Clearly, not only do we need links between the various levels at which evolution is studied, but this need is being filled through the emergence of a molecular population genetics. Or, more strictly, a molecular population genetics concerned with multi-level selection, because, as chronicled by Kimura (1983), a molecular population genetics dealing with the relative strengths of drift and selection has been around since the mid-1960s, concerned with evolution by substitution of one base for another in coding DNA. A prime task of the new molecular population genetics should be finding out the actual molecular changes which occur in response to selection, both in the short and in the long term.
Evolutionary biologists generally fall into one of two types. There are those who uncover what forms of selection are acting on organisms to bring adaptive evolution about. Then there are those who study the genetic machinery in the search for long-term effects of selection. While these two groups have not always taken much notice of each other, the two approaches are not only complementary, but should be combined. The realisation that DNA can be, and almost certainly often is, selfish should heighten the appreciation of the links between the two approaches.
Finally, I ask you to look again at the heads of those two remarkable animals, Drosophila heteroneura and D. silvestris. What has happened at the molecular level to bring about such a massive change? I hope that molecular population geneticists will see it as a major task to map the genetic changes involved in major alterations in development of this kind and then sequence them to see what has happened. When we know what happened to so diversify these two bizarrely-different yet closely related fly species, we will know a lot more about the process of adaptation itself.
I thank Bill Brown, Michael Crosland, Tony Mackinlay, George Milklos, and Christian Peeters for helpful comments on the manuscript, and the Australian Research Grants Scheme and the University of New South Wales for supporting my work on evolutionary genetics.
Arnold, A.J. and Fristrup, K., 1982. The theory of evolution by natural selection: an hierarchical expansion. Paleobiology 8, 113-129.
Ayala, F.J., 1966. Evolution of fitness. 1. Improvement in the productivity and size of irradiated populations of Drosophila serrata and D. birchii. Genetics 53, 883-895.
Blick, J., 1977. Selection for traits which lower individual reproduction. J. Theor. Biol. 67, 597-601.
Bonner, J.T., 1980. THE EVOLUTION OF CULTURE IN ANIMALS. Princeton University Press, Princeton.
Boyd, R. and Richerson, P.J., 1985. CULTURE AND THE EVOLUTIONARY PROCESS. Chicago University Press, Chicago.
Brookfield, J.F.Y., Montgomery, E. and Langley, C.H., 1984. Apparent absence of transposable elements related to the P elements of D. melanogaster in other species of Drosophila. Nature 310, 330-332.
Brown, A.L., 1984. On the origin of the Alu family of repeated sequences. Nature 312, 106.
Bull, J.J. and Charnov, E.L., 1985. On irreversible evolution. Evolution 39, 1149-1155.
Bumpus, H.C., 1899. The elimination of the unfit as illustrated by the introduced sparrow, Passer domesticus. Biol. Lectures, Wood’s Hole Marine Biol. Sta. 6, 209-226
Cavalli-Sforza, L.L. and Feldman, M.W., 1981. CULTURAL TRANSMISSION AND EVOLUTION: A QUANTITATIVE APPROACH. Princeton University Press, Princeton.
Chao, L., Vargas, C., Spear, B.B. and Cox, E.C., 1983. Transposable elements as mutator genes in evolution. Nature 303, 633-635.
Charlesworth, B. and Charlesworth, D., 1983. The population dynamics of transposable elements. Genet. Res. 42, 1-27.
Crozier, R.H., 1979. Genetics of sociality. in SOCIAL INSECTS. Vol. 1, pp 223-286 H.R. Hermann, (Ed.). Academic Press, New York.
Crozier, R.H., 1982. On insects and insects: twists and turns in our understanding of the evolution of sociality. in THE BIOLOGY OF SOCIAL INSECTS, pp 4-10 M.D. Breed, C.D. Michener, H.E. Evans (Eds.). Proc. 9 Congr. IUSSI. Wesiview Press, Boulder, Colorado.
Crozier, R.H. and Page, R.E., 1985. On being the right size: male contributions and multiple mating in social Hymenoptera. Behav. Ecol. Sociobiol. 18, 105-115.
