Genomika adaptacji

• Authors: Mateusz Stanisław Konczal

Title variants

EN

Adaptation genomics.

• Languages of publication: PL EN

Abstracts

PL

Genomika adaptacji to multidyscyplinarny projektem badawczy, którego celem jest zidentyfikowanie wzorców genomowych związanych z procesem adaptacji. W poniższym artykule staram się zapoznać czytelników z podstawowymi pojęciami związanymi z zagadnieniem genomiki adaptacji. Badania w tym obszarze można podzielić na trzy grupy: laboratoryjne eksperymenty naśladujące naturalne procesy ewolucyjne, badania nad konwergencją i paralelizmem oraz badania prowadzone na całych genomach poszukujące związku alleli z wybranymi cechami. Różne podejścia badawcze wiążą się z koniecznością zróżnicowanej interpretacji uzyskiwanych wyników. W poniższym artykule omawiam szczegółowo te trzy podejścia oraz podaję przykłady prac związanych z konkretną strategią badawczą. Następnie uogólniam uzyskane wyniki, czego wynikiem jest obraz adaptacji jako skomplikowanego na poziomie molekularnym procesu. Powtarzalność adaptacji można zaobserwować na poziomie szlaków metabolicznych; liczba fragmentów genomu ewoluująca pod wpływem działania doboru pozytywnego jest większa niż sądzono wcześniej; niestety inne problemy pozostają jednak wciąż bez satysfakcjonującej odpowiedzi.

EN

Adaptation genomics is a multidisciplinary research program, which aims at detecting genomic patterns resulting from the process of adaptation. Studies in this field can be divided into 3 groups: laboratory experiments that model evolutionary processes, studies on convergence and parallelism and genome wide association studies. Results from particular scientific approaches should be interpreted in different ways. The three approaches accompanied by examples are discussed in detail and then I try to draw some generalizations, which indicate that adaptation is a complex process, also at the molecular level . Repeatability of adaptation is evident at the level of metabolic pathways and large number of genes in genome evolve under positive selection. Unfortunately other problems remain unresolved. Basic terminology related to the field of adaptation genomics is introduced.

• Journal: Kosmos
• Year: 2013
• Volume: 62
• Issue: 1
• Pages: 13-29

Dates

published

2013

Contributors

author

Mateusz Stanisław Konczal

• Instytut Nauk o Środowisku Uniwersytet Jagielloński Gronostajowa 7, 30-387 Kraków, Polska

