1932

Abstract

Bottlenecks in population size can reduce fitness and evolutionary potential, yet introduced species often become invasive. This poses a dilemma referred to as the genetic paradox of invasion. Three characteristics must hold true for an introduced population to be considered paradoxical in this sense. First, it must pass through a bottleneck that reduces genetic variation. Second, despite the bottleneck, the introduced population must not succumb to the many problems associated with low genetic variation. Third, it must adapt to the novel environment. Some introduced populations are not paradoxical as they do not combine these conditions. In some cases, an apparent paradox is spurious, as seen in introduced populations with low diversity in neutral markers that maintain high genetic variation in ecologically relevant traits. Even when the genetic paradox is genuine, unique aspects of a species' biology can allow a population to thrive. We propose research directions into remaining paradoxical aspects of invasion genetics.

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2016-11-01
2024-04-23
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Literature Cited

  1. Alcala N, Jensen JD, Telenti A, Vuilleumier S. 2016. The genomic signature of population reconnection following isolation: from theory to HIV. G3 6:107–20 [Google Scholar]
  2. Allendorf FW, Lundquist LL. 2003. Introduction: population biology, evolution, and control of invasive species. Conserv. Biol. 17:24–30 [Google Scholar]
  3. Armbruster P, Bradshaw WE, Holzapfel CM. 1998. Effects of postglacial range expansion on allozyme and quantitative genetic variation of the pitcher-plant mosquito, Wyeomyia smithii. Evolution 52:1697–704 [Google Scholar]
  4. Avila V, Amador C, Garcia-Dorado A. 2010. The purge of genetic load through restricted panmixia in a Drosophila experiment. J. Evol. Biol. 23:1937–46 [Google Scholar]
  5. Baker HG, Stebbins GL. 1965. The Genetics of Colonizing Species New York: Academic
  6. Barrett RDH, Schluter D. 2008. Adaptation from standing genetic variation. Trends Ecol. Evol. 23:38–44 [Google Scholar]
  7. Barrett SCH, Charlesworth D. 1991. Effects of a change in the level of inbreeding on the genetic load. Nature 352:522–24 [Google Scholar]
  8. Barton NH, Charlesworth B. 1984. Genetic revolutions, founder effects, and speciation. Annu. Rev. Ecol. Syst. 15:133–64 [Google Scholar]
  9. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C. 2004. Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427:164–67 [Google Scholar]
  10. Bock DG, Caseys C, Cousens RD, Hahn MA, Heredia SM. et al. 2015. What we still don't know about invasion genetics. Mol. Ecol. 24:2277–97 [Google Scholar]
  11. Bonduriansky R, Day T. 2009. Nongenetic inheritance and its evolutionary implications. Annu. Rev. Ecol. Evol. Syst. 40:103–25 [Google Scholar]
  12. Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D. 2005. Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11 [Google Scholar]
  13. Capy P, Gasperi G, Biemont C, Bazin C. 2000. Stress and transposable elements: co-evolution or useful parasites?. Heredity 85:101–6 [Google Scholar]
  14. Casacuberta E, González J. 2013. The impact of transposable elements in environmental adaptation. Mol. Ecol. 22:1503–17 [Google Scholar]
  15. Colautti RI, Lau JA. 2015. Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Mol. Ecol. 24:1999–2017 [Google Scholar]
  16. Cornuet JM, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M. et al. 2014. DIYABC v2.0: A software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30:1187–89 [Google Scholar]
