Hostname: page-component-848d4c4894-x5gtn Total loading time: 0 Render date: 2024-05-03T15:44:08.563Z Has data issue: false hasContentIssue false
  • English
  • Français

Fossils, genes, and the origin of novelty

Published online by Cambridge University Press:  26 February 2019

Neil H. Shubin  and
Charles R. Marshall
Neil H. Shubin
Affiliation:
Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6018
Charles R. Marshall
Affiliation:
Department of Earth and Planetary Sciences, and Organismic and Evolutionary Biology, 20 Oxford Street, Harvard University, Cambridge, Massachusetts 02138. E-mail: marshall@eps.harvard.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

The origin of evolutionary novelty involves changes across the biological hierarchy: from genes and cells to whole organisms and ecosystems. Understanding the mechanisms behind the establishment of new designs involves integrating scientific disciplines that use different data and, often, different means of testing hypotheses. Discoveries from both paleontology and developmental genetics have shed new light on the origin of morphological novelties. The genes that play a major role in establishing the primary axes of the body and appendages, and that regulate the expression of the genes that are responsible for initiating the making of structures such as eyes, or hearts, are highly conserved between phyla. This implies that it is not new genes, per se, that underlie much of morphological innovation, but that it is changes in when and where these and other genes are expressed that constitute the underlying mechanistic basis of morphological innovation. Gene duplication is also a source of developmental innovation, but it is possible that it is not the increased number of genes (and their subsequent divergence) that is most important in the evolution of new morphologies; rather it may be the duplication of their regulatory regions that provides the raw material for morphological novelty. Bridging the gap between microevolution and macroevolution will involve understanding the mechanisms behind the production of morphological variation. It appears that relatively few genetic changes may be responsible for most of the observed phenotypic differences between species, at least in some instances. In addition, advances in our understanding of the mechanistic basis of animal development offer the opportunity to deepen our insight into the nature of the Cambrian explosion. With the advent of whole-genome sequencing, we should see accelerated progress in understanding the relationship between the genotype, phenotype, and environment: post-genomics paleontology promises to be most exciting.

