1932

Abstract

Parallel evolution across replicate populations has provided evolutionary biologists with iconic examples of adaptation. When multiple populations colonize seemingly similar habitats, they may evolve similar genes, traits, or functions. Yet, replicated evolution in nature or in the laboratory often yields inconsistent outcomes: Some replicate populations evolve along highly similar trajectories, whereas other replicate populations evolve to different extents or in distinct directions. To understand these heterogeneous outcomes, biologists are increasingly treating parallel evolution not as a binary phenomenon but rather as a quantitative continuum ranging from parallel to nonparallel. By measuring replicate populations’ positions along this (non)parallel continuum, we can test hypotheses about evolutionary and ecological factors that influence the extent of repeatable evolution. We review evidence regarding the manifestation of (non)parallel evolution in the laboratory, in natural populations, and in applied contexts such as cancer. We enumerate the many genetic, ecological, and evolutionary processes that contribute to variation in the extent of parallel evolution.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-110617-062240
2018-11-02
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/es/49/1/annurev-ecolsys-110617-062240.html?itemId=/content/journals/10.1146/annurev-ecolsys-110617-062240&mimeType=html&fmt=ahah

Literature Cited

  1. Abbosh C, Birkbak NJ, Wilson GA, Jamal-Hanjani M, Constantin T et al. 2017. Phylogenetic ctDNA analysis depicts early-stage lung cancer evolution. Nature 545:446–51
    [Google Scholar]
  2. Abouheif E. 2008. Parallelism as the pattern and process of mesoevolution. Evol. Dev. 10:3–5
    [Google Scholar]
  3. Adams DC, Collyer ML 2009. A general framework for the analysis of phenotypic trajectories in evolutionary studies. Evolution 65:1143–54
    [Google Scholar]
  4. Agrawal AA. 2017. Toward a predictive framework for convergent evolution: integrating natural history, genetic mechanisms, and consequences for the diversity of life. Am. Nat. 190:S1–12
    [Google Scholar]
  5. Alfaro M, Bolnick DI, Wainwright PC 2004. Evolutionary dynamics of complex biomechanical traits: an example from the 4-bar lever system of labrids. Evolution 58:495–503
    [Google Scholar]
  6. Alfaro M, Bolnick DI, Wainwright PC 2005. Evolutionary consequences of many-to-one mapping of jaw morphology to mechanics in labrid fishes. Am. Nat. 165:e140–54
    [Google Scholar]
  7. Arendt J, Reznick DN 2008. Convergence and parallelism reconsidered: What have we learned about the genetics of adaptation. Trends Ecol. Evol. 23:26–32
    [Google Scholar]
  8. Arnold SJ. 1983. Morphology, performance, and fitness. Am. Zool. 23:347–61
    [Google Scholar]
  9. Auld SKJR, Brand J 2017. Environmental variation causes different (co) evolutionary routes to the same adaptive destination across parasite populations. Evol. Lett. 1:5245–54
    [Google Scholar]
  10. Baguñà J, Garcia-Fernàndez J 2003. Evo-Devo: the long and winding road. Int. J. Dev. Biol. 47:705–13
    [Google Scholar]
  11. Bailey SF, Blanquart F, Bataillon T, Kassen R 2017. What drives parallel evolution. BioEssays 39:e201600176
    [Google Scholar]
  12. Bailey SF, Rodrigue N, Kassen R 2015. The effect of selection environment on the probability of parallel evolution. Mol. Biol. Evol. 32:1436–48
    [Google Scholar]