  17. Cristescu ME. 2015. Genetic reconstructions of invasion history. Mol. Ecol. 24:2212–25 [Google Scholar]
  18. Crnokrak P, Barrett SCH. 2002. Perspective: purging the genetic load: a review of the experimental evidence. Evolution 56:2347–58 [Google Scholar]
  19. Danchin E, Charmantier A, Champagne FA, Mesoudi A, Pujol B, Blanchet S. 2011. Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nat. Rev. Genet. 12:475–86 [Google Scholar]
  20. Davidson AM, Jennions M, Nicotra AB. 2011. Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecol. Lett. 14:419–31 [Google Scholar]
  21. Des Marais DL, Hernandez KM, Juenger TE. 2013. Genotype-by-environment interaction and plasticity: exploring genomic responses of plants to the abiotic environment. Annu. Rev. Ecol. Evol. Syst. 44:5–29 [Google Scholar]
  22. Dlugosch KM, Anderson SR, Braasch J, Cang FA, Gillette H. 2015. The devil is in the details: genetic variation in introduced populations and its contributions to invasion. Mol. Ecol. 24:2095–111 [Google Scholar]
  23. Dlugosch KM, Parker IM. 2008. Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol. Ecol. 17:431–49 [Google Scholar]
  24. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM. et al. 2012. Widespread dynamic DNA methylation in response to biotic stress. PNAS 109:E2183–91 [Google Scholar]
  25. Duggan IC, Rixon CAM, MacIsaac HJ. 2006. Popularity and propagule pressure: determinants of invasion success in aquarium fish. Biol. Invasions 8:393–98 [Google Scholar]
  26. Edmonds CA, Lillie AS, Cavalli-Sforza LL. 2004. Mutations arising in the wave front of an expanding population. PNAS 101:975–79 [Google Scholar]
  27. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K. et al. 2011. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLOS ONE 6:e19379 [Google Scholar]
  28. Estoup A, Guillemaud T. 2010. Reconstructing routes of invasion using genetic data: why, how and so what?. Mol. Ecol. 19:4113–30 [Google Scholar]
  29. Excoffier L, Dupanloup I, Huerta-Sánchez E, Sousa VC, Foll M. 2013. Robust demographic inference from genomic and SNP data. PLOS Genet 9:e1003905 [Google Scholar]
  30. Facon B, Genton B, Shykoff J, Jarne P, Estoup A, David P. 2006. A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol. Evol. 21:130–35 [Google Scholar]
  31. Facon B, Hufbauer RA, Tayeh A, Loiseau A, Lombaert E. et al. 2011. Inbreeding depression is purged in the invasive insect Harmonia axyridis. Curr. Biol. 21:424–27 [Google Scholar]
  32. Facon B, Pointier JP, Jarne P, Sarda V, David P. 2008. High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Curr. Biol. 18:363–67 [Google Scholar]
  33. Fauvergue X, Vercken E, Malausa T, Hufbauer RA. 2012. The biology of small, introduced populations, with special reference to biological control. Evol. Appl. 5:424–43 [Google Scholar]
  34. Flori L, Fritz S, Jaffrézic F, Boussaha M, Gut I. et al. 2009. The genome response to artificial selection: a case study in dairy cattle. PLOS ONE 4:e6595 [Google Scholar]
  35. Fountain T, Duvaux L, Horsburgh G, Reinhard K, Butlin RK. 2014. Human-facilitated metapopulation dynamics in an emerging pest, Cimex lectularius. Mol. Ecol. 23:1071–84 [Google Scholar]
  36. Gaines TA, Zhang W, Wang D, Bukun B, Chisholm ST. et al. 2010. Gene amplification confers glyphosate resistance in Amaranthus palmeri. PNAS 107:1029–34 [Google Scholar]
  37. Gandon S, Hochberg ME, Holt RD, Day T. 2013. What limits the evolutionary emergence of pathogens?. Philos. Trans. R. Soc. B 368:20120086 [Google Scholar]
  38. García Guerreiro MP, Chávez-Sandoval BE, Balanyà J, Serra L, Fontdevila A. 2008. Distribution of the transposable elements bilbo and gypsy in original and colonizing populations of Drosophila subobscura. BMC Evol. Biol. 8:234 [Google Scholar]
