Do clones degenerate over time? Explaining the genetic variability of asexuals through population genetic models

. 2011 Mar 03 ; 6 () : 17. [epub] 20110303

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid21371316

BACKGROUND: Quest for understanding the nature of mechanisms governing the life span of clonal organisms lasts for several decades. Phylogenetic evidence for recent origins of most clones is usually interpreted as proof that clones suffer from gradual age-dependent fitness decay (e.g. Muller's ratchet). However, we have shown that a neutral drift can also qualitatively explain the observed distribution of clonal ages. This finding was followed by several attempts to distinguish the effects of neutral and non-neutral processes. Most recently, Neiman et al. 2009 (Ann N Y Acad Sci.:1168:185-200.) reviewed the distribution of asexual lineage ages estimated from a diverse array of taxa and concluded that neutral processes alone may not explain the observed data. Moreover, the authors inferred that similar types of mechanisms determine maximum asexual lineage ages in all asexual taxa. In this paper we review recent methods for distinguishing the effects of neutral and non-neutral processes and point at methodological problems related with them. RESULTS AND DISCUSSION: We found that contemporary analyses based on phylogenetic data are inadequate to provide any clear-cut answer about the nature and generality of processes affecting evolution of clones. As an alternative approach, we demonstrate that sequence variability in asexual populations is suitable to detect age-dependent selection against clonal lineages. We found that asexual taxa with relatively old clonal lineages are characterised by progressively stronger deviations from neutrality. CONCLUSIONS: Our results demonstrate that some type of age-dependent selection against clones is generally operational in asexual animals, which cover a wide taxonomic range spanning from flatworms to vertebrates. However, we also found a notable difference between the data distribution predicted by available models of sequence evolution and those observed in empirical data. These findings point at the possibility that processes affecting clonal evolution differ from those described in recent studies, suggesting that theoretical models of asexual populations must evolve to address this problem in detail. REVIEWERS: This article was reviewed by Isa Schön (nominated by John Logsdon), Arcady Mushegian and Timothy G. Barraclough (nominated by Laurence Hurst).

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Kondrashov AS. Classification of hypotheses on the advantage of amphimixis. J Hered. 1993;84:372–383. PubMed

West SA, Lively CM, Read AF. A pluralist approach to sex and recombination. J Evol Biol. 1999;12:1003–1012. doi: 10.1046/j.1420-9101.1999.00119.x. DOI

Paland S, Lynch M. Transitions to asexuality result in excess amino-acid substitutions. Science. 2006;311:990–992. doi: 10.1126/science.1118152. PubMed DOI

Neiman M, Hehman G, Miller JT, Logsdon JM Jr, Taylor DR. Accelerated Mutation Accumulation in Asexual Lineages of a Freshwater Snail. Mol Biol Evol. 2010;27:954–63. doi: 10.1093/molbev/msp300. PubMed DOI PMC

Guex GD, Hotz H, Semlitsch RD. Deleterious alleles and differential viability in progeny of natural hemiclonal frogs. Evolution. 2002;56:1036–1044. PubMed

Schön I, Martens K. No slave to sex. Proc R Soc Lond, B, Biol Sci. 2003;B 22:827–833. PubMed PMC

Mee MA, Rowe L. A comparison of parasite load in sexual and asexual Phoxinus (Pisces: Cyprinidae) Can J Zool. 2006;84:808–816. doi: 10.1139/Z06-064. DOI

Birky CW Jr, Wolf C, Maughan H, Herbertson L, Henry E. Speciation and selection without sex. Hydrobiologia. 2005;546:29–45. doi: 10.1007/s10750-005-4097-2. DOI

Loewe L, Lamatsch DK. Quantifying the threat of extinction from Muller's ratchet in the diploid Amazon molly (Poecilia Formosa) BMC Evolutionary Biology. 2008;8:88. doi: 10.1186/1471-2148-8-88. PubMed DOI PMC

Janko K, Culling MA, Rab P, Kotlik P. Ice age cloning - comparison of the Quaternary evolutionary histories of sexual and clonal forms of spiny loaches (Cobitis : Teleostei) using the analysis of mitochondrial DNA variation. Mol Ecol. 2005;14:2991–3004. doi: 10.1111/j.1365-294X.2005.02583.x. PubMed DOI