  13. Baldwin BG, Sanderson MJ 1998. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). PNAS 95:9402–6
    [Google Scholar]
  14. Barrett RDH, Schluter D 2008. Adaptation from standing genetic variation. Trends Ecol. Evol. 23:38–44
    [Google Scholar]
  15. Bitocchi E, Bellucci E, Giardini A, Rau D, Rodriguez M et al. 2013. Molecular analysis of the parallel domestication of the common bean (Phaseolus vulgaris) in Mesoamerica and the Andes. New Phytol 197:300–13
    [Google Scholar]
  16. Bollback JP, Huelsenbeck JP 2009. Parallel genetic evolution within and between bacteriophage species of varying degrees of divergence. Genetics 181:225–34
    [Google Scholar]
  17. Brinsmead J, Fox MG 2002. Morphological variation between lake- and stream-dwelling rock bass and pumpkinseed populations. J. Fish Biol. 61:1619–38
    [Google Scholar]
  18. Brodie EDB. 1992. Correlational selection for color pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution 46:1284–98
    [Google Scholar]
  19. Burch CL, Chao L 2000. Evolvability of an RNA virus is determined by its mutational neighborhood. Nature 406:625–28
    [Google Scholar]
  20. Burrell RA, McGranahan N, Bartek J, Swanton C 2013. The causes and consequences of genetic heterogeneity in cancer evolution. Nature 501:338–45
    [Google Scholar]
  21. Calman WT. 1935. Presidential address: the meaning of biological classification. Proc. Linn. Soc. Lond. 147:145–58
    [Google Scholar]
  22. Carscadden KA, Cadotte MW, Gilbert B 2017. Trait dimensionality and population choice alter estimates of phenotypic dissimilarity. Ecol. Evol. 7:2273–85
    [Google Scholar]
  23. Chan YF, Marks ME, Jones FC, Villarreal G, Shapiro MD et al. 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327:302–5
    [Google Scholar]
  24. Charlesworth B. 2013. Why we are not dead one hundred times over. Evolution 67:3354–61
    [Google Scholar]
  25. Chevin L-M, Lande R, Mace GM 2010. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLOS Biol 8:e1000357
    [Google Scholar]
  26. Cohen D. 1967. Optimizing reproduction in a randomly varying environment when a correlation may exist between the conditions at the time a choice has to be made and the subsequent outcome. J. Theor. Biol. 16:1–14
    [Google Scholar]
  27. Collyer ML, Adams DC 2007. Analysis of two-state multivariate phenotypic change in ecological studies. Ecology 88:683–92
    [Google Scholar]
  28. Collyer ML, Sekora DJ, Adams DC 2015. A method for analysis of phenotypic change for phenotypes described by high-dimensional data. Heredity 115:357–65
    [Google Scholar]
  29. Colosimo PA, Hosemann KE, Balabhadra S, Villarreal G, Dickson A et al. 2005. Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307:1928–33
    [Google Scholar]
  30. Conte GL, Arnegard ME, Best J, Chan YF, Jones FC et al. 2015. Extent of QTL reuse during repeated phenotypic divergence of sympatric threespine stickleback. Genetics 201:1189–200
    [Google Scholar]
  31. Conte GL, Arnegard ME, Peichel CL, Schluter D 2012. The probability of genetic parallelism and convergence in natural populations. Proc. R. Soc. B 279:5039–47
    [Google Scholar]
  32. Coop G, Witonsky D, Di Rienzo A, Pritchard JK 2010. Using environmental correlations to identify loci underlying local adaptation. Genetics 185:1411–23
    [Google Scholar]
  33. Cooper TF, Ostrowski EA, Travisano M 2007. A negative relationship between mutation pleiotropy and fitness effect in yeast. Evolution 61:1495–99
    [Google Scholar]