Crozier, R.H., Pamilo, P., Taylor, R.W. and Crozier, Y.C., 1986. Evolutionary patterns in some putative Australian species in the ant genus Rhytidoponera. Aust. J. Zool., 34, 535-560.
Davidson, E.H. and Britten, R.J., 1979. Regulation of gene expression: possible role of repetitive sequences. Science 204, 1052-1059.
Dawkins, R., 1976. THE SELFISH GENE, pp 12-21, 47, 213. Oxford University Press, Oxford.
Dawkins, R., 1982. THE EXTENDED PHENOTYPE, p 39. Freeman, San Francisco.
Dobzhansky, T., 1973. Nothing in biology makes any sense except in the fight of evolution. Amer, Biol. Teacher (March), 125-129.
Doolittle, W.F., 1982. Selfish DNA after fourteen months. in GENOME EVOLUTION, pp.3-28 G.A. Dover, R.S. Flavell (Eds). Academic Press, New York.
Doolittle, W.F., Kirkwood, T.9.L. and Dempster, M.A.H., 1984. Selfish DNAs with self-restraint. Nature 307, 501-502.
Doolittle, W.F. and Sapienza, C., 1980. Selfish genes, the phenotype paradigm and genome evolution. Nature 284, 601-603.
Dover, G.A., 1982. Molecular drive: a cohesive mode of species evolution. Nature 299, 111-117.
Dover, G.A., 1984. FORCES OF EVOLUTION. New York Acad. Sci., New York. [Not seen in the original.]
Dover, G.A., Brown, S., Coen, E., Dallas, J., Strachan, T. and Trick, M., 1982. The dynamics of genome evolution and species differentiation. in GENOME EVOLUTION, pp. 343-372 G.A. Dover, R.B. Flavell (Eds). Academic Press, New York.
Engels, W.R., 1983. The P family of transposable elements in Drosophila. Annu. Rev. Genet. 17, 315-344.
Economou-Pachnis, A. and Tsichlis, P.N., 1985. Insertion of an Alu SINE in the human homologue of the Mivi-2 locus. Nucleic Acid Res. 13, 8379-8387.
Finnegan, D.J., Will, B.H., Bayev, A.A., Bowcock, A.M. and Brown, L., 1982. Transposable elements in eukaryotes. in GENOME EVOLUTION, pp 29-40 G.A. Dover, R.B. Flavell (Eds). Academic Press, New York.
Flavell, A.J., 1984. Role of reverse transcription in the generation of extrachromosomal copia mobile genetic elements. Nature 310, 514-515.
Fleischer, R.C. and Johnston, R.F., 1982. Natural selection on body size and proportions in house sparrows. Nature 298, 747-749.
Gould, S.J., 1980. The evolutionary biology of constraint. Daedalus 109, 39-52.
Grime, J.P. and Mowforth, M.A. 1982. Variation in genome size – an ecological interpretation. Nature 299, 151-153.
Hamilton, W.D., 1963. The evolution of altruistic behavior. Amer. Nat. 97, 354-356.
Hamilton, W.D., 1964. The genetical evolution of social behaviour. I and II. J. Theoret. Biol. 7, 1-52.
Hamilton, W.D., 1972. Altruism and related phenomena, mainly in social insects. Annu. Rev. Ecol. Syst. 3, 193-232.
Hickey, D. A_ 1982. Selfish DNA: a sexually-transmitted nuclear parasite. Genetics 101, 519-531.
Hull, D.L., 1980. Individuality and selection. Annu. Rev. Ecol. Syst. 11, 311-332.
Hunt, J.A., Bishop, J.G. and Carson, H.L., 1984. Chromosomal mapping of a middle-repetitive DNA sequence in a cluster of five species of Hawaiian Drosophila. Proc. Nati. Acad. Sci., USA 81, 7146-7150.
Jacob, F., 1983. Molecular tinkering in evolution. in EVOLUTION FROM MOLECULES TO MEN, pp. 131-144 D.S. Bendall (Ed.). Cambridge University Press, Cambridge.
Johnston, R.F. and Selander, FIX, 1971. Evolution in the house sparrow. 11. Adaptive differentiation in North American populations. Evolution 25, 1-28.
