Population Bottlenecks in Quasispecies Dynamics
- 18 Citations
- 1.3k Downloads
Abstract
The characteristics of natural populations result from different stochastic and deterministic processes that include reproduction with error, selection, and genetic drift. In particular, population fluctuations constitute a stochastic process that may play a very relevant role in shaping the structure of populations. For example, it is expected that small asexual populations will accumulate mutations at a higher rate than larger ones. As a consequence, in any population the fixation of mutations is accelerated when environmental conditions cause population bottlenecks. Bottlenecks have been relatively frequent in the history of life and it is generally accepted that they are highly relevant for speciation. Although population bottlenecks can occur in any species, their effects are more noticeable in organisms that form large and heterogeneous populations, such as RNA viral quasispecies. Bottlenecks can also positively select and isolate particles that still keep the ability to infect cells from a disorganized population created by crossing the error threshold.
Keywords
Deleterious Mutation Vesicular Stomatitis Virus Population Bottleneck Compensatory Mutation Selection EquilibriumPreview
Unable to display preview. Download preview PDF.
References
- Andersson DI, Hughes D (1996) Muller’s ratchet decreases fitness of a DNA-based microbe. Proc Natl Acad Sci U S A 93:906–907PubMedGoogle Scholar
- Artenstein M, Miller WS (1966) Air sampling for respiratory disease agents in army recruits. Bacteriol Rev 30:571–572PubMedGoogle Scholar
- Ayala FJ, Escalante A, O’Huigin C, Klein J (1994)Molecular genetics of speciation and human origins. Proc Natl Acad Sci U S A 91:6787–6794PubMedGoogle Scholar
- Bachtrog D, Gordo I (2004) Adaptive evolution of asexual populations under Muller’s ratchet. Evolution 58:1403–1413PubMedGoogle Scholar
- Batschelet E, Domingo E, Weissmann C (1976) The proportion of revertant and mutant phage in a growing population, as a function of mutation and growth rate. Gene 1:27–32CrossRefPubMedGoogle Scholar
- Bell G (1988a) Recombination and the immortality of the germ line. J Evol Biol 1:67–82CrossRefGoogle Scholar
- Bell G (1988b) Sex and death in protozoa. The history of an obsession. Cambridge University Press, CambridgeGoogle Scholar
- Bergstrom CT, Pritchard JK (1998) Germline bottlenecks and the evolutionary maintenance of mitochondrial genomes. Genetics 149:2135–2146PubMedGoogle Scholar
- Bergstrom CT, McElhany P, Real LA (1999) Transmission bottlenecks as determinants of virulence in rapidly evolving pathogens. Proc Natl Acad Sci U S A 96:5095–5100PubMedGoogle Scholar
- Bull JJ, Badgett Mr, Rokyta D, Molineux IJ (2003) Experimental evolution yields hundreds of mutations in a functional viral genome. J Mol Evol 57:241–248CrossRefPubMedGoogle Scholar
- Burch CL, Chao L (2004) Epistasis and its relationship to canalization in the RNA virus phi 6. Genetics 167:559–567CrossRefPubMedGoogle Scholar
- Chao L (1990) Fitness of RNA virus decreased by Muller’s ratchet. Nature 348:454–455CrossRefPubMedGoogle Scholar
- Chao L, Hanley KA, Burch CL, Dahlberg C, Turner PE (2000) Kin selection and parasite evolution: higher and lower virulence with hard and soft selection. Quart Rev Biol 75:261–275CrossRefPubMedGoogle Scholar
- Charlesworth D, Morgan MT, Charlesworth B (1993) Mutation accumulation in finite outbreeding and inbreeding populations. Genet Res 61:39–56Google Scholar