  34. Cooper TF, Rozen DE, Lenski RE 2003. Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. PNAS 100:1072–77
    [Google Scholar]
  35. Cope ED. 1876. The progress of discovery of the laws of evolution. Am. Nat. 10:218–21
    [Google Scholar]
  36. Cope ED, Kingsley JS 1891. Editorial. Am. Nat. 25:558–60
    [Google Scholar]
  37. Costanzo M, VanderSluis B, Koch EN, Baryshnikova A, Pons C et al. 2016. A global genetic interaction network maps a wiring diagram of cellular function. Science 353:aaf1420
    [Google Scholar]
  38. Coyle SM, Huntingford FA, Peichel CL 2007. Parallel evolution of Pitx1 underlies pelvic reduction in Scottish threespine stickleback (Gasterosteus aculeatus). J. Hered. 98:581–86
    [Google Scholar]
  39. Darwin C. 1859. On the Origin of Species Cambridge, MA:Harvard Univ. Press
  40. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML 2011. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat. Rev. Genet. 12:499–510
    [Google Scholar]
  41. Day T. 2012. Computability, Godel's incompleteness theorem, and an inherent limit on the predictability of evolution. J. R. Soc. Interface 9:624–39
    [Google Scholar]
  42. de Visser JA, Krug J 2014. Empirical fitness landscapes and the predictability of evolution. Nat. Rev. Genet. 15:480–90
    [Google Scholar]
  43. Decaestecker E, Gaba S, Raeymaekers JAM, Stoks R, Van Kerckhoven L et al. 2007. Host-parasite ‘red queen’ dynamics archived in pond sediment. Nature 450:870–73
    [Google Scholar]
  44. Derome N, Duchesne P, Bernatchez L 2006. Parallelism in gene transcription among sympatric lake whitefish (Coregonus clupeaformis Mitchill) ecotypes. Mol. Ecol. 15:1239–49
    [Google Scholar]
  45. Dobzhansky T. 1933. Geographical variation in lady-beetles. Am. Nat. 67:97–126
    [Google Scholar]
  46. Douglas SM, Chubiz LM, Harcombe WR, Ytreberg FM, Marx CJ 2016. Parallel mutations result in a wide range of cooperation and community consequences in a two-species bacterial consortium. PLOS ONE 11:e0161837
    [Google Scholar]
  47. Dunn B, Levine RP, Sherlock G. 2005. Microarray karyotyping of commercial wine yeast strains reveals shared, as well as unique, genomic signatures. BMC Genom 6:53
    [Google Scholar]
  48. Ellner SP, Geber MA, Hairston NG 2011. Does rapid evolution matter? Measuring the rate of contemporary evolution and its impacts on ecological dynamics. Ecol. Lett. 14:603–14
    [Google Scholar]
  49. Elmer KR, Fan S, Kusche H, Spreitzer ML, Kautt AF et al. 2014. Parallel evolution of Nicaraguan crater lake cichlid fishes via non-parallel routes. Nat. Commun. 5:5168
    [Google Scholar]
  50. Elmer KR, Meyer A 2011. Adaptation in the age of ecological genomics: insights from parallelism and convergence Trends Ecol. Evol 26:298–306
    [Google Scholar]
  51. Eroukhmanoff F, Hargeby A, Arnberg NN, Hellgren O, Bensch S, Svensson EI 2009. Parallelism and historical contingency during rapid ecotype divergence in an isopod. J. Evol. Biol. 22:1098–110
    [Google Scholar]
  52. Evans ML, Chapman LJ, Mitrofanov I, Bernatchez L 2013. Variable extent of parallelism in respiratory, circulatory, and neurological traits across lake whitefish species pairs. Ecol. Evol. 3:546–57
    [Google Scholar]
  53. Falconer DS. 1952. The problem of environment and selection. Am. Nat. 86:293–98
    [Google Scholar]
  54. Feiner N, Rago A, While GM, Uller T 2017. Signatures of selection in embryonic transcriptomes of lizards adapting in parallel to cool climate. Evolution 72:67–81
