Molecular Evidence for Deep Precambrian Divergences Among Metazoan Phyla

Darwin C., On The Origin of Species by Means of Natural Selection (Murray, London, 1859).

Gould S. J., Wonderful Life (Norton, New York, 1989).

Lipps J. H., Signor P. W., Eds., Origin and Early Evolution of Metazoa (Plenum, New York, 1992).

Bowring S. A., et al., Science 261, 1293 (1993).

Schopf J. W., Klein C., Eds., The Proterozoic Biosphere. A Multidisciplinary Study (Cambridge Univ. Press, Cambridge, 1992).

Valentine J. W., Awramik S. M., Signor P. W., Sadler P. M., Evol. Biol. 25, 279 (1991).

Boaden P. J. S., Zool. J. Linn. Soc. 96, 217 (1989);

Davidson E. H., Cameron R. A., Peterson K. J., Science 270, 1319 (1995).

Conway Morris S., Nature 361, 219 (1993).

Butterfield N. J., Lethaia 28, 1 (1995).

Whittington H. B., The Burgess Shale (Yale Univ. Press, New Haven, CT, 1985).

Runnegar B., Alcheringa 6, 223 (1982).

Glaessner M. F., The Dawn of Animal Life (Cambridge Univ. Press, Cambridge, 1984).

Runnegar B., Palaeontology 29, 1 (1986).

Runnegar B., Lethaia 15, 199 (1982).

Erwin D. H., ibid. 22, 251 (1989).

Phillipe H., Chenuil A., Adoutte A., Dev. Suppl. 1994, 15 (1994).

Zuckerkandl E., Pauling L., in Evolving Genes and Proteins, Bryson V., Vogel H. J., Eds. (Academic Press, New York, 1965), pp. 97–166

Kimura M., The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, Cambridge, 1983).

Gillespie J. H., The Causes of Molecular Evolution (Oxford Univ. Press, Oxford, 1991).

Britten R. J., Science 231, 1393 (1986);

Li W.-H., Wu C.-I., Mol. Biol. Evol. 4, 74 (1987).

Doolittle R. F., Feng D.-F., Tsang T., Cho G., Little E., Science 271, 470 (1996);

Hedges S. B., Parker P. H., Sibley C. G., Kumar S., Nature 381, 226 (1996).

Sequences were obtained from the National Center for Biotechnology Information repository of the GenBank and SwissProt databases and aligned with ClustalW [Thompson J. D., Higgins D. G., Gibson T. J., Nucleic Acids Res. 22, 4673 (1994); alignments were verified by eye, and positions not represented by all species were eliminated from further analysis. Each calibration data set included sequences from a maximum of three taxonomic families per order and one species per family. Sequence divergence matrices were calculated according to Kimura's method (18) with PHYLIP 3.5 (27). Sequence divergence rates were calculated as the model I regression through all pairwise sequence divergences within the chordates (or chordates, echinoderms, and mollusks for 18S rRNA), plotted against divergence times based on first appearances in the fossil record. Regressions were not forced through the origin; the slightly positive intercepts are probably a simple consequence of having to rely primarily on first appearances in the fossil record for our rate calibrations, which tends to cause underestimation of divergence times. Forcing regressions through the origin results in average invertebrate-chordate divergence estimates approximately 100 to 150 My less than those presented in Table 2, which would not alter our conclusions. Invertebrate-chordate sequence divergences were calculated by taking the mean of the sequence divergence between each invertebrate and all the chordates. Complete species lists, accession numbers, alignments, distance matrices, and divergence time matrices are available on request or from our World Wide Web page (http://life.bio.sunysb.edu/ee/precambrian)

Smith A. B., Systematics and the Fossil Record (Blackwell, Oxford, 1994).