Kaneshiro, K. and Vat, F.C., 1977. Natural hybridization between a sympatric pair of Hawaiian Drosophila. Amer. Nat. 111, 897-902.
Kaplan, N., Darden, T. and Langley, C.H., 1985. Evolution and extinction of transposable elements in Mendelian populations. Genetics 109, 459-480.
Kimura, M., 1983. THE NEUTRAL THEORY OF MOLECULAR EVOLUTION. Cambridge University Press, Cambridge.
LaBarbera, M., 1983. Why the wheels won’t go. Amer. Nat. 121, 395-408.
Lamb, B.C., 1984. The properties of meiotic gene conversion important in its effects on evolution. Heredity 53, 113-138.
Lamb, B.C., 1985. The relative importance of meiotic gene conversion, selection and mutation pressure, in population genetics and evolution. Genetica 67, 39-49.
Lande, R., 1981. The minimum number of genes contributing to quantitative variation between and within populations. Genetics 99, 541-553.
Lande, R. and Arnold, S.J., 1983. The measurement of selection on correlated characters. Evolution 37, 1210-1226.
Lumsden, C.A. and Wilson, E.O., 1981. GENES, MIND, AND CULTURE. THE COEVOLUTIONARY PROCESS. Harvard University Press, Cambridge.
Mackay, T. F. C., 1985. Transposable element-induced response to artificial selection in Drosophila melanogaster. Genetics 111, 351-374.
Maynard Smith, J., 1964. Group selection and kin selection. Nature 201, 1145-1147.
Maynard Smith, J., 1982. EVOLUTION AND THE THEORY OF GAMES. Cambridge University Press, Cambridge.
Maynard Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Godwin, B., Lande, R., Raup, D. and Wolpert, L., 1985. Developmental constraints and evolution. Quart. Rev. Biol. 60, 265-287.
Mikios, G.L.G., 1982. Sequencing and manipulating highly repeated DNA. in GENOME EVOLUTION, pp 41-68 G.A. Dover, R.B. Flavell (Eds). Academic Press, New York.
Mikios, G.L.G., 1985. Localized highly repetitive DNA sequences in vertebrate and invertebrate genomes. in MOLECULAR EVOLUTIONARY GENETICS, pp 241-321 R.J. Macintyre (Ed). Plenum, New York.
Monod, J., 1972. CHANCE AND NECESSITY. Vintage, New York.
Montgomery, E.A. and Langley, C.H., 1983. Transposable elements in Mendelian populations. II. Distribution of three copia-like elements in a natural population of Drosophila melanogaster. Genetics 104, 473-483.
Mortlake, R.P., 1983. Experiments in evolution using microorganisms. BioScience 33, 308-313.
Murphy, E.C., 1985. Bergmann’s Rule, seasonality, and geographic variation in body size of house sparrows. Evolution 39, 1327-1334.
Nagylaki, T. and Petes, T.D., 1982. Intrachromosomal gene conversion and the maintenance of sequence homogeneity among repeated genes. Genetics 100, 315-337.
Ohno, S., 1984. Birth of a unique enzyme from an alternative reading frame of the preexisted, internally repetitious coding sequence. Proc. Nati. Acad. Sci., USA 81, 2421-2425.
Ohta, T., 1985. A model of duplicative transposition and gene conversion for repetitive DNA families. Genetics 110, 513-524.
Ohta, T. and Dover, G.A., 1984. The cohesive population genetics of molecular drive. Genetics 108, 501-521.
Orgel, L.E. and Crick, F.H.C., 1980. Selfish DNA: the ultimate parasite. Nature 284, 604-607.
Paquin, C.E. and Adams, J., 1983. Relative fitness can decrease in evolving asexual populations of S. cerevisiae. Nature 306, 368-370.
Penny, D., 1983. Charles Darwin, gradualism and punctuated equilibria. Syst. Zool. 32, 72-74.
Penny, D. and Hendy, M.D., 1985. The use of tree comparison metrics. Syst. Zool. 34, 75-82.