References

• Akey J. M., 2009. Constructing genomic maps of positive selection in humans: Where do we go from here? Genome Res. 19, 711-722.
• Araya C. L., Payen C., Dunham M. J., Fields S., 2010. Whole-genome sequencing of a laboratory-evolved yeast strain. BMC Genomics 11.
• Atwell S., Huang Y. S., Vilhjálmsson B. J., Willems G., Horton M., Li Y., Meng D., Platt A., Tarone A. M., Hu T. T., Jiang R., Muliyati N. W., Zhang X., Amer M. A., Baxter I., Brachi B. i współaut., 2010. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465, 627-631.
• Barrett R. D. H., Hoekstra H. E., 2011. Molecular spandrels: tests of adaptation at the genetic level. Nat. Rev. Genet. 12, 767-780.
• Barrett R. D. H., Rogers S. M., Schluter D., 2008. Natural selection on a major armor gene in threespine stickleback. Science 322, 255-257.
• Barrick J. E., Yu D. S., Yoon S. H., Jeong H., Oh T. K., Schneider D., Lenski R. E., Kim J. F., 2009. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461, 1243-1247.
• Begun D. J., Holloway A. K., Stevens K., Hillier L.W., Poh Y. P., Hahn M. W., Nista P. M., Jones C. D., Kern A. D., Dewey C. N., Pachter L., Myers E., Langley C. H., 2007. Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biology 5.
• Bell M. A., Orti G., Walker J. A., Koenings J. P., 1993. Evolution of Pelvic Reduction in Threespine Stickleback Fish - a Test of Competing Hypotheses. Evolution 47, 906-914.
• Bersaglieri T., Sabeti P. C., Patterson N., Vanderploeg T., Schaffner S. F., Drake J. A., Rhodes M., Reich D. E., Hirschhorn J. N., 2004. Genetic signatures of strong recent positive selection at the lactase gene. Am. J. Human Genet. 74, 1111-1120.
• Biswas S., Akey J. M., 2006. Genomic insights into positive selection. Trends Genet. 22, 437-446.
• Burke M. K., Dunham J. P., Shahrestani P., Thornton K. R., Rose M. R., Long A. D., 2010. Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467, 587-590.
• Cao J., Schneeberger K., Ossowski S., Guenther T., Bender S., Fitz J., Koenig D., Lanz C., Stegle O., Lippert C., Wang X., Ott F., Mueller J., Alonso-Blanco C., Borgwardt K., Schmid K. J., Weigel D., 2011. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat. Genet. 43, 956-963.
• Chan Y. F., Marks M. E., Jones F. C., Villarreal G. Jr., Shapiro M. D., Brady S. D., Southwick A. M., Absher D. M., Grimwood J., Schmutz J., Myers R. M., Petrov D., Jonsson B., Schluter D., Bell M. A., Kingsley D. M., 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327, 302-305.
• Conrad T. M., Joyce A. R., Applebee M. K., Barrett C. L., Xie B., Gao Y., Palsson B. T., 2009. Whole-genome resequencing of Escherichia coli K-12 MG1655 undergoing short-term laboratory evolution in lactate minimal media reveals flexible selection of adaptive mutations. Genome Biology 10.
• Derome N., Bernatchez L., 2006. The transcriptomics of ecological convergence between 2 limnetic coregonine fishes salmonidae. Mol. Biol. Evol. 23, 2370-2378.
• Dettman J. R., Rodrigue N., Melnyk A. H., Wong A., Bailey S. F., Kassen R., 2012. Evolutionary insight from whole-genome sequencing of experimentally evolved microbes. Mol. Ecol. 21, 2058-2077.
• Diz A. P., Martínez-Fernández M., Rolán-Alvarez E., 2012. Proteomics in evolutionary ecology: Linking the genotype with the phenotype. Mol. Ecol. 21, 1060-1080.
• Ellegren H., Sheldon B. C., 2008. Genetic basis of fitness differences in natural populations. Nature 452, 169-175.
• Elmer K. R., Meyer A., 2011. Adaptation in the age of ecological genomics: Insights from parallelism and convergence. Trends Ecol. Evol. 26, 298-306.
• Fay J. C., Wu C. I., 2000. Hitchhiking under positive Darwinian selection. Genetics 155, 1405-1413.
• Fay J. C., Wyckoff G. J., Wu C. I., 2002. Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature 415, 1024-1026.
• Fisher R. A., 1930. Genetical theory of natural selection. Oxford Univeristy Press, Oxford.
• Flint J., Mackay T. F. C., 2009. Genetic architecture of quantitative traits in mice, flies, and humans. Genome Res. 19, 723-733.
• Foster S. A., Baker J. A., 2004. Evolution in parallel: new insights from a classic system. Trends Ecol. Evol. 19, 456-459.
• Fraser H. B., 2011. Genome-wide approaches to the study of adaptive gene expression evolution: Systematic studies of evolutionary adaptations involving gene expression will allow many fundamental questions in evolutionary biology to be addressed. BioEssays 33, 469-477.
• Fumagalli M., Sironi M., Pozzoli U., Ferrer-Admettla A., Pattini L., Nielsen R., 2011. Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLoS Genetics 7.
