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Lecture 11 Molecular Evolution

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Lecture 11 Molecular Evolution Lecture 11 Molecular evolution Jim Watson, Francis Crick, and DNA Molecular Evolution 4 characteristics 1. c-value paradox 2. Molecular evolution is sometimes decoupled from morphological evolution 3. Molecular clock 4. Neutral theory of Evolution Molecular Evolution 1. c-value!!!!!! paradox Kb! ! Navicola (diatom) ! !! 35,000! Drosophila (fruitfly) ! !180,000! Gallus (chicken) ! ! 1,200,000! Cyprinus (carp) 1,700,000! Boa (snake) 2,100,000! Rattus (rat) 2,900,000! Homo (human) 3,400,000! Schistocerca (locust) 9,300,000! Allium (onion) 18,000,000! Lilium (lily) 36,000,000! Ophioglossum (fern) 160,000,000! Amoeba (amoeba) 290,000,000! Isochores Cold-blooded vertebrates L (low GC) Warm-blooded vertebrates L H1 L H2 L H3 (low GC) (high GC) Isochores - Chromatin structure - Time of replication - Gene types - Gene concentration - Retroviruses Warm-blooded vertebrates L H1 L H2 L H3 (low GC) (high GC) (Mb) GC, % GC, % Isochores of human chromosome 21 (Macaya et al., 1976) Costantini et al., 2006 Molecular Evolution 2. Molecular evolution is sometimes decoupled from morphological evolution Morphological Genetic Similarity Similarity 1. low low 2. high high 3. high low 4. low high Molecular Evolution Morphological Genetic Similarity Similarity 3. high low Living fossils Latimeria, Coelacanth Limulus, Horseshoe crab Molecular Evolution Morphological Genetic Similarity Similarity - distance between humans and chimpanzees is less than 4. low high between sibling species of Drosophila. - for example, from a sample of 11 proteins representing 1271 amino acids, only 5 differ between humans and chimps. - the other six proteins are identical in primary structure. - most proteins that have been sequenced exhibit no amino acid differences - e.g., alphaglobin Pan, Chimp Homo, Human Molecular clock - when the rates of silent substitution at a gene are compared to its rate of replacement substitution, the former typically exceeds the latter by a factor of 5-10. Conclusion: the majority of evolution involves the substitution of silent mutations – likely by random drift. - these observations led to the proposal of the neutral theory of molecular evolution in 1968 by Motoo Kimura. “the survival of the luckiest” Motoo Kimura 1924-1994" The neutral theory of molecular evolution 1. most mutations are harmful and thus removed by “negative” (or “purifying”) natural selection. 2. some mutations are neutral and thus accumulate in natural populations by random genetic drift. 3. very rarely, beneficial mutations occur and are fixed by “positive” Natural selection. 4. The rate of evolution of a molecule is determined by its degree of “functional constraint”. The neutral theory of molecular evolution 1. most mutations are harmful and thus removed by “negative” (or “purifying”) natural selection. 2. some mutations are neutral and thus accumulate in natural populations by random genetic drift. 3. very rarely, beneficial mutations occur and are fixed by “positive” Natural selection. 4. The rate of evolution of a molecule is determined by its degree of “functional constraint”. The neutral theory of molecular evolution 5. neutral mutations and random genetic drift are responsible for virtually all molecular evolution. -!this theory gave rise to a bitter dispute known as the neutralist- selectionist controversy. -!the controversy raged throughout the 1970’s and 1980’s and has not been satisfactorily resolved. -!the essence of this controversy is not whether natural selection or random genetic drift operate at the molecular level, but rather what is the relative importance of each. - Testing the validity of the neutral theory has been very difficult. “Classical” versus “balanced” views of genome structure • controversy began in the 1920’s with the establishment of two schools of genetics. • the “Naturalists” studied natural populations (e.g. Dobzhansky, Mayr). • the “Mendelians” studied genetics exclusively in the laboratory (e.g., Morgan, Sturtevant, Muller). Classical Balanced + + - + + + A1 B2 C1 D4 E3 F6 + + + + + + A3 B2 C4 D5 E5 - Most loci homozygous Most loci heterozygous for “wild type” alleles Polymorphism rare Polymorphism common + = “wild type” allele - = deleterious recessive allele Why is this distinction important? Classical Balanced Speciation Difficult Easy (mutation- (opportunity- limited) limited) Selection Purifying Balancing Population Inter > Intra Intra > Inter variation Polymorphism transient balanced (short-lived) (long-lived) Allozyme electrophoresis setup Starch gel stained for Phosphoglucomutase (Pgm) Extensive allozyme variation exists in nature Vertebrates (648 species) Extensive allozyme variation exists in nature… …so this confirms the balanced view? Vertebrates (648 species) NO! MOST POLYMORPHISMS MAY BE NEUTRAL! The neutral theory of molecular evolution • first proposed by Motoo Kimura in 1968. The neutral theory of molecular evolution • first proposed by Motoo Kimura in 1968. • two observations led Kimura to develop neutral theory: 1. “Excessive” amounts of protein (allozyme) polymorphism • this would impart a severe "segregational load" if adaptive. Example: sickle cell anemia A A A S S S Genotype Hb Hb Hb Hb Hb Hb Fitness 1-s 1 1-t s=0.12 t=0.86 Segregational load = st/(s + t) = 0.11 • this means that 11% of the population dies every generation because of this polymorphism! 