    [Google Scholar]
  55. Ferea TL, Botstein D, Brown PO, Rosenzweig RF 1999. Systematic changes in gene expression patterns following adaptive evolution in yeast. PNAS 96:9721–26
    [Google Scholar]
  56. Fernández-Ortuño D, Torés JA, de Vicente A, Pérez-García A 2008. Field resistance to QoI fungicides in Podosphaera fusca is not supported by typical mutations in the mitochondrial cytochrome b gene. Pest Manag. Sci. 64:694–702
    [Google Scholar]
  57. Fitzpatrick SW, Torres-Dowdall J, Reznick DN, Ghalambor CK, Funk WC 2014. Parallelism isn't perfect: could disease and flooding drive a life-history anomaly in Trinidadian guppies. Am. Nat. 183:290–300
    [Google Scholar]
  58. Fong SS, Joyce AR, Palsson B 2005. Parallel adaptive evolution cultures of Escherichia coli lead to convergent growth phenotypes with different gene expression states. Genome Res 2005:1365–72
    [Google Scholar]
  59. Fuller DQ, Denham T, Arroyo-Kalin M, Lucas L, Stevens CJ et al. 2014. Convergent evolution and parallelism in plant domestication revealed by an expanding archaeological record. PNAS 111:6147–52
    [Google Scholar]
  60. Gates RR. 1912. Parallel mutations in Oenothera biennis. Nature 89:659–60
    [Google Scholar]
  61. Gates RR. 1936. Mutations and natural selection. Am. Nat. 70:505–16
    [Google Scholar]
  62. Gerstein AC, Lo DS, Otto SP 2012. Parallel genetic changes and nonparallel gene-environment interactions characterize the evolution of drug resistance in yeast. Genetics 192:241–52
    [Google Scholar]
  63. Gillespie JH. 1994. The Causes of Molecular Evolution Oxford, UK: Oxford Univ. Press
  64. Gillespie R. 2004. Community assembly through adaptive radiation in Hawaiian spiders. Science 303:356–59
    [Google Scholar]
  65. Gíslason D, Ferguson MM, Skulason S, Snorrason SS 1999. Rapid and coupled phenotypic and genetic divergence in Icelandic arctic char (Salvelinus alpinus). Can. J. Fish. Aquat. Sci. 56:2229–34
    [Google Scholar]
  66. Gompel N, Brud'homme B 2009. The causes of repeated genetic evolution. Dev. Biol. 332:36–47
    [Google Scholar]
  67. Gould SJ. 2002. The Structure of Evolutionary Theory Cambridge, MA: Harvard Univ. Press
  68. Gratten J, Wilson A, McRae A, Beraldi D, Visscher P et al. 2008. A localized negative genetic correlation constrains microevolution of coat color in wild sheep. Science 319:318–20
    [Google Scholar]
  69. Graves JL Jr., Hertweck KL, Phillips MA, Han MV, Cabral LG et al. 2017. Genomics of parallel experimental evolution in Drosophila. Mol. Biol. Evol. 34:831–42
    [Google Scholar]
  70. Haas O, Simpson GG 1945. Analysis of some phylogenetic terms, with attempts at redefinition. Proc. Am. Philos. Soc. 90:319–49
    [Google Scholar]
  71. Harvey PH, Pagel MD 1991. The Comparative Method in Evolutionary Biology New York: Oxford Univ. Press
  72. Hendry AP, Kaeuffer RE, Crispo E, Peichel CL, Bolnick DI 2013. Evolutionary inferences from exchangeability: individual classification approaches based on the ecology, morphology, and genetics of lake-stream stickleback population pairs. Evolution 67:3429–41
    [Google Scholar]
  73. Hendry AP, Taylor EB 2004. How much of the variation in adaptive divergence can be explained by gene flow? An evaluation using lake-stream stickleback pairs. Evolution 58:2319–31
    [Google Scholar]
  74. Herron MD, Doebeli M 2013. Parallel evolutionary dynamics of adaptive diversification in Escherichia coli. PLOS Biol 11:e10001490
    [Google Scholar]