  39. García Guerreiro MP, Fontdevila A. 2011. Osvaldo and Isis retrotransposons as markers of the Drosophila buzzatii colonization in Australia. BMC Evol. Biol. 11:111 [Google Scholar]
  40. Gardner A, West SA. 2010. Greenbeards. Evolution 64:25–38 [Google Scholar]
  41. Gautier M. 2015. Genome-wide scan for adaptive divergence and association with population-specific covariates. Genetics 201:1555–79 [Google Scholar]
  42. Gautier M, Foucaud J, Gharbi K, Cezard T, Galan M. et al. 2013. Estimation of population allele frequencies from next-generation sequencing data: pooled versus individual genotyping. Mol. Ecol. 22:3766–79 [Google Scholar]
  43. Glémin S. 2003. How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57:2678–87 [Google Scholar]
  44. Gomulkiewicz R, Holt RD, Barfield M, Nuismer SL. 2010. Genetics, adaptation, and invasion in harsh environments. Evol. Appl. 3:97–108 [Google Scholar]
  45. Gonzalez A, Ronce O, Ferriere R, Hochberg ME. 2013. Evolutionary rescue: an emerging focus at the intersection between ecology and evolution. Philos. Trans. R. Soc. B 368:161020120404 [Google Scholar]
  46. González J, Lenkov K, Lipatov M, Macpherson JM, Petrov DA. 2008. High rate of recent transposable element-induced adaptation in Drosophila melanogaster. PLOS Biol. 6:e251 [Google Scholar]
  47. Goodnight CJ. 1988. Epistasis and the effect of founder events on the additive genetic variance. Evolution 42:441–54 [Google Scholar]
  48. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD. 2009. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLOS Genet. 5:e1000695 [Google Scholar]
  49. Hallatschek O, Nelson DR. 2010. Life at the front of an expanding population. Evolution 64:193–206 [Google Scholar]
  50. Heilbron K, Toll-Riera M, Kojadinovic M, MacLean RC. 2014. Fitness is strongly influenced by rare mutations of large effect in a microbial mutation accumulation experiment. Genetics 197:981–90 [Google Scholar]
  51. Helanterä H, Strassmann JE, Carrillo J, Queller DC. 2009. Unicolonial ants: Where do they come from, what are they and where are they going?. Trends Ecol. Evol. 24:341–49 [Google Scholar]
  52. Hill WG. 2007. Impact of selection on effective population size: a commentary on “Inbreeding in artificial selection programmes” by Alan Robertson. Genet. Res. 89:273–74 [Google Scholar]
  53. Hirase S, Ozaki H, Iwasaki W. 2014. Parallel selection on gene copy number variations through evolution of three-spined stickleback genomes. BMC Genom. 15:735 [Google Scholar]
  54. Holt RD, Barfield M, Gomulkiewicz R. 2005. Theories of niche conservatism and evolution: Could exotic species be potential tests?. Species Invasions: Insights into Ecology, Evolution, and Biogeography DF Sax, JJ Stachowicz, SD Gaines 259–90 Sunderland, MA: Sinauer [Google Scholar]
  55. Holt RD, Gomulkiewicz R, Barfield M. 2003. The phenomenology of niche evolution via quantitative traits in a “black-hole” sink. Proc. R. Soc. B 270:215–24 [Google Scholar]
  56. Hufbauer RA, Facon B, Ravigné V, Turgeon J, Foucaud J. et al. 2012. Anthropogenically induced adaptation to invade (AIAI): Contemporary adaptation to human-altered habitats within the native range can promote invasions. Evol. Appl. 5:89–101 [Google Scholar]
  57. Hufbauer RA, Rutschmann A, Serrate B, Vermeil de Conchard H, Facon B. 2013. Role of propagule pressure in colonization success: disentangling the relative importance of demographic, genetic and habitat effects. J. Evol. Biol. 26:1691–99 [Google Scholar]
  58. Jablonka E. 2013. Epigenetic inheritance and plasticity: the responsive germline. Prog. Biophys. Mol. Biol. 111:99–107 [Google Scholar]