• Futuyma D. J., 2008. Ewolucja. Wydawnictwo Uniwersytetu Warszawskiego, Warszawa.
• Garland T. Jr., Kelly S.A., 2006. Phenotypic plasticity and experimental evolution. J. Exp. Biol. 209, 2344-2361.
• Gibson G., 2012. Rare and common variants: Twenty arguments. Nat. Rev. Genet. 13, 135-145.
• Hamblin M. T., Di Rienzo A., 2000. Detection of the signature of natural selection in humans: Evidence from the Duffy blood group locus. Am. J. Human Genet. 66, 1669-1679.
• Harbison S. T., Chang S., Kamdar K. P., Mackay T. F., 2005. Quantitative genomics of starvation stress resistance in Drosophila. Genome Biology 6.
• Harvey P. H., Pagel M. D., 1991. The comparative method in evolutionary biology. Oxford University Press, Oxford.
• Hedrick P. W., 2011. Population genetics of malaria resistance in humans. Heredity 107, 283-304.
• Hermisson J., Pennings P. S., 2005. Soft sweeps: Molecular population genetics of adaptation from standing genetic variation. Genetics 169, 2335-2352.
• Hernandez R. D., Kelley J. L., Elyashiv E., Melton S. C., Auton A., McVean G., Sella G., Przeworski M., 2011. Classic selective sweeps were rare in recent human evolution. Science 331, 920-924.
• Herring C. D., Raghunathan A., Honisch C., Patel T., Applebee M. K., Joyce A. R., Albert T. J., Blattner F. R., van den Boom D., Cantor C. R., Palsson B. O., 2006. Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nature Genet. 38, 1406-1412.
• Hohenlohe P. A., Bassham S., Etter P. D., Stiffer N., Johnson E. A., 2010 Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genetics 6.
• Hudson R. R., Kreitman M., Aguadé M., 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116, 153-159.
• Hughes A. L., 2011. Evolution of adaptive phenotypic traits without positive Darwinian selection. Heredity 108, 347-353.
• Jeffery W. R., 2009. Regressive evolution in astyanax cavefish. Ann. Rev. Genet. 43, 25-47.
• Jones F. C., Grabherr M. G., Chan Y. F., Russell P., Mauceli E., Johnson J., Swofford R., Kingsley D. M., 2012. The genomic basis of adaptive evolution in treespine sticklebacks. Nature 484, 55-61.
• Karasov T., Messer P. W., Petrov D. A., 2010. Evidence that Adaptation in Drosophila Is Not Limited by Mutation at Single Sites. PLoS Genetics 6.
• Kimura M., 1983. The neutral theory of molecular evolution. Cambridge University Press, New York.
• Kondrashov F. A., Kondrashov A. S., 2010. Measurements of spontaneous rates of mutations in the recent past and the near future. Philosoph.Transact. Royal Soc. B: Biol. Sci. 365, 1169-1176.
• Korona R., 2009. Granice adapcjonizmu. Kosmos 58, 395-402.
• Lee D. H., Palsson B. O., 2010. Adaptive evolution of escherichia coli K-12 MG1655 during growth on a nonnative carbon source, L-l,2-propanediol. Appl. Environ. Microbiol. 76, 4158-4168.
• Lenski R. E., Rose M. R., Simpson S. C., Tadler S. C., 1991. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2000 generations. Am Natural 138, 1315-1341.
• Linnen C. R., Kingsley E. P., Jensen J. D., Hoekstra H. E., 2009. On the origin and spread of an adaptive allele in deer mice. Science 325, 1095-1098.
• Lohmueller K. E., Albrechtsen A., Li Y., Kim S. Y., Korneliussen T., Vinckenbosch N., Tian G., Huerta-Sanchez E., Feder A. F., Grarup N., Jørgensen T., Jiang T., Witte D. R., Sandbæk A., Hellmann I., Lauritzen T., Hansen T., Pedersen O., Wang J., Nielsen R., 2011. Natural selection affects multiple aspects of genetic variation at putatively neutral sites across the human genome. PLoS Genetics 7.
• Losos J. B., 2011. Convergence, adaptation, and constraint. Evolution 65, 1827-1840.
• Manceau M., Domingues V. S., Linnen C. R., Rosenblum E. B., Hoekstra H. E., 2010. Convergence in pigmentation at multiple levels: Mutations, genes and function. Philosoph.Transact. Royal Soc. B: Biol. Sci. 365, 2439-2450.
• Manolio T. A., Collins F. S., Cox N. J., Goldstein D. B., Hindorff L. A., Hunter D. J., McCarthy M. I., Ramos E. M., Cardon L. R., Chakravarti A., Cho J. H., Guttmacher A. E., Kong A., Kruglyak L., Mardis E., Rotimi C. N., Slatkin M., Valle D., Whittemore A. S., Boehnke M., Clark A. G., Eichler E. E., Gibson G., Haines J. L., MacKay T. F. C., McCarroll S. A., Visscher P. M., 2009. Finding the missing heritability of complex diseases. Nature 461, 747-753.
• Maynard Smith J., Haigh J., 1974. The hitch-hiking effect of favourable gene. Genet. Res. 23, 23-35.
• McDonald J. H., Kreitman M., 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652-654.
• Merilä J., Sheldon B. C., 1999. Genetic architecture of fitness and nonfitness traits: Empirical patterns and development of ideas. Heredity 83, 103-109.
