Molecular Evidence for Natural Selection

neutral theory, nearly neutral theory, population genetics ABSTRACT Our understandi ng of the causes of molec ular evolution is not as certain as it was a decade ago when Kimura's neutral theory appeared to explain major features of DNA conservation and change. The last ten years have seen the development of empirical approaches and statistical tests for detecting selec­ tion in DNA and a proliferation of data that challenge our current understanding of the molecular evolutionary process. We begin this review with a discussion of protein polymorphism and divergence: two major areas of research where the strictly neutral model cannot explain general patterns in the data. We then present a survey of statistical methods for detecting positive selection, which includes tests for balancing selection, for sequence convergence, and for un­ usually high rates of evolution that cannot be accounted for by neutral models. Finally, we present findings of a number of groups working on within- and between-species variation in Drosophila: These highlight the importance of adaptive evolution, purifying selection, and recombination in understanding levels and patterns of nucleotide variation.

[1]  B. Charlesworth,et al.  The effect of deleterious mutations on neutral molecular variation. , 1993, Genetics.

[2]  M. Nei,et al.  Extent of protein polymosphism and the neutral mutation theory , 1984 .

[3]  S. Easteal,et al.  Consistent variation in amino-acid substitution rate, despite uniformity of mutation rate: protein evolution in mammals is not neutral. , 1994, Molecular biology and evolution.

[4]  J H Gillespie,et al.  Variability of evolutionary rates of DNA. , 1986, Genetics.

[5]  M. Nei,et al.  Statistical studies on protein polymorphism in natural populations. I. Distribution of single locus heterozygosity. , 1977, Genetics.

[6]  J. Gillespie SUBSTITUTION PROCESSES IN MOLECULAR EVOLUTION. II. EXCHANGEABLE MODELS FROM POPULATION GENETICS , 1994, Evolution; international journal of organic evolution.

[7]  G. Moore,et al.  Molecular Evolution in the Descent of Man , 1971, Nature.

[8]  N L Kaplan,et al.  The coalescent process in models with selection. , 1988, Genetics.

[9]  M. Goodman,et al.  Globins: a case study in molecular phylogeny. , 1987, Cold Spring Harbor symposia on quantitative biology.

[10]  S. Yokoyama,et al.  Convergent evolution of the red- and green-like visual pigment genes in fish, Astyanax fasciatus, and human. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[11]  T. Ohta Further examples of evolution by gene duplication revealed through DNA sequence comparisons. , 1994, Genetics.

[12]  Wen-Hsiung Li,et al.  Low nucleotide diversity in man. , 1991, Genetics.

[13]  V. Vacquier,et al.  The Divergence of Species-Specific Abalone Sperm Lysins is Promoted by Positive Darwinian Selection. , 1992, The Biological bulletin.

[14]  M. Goodman The role of immunochemical differences in the phyletic development of human behavior. , 1961, Human biology.

[15]  M. Aguadé,et al.  Genetic uniformity in two populations of Drosophila melanogaster as revealed by filter hybridization of four-nucleotide-recognizing restriction enzyme digests. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[16]  G. A. Watterson Mutant substitutions at linked nucleotide sites , 1982, Advances in Applied Probability.

[17]  M. Nei,et al.  Positive Darwinian selection promotes charge profile diversity in the antigen-binding cleft of class I major-histocompatibility-complex molecules. , 1990, Molecular biology and evolution.

[18]  D. Hartl,et al.  Selection intensity for codon bias. , 1994, Genetics.

[19]  C. Aquadro Molecular Population Genetics of Drosophila , 1993 .

[20]  J. Avise,et al.  Balancing selection at allozyme loci in oysters: implications from nuclear RFLPs. , 1992, Science.

[21]  T. Dobzhansky Genetics of the Evolutionary Process , 1970 .

[22]  D. Hartl,et al.  Population genetics of polymorphism and divergence. , 1992, Genetics.

[23]  J H Gillespie,et al.  The molecular clock may be an episodic clock. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[24]  R. Hudson Gene genealogies and the coalescent process. , 1990 .

[25]  M. Choudhary,et al.  A Comprehensive Study of Genic Variation in Natural Populations of Drosophila melanogaster. III. Variations in Genetic Structure and Their Causes between Drosophila melanogaster and Its Sibling Species Drosophila simulans. , 1987, Genetics.

[26]  M. Nei,et al.  Testing the neutral mutation hypothesis by distribution of single locus heterozygosity , 1976, Nature.

[27]  R. Lewontin,et al.  A molecular approach to the study of genic heterozygosity in natural populations. I. The number of alleles at different loci in Drosophila pseudoobscura. , 1966, Genetics.

[28]  T. Blundell,et al.  Is the evolution of insulin Darwinian or due to selectively neutral mutation? , 1975, Nature.

[29]  R. Hudson,et al.  Inferring the evolutionary histories of the Adh and Adh-dup loci in Drosophila melanogaster from patterns of polymorphism and divergence. , 1991, Genetics.