  59. Keller SR, Taylor DR. 2008. History, chance, and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection. Ecol. Lett. 8:852–56 [Google Scholar]
  60. Kingsolver JG, Diamond SE, Siepielski AM, Carlson SM. 2012. Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions. Evol. Ecol. 26:1101–18 [Google Scholar]
  61. Kinoshita T, Jacobsen SE. 2012. Opening the door to epigenetics in PCP. Plant Cell Physiol. 53:763–65 [Google Scholar]
  62. Kirkpatrick M, Jarne P. 2000. The effect of a bottleneck on inbreeding depression and the genetic load. Am. Nat. 155:154–67 [Google Scholar]
  63. Knopp T, Cano JM, Crochet PA, Marila J. 2007. Contrasting levels of variation in neutral and quantitative genetic loci on island populations of moor frogs (Rana arvalis). Conserv. Genet. 8:45–56 [Google Scholar]
  64. Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JB. 2004. Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–81 [Google Scholar]
  65. Krieger MJB, Ross KG. 2002. Identification of a major gene regulating complex social behavior. Science 295:328–32 [Google Scholar]
  66. Lande R. 1980. Genetic variation and phenotypic evolution during allopatric speciation. Am. Nat. 116:463–79 [Google Scholar]
  67. Lande R. 2009. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J. Evol. Biol. 22:1435–46 [Google Scholar]
  68. Lande R. 2015. Evolution of phenotypic plasticity in colonizing species. Mol. Ecol. 24:2038–45 [Google Scholar]
  69. Lavergne S, Molofsky J. 2007. Increased genetic variation and evolutionary potential drive the success of an invasive grass. PNAS 104:3883–88 [Google Scholar]
  70. Lee CE, Gelembiuk GW. 2008. Evolutionary origins of invasive populations. Evol. Appl. 1:427–48 [Google Scholar]
  71. Lee CE, Remfert JL, Chang Y-M. 2007. Response to selection and evolvability of invasive populations. Genetica 129:179–92 [Google Scholar]
  72. Leider SA, Hulett PL, Loch JJ, Chilcote MW. 1990. Electrophoretic comparison of the reproductive success of naturally spawning transplanted and wild steelhead trout through the returning adult stage. Aquaculture 88:239–52 [Google Scholar]
  73. Leniaud L, Pichon A, Uva P, Bagneres AG. 2009. Unicoloniality in Reticulitermes urbis: a novel feature in a potentially invasive termite species. Bull. Entomol. Res. 99:1–10 [Google Scholar]
  74. Li YF, Costello JC, Holloway AK, Hahn MW. 2008. “Reverse ecology” and the power of population genomics. Evolution 62:2984–94 [Google Scholar]
  75. Liebl AL, Martin LB. 2012. Exploratory behaviour and stressor hyper-responsiveness facilitate range expansion of an introduced songbird. Proc. R. Soc. B 279:4375–81 [Google Scholar]
  76. Liebl AL, Schrey AW, Richards CL, Martin LB. 2013. Patterns of DNA methylation throughout a range expansion of an introduced songbird. Integr. Comp. Biol. 53:351–58 [Google Scholar]
  77. Lotterhos KE, Whitlock MC. 2014. Evaluation of demographic history and neutral parameterization on the performance of FST outlier tests. Mol. Ecol. 23:2178–92 [Google Scholar]
  78. Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science 290:1151–55 [Google Scholar]
  79. Martin G, Aguilée R, Ramsayer J, Kaltz O, Ronce O. 2013. The probability of evolutionary rescue: towards a quantitative comparison between theory and evolution experiments. Philos. Trans. R. Soc. B 368:161020120088 [Google Scholar]
  80. Maynard Smith J, Haigh J. 1974. The hitch-hiking effect of a favourable gene. Genet. Res. 23:23–35 [Google Scholar]
  81. McKay JK, Latta RG. 2002. Adaptive population divergence: markers, QTL and traits. Trends Ecol. Evol. 17:285–91 [Google Scholar]