Type
Research Article
Information
Paleobiology , Volume 26 , Issue S4: Deep Time: Paleobiology's Perspective , 2000 , pp. 324 - 340
Copyright
Copyright © 2000 by The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Averof, M., and Patel, N. 1997. Crustacean appendage evolution associated with changes in Hox gene expression. Nature 388:682–686.Google Scholar
Banfield, J. F., and Marshall, C. R. 2000. Genomics and the geosciences. Science 287:605–606.Google Scholar
Basler, D., and Struhl, G. 1994. Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368:208–214.Google Scholar
Bengtson, S., ed. 1994. Early life on Earth (Nobel Symposium No.84). Columbia University Press, New York.Google Scholar
Bradshaw, H. D., Otto, K., Frewen, B., McKay, J. K., and Schemske, D. 1998. Quantitative trait loci affecting differences in floral morphology between two species of monkey flower (Mimulus). Genetics 149:367–382.Google Scholar
Brooke, N. M., Garciafernandez, J., and Holland, P. W. H. 1998. The paraHox gene cluster is an evolutionary sister of the Hox gene cluster. Nature 392:920–922.Google Scholar
Budd, G. E. 1999. Does evolution in body patterning genes drive morphological change—or vice versa? BioEssays 21:326–332.Google Scholar
Burke, A. C., Nelson, C. E., Morgan, B. A., and Tabin, C. 1995. Hox genes and the evolution of vertebrate axial morphology. Development 121:333–346.Google Scholar
Carroll, R. L. 1988. Vertebrate paleontology and evolution. W. H. Freeman, New York.Google Scholar
Carroll, S. B. 1995. Homeotic genes and the evolution of arthropods and chordates. Nature 376:479–485.Google Scholar
Carroll, S. B. 2000. Endless forms: the evolution of gene regulation and morphological diversity. Cell 101:577–580.Google Scholar
Chang, D. T., Lopez, A., Vonkessler, D. P., Chiang, C., Simandl, B. K., Zhao, R. B., Seldin, M. F., Fallon, J. F., and Beachy, P. A. 1994. Products, genetic linkage and limb patterning activity of a murine hedgehog gene. Development 120:3339–3353.Google Scholar
Cohn, M. J., and Coates, M. 1999. Vertebrate axial and appendicular patterning: the early development of paired appendages. American Zoologist 39:676–685.Google Scholar
Cohn, M. J., and Tickle, C. 1996. Limbs—a model for pattern formation within the vertebrate body plan. Trends in Genetics 12:253–257.Google Scholar
Cohn, M. J., and Tickle, C. 1999. Developmental basis of limblessness and axial patterning in snakes. Nature 399:474–479.Google Scholar
Couso, J. P., Bate, M., and Martinez-Arias, A. A. 1993. Wingless-dependent polar coordinate system in Drosophila imaginal discs. Science 259:484–489.Google Scholar
Davidson, E. H., Peterson, K. J., and Cameron, R. A. 1995. Origin of adult bilaterian body plans: evolution of developmental regulatory mechanisms. Science 270:1319–1325.Google Scholar
de Rosa, R., Grenier, J., Andreeva, T., Cook, C., Adoutte, A., Akam, M., Carroll, S. B., and Balavoine, G. 1999. Hox genes in brachiopods and priapulids and protostome evolution. Nature 399:772–776.Google Scholar
Diaz-Benjumea, F., and Cohen, S. M. 1993. Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 75:741–752.Google Scholar
Doebley, J., and Stec, A. 1991. Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 129:285–295.Google Scholar
Doebley, J., and Wang, R.-L. 1997. Genetics and the evolution of plant form: an example from maize. Cold Spring Harbor Symposia on Quantitative Biology 22:361–367.Google Scholar
Duboule, D., and Wilkins, A. S. 1998. The evolution of ‘bricolage'. Trends in Genetics 14:54–59.Google Scholar
Erwin, D. H. 2000. Macroevolution is more than repeated rounds of microevolution. Evolution and Development 2:78–84.Google Scholar
Ferea, T. L., Botstein, D., Brown, P. O., and Rosenzweig, R. F. 1999. Systematic changes in gene expression patterns following adaptive evolution in yeast. Proceedings of the National Academy of Sciences USA 96:9721–9726.Google Scholar
Finnerty, J. R., and Martindale, M. Q. 1998. The evolution of the Hox cluster: insights form outgroups. Current Opinion in Genetics and Development 8:681–687.Google Scholar
Finnerty, J. R., and Martindale, M. Q. 1999. Ancient origins of axial patterning genes: Hox genes and ParaHox genes in the Cnidaria. Evolution and Development 1:16–23.Google Scholar
Fisher, R. A. 1930. The genetical theory of natural selection. Oxford University Press, Oxford.Google Scholar
Gans, C. 1975. Tetrapod limblessness: evolution and functional corollaries. American Zoologist 15:455–467.Google Scholar
Garey, J. R., and Schmidt-Rhaesa, A. 1998. The essential role of “minor” phyla in molecular studies of animal evolution. American Zoologist 38:907–917.Google Scholar
Gerhart, J., and Kirschner, M. 1997. Cells, embryos and evolution. Blackwell Science, Malden Mass.Google Scholar
Gould, S. J. 1977. Ontogeny and phylogeny. Harvard University Press, Cambridge.Google Scholar
Haldane, J. B. S. 1932. The causes of evolution. Longmans and Green, London.Google Scholar
Holland, P. W. H. 1998. Major transitions in animal evolution: a developmental genetic perspective. American Zoologist 38:829–842.Google Scholar
Irvine, K., and Weischaus, E. 1994. fringe, a boundary-specific signaling molecule, mediates interactions between dorsal and ventral cells during Drosophila wing development. Cell 79:595–606.Google Scholar
Jacob, F. 1977. Evolution and tinkering. Science 196:1161–1166.Google Scholar
Jones, C. D. 1998. The genetic basis of Drosophila sechellia's resistance to a host plant toxin. Genetics 149:1899–1908.Google Scholar
Kimura, M. 1983. The neutral theory of molecular evolution. Cambridge University Press, Cambridge.Google Scholar
Knoll, A. H., and Carroll, S. B. 1999. Early animal evolution: emerging views from comparative biology and geology. Science 284:2129–2137.Google Scholar