Stratigraphic ranges were obtained from Benton M. J., Ed., The Fossil Record 2 (Chapman and Hall, London, 1993). Space limitations preclude listing all pairwise divergence time estimates based on the fossil record, but some examples follow: Chondrichthyes versus Sarcopterygii or Actinopterygii = 415 million years ago (Ma); Dipnoi or Latimeria versus Tetrapoda = 408 Ma; Amphibia versus Archosauria, Lepidosauria, or Mammalia = 349 Ma; Crocodylia versus Aves = 235 Ma; Teleostei versus Chondrostei = 223 Ma; Urodela versus Anura = 208 Ma; Monotrema versus Marsupialia or Eutheria = 160 Ma; Serpentes versus Sauria = 157 Ma; Salmoniformes or Cypriniformes versus Anguilliformes = 152 Ma; Marsupialia versus Eutheria = 112 Ma; Varanidae versus Iguanidae = 83 Ma; Cetacea versus Artiodactyla = 56 Ma; Muridae versus Sciuridae or Caviidae = 42 Ma; Phocidae versus Felidae = 38 Ma; and Hominidae versus Tarsiidae = 38 Ma.

Dayhoff M. O., Atlas of Protein Sequence and Structure, vol. 5, suppl. 3 (National Biomedical Research Foundation, Washington, DC, 1978).

Sokal R. R., Rohlf F. J., Biometry (Freeman, New York, ed. 3, 1995).

Felsenstein J., PHYLIP (Phylogeny Inference Package), version 3.5c (distributed by the author, Dept. of Genetics, University of Washington, Seattle, WA, 1993).

Brusca R. C., Brusca G. J., Invertebrates (Sinauer, Sunderland, MA, 1990);

Nielsen C., Animal Evolution (Oxford Univ. Press, Oxford, 1995).

Sarich V. M., Wilson A. C., Science 179, 1144 (1973).

Felsenstein J., Syst. Zool. 27, 401 (1978);

Huelsenbeck J. P., Hillis D. M., Syst. Biol. 42, 247 (1993).

Field K. G., et al., Science 239, 748 (1988);

Christen R., et al., EMBO J. 10, 499 (1991);

Turbeville J. M., Field K. G., Raff R. A., Mol. Biol. Evol. 9, 235 (1992);

Wada H., Satoh N., Proc. Natl. Acad. Sci. U.S.A. 91, 1801 (1994);

Halanych K. M., et al., Science 267, 1641 (1995).

Gehling J. G., Alcheringa 11, 337 (1987).

Gehling J. G., Mem. Geol. Soc. India 20, 181 (1991);

Jenkins R. J. F., in Origin and Early Evolution of the Metazoa, Lipps J. H., Signor P. W., Eds. (Plenum, New York, 1992), pp. 181–223

Sun W., Wang G., Zhou B., Precambrian Res. 31, 377 (1986);

Hoffmann H. J., in Early Life on Earth, Bengtson S., Ed. (Columbia Univ. Press, New York, 1994), pp. 342–357

Robbins E. I., Porter K. G., Haberyan K. A., Proc. Natl. Acad. Sci. U.S.A. 82, 5809 (1985).

Fortey R. A., Briggs D. E. G., Wills M. A., Biol. J. Linn. Soc. 57, 13 (1996).

Fortey R. A., Owens R. M., in Major Evolutionary Radiations, Taylor P. D., Larwood G., Eds. (Clarendon, Oxford, 1990), pp. 139–164

Briggs D. E. G., Fortey R. A., Science 246, 241 (1989).

Runnegar B., Bengtson S., in Paleobiology: A Synthesis, Briggs D. E. G., Crowther P. R., Eds. (Blackwell, Oxford, 1990), pp. 24–29

Duboule D., Dollé P., EMBO J. 8, 1497 (1989);

McGinnis W., Krumlauf R., Cell 68, 283 (1992).

DeRobertis E. M., in Guidebook to the Homeobox Genes, Duboule D., Ed. (IRL, Oxford, 1994), pp. 13–23;

Scott M. P., Cell 79, 1121 (1994);

Patel N., Science 266, 581 (1994).

Valentine J. W., Erwin D. H., Jablonski D., Dev. Biol. 173, 373 (1996).

Goodman M., Moore W. G., Matsuda G., Nature 253, 603 (1975).

We thank J. Felsenstein, J. Rohlf, R. Sokal, B. Runnegar, A. Bely, J. Boore, and R. Zardoya for invaluable help with these analyses, and A. Bely, D. Futuyma, D. Jablonski, and A. Knoll for helpful comments on the manuscript. Supported by grants from NSF to all three authors and from the A. P. Sloan Foundation to G.A.W