  82. Merilä J, Crnokrak P. 2001. Comparison of genetic differentiation at marker loci and quantitative traits. J. Evol. Biol. 14:892–903 [Google Scholar]
  83. Mesoudi A, Blanchet S, Charmantier A, Danchin E, Fogarty L. et al. 2013. Is non-genetic inheritance just a proximate mechanism ? A corroboration of the extended evolutionary synthesis. Biol. Theory 7:189–95 [Google Scholar]
  84. Meyers LA, Ancel FD, Lachmann M. 2005. Evolution of genetic potential. PLOS Comput. Biol. 1:236–43 [Google Scholar]
  85. Milberg P, Lamont BB, Perez-Fernandez MA. 1999. Survival and growth of native and exotic composites in response to a nutrient gradient. Plant Ecol 145:125–32 [Google Scholar]
  86. Mullarkey AA, Byers DL, Anderson RC. 2013. Inbreeding depression and partitioning of genetic load in the invasive biennial Alliaria petiolata (Brassicaceae). Am. J. Bot. 100:509–18 [Google Scholar]
  87. Nei M, Maruyama T, Chakraborty R. 1975. The bottleneck effect and genetic variability in populations. Evolution 29:1–10 [Google Scholar]
  88. Neiman M, Linksvayer TA. 2006. The conversion of variance and the evolutionary potential of restricted recombination. Heredity 96:111–21 [Google Scholar]
  89. Ossowski S, Schneeberger K, Lucas-Lledö JI, Warthmann N, Clark RM. et al. 2010. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327:92–94 [Google Scholar]
  90. Otto SP, Whitlock MC. 1997. The probability of fixation in populations of changing size. Genetics 146:723–33 [Google Scholar]
  91. Palacio-López K, Gianoli E. 2011. Invasive plants do not display greater phenotypic plasticity than their native or noninvasive counterparts: a meta-analysis. Oikos 120:1393–401 [Google Scholar]
  92. Patterson N, Moorjani P, Luo Y, Mallick S, Rohland N. et al. 2012. Ancient admixture in human history. Genetics 192:1065–93 [Google Scholar]
  93. Pavlidis P, Jensen JD, Stephan W, Stamatakis A. 2012. A critical assessment of storytelling: gene ontology categories and the importance of validating genomic scans. Mol. Biol. Evol. 29:3237–48 [Google Scholar]
  94. Peischl S, Excoffier L. 2015. Expansion load: recessive mutations and the role of standing genetic variation. Mol. Ecol. 24:2084–94 [Google Scholar]
  95. Peter BM, Huerta-Sanchez E, Nielsen R. 2012. Distinguishing between selective sweeps from standing variation and from a de novo mutation. PLOS Genet. 8:e1003011 [Google Scholar]
  96. Pfrender ME, Spitze K, Hicks J, Morgan K, Latta L, Lynch M. 2000. Lack of concordance between genetic diversity estimates at the molecular and quantitative-trait levels. Conserv. Genet. 1:263–69 [Google Scholar]
  97. Pudlo P, Marin JM, Estoup A, Cornuet JM, Gautier M, Robert CP. 2016. Reliable ABC model choice via random forests. Bioinformatics 32:859–66 [Google Scholar]
  98. Rapp RA, Wendel JF. 2005. Epigenetics and plant evolution. New Phytol. 165:562–64 [Google Scholar]
  99. Reed DH, Frankham R. 2001. How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–103 [Google Scholar]
  100. Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M. 2006. Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol. Lett. 9:981–93 [Google Scholar]
  101. Rius M, Darling JA. 2014. How important is intraspecific genetic admixture to the success of colonising populations?. Trends Ecol. Evol. 29:233–42 [Google Scholar]
  102. Robertson A. 1961. Inbreeding in artificial selection programmes. Genet. Res. 2:189–94 [Google Scholar]
  103. Rollins LA, Richardson MF, Shine R. 2015. A genetic perspective on rapid evolution in cane toads (Rhinella marina). Mol. Ecol. 24:2264–76 [Google Scholar]
  104. Roman J, Darling JA. 2007. Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol. Evol. 22:454–64 [Google Scholar]
