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Chance and necessity: the evolution of morphological complexity and diversity

Nature volume 409, pages 11021109 (22 February 2001) | Download Citation

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Abstract

The primary foundation for contemplating the possible forms of life elsewhere in the Universe is the evolutionary trends that have marked life on Earth. For its first three billion years, life on Earth was a world of microscopic forms, rarely achieving a size greater than a millimetre or a complexity beyond two or three cell types. But in the past 600 million years, the evolution of much larger and more complex organisms has transformed the biosphere. Despite their disparate forms and physiologies, the evolution and diversification of plants, animals, fungi and other macroforms has followed similar global trends. One of the most important features underlying evolutionary increases in animal and plant size, complexity and diversity has been their modular construction from reiterated parts. Although simple filamentous and spherical forms may evolve wherever cellular life exists, the evolution of motile, modular mega-organisms might not be a universal pattern.

“Drawn out of the realm of pure chance, the accident enters into that of necessity, of the most implacable certainties.” J. Monod1

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References

  1. 1.

    Chance and Necessity (Vintage Books, New York, 1971).

  2. 2.

    The Evolution of Complexity by Means of Natural Selection (Princeton Univ. Press, Princeton, 1988).

  3. 3.

    Metazoan complexity and evolution: is there a trend? Evolution 50, 477–492 (1996).

  4. 4.

    & Directionality in the history of life: diffusion from the left wall or repeated scaling of the right? Paleobiology 26(Suppl.) 1–14 (2000).

  5. 5.

    Full House (Harmony Books, New York, 1996).

  6. 6.

    Cambrian and recent morphological disparity. Science 258, 1816–1818 (1992).

  7. 7.

    Mechanisms of large-scale evolutionary trends. Evolution 48, 1747–1763 (1994).

  8. 8.

    An explanation for Cope's rule. Evolution 27, 1–26 (1973).

  9. 9.

    Time in evolutionary process. Studium Generale 23, 266–272 (1970).

  10. 10.

    Presidential Address. Trends as changes in variance: a new slant on progress and directionality in evolution. J. Paleont. 62, 319–329 (1988).

  11. 11.

    Contrasting the underlying patterns of active trends in morphological evolution. Evolution 50, 990–1007 (1996).

  12. 12.

    A Brief History of Time: From the Big Bang to Black Holes (Bantam Books, Toronto, 1988).

  13. 13.

    The origins of multicellularity. Integ. Biol. 1, 28–36 (1998).

  14. 14.

    Microfossils of the Early Archean Apex chert: new evidence of the antiquity of life. Science 260, 640–645 (1993).

  15. 15.

    The early evolution of eukaryotes: a geological perspective. Science 256, 622–627 (1992).

  16. 16.

    Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellullarity, and the Mesoproterozoic/neoproterozoic radiation of eukaryotes. Paleobiology 26, 386–404 (2000).

  17. 17.

    et al. Age of Neoproterozoic bilaterian body of trace fossils, White Sea, Russia: implications for metazoan evolution. Science 288, 841–845 (2000).

  18. 18.

    & Early animal evolution: emerging views from comparative biology and geology. Science 284, 2129–2137 (1999).

  19. 19.

    , & The Fossils of the Burgess Shale (Smithsonian Institution Press, Washington DC, 1994).

  20. 20.

    & The Origin and Early Diversification of Land Plants (Smithsonian Institution Press, Washington DC, 1997).

  21. 21.

    Origin of Land Plants (Wiley, New York, 1993).

  22. 22.

    Volvox: Molecular Genetic Origins of Multicellularity and Cellular Differentiation (Cambridge Univ. Press, Cambridge, 1998).

  23. 23.

    , , & The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature 394, 671–674 (1998).

  24. 24.

    , & Morphological complexity increase in metazoans. Paleobiology 20, 131–142 (1994).

  25. 25.

    & Vertebrate innovations. Proc. Natl Acad. Sci. USA 97, 4434–4437 (2000).

  26. 26.

    et al. Hox genes in brachiopods and priapulids and protostome evolution. Nature 399, 772–776 (1999).