Law JH, Crespi BJ. Recent and ancient asexuality in Timema walkingsticks. Evolution. 2002;56:1711–1717. PubMed

Neiman A, Jokela J, Lively CM. Variation in asexual lineage age in Potamopyrgus antipodarum, a New Zealand snail. Evolution. 2005;59:1945–1952. PubMed

Janko K, Drozd P, Flegr J, Pannell J. Clonal turnover versus clonal decay: A null model for observed patterns of asexual longevity, diversity and distribution. Evolution. 2008;62:1264–1270. doi: 10.1111/j.1558-5646.2008.00359.x. PubMed DOI

Neigel JE, Avise JC. Application of a random walk-model to geographic distributions of animal mitochondrial DNA variation. Genetics. 1993;135:1209–1220. PubMed PMC

Schwander T, Crespi BJ. Twigs on the tree of life? Neutral and selective models for integrating macroevolutionary patterns with microevolutionary processes in the analysis of asexuality. Mol Ecol. 2009;18:28–42. doi: 10.1111/j.1365-294X.2008.03992.x. PubMed DOI

Birky CW, Jr, Barraclough TG. In: Lost Sex. VanDijk P, Martens K, Schön I, editor. Springer; 2009. Asexual speciation; pp. 201–216. full_text.

Neiman A, Meirmans S, Meirmans PG. What Can Asexual Lineage Age Tell Us about the Maintenance of Sex? The Year in Evolutionary Biology 2009: Ann NY Acad Sci. 2009;1168:185–200. doi: 10.1111/j.1749-6632.2009.04572.x. PubMed DOI

Javaux EI. In: Eukaryotic Membranes and Cytoskeleton: Origins and Evolution. GPJ~Kely, editor. Landes Bioscience and Springer Science + Business Media; 2007. The Early Eukaryotic Fossil Record; pp. 1–15. full_text.

R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2008. http://www.R-project.org

Šizling A, Storch D, Reif J, Gaston KJ. Invariance in species-abundance distributions. Theor Ecol. 2009;2:89–103.

McGill BJ. A test of the unified neutral theory of biodiversity. Nature. 2003;422:881–885. doi: 10.1038/nature01583. PubMed DOI

Preston FW. Pseudo-lognormal distributions. Ecology. 1981;62:355–364. doi: 10.2307/1936710. DOI

Glathart JL, Preston FW. Theory of the behaviour of glassware in service. J Am Ceramic Society. 1948;31:153–170. doi: 10.1111/j.1151-2916.1948.tb14284.x. DOI

Akaike H. A new look at the statistical model identification. IEEE Trans Automat Contr. 1974;19:716–723. doi: 10.1109/TAC.1974.1100705. DOI

Stadler T. On incomplete sampling under birth-death models and connections to the sampling-based coalescent. J Theor Biol. 2009;261:58–66. doi: 10.1016/j.jtbi.2009.07.018. PubMed DOI

Kimura M, Crow JF. The number of alleles that can be maintained in a finite population. Genetics. 1964;49:725–738. PubMed PMC

Angers B, Schlosser IJ. The origin of Phoxinus eos-neogaeus unisexual hybrids. Mol Ecol. 2007;16:4562–4571. doi: 10.1111/j.1365-294X.2007.03511.x. PubMed DOI

Arnaud-Haond S, Duarte CM, Alberto F, Serrao EA. Standardizing methods to address clonality in population studies. Mol Ecol. 2007;16:5115–5139. doi: 10.1111/j.1365-294X.2007.03535.x. PubMed DOI

Higgs P, Woodcock G. The accumulation of mutations in asexual populations and the structure of genealogical trees in the presence of selection. J Math Biol. 1995;33:677–702. doi: 10.1007/BF00184644. DOI

Gordo I, Navarro A, Charlesworth B. Muller's ratchet and the pattern of variation at a neutral locus. Genetics. 2002;161:835–847. PubMed PMC

Charlesworth B, Morgan MT, Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993;134:1289–1303. PubMed PMC

Martens K, Loxdale HD, Schön I. In: Lost Sex. VanDijk P, Martens K, Schön I, editor. Springer; 2009. The Elusive Clone - In Search of Its True Nature and Identity; pp. 187–200. full_text.