- Clarke D, Duarte E, Moya A, Elena S, Domingo E, Holland JJ (1993) Genetic bottlenecks and population passages cause profound fitness differences in RNA viruses. J Virol 67:222–228PubMedGoogle Scholar
- Colato A, Fontanari JF (2001) Soluble model for the accumulation of mutations in asexual populations. Phys Rev Lett 87:238102CrossRefPubMedGoogle Scholar
- Crotty S, Cameron CE, Andino R (2001) RNA virus error catastrophe: direct molecular test by using ribavirin. Proc Natl Acad Sci U S A 98:6895–6900CrossRefPubMedGoogle Scholar
- Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper & Row, New YorkGoogle Scholar
- De la Peña M, Elena SF, Moya A (2000) Effect of deleterious mutation-accumulation of the fitness of RNA bacteriophage MS2. Evolution 54:686–691PubMedGoogle Scholar
- Drake JW, Holland JJ (1999) Mutation rates among RNA viruses. Proc Natl Acad Sci U S A 96:13910–13913CrossRefPubMedGoogle Scholar
- Duarte E, Clarke D, Moya A, Domingo E, Holland J (1992) Rapid fitness losses in mammalian RNA virus clones due to Muller’s ratchet. Proc Natl Acad Sci U S A 89:6015–6019PubMedGoogle Scholar
- Duarte EA, Clarke DK, Elena SF, Moya A, Domingo E, Holland JJ (1993) Manytrillionfold amplification of single RNA virus particles fails to overcome the Muller’s ratchet effect. J Virol 67:3620–3623PubMedGoogle Scholar
- Earl DJ, Deem MW (2004) Evolvability is a selectable trait. Proc Natl Acad Sci U S A 101:11531–11536CrossRefPubMedGoogle Scholar
- Eigen M (2002) Error catastrophe and antiviral strategy. Proc Natl Acad Sci U S A 99:13374–13376CrossRefPubMedGoogle Scholar
- Eigen M, Biebricher CK (1988) Sequence space and quasispecies distribution. In: E Domingo, JJ Holland, Ahlquist P (eds) Variability of RNA genomes, 1st edn. Vol III. CRC Press, Boca Raton, pp 211–245Google Scholar
- Eigen M, Schuster P (1979). The hypercycle: a principle of natural self-organization. Springer-Verlag, Berlin Heidelberg New YorkGoogle Scholar
- Elena SF (1999) Little evidence for synergism among deleterious mutations in a nonsegmented RNA virus. J Mol Evol 49:703–707PubMedGoogle Scholar
- Elena SF, Moya A (1999) Rate of deleterious mutation and the distribution of its effects on fitness in vesicular stomatitis virus. J Evol Biol 12:1078–1088CrossRefGoogle Scholar
- Elena SF, González-Candelas F, Novella IS, Duarte EA, Clarke DK, Domingo E, Holland JJ, Moya A (1996) Evolution of fitness in experimental populations of vesicular stomatitis virus. Genetics 142:673–679PubMedGoogle Scholar
- Elena SF, Dávila M, Novella IS, Holland JJ, Domingo E, Moya A (1998) Evolutionary dynamics of fitness recovery from the debilitating effects of Muller’s ratchet. Evolution 52:309–314Google Scholar
- Escarmís C, Dávila M, Charpentier N, Bracho A, Moya A, Domingo E (1996) Genetic lesions associated with Muller’s ratchet in an RNA virus. J Mol Biol 264:255–267CrossRefPubMedGoogle Scholar
- Escarmís C, Dávila M, Domingo E (1999) Multiple molecular pathways for fitness recovery of an RNA virus debilitated by operation of Muller’s ratchet. J Mol Biol 28:495–505Google Scholar
- Escarmís C, Gómez-Mariano G, Dávila M, Lázaro E, Domingo E (2002) Resistance to extinction of low fitness virus subjected to plaque-to-plaque transfers: diversification by mutation clustering. J Mol Biol 315:647–661CrossRefPubMedGoogle Scholar
- Ewald PW (1987) Transmission modes and evolution of the parasitism-mutualism continuum. Ann N Y Acad Sci 503:295–306PubMedGoogle Scholar