  27. 27.

    Proterozoic and early Cambrian protists: evidence for accelerating evolutionary tempo. Proc. Natl Acad. Sci. USA 91, 6743–6750 (1994).

  28. 28.

    The Crucible of Creation: The Burgess Shale and the Rise of Animals (Oxford Univ. Press, Oxford, 1998).

  29. 29.

    & A critical reappraisal of the fossil record of the bilaterian phyla. Biol. Rev. 75, 253–295 (2000).

  30. 30.

    Models for the diversification of life. Trends Ecol. Evol. 12, 490–495.

  31. 31.

    The method of creation of organic forms. Proc. Am. Phil. Soc. 12, 229–263 (1871).

  32. 32.

    Cope's rule and the dynamics of body mass evolution in North American fossil mammals. Science 280, 731–734 (1998).

  33. 33.

    Fossil horses from “Eohippus” (Hyracoherium) to Equus: scaling, Cope's law, and the evolution of body size. Paleobiology 12, 355–369 (1986).

  34. 34.

    Body-size evolution in Cretaceous molluscs and the status of Cope's rule. Nature 385, 250–252 (1997).

  35. 35.

    & A common plan for dorsoventral patterning in Bilateria. Nature 380, 37–40 (1996).

  36. 36.

    The ancestry of segmentation. Nature 387, 25–26 (1997).

  37. 37.

    Late Precambrian bilaterians: grades and clades. Proc. Natl Acad. Sci. USA 91, 6751–6757 (1994).

  38. 38.

    Evolutionary trends in the articulate brachiopod hinge mechanism. Paleobiology 18, 344–366 (1992).

  39. 39.

    , & Evolution of complexity in Paleozoic ammonoid structures. Science 286, 760–763 (1999).

  40. 40.

    Evolution of the world fauna of aquatic free-living arthropods. Evolution 28, 337–366 (1974).

  41. 41.

    Evolutionary change in the morphological complexity of the mammalian vertebral column. Evolution 47, 730–740 (1993).

  42. 42.

    The morphology of Opabinia regalis and the reconstruction of the arthropod stem-group. Lethaia 29, 1–14 (1996).

  43. 43.

    Discordance and concordance between morphological and taxonomic diversity. Paleobiology 19, 185–204 (1993).

  44. 44.

    The skeleton space: a finite set of organic designs. Evolution 47, 341–360 (1993).

  45. 45.

    , & Evolutionary exploitation of design options by the first animals with hard skeletons. Science 288, 1239–1242 (2000).

  46. 46.

    The Basis of Progressive Evolution (Univ. North Carolina Press, Chapel Hill, 1969).

  47. 47.

    On the early origins of major biologic groups. Paleobiology 9, 107–115 (1983).

  48. 48.

    Systematics and the Fossil Record (Blackwell Scientific Publications, Oxford, 1994).

  49. 49.

    Materials for the Study of Variation (Macmillan, London, 1894).

  50. 50.

    Reduplication in evolution. Quart. Rev. Biol. 10, 272–290 (1935).

  51. 51.

    Evolution above the Species Level (Columbia Univ. Press, New York, 1960).

  52. 52.

    Complexity and evolution: what everybody knows. Biol. Philosophy 6, 303–324 (1991).

  53. 53.

    Plant Allometry: The Scaling of Form and Process (Univ. Chicago Press, Chicago, 1994).

  54. 54.

    , & Origin of bilaterian body plans: evolution of developmental regulatory mechanisms. Science 270, 1319–1325 (1995).

  55. 55.

    , & From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design (Blackwell, Cambridge, 2001).

  56. 56.

    & The ABCs of floral evolution. Cell 101, 5–8 (2000).

  57. 57.

    et al. Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol. Cell 5, 569–579 (2000).

  58. 58.

    Homeotic genes and the evolution of arthropods and chordates. Nature 376, 479–485 (1995).

  59. 59.

    & Selector genes and limb identity in arthropods and vertebrates. Cell 97, 283–286 (1999).

  60. 60.