Combadao J, Campos PRA, Dionisio F, Gordo I. Small-world networks decrease the speed of Muller's ratchet. Genet Res. 2007;89:7–18. doi: 10.1017/S0016672307008658. PubMed DOI

Bachtrog D. Evidence that positive selection drives the Y-chromosome degeneration in Drosophila miranda. Nat Genet. 2004;36:518–522. doi: 10.1038/ng1347. PubMed DOI

Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:585–595. PubMed PMC

Fu Y-X, Li W-H. Statistical tests of neutrality of mutations. Genetics. 1993;133:693–709. PubMed PMC

Ramos-Onsins SE, Rozas J. Statistical Properties of New Neutrality Tests Against Population Growth. Mol Biol Evol. 2002;19:2092–2100. PubMed

Avise JC, Quattro JM, Vrijenhoek RC. Molecular clones within organismal clones. Evol Biol. 1992;26:225–246.

Janko K, Bohlen J, Lamatsch D, Flajšhans M, Kotlík P, Ráb P, Šlechtová V. Evidence for gynogenesis as the reproductive mode of hybrid loaches (Cobitis: Teleostei): on the evolution of polyploidy in asexual vertebrates. Genetica. 2007;131:185–194. doi: 10.1007/s10709-006-9130-5. PubMed DOI

Balsano JS, Rasch EM, Monaco PJ. In: Ecology and Evolution of Livebearing Fishes (Poeciliidae) Meffe G, Snelson FF Jr, editor. Englewood Cliffs, NJ: Prentice Hall; 1989. The evolutionary ecology of Poecilia formosa and its triploid associate; pp. 277–297.

Alves MJ, Coelho MM, Collares-Pereira MJ. Evolution on action through hybridization and polyploidy in an Iberian freshwater fish: a genetic review. Genetica. 2001;111:375–385. doi: 10.1023/A:1013783029921. PubMed DOI

Pongratz N, Storhas M, Carranza S, Michiels NK. Phylogeography of competing sexual and parthenogenetic forms of a freshwater flatworm: patterns and explanations. BMC Evol Biol. 2003;3:23. doi: 10.1186/1471-2148-3-23. PubMed DOI PMC

Galtier N, Depaulis F, Barton NH. Detecting bottlenecks and selective sweeps from DNA sequence polymorphism. Genetics. 2000;155:981–987. PubMed PMC

Lessa EP, Cook JA, Patton JL. Genetic footprints of demographic expansion in North America, but not Amazonia, during the Late Quaternary. Proc Natl Acad Sci USA. 2003;100:10031–10034. doi: 10.1073/pnas.1730921100. PubMed DOI PMC

Bazin E, Glemin S, Galtier N. Population size does not influence mitochondrial genetic diversity in animals. Science. 2006;312:570–572. doi: 10.1126/science.1122033. PubMed DOI

Wendel JF. Genome evolution in polyploids. Plant Mol Biol. 2000;42:225–249. doi: 10.1023/A:1006392424384. PubMed DOI

Farraway J. Linear Models with R. Boca Raton, London, New York, Washington D.C.: Chapman & Hall/CRC; 2005.

Sakamoto Y, Ishiguro M, Kitagawa G. Akaike Information Criterion Statistics. D Reidel Publishing Company; 1986.

Anderson DR. Model Based Inference in the Life Sciences: A Primer on Evidence. Springer Science+Business Media, LLC; 2008.

Beerli P, Felsenstein J. Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA. 2001;98:4563–4568. doi: 10.1073/pnas.081068098. PubMed DOI PMC

Nielsen R, Wakeley J. Distinguishing Migration From Isolation: A Markov Chain Monte Carlo Approach. Genetics. 2001;158:885–896. PubMed PMC

Teshima KM, Tajima F. The Effect of Migration during the Divergence. Theor Popul Biol. 2002;62:81–95. doi: 10.1006/tpbi.2002.1580. PubMed DOI

Wilkinson-Herbots HM. The distribution of the coalescence time and the number of pairwise nucleotide differences in the "isolation with migration" model. Theor Popul Biol. 2008;73:277–288. doi: 10.1016/j.tpb.2007.11.001. PubMed DOI

Ciofi C, Beaumont MA, Swingland IR, Bruford MW. Genetic divergence and units for conservation in the Komodo dragon Varanus komodoensis. Proc R Soc Lond, B, Biol Sci. 1999;266:2269–2274. doi: 10.1098/rspb.1999.0918. DOI