Krauss, S., Concordet, J. P., and Ingham, P. W. 1993. A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75:1431–1444.Google Scholar
Laufer, E., and Tabin, C. 1993. Hox genes and serial homology. Nature 361:692–693.Google Scholar
Lee, J. J., von Kessler, D. P., Parks, S., and Beachy, P. A. 1992. Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell 71:33–50.Google Scholar
Maienschein, J. 1991. The origins of Entwicklungsmechanik. Developmental Biology 7:43–61.Google Scholar
Marshall, C. R. 1995. Darwinism in an age of molecular revolution. Pp. 1–30 in Marshall, C. R. and Schopf, J. W., eds. Evolution and the molecular revolution. Jones and Bartlett, Sudbury, Mass.Google Scholar
Marshall, C. R., Orr, H. A., and Patel, N. H. 1999. Morphological innovation and developmental genetics. Proceedings of the National Academy of Sciences USA 96:9995–9996.Google Scholar
Mercader, N., Leonardo, E., Azpiazu, N., Serrano, A., Morata, G., Martinez, A. C., and Torres, M. 1999. Conserved regulation of proximodistal limb axis development by Meis/Hth. Nature 402:425–429.Google Scholar
Müller, G., and Wagner, G. P. 1991. Novelty in evolution: restructuring the concept. Annual Reviews of Ecology and Systematics 22:229–256.Google Scholar
Muller, H. J. 1935. The origination of chromatin deficiencies as minute deletions subject to insertion elsewhere. Genetics 17:237–252.Google Scholar
Ohno, S. 1970. Evolution by gene duplication. Springer, Berlin.Google Scholar
Orr, H. A. 1997. The population genetics of adaptation—the distribution of factors fixed during adaptive evolution. Evolution. 52:935–949.Google Scholar
Orr, H. A., and Irving, S. 1998. The genetics of adaptation—the genetic basis of resistance to wasp parasitism in Drosophila melanogaster. Evolution 51:1877–1885.Google Scholar
Panganiban, G., Irvine, S. M., Lowe, C., Roehl, H., Corley, L., Sherbon, B., Grenier, J. K., Fallon, J. F., Kimble, J., Walker, M., Wray, G. A., Swalla, B. J., Martindale, M. Q., and Carroll, S. B. 1997. The origin and evolution of animal appendages. Proceedings of the National Academy of Sciences USA 94:5162–5166.Google Scholar
Parr, B. A., and McMahon, A. P. 1995. Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374:350–353.Google Scholar
Peterson, K. J., and Davidson, E. H. 2000. Regulatory evolution and the origin of bilaterians. Proceedings of the National Academy of Sciences USA 97:4430–4433.Google Scholar
Peterson, K. J., Cameron, R. A., and Davidson, E. H. 1997. Setaside cells in maximal indirect development: evolutionary and developmental significance. BioEssays 19:623–631.Google Scholar
Peterson, K. J., Cameron, R. A., and Davidson, E. H. 2000. Bilaterian origins: significance of new experimental observations. Developmental Biology 219:1–7.Google Scholar
Raff, R. 1997. The shape of life. University of Chicago Press, Chicago.Google Scholar
Riddle, R. D., Johnson, R. L., Laufer, E., and Tabin, C. 1993. Sonichedgehog mediates the polarizing activity of the ZPA. Cell 75:1401–1416.Google Scholar
Riddle, R. D., Ensini, M., Nelson, C., Tsuchida, T., Jessell, T. M., and Tabin, C. 1995. Induction of the LIM homeobox gene Lmx-1 by Wnt-7a establishes dorsoventral pattern in the vertebrate limb. Cell 83:631–640.Google Scholar
Rodriguez-Esteban, C., Schwabe, J. W. R., Delapena, J., Foys, B., Eshelman, B., Belmonte, J. C. I. 1997. Radical fringe positions the apical ectodermal ridge at the dorsoventral boundary of the vertebrate limb. Nature 386:360–366.Google Scholar
Romano, S. L., and Palumbi, S. R. 1996. Evolution of scleractinian corals inferred from molecular systematics. Science 271:640–642.Google Scholar
Rutherford, S. L., and Lindquist, S. 1998. Hsp90 as a capacitor for morphological evolution. Nature 396:336–342.Google Scholar
Shubin, N. H. 1995. The evolution of paired fins and the origin of tetrapod limbs: phylogenetic and transformational approaches. Evolutionary Theory 28:39–86.Google Scholar
Shubin, N. H., Tabin, C., and Carroll, S. B. 1997. Fossils, genes and the evolution of animal limbs. Nature 388:639–648.Google Scholar
Smith, A. B. 1999. Dating the origin of metazoan body plans. Evolution and Development 1:138–142.Google Scholar
Stern, D. 1998. A role of Ultrabithorax in morphological differences between species. Nature 396:463–466.Google Scholar
Tabata, T., Eaton, S., and Kornberg, T. B. 1992. The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes and Development 6:2635–2645.Google Scholar
Tabin, C. J., Carroll, S. B., and Panganiban, G. 1999. Out on a limb: parallels in vertebrate and invertebrate limb patterning and the origin of appendages. American Zoologist 39:650–663.Google Scholar
Tanksley, S. D. 1993. Mapping polygenes. Annual Reviews of Genetics 27:205–233.Google Scholar
Valentine, J. W., Jablonski, D., and Erwin, D. H. 1999. Fossils, molecules and embryos: new perspectives on the Cambrian explosion. Development 126:851–859.Google Scholar
Van Valen, L. M. 1982. Homology and causes. Journal of Morphology 173:305–312.Google Scholar
Vogel, A., Rodriguez, C., Warnken, W., and Belmonte, J. C. I. 1995. Dorsal cell fate specified by chick Lmx1 during vertebrate limb development. Nature 378:716–720.Google Scholar
Williams, J. A., Paddock, S. W., and Carroll, S. B. 1993. Pattern formation in a secondary field: a hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete sub-regions. Development 117:571–584.Google Scholar
Wray, G. A., and Abouheif, E. 1998. When is homology not homology. Current Opinion in Genetics and Development 8:675–680.Google Scholar
Zhu, M., Yu, X. B., and Janvier, P. 1999. A primitive fossil fish sheds light on the origin of bony fishes. Nature 397:607–610.Google Scholar