- Felsenstein J (1974) Evolutionary advantage of recombination. Genetics 78:737–756PubMedGoogle Scholar
- Fisher RA (1922) On the dominance ratio. Proc R Soc Edin 42:321–341Google Scholar
- Fisher RA (1930) The genetical theory of natural selection, 2nd edn. Clarendon, New YorkGoogle Scholar
- Froissart R, Wilke CO, Montville R, Remold SK, Chao L, Turner PE (2004) Co-infection weakens selection against epistatic mutations in RNA viruses. Genetics 168:9–19CrossRefPubMedGoogle Scholar
- Fry JD, Keightley PD, Heinsihn SL, Nuzhdin SV (1999) New estimates of the rates and effects of mildly deleterious mutation in Drosophila melanogaster. Proc Natl Acad Sci U S A 96:574–579CrossRefPubMedGoogle Scholar
- Funchain P, Yeung A, Stewart JL, Lin R, Slupska MM, Miller JH (2000) The consequences of growth of a mutator strain of Escherichia coli as measured by loss of function among multiple gene targets and loss of fitness. Genetics 154:959–970PubMedGoogle Scholar
- Gerone PJ, Couch RB, Ketter GV, Douglas RG, Derrenbacher EB, Knight V (1966) Assessment of experimental and natural viral aerosols. Bacteriol Rev 30:576–588PubMedGoogle Scholar
- Gordo I, Charlesworth B (2000) The degeneration of asexual haploid populations and the speed of Muller’s ratchet. Genetics 154:1379–1387PubMedGoogle Scholar
- Grande-Pérez A, Sierra S, Castro MG, Domingo E, Lowenstein PR (2002) Molecular indetermination in the transition to error catastrophe: systematic elimination of lymphocytic choriomeningitis virus through mutagenesis does not correlate linearly with large increases in mutant spectrum complexity. Proc Natl Acad Sci U S A 99:12938–12943PubMedGoogle Scholar
- Haigh J (1978) Accumulation of deleterious genes in a population — Muller’s ratchet. Theor Pop Biol 14:251–267CrossRefGoogle Scholar
- Haldane JBS (1924) A mathematical theory of natural and artificial selection. Part I. Trans Camb Phil Soc 23:19–41Google Scholar
- Haldane JBS (1927) A mathematical theory of natural and artificial selection. V. Selection and mutation. Proc Camb Phil Soc 23:838–844Google Scholar
- Harpending H, Rogers A (2000) Genetic perspectives on human origin and speciation. Annu Rev Genomics Human Genet 1:361–385Google Scholar
- Hovi T, Lindholm N, Savolainen C, Stenvik M, Burns C (2004) Evolution of wild-type 1 poliovirus in two healthy siblings excreting the virus over a period of 6 months. J Gen Virol 85:369–377CrossRefPubMedGoogle Scholar
- Huynen MA, Stadler PF, Fontana W (1996) Smoothness within ruggedness: the role of neutrality in adaptation. Proc Natl Acad Sci U S A 93:397–401CrossRefPubMedGoogle Scholar
- Kibota TT, Lynx M (1996) Estimate of the genomic mutation rate deleterious to overall fitness in E. coli. Nature 381:694–696CrossRefPubMedGoogle Scholar
- Kimura M, Maruyama T (1966) The mutational load with epistatic gene interactions in fitness. Genetics 54:1337–1351Google Scholar
- Kondrashov AS (1982) Selection against harmful mutations in large sexual and asexual populations. Genet Res 40:325–332PubMedGoogle Scholar
- Kondrashov AS (1994) Muller’s ratchet under epistatic selection. Genetics 136:1469–1473PubMedGoogle Scholar
- Lázaro E, Escarmís C, Domingo E, Manrubia SC (2002) Modeling viral genome fitness evolution associated with serial bottleneck events: evidence of stationary states of fitness. J Virol 76:8675–8681PubMedGoogle Scholar
- Lázaro E, Escarmis C, Pérez-Mercader J, Manrubia SC, Domingo E (2003) Resistance of virus to extinction on bottleneck passages: study of a decaying and fluctuating pattern of fitness loss. Proc Natl Acad Sci U S A 100:10830–10835PubMedGoogle Scholar