[30]  H. Spencer,et al.  The maintenance of single-locus polymorphism. IV. Models with mutation from existing alleles. , 1992, Genetics.

[31]  W. Ewens Population Genetics Theory - The Past and the Future , 1990 .

[32]  H. Harris C. Genetics of Man Enzyme polymorphisms in man , 1966, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[33]  R. Lewontin,et al.  A molecular approach to the study of genic heterozygosity in natural populations. IV. Patterns of genic variation in central, marginal and isolated populations of Drosophila pseudoobscura. , 1969, Genetics.

[34]  M. Nei Genetic polymorphism and the role of mutation in evolution , 1983 .

[35]  M. Kreitman,et al.  Molecular analysis of an allozyme cline: alcohol dehydrogenase in Drosophila melanogaster on the east coast of North America. , 1993, Genetics.

[36]  J. Crow,et al.  Mutation rate and dominance of genes affecting viability in Drosophila melanogaster. , 1972, Genetics.

[37]  C. Aquadro,et al.  Molecular population genetics of the distal portion of the X chromosome in Drosophila: evidence for genetic hitchhiking of the yellow-achaete region. , 1991, Genetics.

[38]  T. Ohta THE NEARLY NEUTRAL THEORY OF MOLECULAR EVOLUTION , 1992 .

[39]  M. Nei Molecular Evolutionary Genetics , 1987 .

[40]  T. Ota,et al.  Positive selection is a general phenomenon in the evolution of abalone sperm lysin. , 1995, Molecular biology and evolution.

[41]  R. Lewontin,et al.  A molecular approach to the study of genic heterozygosity in natural populations. II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura. , 1966, Genetics.

[42]  N. Takahata,et al.  On the overdispersed molecular clock. , 1987, Genetics.

[43]  D. Skibinski,et al.  A quantitative test of the neutral theory using pooled allozyme data. , 1993, Genetics.

[44]  J. Oakeshott,et al.  Nucleotide variation at the hypervariable esterase 6 isozyme locus of Drosophila simulans. , 1995, Molecular biology and evolution.

[45]  H. Akashi,et al.  Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA. , 1995, Genetics.

[46]  N L Kaplan,et al.  The "hitchhiking effect" revisited. , 1989, Genetics.

[47]  T MUKAI,et al.  THE GENETIC STRUCTURE OF NATURAL POPULATIONS OF DROSOPHILA MELANOGASTER. I. SPONTANEOUS MUTATION RATE OF POLYGENES CONTROLLING VIABILITY. , 1964, Genetics.

[48]  C. Aquadro,et al.  Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster , 1992, Nature.

[49]  F J Ayala,et al.  Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster. , 1994, Genetics.

[50]  W. Eanes,et al.  Evidence for adaptive evolution of the G6pd gene in the Drosophila melanogaster and Drosophila simulans lineages. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[51]  W. B. Watt,et al.  Allozymes in evolutionary genetics: self-imposed burden or extraordinary tool? , 1994, Genetics.

[52]  R. Lewontin,et al.  Heterosis as an explanation for large amounts of genic polymorphism. , 1978, Genetics.

[53]  J. Gillespie The causes of molecular evolution , 1991 .

[54]  M. Nei,et al.  Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[55]  F. Tajima Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. , 1989, Genetics.

[56]  M. Nei,et al.  Statistical Studies on Protein Polymorphism in Natural Populations. III. Distribution of Allele Frequencies and the Number of Alleles per Locus. , 1980, Genetics.

[57]  J. Ajioka,et al.  Lack of polymorphism on the Drosophila fourth chromosome resulting from selection. , 1991, Genetics.

[58]  J. Klein,et al.  MHC polymorphism pre-dating speciation , 1988, Nature.

[59]  M. Kimura,et al.  The neutral theory of molecular evolution. , 1983, Scientific American.

[60]  N L Kaplan,et al.  The coalescent process in models with selection and recombination. , 1988, Genetics.

[61]  J H Gillespie,et al.  Lineage effects and the index of dispersion of molecular evolution. , 1989, Molecular biology and evolution.

[62]  Wen-Hsiung Li,et al.  The molecular clock runs more slowly in man than in apes and monkeys , 1987, Nature.

[63]  W. Fitch,et al.  Positive Darwinian evolution in human influenza A viruses. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[64]  J. Kingman,et al.  Mathematics of genetic diversity , 1982 .

[65]  W. Li,et al.  Rates of nucleotide substitution are evidently higher in rodents than in man. , 1987, Molecular biology and evolution.

[66]  T. Ohta,et al.  Amino acid substitution at the Adh locus of Drosophila is facilitated by small population size. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[67]  Wen-Hsiung Li,et al.  Fundamentals of molecular evolution , 1990 .

[68]  A. Wilson,et al.  Sequence convergence and functional adaptation of stomach lysozymes from foregut fermenters. , 1987, Cold Spring Harbor symposia on quantitative biology.