Butlin RK, Schön I, Martens K. Origin, age and diversity of clones - Commentary. J Evol Biol. 1999;12:1020–1022. doi: 10.1046/j.1420-9101.1999.00126.x. DOI

Lynch M, Burger R, Butcher D, Gabriel W. The mutational meltdown in asexual populations. J Hered. 1993;84:339–344. PubMed

Jain K. Loss of Least-Loaded Class in Asexual Populations Due to Drift and Epistasis. Genetics. 2008;179:2125–2134. doi: 10.1534/genetics.108.089136. PubMed DOI PMC

De Visser J, Elena S. The evolution of sex: empirical insights into the roles of epistasis and drift. Nat Rev Genet. 2007;8:139–149. doi: 10.1038/nrg1985. PubMed DOI

Pannell JR. Coalescence in metapopulation with recurrent local extinction and recolonisation. Evolution. 2003;57:949–961. PubMed

Swofford DL. PAUP* Phylogenetic Analysis Using Parsimony (*and Other Methods) Sinauer Associates, Sunderland, Massachusetts; 1999.

Rozas J, Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999;15:174–175. doi: 10.1093/bioinformatics/15.2.174. PubMed DOI

Schaeffer SW. Molecular population genetics of sequence length diversity in the Adh region of Drosophila pseudoobscura. Genet Res Camb. 2002;80:163–175. doi: 10.1017/S0016672302005955. PubMed DOI

Robertson AV, Ramsden C, Niedzwiecki J, Fu J, Bogart JP. An unexpected recent ancestor of unisexual Ambystoma. Mol Ecol. 2006;15:3339–3351. doi: 10.1111/j.1365-294X.2006.03005.x. PubMed DOI

Cunha C, Coelho MM, Carmona JA, Doadrio I. Phylogeographical insights into the origins of the Squalius alburnoides complex via multiple hybridization events. Mol Ecol. 2004;13:2807–2817. doi: 10.1111/j.1365-294X.2004.02283.x. PubMed DOI

Paland S, Colbourne JK, Lynch M. Evolutionary history of contagious asexuality in Daphnia pulex. Evolution. 2005;59:800–813. PubMed

Adams M, Foster R, Hutchinson MN, Hutchinson RG, Donnellan SC. The Australian lizard Menetia greyi: a new instance of widespread vertebrate parthenogenesis. Evolution. 2003;57:2619–2627. PubMed

Johnson SG. Geographical ranges, population structure, and ages of sexual and parthenogenetic snail lineages. Evolution. 2006;60:1417–1426. PubMed

Mantovani B, Passamonti M, Scali V. The Mitochondrial Cytochrome Oxidase II Gene in Bacillus Stick Insects: Ancestry of Hybrids, Androgenesis, and Phylogenetic Relationships. Mol Phyl Evol. 2001;19:157–163. doi: 10.1006/mpev.2000.0850. PubMed DOI

Provencher LM, Morse GE, Weeks AR, Normark BB. Parthenogenesis in the Aspidiotus nerii complex (Hemiptera: Diaspididae): a single origin of a worldwide, polyphagous lineage associated with Cardinium bacteria. Ann Entomol Soc Am. 2005;98:629–635. doi: 10.1603/0013-8746(2005)098[0629:PITANC]2.0.CO;2. DOI

Möller D. PhD thesis. University of Hamburg; 2001. Aspekte zur Populationsgenetik des eingeschlechtlichen Amazonenkärpflings/Poecilia formosa /(Girard 1859) unter Berücksichtigung der genetischen parentalen Arten, dem Breitflossenkärpfling/Poecilia latipinna /(LeSueur 1821) und dem Atlantikkärpfling/Poecilia mexicana,/Steindachner 1863.

Kearney M, Blacket MJ. The evolution of sexual and parthenogenetic Warramaba: a window onto Plio-Pleistocene diversification processes in an arid biome. Mol Ecol. 2008;17:5257–5275. doi: 10.1111/j.1365-294X.2008.03991.x. PubMed DOI

Scali V. Revision of the Iberian stick insect genus Leptynia Pantel and description of the new genus Pijnackeria. Ital J Zool (Modena) 2009;76:381–391. doi: 10.1080/11250000802702062. DOI

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