    Arthropods: developmental diversity within a (super) phylum. Proc. Natl Acad. Sci. USA 97, 4438–4441 (2000).

  61. 61.

    , , , & Evolution of the entire arthropod Hox gene set predated the origin and radiation of the onychophoran/arthropod clade. Curr. Biol. 7, 547–553 (1997).

  62. 62.

    A gene complex controlling segmentation in Drosophila. Nature 276, 565–570 (1978).

  63. 63.

    The molecular basis for metameric pattern in the Drosophila embryo. Development 101, 1–22 (1987).

  64. 64.

    The Shape of Life (Univ. Chicago Press, Chicago, 1996).

  65. 65.

    & Modularity and dissociation in the evolution of gene expression territories in development. Evol. Dev. 2, 102–113 (2000).

  66. 66.

    & Cells, Embryos, and Evolution (Blackwell Science, Malden, 1997).

  67. 67.

    & Evolvability. Proc. Natl Acad. Sci. USA 95, 8420–8427 (19998).

  68. 68.

    , , & The transcriptional profile of early to middle sporulation in Bacillus subtilis. Proc. Natl Acad. Sci. USA 97, 8063–8068 (2000).

  69. 69.

    Molecular mechanisms of cell-type determination in yeast. Curr. Opin. Genet. Dev. 5, 552–558 (1998).

  70. 70.

    et al. The genome sequence of Drosophila melanogaster. Science 287, 2185–2195 (2000).

  71. 71.

    & The taxonomy of developmental control in C. elegans. Science 282, 2033–2041 (1998).

  72. 72.

    & Archetypal organization of the amphioxus Hox gene cluster. Nature 370, 563–566 (1994).

  73. 73.

    At Home in the Universe (Oxford University Press, New York, 1995).

  74. 74.

    Does evolution in body patterning genes drive morphological change—or vice versa? BioEssays 21, 326–332 (1999).

  75. 75.

    Life's Other Secret (Wiley, New York, 1998).

  76. 76.

    et al. The minimal gene complement of Mycoplasma genome. Science 270, 397–404 (1995).

  77. 77.

    et al. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396, 133–143 (1998).

  78. 78.

    et al. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269, 496–412 (1995).

  79. 79.

    et al. The complete genome sequence of Escherichia coli K-12. Science 277, 1453–1462 (1997).

  80. 80.

    et al. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665–668 (2000).

  81. 81.

    et al. The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature 392, 353–358 (1998).

  82. 82.

    et al. Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature 404, 502–506 (2000).

  83. 83.

    et al. The complete genome sequence of the hyperthermophilic, suphate-reducing archaeon Archaeoglobus fulgidus. Nature 390, 364–370 (1997).

  84. 84.

    Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273, 1058–1073 (1996).

  85. 85.

    et al. Sequence analysis of the genome of the unicellular Cyanobacterium Synechocystis sp. strain. DNA Res. 3, 109–136 (1996).

  86. 86.

    et al. The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390, 249–256 (1997).

  87. 87.

    et al. The yeast genome directory. Nature 387, 5–105 (1997).

  88. 88.

    European Union Arabidopsis Genome Sequencing Consortium & Cold Spring Harbor, Washington University in St Louis and PE Biosystems Arabidopsis Sequencing Consortium. Sequence and analysis of chromosome 4 of the plant Arabidopsis thaliana. Nature 402, 769–777 (1999).

  89. 89.

    et al. Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402, 761–768 (1999).

  90. 90.

    et al. Comparative genomics of the eukaryotes. Science 287, 2204–2215 (2000).

  91. 91.

    , , & Archean molecular fossils and the early rise of eukaryotes. Science 285, 1033–1036 (1999).

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Acknowledgements

I thank A. Knoll for discussions and helpful pointers; R. Losick and A. Johnson for information on microbial gene regulation; G. Budd, J. Crow, N. King and J. True for suggestions on the text; J. Carroll for preparation of the manuscript; and L. Olds for the artwork. S.B.C. is an Investigator of the Howard Hughes Medical Institute.

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Correspondence to Sean B. Carroll.

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