- Lea S, Hernández J, Blakemore W, Bricchi E, Curry S, Domingo E, Fry E, Ghazaleh RA, King A, Newman J, Stuart D, Mateu MG (1994) The structure and antigenicity of a type C foot-and-mouth disease virus. Structure 2:123–139CrossRefPubMedGoogle Scholar
- Lynch M, Gabriel W (1990) Mutation load and the survival of small populations. Evolution 44:1725–1737Google Scholar
- Maisnier-Patin S, Berg OG, Liljas L, Andersson DI (2002) Compensatory adaptation to the deleterious effect of antibiotic resistance in Salmonella typhimurium. Mol Microbiol 46:355–366CrossRefPubMedGoogle Scholar
- Manrubia SC, Lázaro E, Pérez-Mercader J, Escarmís C, Domingo E (2003) Fitness distributions in exponentially growing asexual populations. Phys Rev Lett 90:188102CrossRefPubMedGoogle Scholar
- Manrubia SC, Escarmís C, Domingo E, Lázaro E (2005) High mutation rates, bottlenecks, and robustness of RNA viral quasispecies. Gene 347:273–282CrossRefPubMedGoogle Scholar
- Mason PW, Grubman MJ, Baxt B (2003) Molecular basis of pathogenesis of FMDV. Virus Res 91:9–32CrossRefPubMedGoogle Scholar
- Maynard Smith J (1978) The evolution of sex. Cambridge University Press, CambridgeGoogle Scholar
- Muller HJ (1964) The relation of recombination to mutational advance. Mut Res 1:2–9Google Scholar
- Novella IS (2004) Negative effect of genetic bottlenecks on the adaptability of vesicular stomatitis virus. J Mol Biol 336:61–67CrossRefPubMedGoogle Scholar
- Novella IS, Ebendick-Corpus BE (2004) Molecular basis of fitness loss and fitness recovery in vesicular stomatitis virus. J Mol Biol 342:1423–1430PubMedGoogle Scholar
- Novella IS, Elena SF, Moya A, Domingo E, Holland JJ (1995a) Size of genetic bottlenecks leading to virus fitness loss is determined by mean initial population fitness. J Virol 69:2869–2872PubMedGoogle Scholar
- Novella IS, Duarte EA, Elena SF, Moya A, Domingo E, Holland JJ (1995b) Exponential increases of RNA virus fitness during large population transmissions. Proc Natl Acad Sci U S A 92:5841–5844PubMedGoogle Scholar
- Novella IS, Quer J, Domingo E, Holland JJ (1999) Exponential fitness gains of RNA virus populations are limited by bottleneck effects. J Virol 73:1668–1671PubMedGoogle Scholar
- Nowak MA, Anderson, RM, Mc Lean AR, Wolfs TF, Goudsmit J, May RM (1991) Antigenic diversity thresholds and the development of AIDS. Science 254:963–969PubMedGoogle Scholar
- Orr HA (2003) The distribution of fitness effects among beneficial mutations. Genetics 163:1519–1526PubMedGoogle Scholar
- Pang S, Schlesinger Y, Daar ES, Moudgil T, Ho DD, Chen ISY (1992) Rapid generation of sequence variation during primary HIV-infection. AIDS 6:453–460PubMedGoogle Scholar
- Pariente N, Airaksinen A, Domingo E (2003) Mutagenesis versus inhibition in the efficiency of extinction of foot-and-mouth disease virus. J Virol 77:7131–7138CrossRefPubMedGoogle Scholar
- Peck JR (1994) A ruby in the rubbish: beneficial mutations, deleterious mutations and the evolution of sex. Genetics 137:597–606PubMedGoogle Scholar
- Quer J, Huerta R, Novella IS, Tsimring L, Domingo E, Holland JJ (1996) Reproducible nonlinear population dynamics and critical points during replicative competitions of RNA virus quasispecies. J Mol Biol 264:465–471CrossRefPubMedGoogle Scholar
- Quer J, Hershey CL, Domingo E, Holland JJ, Novella IS (2001) Contingent neutrality in competing viral populations. J Virol 75:7315–7320CrossRefPubMedGoogle Scholar
