: Bateson, W., (1909) Mendel's Principles of Heredity, , Cambridge, UK: Cambridge University Press; Goldschmidt, R., (1940) The Material Basis of Evolution, , New Haven, CT: Yale University Press; Huxley, J., (1942) Evolution: The Modern Synthesis, , Cambridge, MA: MIT Press; Arthur, W., (2004) Biased Embryos and Evolution, , Cambridge, UK: Cambridge University Press; Amundson, R., (2005) The Changing Role of the Embryo In Evolutionary Thought, , Cambridge, UK: Cambridge University Press; Simpson, G.G., (1944) Tempo and Mode In Evolution, , New York, NY: Columbia University Press; Maynard-Smith, J.R., Burian, R., Kaufffman, S., Alberch, P., Campbell, J., Goodwin, B., Lande, R., Wolpert, L., Developmental constraints and evolution (1985) Q. Rev. Biol, 60, pp. 265-287. , (doi:10.1086/414425); Losos, J.B., Convergence, adaptation, and constraint (2011) Evolution, 65, pp. 1827-1840. , (doi:10.1111/j.1558-5646.2011.01289.x); Wake, D.B., Wake, M.H., Specht, C.D., Homoplasy: From detecting pattern to determining process and mechanism of evolution (2011) Science, 331, pp. 1032-1035. , (doi:10.1126/science.1188545); Wake, D.B., Homoplasy: The result of natural selection, or evidence of design limitations (1991) Am. Nat, 138, pp. 543-567. , (doi:10.1086/285234); Gould, S.J., (2002) The Structure of Evolutionary Theory, , Cambridge, MA: Harvard University Press; Schluter, D., Clifford, E.A., Nemethy, M., McKinnon, J.S., Parallel evolution and inheritance of quantitative traits (2004) Am. Nat, 163, pp. 809-822. , (doi:10.1086/383621); Whittall, J.B., Voelckel, C., Hodges, S.A., Convergence, constraint and the role of gene expression during adaptive radiation: Floral anthocyanins in Aquilegia (2006) Mol. Ecol, 15, pp. 4645-4657. , doi:10.1111/j.1365-294X.2006.03114.x); Atallah, J., Liu, N.H., Dennis, P., Hon, A., Larsen, E.W., Developmental constraints and convergent evolution in Drosophila sex comb formation (2009) Evol. Dev, 11, pp. 205-218. , (doi:10.1111/j.1525-142X.2009.00320.x); des Marais, D.L., Rausher, M.D., Parallel evolution at multiple levels in the origin of hummingbird pollinated flowers in Ipomoea (2010) Evolution, 64, pp. 2044-2054; Hamburger, V., Embryology and the modern synthesis in evolutionary theory (1980) The Evolutionary Synthesis, pp. 97-112. , (eds E. Mayr & W. B. 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year = "2012",

doi = "10.1098/rspb.2011.0840",

language = "English (US)",

volume = "279",

pages = "739--748",

journal = "Proceedings of the Royal Society B: Biological Sciences",

issn = "0962-8452",

publisher = "Royal Society of London",

number = "1729",

}

TY - JOUR

T1 - Repeated modification of early limb morphogenesis programmes underlies the convergence of relative limb length in Anolis lizards

AU - Sanger, T.J.

AU - Revell, L.J.

AU - Gibson-Brown, J.J.

AU - Losos, J.B.