2. The molecular clock • first reported by Zuckerkandl and Pauling in 1962. 2. The molecular clock • first reported by Zuckerkandl and Pauling in 1962. Method: 1.! Obtain homologous amino acid sequences from a group of taxa. 2. Estimate divergence times (from the fossil record) 3.! Assess relationship between protein divergence and evolutionary time. The molecular clock No. of amino α-globin gene in acid substitutions vertebrates 100! 200 300 400 500 Time (millions of years) The molecular clock ticks at different rates for synonymous and nonsynonymous mutations Kimura argued that the molecular clock reflects the action of random drift, not selection! No. of amino α-globin gene in acid substitutions vertebrates 100! 200 300 400 500 Time (millions of years) Main features of the neutral theory 1. The rate of protein evolution is roughly constant per site per year. - this is the "molecular clock" hypothesis. - why per site PER YEAR, not per site PER GENERATION? 2. Rate of substitution of neutral alleles equals the mutation rate to neutral alleles. • let µ = neutral mutation rate at a locus. • the rate of appearance of a neutral allele = 2Nµ. • the frequency of the new neutral allele = 1/2N. • this frequency represents the allele’s probability of fixation. 2. Rate of substitution of neutral alleles equals the mutation rate to neutral alleles. Rate of evolution = rate of appearance x probability of fixation = 2Nµ x 1/2N = µ • this rate is unaffected by population size! 3. Heterozygosity (H) levels are determined by the “neutral parameter”, 4Neµ. H = 4Neµ/(4Neµ + 1) 4. Rates of protein evolution vary with degree of selective constraint. • “selective constraint” represents the ability of a protein to “tolerate” random mutations. • for highly constrained molecules, most mutations are deleterious and few are neutral. • for weakly constrained molecules, more mutations are neutral and few are deleterious. Degree of constraint dictates rate of evolution α-globin No. of amino acid substitions histone H4 100! 200 300 400 500 Time (millions of years) high constraint → low µ → low H, slow rate of evolution low constraint → high µ → high H, fast rate of evolution Testing the neutral theory by studying DNA sequences 1. Comparisons of polymorphism and divergence • studying DNA sequences enables the comparison of replacement and silent mutations! N A E R T R D. melanogaster AAT GCG GAA CGG ACT CGT --C --- --- --- --- --- --- --- --- --- T-- --- D. simulans --- --C -T- --- --- --C --- --- -T- --- --- --C --- --- -T- --- --- --C N A E R T R D. melanogaster AAT GCG GAA CGG ACT CGT --C --- --- --- --- --- --- --- --- --- T-- --- D. simulans --- --C -T- --- --- --C --- --- -T- --- --- --C --- --- -T- --- --- --C Mutations are either: 1. fixed between species 2. polymorphic within species Mutations are also either: 1. silent 2. replacement Polymorphic Fixed Replacement a c Silent b d • the degree of selective constraint determines the ratio of a:b and c:d. • however, because polymorphism is a transient phase of molecular evolution, the neutral theory predicts that ratio a:b = ratio c:d ↑ ↑ short term evolution = long term evolution This is the McDonald-Kreitman test Two examples: 1. The alcohol dehydrogenase (Adh) locus in Drosophila melanogaster, D. yakuba and D. simulans polymorphic fixed replacement 2 7 silent 42 17 G = 7.43, P < 0.001 Conclusion: too many fixed replacements! Two examples: 2. The glucose-6-phosphate dehydrogenase (G6pdh) locus in D. melanogaster and D. simulans. polymorphic fixed replacement 2 21 silent 36 26 G = 19.0, P < 0.0001 Conclusion: too many fixed replacements! 2. Tests for positive selection • positive selection occurs when the rate of replacement substitution exceeds the rate of silent substitution. • although rare, is widely documented at two broad classes of genes: 1. Genes involved in host-pathogen interactions • notably the major histocompatibility complex (MHC) and pathogen surface coat proteins. 2. Genes functioning in reproduction • notably seminal fluid proteins and surface proteins on sperm and egg. Conclusion: Natural selection may be more important in directing molecular evolution than previously believed! Nearly Neutral Theory of Evolution Tomoko Ohta .
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