- Rouzine IM, Wakeley J, Coffin JM (2003) The solitary wave of asexual evolution. Proc Natl Acad Sci U S A 100:587–592PubMedGoogle Scholar
- Sanjuán R, Moya A, Elena SF (2004) The contribution of epistasis to the architecture of fitness in an RNA virus. Proc Natl Acad Sci U S A 101:15376–15379PubMedGoogle Scholar
- Severson WE, Schmaljohn CS, Javadian A, Jonsson CB (2003) Ribavirin causes error catastrophe during Hantaan virus replication. J Virol 77:481–488PubMedGoogle Scholar
- Sierra S, Dávila M, Lowenstein PR, Domingo E (2000) Response of foot-and-mouth disease virus to increased mutagenesis. Influence of viral load and fitness in loss of infectivity J Virol 74:8316–8323CrossRefPubMedGoogle Scholar
- Stephan W, Chao L, Smale J (1993) The advance of Muller’s ratchet in a haploid asexual population: approximate solution based on diffusion theory. Genet Res 61:225–232PubMedGoogle Scholar
- Swetina J, Schuster P (1982) Self-replication with errors. A model for polynucleotide replication. Biophys Chem 16:329–345CrossRefPubMedGoogle Scholar
- Vassilieva LL, Hook AM, Lynch M (2000) The fitness effects of spontaneous mutations in Caenorhabditis elegans. Evolution 54:1234–1246PubMedGoogle Scholar
- Wagner GP, Gabriel W (1990) Quantitative variation in finite parthenogenetic populations: what stops Muller’s ratchet in the absence of recombination? Evolution 44:715–731Google Scholar
- Weaver SC, Brault AC, Kang W, Holland JJ (1999) Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J Virol 73:4316–4326PubMedGoogle Scholar
- Wilke CO (2003) Probability of fixation of an advantageous mutant in a viral quasispecies. Genetics 163:467–474PubMedGoogle Scholar
- Wilke CO, Wang JL, Ofria C, Lenski RE, Adami C (2001) Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature 412:331–333CrossRefPubMedGoogle Scholar
- Wilke CO, Lenski RE, Adami C (2003) Compensatory mutations cause excess of antagonistic epistasis in RNA secondary structure folding. BMC Evol Biol 3:3CrossRefPubMedGoogle Scholar
- Wilson DS, Pollock GB, Dugatkin LA (1992) Can altruism evolve in purely viscous populations? Evol Ecol 6:331–341CrossRefGoogle Scholar
- Wittke V, Robb TE, Thu HM, Nisalak A, Nimmanniyya S, Kalayanrooj S, Vaughn DW, Endy TP, Holmes EC, Aaskov JG (2002) Extinction and rapid emergence of strains of dengue 3 virus during an interepidemic period. Virology 301:148–156CrossRefPubMedGoogle Scholar
- Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159Google Scholar
- Wright S (1939) Statistical genetics in relation to evolution. Paris: HermannGoogle Scholar
- Yuste E, López-Galindez C, Domingo E (2000) Unusual distribution of mutations associated with serial bottleneck passages of human immunodeficiency virus type 1. J Virol 74:9546–9552CrossRefPubMedGoogle Scholar
- Yuste E, Sánchez-Palomino S, Casado C, Domingo E, López-Galíndez C (1999) Drastic fitness loss in human immunodeficiency virus type 1 upon serial bottleneck events. J Virol 73:2745–2751PubMedGoogle Scholar
- Yuste E, Bordería AV, Domingo E, López-Galíndez C (2005) Few mutations in the 5′ leader region mediate fitness recovery of debilitated human immunodeficiency type 1 viruses. J Virol 79:5421–5427PubMedGoogle Scholar
- Zeyl C, Mizesko M, de Visser JA (2001) Mutational meltdown in laboratory yeast populations. Evolution 55:909–917PubMedGoogle Scholar
- Zhang X-S, Wang J, Hill WG (2004) Redistribution of gene frequency and changes of genetic variation following a bottleneck in population size. Genetics 167:1475–1492PubMedGoogle Scholar