N1 - Cited By :27 Export Date: 17 April 2018 CODEN: PRLBA Correspondence Address: Sanger, T. J.; Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, United States; email: tsanger@oeb.harvard.edu References: Bateson, W., (1909) Mendel's Principles of Heredity, , Cambridge, UK: Cambridge University Press; Goldschmidt, R., (1940) The Material Basis of Evolution, , New Haven, CT: Yale University Press; Huxley, J., (1942) Evolution: The Modern Synthesis, , Cambridge, MA: MIT Press; Arthur, W., (2004) Biased Embryos and Evolution, , Cambridge, UK: Cambridge University Press; Amundson, R., (2005) The Changing Role of the Embryo In Evolutionary Thought, , Cambridge, UK: Cambridge University Press; Simpson, G.G., (1944) Tempo and Mode In Evolution, , New York, NY: Columbia University Press; Maynard-Smith, J.R., Burian, R., Kaufffman, S., Alberch, P., Campbell, J., Goodwin, B., Lande, R., Wolpert, L., Developmental constraints and evolution (1985) Q. Rev. Biol, 60, pp. 265-287. , (doi:10.1086/414425); Losos, J.B., Convergence, adaptation, and constraint (2011) Evolution, 65, pp. 1827-1840. , (doi:10.1111/j.1558-5646.2011.01289.x); Wake, D.B., Wake, M.H., Specht, C.D., Homoplasy: From detecting pattern to determining process and mechanism of evolution (2011) Science, 331, pp. 1032-1035. , (doi:10.1126/science.1188545); Wake, D.B., Homoplasy: The result of natural selection, or evidence of design limitations (1991) Am. Nat, 138, pp. 543-567. , (doi:10.1086/285234); Gould, S.J., (2002) The Structure of Evolutionary Theory, , Cambridge, MA: Harvard University Press; Schluter, D., Clifford, E.A., Nemethy, M., McKinnon, J.S., Parallel evolution and inheritance of quantitative traits (2004) Am. Nat, 163, pp. 809-822. , (doi:10.1086/383621); Whittall, J.B., Voelckel, C., Hodges, S.A., Convergence, constraint and the role of gene expression during adaptive radiation: Floral anthocyanins in Aquilegia (2006) Mol. Ecol, 15, pp. 4645-4657. , doi:10.1111/j.1365-294X.2006.03114.x); Atallah, J., Liu, N.H., Dennis, P., Hon, A., Larsen, E.W., Developmental constraints and convergent evolution in Drosophila sex comb formation (2009) Evol. Dev, 11, pp. 205-218. , (doi:10.1111/j.1525-142X.2009.00320.x); des Marais, D.L., Rausher, M.D., Parallel evolution at multiple levels in the origin of hummingbird pollinated flowers in Ipomoea (2010) Evolution, 64, pp. 2044-2054; Hamburger, V., Embryology and the modern synthesis in evolutionary theory (1980) The Evolutionary Synthesis, pp. 97-112. , (eds E. Mayr & W. B. Provine, Cambridge, MA: Harvard University Press; Gould, S.J., (1977) Ontogeny and Phylogeny, , Cambridge, MA: Harvard University Press; Duboule, D., Dolle, P., The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes (1989) EMBO J, 8, pp. 1497-1505; Shapiro, M.D., Marks, M.E., Peichel, C.L., Blackman, B.K., Nereng, K.S., Jonsson, B., Schluter, D., Kingsley, D.M., Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks (2004) Nature, 428, pp. 717-723. , (doi:10.1038/nature02415); Colosimo, P.F., Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles (2005) Science, 307, pp. 1928-1933. , (doi:10.1126/science.1107239); Prud'homme, B., Gompel, N., Rokas, A., Kassner, V.A., Williams, T.M., Yeh, S., True, J.R., Carroll, S.B., Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene (2006) Nature, 440, pp. 1050-1053. , (doi:10.1038/nature04597); Derome, N., Duchesne, P., Bernatchez, L., Parallelism in gene transcription among sympatric lake whitefish (Coregonus clupeaformis Mitchill) ecotypes (2006) Mol. Ecol, 15, pp. 1239-1249. , (doi:10.1111/j.1365-294X.2005.02968.x); Arendt, J., Reznick, D., Convergence and parallelism reconsidered: What have we learned about the genetics of adaptation? (2008) Trends Ecol. Evol, 23, pp. 26-32. , (doi:10.1016/j.tree.2007.09.011); Manceau, M., Domingues, V.S., Linnen, C.R., Rosenblum, E.B., Hoekstra, H.E., Convergence in pigmentation at multiple levels: Mutations, genes and function (2010) Phil. Trans. R. Soc. B, 1552, pp. 2439-2450. , (doi:10.1098/rstb.2010.0104); Elmer, K.R., Meyer, A., Adaptation in the age of ecological genomics: Insights from parallelism and convergence (2011) Trends Ecol. Evol, 26, pp. 298-306. , (doi:10.1016/j.tree.2011.02.008); Cooper, W.J., Albertson, R.C., Quantification and variation in experimental studies of morphogenesis (2008) Dev. Biol, 321, pp. 295-302. , (doi:10.1016/j.ydbio.2008.06.025); Klingenberg, C.P., Evolution and development of shape: Integrating quantitative approaches (2010) Nat. Rev. Genet, 11, pp. 623-635; Grant, P.R., (1999) Ecology and Evolution of Darwin's Finches, , Princeton, NJ: Princeton University Press; Schluter, D., (2000) The Ecology of Adaptive Radiation, , Oxford, UK: Oxford University Press; Losos, J.B., (2009) Lizards In An Evolutionary Tree: Ecology and Adaptive Radiation of Anoles, , Berkeley, CA: University of California Press; Cohn, M.J., Tickle, C., Developmental basis of limblessness and axial patterning in snakes (1999) Nature, 399, pp. 474-479. , (doi:10.1038/20944); Abzhanov, A., Kuo, W.P., Hartmann, C., Grant, B.R., Grant, P.R., Tabin, C.J., The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches (2006) Nature, 442, pp. 563-567. , (doi:10.1038/nature04843); Abzhanov, A., Protas, M., Grant, B.R., Grant, P.R., Tabin, C.J., Bmp4 and morphological variation of beaks in Darwin's finches (2004) Science, 305, pp. 1462-1465. , (doi:10.1126/science.1098095); Farnum, C.E., Tinsley, M., Hermanson, J.W., Postnatal bone elongation of the manus versus pes: Analysis of the chondrocytic differentiation cascade in Mus musculus and Eptesicus fuscus (2008) Cells Tissues Organs, 187, pp. 48-58. , (doi:10.1159/000109963); Farnum, C.E., Tinsley, M., Hermanson, W., Forelimb versus hindlimb skeletal development in the big brown bat, Eptesicus fuscus: Functional divergence is reflected in chondrocytic performance in autopodial growth plates (2008) Cells Tissues Organs, 187, pp. 35-47. , (doi:10.1159/000109962); Adams, D.C., Nistri, A., Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae) (2010) BMC Evol. 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PY - 2012