Plotkin, H.C. and Odling-Smee, F.J., 1981. A multiple-level model of evolution and its implication for sociobiology. Behav. Brain Sci. 4, 225-268.
Raff, R.A. and Kaufman, T.C., 1983. EMBRYOS, GENES, AND EVOLUTION, pp 288-299, 319. Macmillan, New York.
Rogers, J.H., 1985. The origin and evolution of retroposons. Int. Rev. Cytol. 93, 187-279.
Rogers, J, 1986. The origin of retroposons. Nature 319, 725.
Rothstein, S.I. and Barash, D.P., 1983. Gene conflicts and the concepts of outlaw and sheriff alleles. J. Social. Biol. Struct. 6, 367-379.
Sang, J.H., 1984. GENETICS AND DEVELOPMENT, pp 8, 42, 46, 61. Longman, London.
Sapienza, C. and Doolittle, W.R, 1980. Genes are things you have whether you want them or not. Cold Spr. Harb. Symp. Quant. Biol. 45, 177-182.
Sharp, P.A., 1983. Conversion of RNA to DNA in mammals: Alu-like elements and pseudogenes. Nature 301, 471-472.
Simpson, G.G., 1964. THIS VIEW OF LIFE. Harcourt, Brace & World, New York.
Spradling, A.C. and Rubin, G.M., 1981. Drosophila genome organization: conserved and dynamic aspects. Annu. Rev. Genet. 15, 219-264.
Stent, G.S., 1972. Prematurity and uniqueness in scientific discovery. Sci. Amer. 227(6), 84-93.
Stent, G.S., 1978. Introduction: the limits of the naturalistic approach to morality. in MORALITY AS A BIOLOGICAL PHENOMENON, pp 13-22 G.S. Stent (Ed.). Dahlem Konferenzen, Abakon Verlagsgesellschaft, Berlin.
Syvanen, M., 1985. The evolutionary implications of mobile genetic elements. Annu. Rev. Genet. 18, 271-293.
Templeton, A.R., 1977. Analysis of head shape differences between two interfertile species of Hawaiian Drosophila. Evolution 31, 630-641.
Trivers, R.L., 1985. SOCIAL EVOLUTION. Benjamin/Cummings, Menlo Park, California.
Ullu, E. and Tschud, C., 1984. Alu sequences are processed 7SL RNA genes. Nature 312, 171-172.
Val, F.C., 1977. Genetic analysis of the morphological differences between two interfertile species of Hawaiian Drosophila. Evolution 31, 611-629.
Van Valen, L.M., 1983. Molecular selection. Evol. Theory 6, 297-298.
Wade, MJ., 1980a. Kin selection: its components. Science 210, 665-667.
Wade, M.J., 1980b. An experimental study of kin selection. Evolution 34, 844-855.
Wallace, B., 1981. BASIC POPULATION GENETICS, pp 552-553. Columbia University Press, New York.
Walsh, J.13., 1985. Interaction of selection and biased gene conversion in a multigene family. Proc. Natl. Acad. Sci. USA 82, 153-157.
Watson, J.D., 1977. MOLECULAR BIOLOGY OF THE GENE. Benjamin, New York.
Wilson, D.S., 1976. Evolution on the level of communities. Science 192, 1358-1360.
Wilson, E.O., 1971. THE INSECT SOCIETIES, p 320. Harvard University Press, Cambridge.
Wilson, E.O., 1975. SOCIOBIOLOGY. Harvard University Press, Cambridge.
Wittenberger, J.F., 1981. ANIMAL SOCIAL BEHAVIOR. Duxbury, Boston.
Wood, RJ. and Bishop, J.A., 1981. Insecticide resistance: populations and evolution. in GENETIC CONSEQUENCES OF MAN MADE CHANGE, pp 97-127. J.A. Bishop, L.M. Cook (Eds). Academic Press, New York.
Wyles, J.S., Kunkel, J.G. and Wilson, A.C., 1983. Birds, behavior, and anatomical evolution. Proc. Natl. Acad. Sci., USA 80, 4394-4397.
R. H. Crozier
School of Zoology
The University of New South Wales
P.O. Box 1
Kensington, NSW 2033
Return to Top