Origin of Novelties

Abstract

The term ‘novelty’ in evolutionary biology is applied to structures or processes that evolve within groups without obvious precursors among their probable ancestors. The genetic system that enables the generation of novelties in multicellular animals evolved in the late Precambrian and Early Cambrian. Continuing change within the elements of this system explains how novelties have arisen within the metazoan phyla over the last 600 million years.

Keywords: Hox genes; macroevolution; genomic evolution; metazoan phyla; cambrian explosion

Figure 1.

Key events in the history of life, from the origin of prokaryotes through the radiation of the metazoan phyla. The origin of eukaryotes resulted from the endosymbiosis of an aerobic eubacterium with an archaebacterium.

Figure 2.

Diagramatic representation of the position of Hox genes along a segment of the chromosome in several groups of multicellular animals. Hox genes, also called master control genes, regulate the expression of structures along the anterior–posterior axis of animals, which corresponds to their left to right and numerical sequence on this diagram. All Hox genes are similar to one another, indicating that they probably arose from a single ancestry gene through duplication, presumably as a result of unequal crossing‐over. The pattern of the common ancestor of advanced metazoan phyla is shown in the fourth line. The arrows oriented dorsally and ventrally indicate evolution leading to a succession of related phyla. New Hox genes arose independently among protostome and chordates. The Hox genes situated on a single chromosome are termed a Hox cluster. Vertebrates, illustrated by the mouse, are unique in having multiple copies of the single Hox cluster present in primitive chordates, such as amphioxus. Reprinted with minor modification from Carroll RL (2000) Towards a new evolutionary synthesis. Trends in Ecology and Evolution15: 27–32. Copyright © 2000 with permission from Elsevier Science.

Figure 3.

Examples of the origin of novelties associated with the areas of expression of Hox genes. (a) A1–A5, the origin of wings in insects. A1, Ramsdelepidion schusteri, a flightless insect related to the living silver fish, from the Upper Carboniferous. This animals lacks wings, but has a series of gills extending from the thorax and abdomen. A2, nymph of a mayfly. Wings are developing from the anterior gills. A3, polyramous limb of a crustacean, which may represent the ancestral condition for insects. A4 and A5, limb of a developing and adult primitive insect, showing separation of the dorsal respiratory lobe from the ventral limb primordium. Areas of expression of the genes ‘apterous’ (in green), which is expressed in the gill portion of the polyramus appendage in crustaceans and is responsible for the dorsal surface of the wing in winged insects, and ‘Distal‐less’ (in blue), regulates the distal end of the legs in both groups. The comparable areas of expression of ‘apterous’ support evidence from the fossil record that insect wings are homologous with the gills in crustaceans. A similar function of this gene has been utilized in regulating the development of a clearly distinct structure. (A1) From Kukalova‐Peck J (1986) New Carboniferous Diplura, Monura, and Thysanura, the hexapod ground plan, and the role of thoracic side lobes in the origin of wings (Insecta). Canadian Journal of Zoology65: 2327–2345. Reproduced with permission of the National Research Council of Canada. (A2) From Kukalova‐Peck J (1978) Insect wings metamorphosis, and the fossil record. Journal of Morphology156: 53–126. Reprinted with permission of Wiley‐Liss, Inc., a subsidiary of John Wiley & Sons, Inc. (A3–A5) From Shubin N, Tabin C and Carroll S (1997) Fossils, genes and the evolution of animal limbs. Nature388: 639–648. (b) B1–B5, origin of the distal end of the limb in the transition from fish to amphibians. B1, bones of the limb of a modern lung fish, showing both preaxial (anterior) and postaxial (posterior) radials, extending from the main axis of development. B2, bones of the osteolepiform fish Eusthenopteron, in which all radials are preaxial. B3, hind limb of the early amphibian Ichthyostega, in which the axis of development angles forward and the distal tarsals and digits develop in a posterior to anterior sequence. B4, area of expression of Hoxd genes in the living zebra fish. B5, area of expression of Hoxd genes in modern tetrapods. The area of expression of Hoxd13 determines the pattern of development of the bones at the distal end of the limb. In the zebra fish, the gene is expressed only posteriorly, for a short period of time, and the bones extend only to the base of the fin web, as was presumably the case in the ancestors of amphibians. In modern amphibians, the gene is expressed for a longer period of time and extends anteriorly, regulating the development of the hand and foot, which bend anteriorly, from the original axis of development. From Carroll R (1997) Patterns and Processes of Vertebrate Evolution. Cambridge, Cambridge University Press. Reprinted with the permission of Cambridge University Press.

close

Further Reading

Burke AC, Nelson CE, Morgan BA and Tabin C (1995) Hox genes and the evolution of vertebrate axial morphology. Development 121: 333–346.

de Rosa R, Grenier JK, Andreeva T et al. (1999) Hox genes in brachiopods and priapulids and protostome evolution. Nature 399: 772–776.

Erwin DH (1999) The origin of bodyplans. American Zoologist 39: 617–629.

Gehring WJ (1998) Master Control Genes in Development and Evolution: The Homeobox Story. New Haven: Yale University Press.

Gehring WJ and Ikeo K (1999) Pax 6 mastering eye morphogenesis and eye evolution. Trends in Genetics 15: 371–377.

Gerhard J and Kirschner M (1997) Cells, Embryos, and Evolution. Malden, MA: Blackwell Science.

Grenier JK, Garber TL, Warren R, Whitington PM and Carroll S (1997) Evolution of the entire arthropod Hox gene set predated the origin and radiation of the onychophoran/arthropod clade. Current Biology 7: 547–553.

Finnerty J (1998) Homeoboxes in sea anemones and other non‐bilaterian animals; implications for the evolution of the Hox cluster and the zootype. Current Topics in Developmental Biology 40: 212–251.

Kidwell MG and Lisch DR (2000) Transposable elements and host genome evolution. Trends in Ecology and Evolution 15: 95–99.

Knoll AH (1995) Proterozoic and Early Cambrian protists: evidence for accelerating evolutionary tempo. In: Fitch WM and Ayala FJ (eds) Tempo and Mode in Evolution, pp. 63–83. Washington DC: National Academy Press.

Lawton‐Rauh AL, Alvarez‐Buylla ER and Purugganan MD (2000) Molecular evolution of flower development. Trends in Ecology and Evolution 15: 144–149.

Schopf JW (1995) Disparate rates, differing fates: tempo and mode of evolution changed from the Precambrian to the Phanerozoic. In: Fitch WM and Ayala FJ (eds) Tempo and Mode in Evolution, pp. 41–61. Washington DC: National Academy Press

Shubin N, Tabin C and Carroll S (1997) Fossils, genes, and the evolution of animal limbs. Nature 388: 639–646.

Xiao S, Yang Z and Knoll A (1998) Three‐dimensional preservation of algae and animal embryos in a Neoproterozoic phosphate. Nature 391: 553–558.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Carroll, Robert L(Jul 2003) Origin of Novelties. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1038/npg.els.0001660]