  105. Ronce O, Kirkpatrick M. 2001. When sources become sinks: migrational meltdown in heterogeneous habitats. Evolution 55:1520–31 [Google Scholar]
  106. Santiago E, Caballero A. 1995. Effective size of populations under selection. Genetics 139:1013–30 [Google Scholar]
  107. Sax DF, Brown JH. 2000. The paradox of invasion. Glob. Ecol. Biogeogr. 9:363–71 [Google Scholar]
  108. Schlötterer C, Kofler R, Versace E, Tobler R, Franssen SU. 2015. Combining experimental evolution with next-generation sequencing: a powerful tool to study adaptation from standing genetic variation. Heredity 114:431–40 [Google Scholar]
  109. Schlötterer C, Tobler R, Kofler R, Nolte V. 2014. Sequencing pools of individuals—mining genome-wide polymorphism data without big funding. Nat. Rev. Genet. 15:749–63 [Google Scholar]
  110. Schrey AW, Coon CAC, Grispo MT, Awad M, Imboma T. et al. 2012. Epigenetic variation may compensate for decreased genetic variation with introductions: a case study using house sparrows (Passer domesticus) on two continents. Genet. Res. Int. 2012:979751 [Google Scholar]
  111. Schwander T, Libbrecht R, Keller L. 2014. Supergenes and complex phenotypes. Curr. Biol. 24:R288–94 [Google Scholar]
  112. Simberloff D. 2009. The role of propagule pressure in biological invasions. Annu. Rev. Ecol. Evol. Syst. 40:81–102 [Google Scholar]
  113. Simberloff D. 2013. Biological invasions: Much progress plus several controversies. Contrib. Sci. 9:7–16 [Google Scholar]
  114. Stapley J, Santure A, Dennis S. 2015. Transposable elements as agents of rapid adaptation may explain the genetic paradox of invasive species. Mol. Ecol. 24:2241–52 [Google Scholar]
  115. Suarez AV, Holway DA, Tsutsui ND. 2008. Genetics of colonizing species—the invasive Argentine ant. Am. Nat. 172:S72–84 [Google Scholar]
  116. Szucs M, Melbourne BA, Tuff T, Hufbauer RA. 2014. The roles of demography and genetics in the early stages of colonization. Proc. R. Soc. B 281:20141073 [Google Scholar]
  117. Tayeh A, Estoup A, Laugier G, Loiseau A, Turgeon J. et al. 2012. Evolution in biocontrol strains: insight from the harlequin ladybird Harmonia axyridis. Evol. Appl. 5:481–88 [Google Scholar]
  118. Travis JMJ, Hammershoj M, Stephenson C. 2005. Adaptation and propagule pressure determine invasion dynamics: insights from a spatially explicit model for sexually reproducing species. Evol. Ecol. Res. 7:37–51 [Google Scholar]
  119. Turelli M, Barton NH. 2006. Will population bottlenecks and multilocus epistasis increase additive genetic variance?. Evolution 60:1763–76 [Google Scholar]
  120. Uller T, Leimu R. 2011. Founder events predict changes in genetic diversity during human-mediated range expansions. Glob. Change Biol. 17:3478–85 [Google Scholar]
  121. Van Heerwaarden B, Willi Y, Kristensen TN, Hoffmann AA. 2008. Population bottlenecks increase additive genetic variance but do not break a selection limit in rainforest Drosophila. Genetics 179:2135–46 [Google Scholar]
  122. Vitalis R, Gautier M, Dawson KJ, Beaumont MA. 2014. Detecting and measuring selection from gene frequency data. Genetics 196:799–817 [Google Scholar]
  123. Vitti JJ, Grossman SR, Sabeti PD. 2013. Detecting natural selection in genomic data. Annu. Rev. Genet. 47:97–120 [Google Scholar]
  124. Walbot V. 1999. UV-B damage amplified by transposons in maize. Nature 397:398–99 [Google Scholar]
  125. Wray GA. 2013. Genomics and the evolution of phenotypic traits. Annu. Rev. Ecol. Evol. Syst. 44:51–72 [Google Scholar]
  126. Yeh PJ, Price TD. 2004. Adaptive phenotypic plasticity and the successful colonization of a novel environment. Am. Nat. 164:531–42 [Google Scholar]
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