Y1 - 2012

N2 - The independent evolution of similar morphologies has long been a subject of considerable interest to biologists. Does phenotypic convergence reflect the primacy of natural selection, or does development set the course of evolution by channelling variation in certain directions? Here, we examine the ontogenetic origins of relative limb length variation among Anolis lizard habitat specialists to address whether convergent phenotypes have arisen through convergent developmental trajectories. Despite the numerous developmental processes that could potentially contribute to variation in adult limb length, our analyses reveal that, in Anolis lizards, such variation is repeatedly the result of changes occurring very early in development, prior to formation of the cartilaginous long bone anlagen. © 2011 The Royal Society.

AB - The independent evolution of similar morphologies has long been a subject of considerable interest to biologists. Does phenotypic convergence reflect the primacy of natural selection, or does development set the course of evolution by channelling variation in certain directions? Here, we examine the ontogenetic origins of relative limb length variation among Anolis lizard habitat specialists to address whether convergent phenotypes have arisen through convergent developmental trajectories. Despite the numerous developmental processes that could potentially contribute to variation in adult limb length, our analyses reveal that, in Anolis lizards, such variation is repeatedly the result of changes occurring very early in development, prior to formation of the cartilaginous long bone anlagen. © 2011 The Royal Society.

U2 - 10.1098/rspb.2011.0840

DO - 10.1098/rspb.2011.0840

M3 - Article

SN - 0962-8452

VL - 279

SP - 739

EP - 748

JO - Proceedings of the Royal Society B: Biological Sciences

JF - Proceedings of the Royal Society B: Biological Sciences

IS - 1729

ER -

Repeated modification of early limb morphogenesis programmes underlies the convergence of relative limb length in Anolis lizards

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