• Mezey J. G., Houle D., 2005. The dimensionality of genetic variation for wing shape in Drosophila melanogaster. Evolution 59, 1027-1038.
• Morran L. T., Schmidt O. G., Gelarden I. A., Parrish Ii R. C., Lively C. M., 2011. Running with the Red Queen: Host-parasite coevolution selects for biparental sex. Science 333, 216-218.
• Mortazavi A., Williams B. A., McCue K., Schaeffer L., Wold B., 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5, 621-628.
• Muller H. J., 1932. Some genetic aspects of sex. Am. Natural. 66, 118-138.
• Nadeau N. J., Jiggins C. D., 2010. A golden age for evolutionary genetics? Genomic studies of adaptation in natural populations. Trends Genet. 26, 484-492.
• Nei M., 2005. Selectionism and neutralism in molecular evolution. Mol. Biol. Evol. 22, 2318-2342.
• Nei M., Gojobori T., 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol.Evol. 3, 418-426.
• Nielsen R., Hellmann I., Hubisz M., Bustamante C., Clark A. G., 2007. Recent and ongoing selection in the human genome. Nature Rev. Genet. 8, 857-868.
• Oleksyk T. K., Smith M. W., O'Brien S. J., 2010. Genome-wide scans for footprints of natural selection. Philosoph.Transact. Royal Soc. B: Biol. Sci. 365, 185-205.
• Orr H. A., 1998. The population genetics of adaptation: The distribution of factors fixed during adaptive evolution. Evolution 52, 935-949.
• Robertson A., 1967. The nature of quantitative genetic variation. [W:] Heritage from Mendel. Brink R. A., Styles E. D., University of Wisconsis Press, Madison, 265-280.
• Rockman M. V., 2012. The QTN program and the alleles that matter for evolution: All that's gold does not glitter. Evolution 66, 1-17.
• Rokyta D. R., Joyce P., Caudle S. B., Wichman H. A., 2005. An empirical test of the mutational landscape model of adaptation using a single-stranded DNA virus. Nature Genet. 37, 441-444.
• Sabeti P. C., Reich D. E., Higgins J. M., Levine H. Z. P., Richter D. J., Schaffner S. F., Gabriel S. B., Platko J. V., Patterson N. J., McDonald G. J., Ackerman H. C., Campbell S. J., Altshuler D., Cooper R., Kwiatkowski D., Ward R., Lander E. S., 2002. Detecting recent positive selection in the human genome from haplotype structure. Nature 419, 832-837.
• Shendure J., Porreca G. J., Reppas N. B., Lin X., McCutcheon J. P., Rosenbaum A. M., Wang M. D., Zhang K., Mitra R. D., Church G. M., 2005. Molecular biology: Accurate multiplex polony sequencing of an evolved bacterial genome. Science 309, 1728-1732.
• Stapley J., Reger J., Feulner P. G. D., Smadja C., Galindo J., Ekblom R., Bennison C., Ball A. D., Beckerman A. P., Slate J., 2010. Adaptation genomics: The next generation. Trends Ecol. Evol. 25, 705-712.
• Stern D. L., Orgogozo V., 2008. The loci of evolution: How predictable is genetic evolution? Evolution 62, 2155-2177.
• Stern D. L., Orgogozo V., 2009. Is genetic evolution predictable? Science 323(5915): 746-751
• Stranger B. E., Stahl E. A., Raj T., 2011. Progress and promise of genome-wide association studies for human complex trait genetics. Genetics 187, 367-383.
• Tajima F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585-595.
• Taylor E. B., McPhail J. D., 2000. Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus. Proc Royal Soc London, Ser. B: Biol. Sci. 267, 2375-2384.
• Tenaillon O., Rodríguez-Verdugo A., Gaut R. L., McDonald P., Bennett A. F., Long A. D., Gaut B. S., 2012. The molecular diversity of adaptive convergence. Science 335, 457-461.
• Teotónio H., Chelo I. M., Bradić M., Rose M. R., Long A. D., 2009. Experimental evolution reveals natural selection on standing genetic variation. Nature Genetics 41, 251-257.
• Toomajian C., Hu T. T., Aranzana M. J., Lister C., Tang C., Zheng H., Zhao K., Calabrese P., Dean C., Nordborg M., 2006. A nonparametric test reveals selection for rapid flowering in the Arabidopsis genome. PLoS Biology 4, 732-738.
• Turner T. L., Stewart A. D., Fields A. T., Rice W. R., Tarone A. M., 2011. Population-based resequencing of experimentally evolved populations reveals the genetic basis of body size variation in Drosophila melanogaster. PLoS Genetics 7.
• Wang L., Spira B., Zhou Z., Feng L., Maharjan R. P., Li X., Li F., McKenzie C., Reeves P. R., Ferenci T., 2010. Divergence involving global regulatory gene mutations in an Escherichia coli population evolving under phosphate limitation. Genome Biol. Evol. 2, 478-487.
• Weir B. S., Cockerham C. C., 1984. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358-1370.
• Wilson R. H., Morgan T. J., Mackay T. F. C., 2006. High-resolution mapping of quantitative trait loci affecting increased life span in Drosophila melanogaster. Genetics 173, 1455-1463.