  75. Hodgkinson A, Eyre-Walker A 2011. Variation in the mutation rate across mammalian genomes. Nat. Rev. Genet. 12:756–66
    [Google Scholar]
  76. Hoekstra HE, Nachman MW 2003. Different genes underlie adaptive melanism in different populations of rock pocket mice. Mol. Ecol. 12:1185–94
    [Google Scholar]
  77. Holland J, Spindler K, Horodyski F, Grabau E, Nichol S, Van de Pol S 1982. Rapid evolution of RNA genomes. Science 215:1577–85
    [Google Scholar]
  78. Hubbs CL. 1944. Concepts of homology and analogy. Am. Nat. 78:289–307
    [Google Scholar]
  79. Ingley SJ, Billmann EJ, Hancock C, Johnson JB 2014. Repeated geographic divergence in behavior: a case study employing phenotypic trajectory analyses. Behav. Ecol. Sociobiol. 68:1577–87
    [Google Scholar]
  80. Ingram T, Mahler DL 2013. SURFACE: detecting convergent evolution from comparative data by fitting Ornstein-Uhlenbeck models with stepwise Akaike Information Criterion. Methods Ecol. Evol. 4:416–25
    [Google Scholar]
  81. Jerison ER, Desai MM 2015. Genomic investigations of evolutionary dynamics and epistasis in microbial evolution experiments. Curr. Opin. Genet. Dev. 35:33–39
    [Google Scholar]
  82. Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55–61
    [Google Scholar]
  83. Josephides C, Swain PS 2017. Predicting metabolic adaptation from networks of mutational paths. Nat. Commun. 8:685
    [Google Scholar]
  84. Kaeuffer R, Peichel CL, Bolnick DI, Hendry AP 2012. Parallel and nonparallel aspects of ecological, phenotypic, and genetic divergence across replicate population pairs of lake and stream stickleback. Evolution 66:402–18
    [Google Scholar]
  85. Kautt AF, Elmer KR, Meyer A 2012. Genomic signatures of divergent selection and speciation patterns in a ‘natural experiment’, the young parallel radiations of Nicaraguan crater lake cichlid fishes. Mol. Ecol. 21:4770–86
    [Google Scholar]
  86. Kenkel CD, Almanza AT, Matz MV 2015. Fine‐scale environmental specialization of reef‐building corals might be limiting reef recovery in the Florida Keys. Ecology 96:3197–212
    [Google Scholar]
  87. Khaitovich P, Hellmann I, Enard W, Nowick K, Leinweber M et al. 2005. Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 309:1850–54
    [Google Scholar]
  88. Kimura M. 1964. Diffusion models in population genetics. J. Appl. Probab. 1:177–232
    [Google Scholar]
  89. Kocher TD, Conroy JA, McKaye KR, Stauffer JR 1993. Similar morphologies of cichlid fish in Lakes Tanganyika and Malawi are due to convergence. Mol. Phylogenetics Evol. 2:158–65
    [Google Scholar]
  90. Kolbe JJ, Leal M, Schoener TW, Spiller DA, Losos JB 2012. Founder effects persist despite adaptive differentiation: a field experiment with lizards. Science 335:1086–89
    [Google Scholar]
  91. Lai Z, Kane NC, Zou Y, Rieseberg LH 2008. Natural variation in gene expression between wild and weedy populations of Helianthus annuus. Genetics 179:1881–90
    [Google Scholar]
  92. Lande R, Arnold SJ 1983. The measurement of selection on correlated characters. Evolution 37:1210–26
    [Google Scholar]
  93. Landry L, Bernatchez L 2010. Role of epibenthic resource opportunities in the parallel evolution of lake whitefish species pairs (Coregonus sp.). J. Evol. Biol. 23:2602–13
    [Google Scholar]
  94. Landry L, Vincent WF, Bernatchez L 2007. Parallel evolution of lake whitefish dwarf ecotypes in association with limnological features of their adaptive landscape. J. Evol. Biol. 20:971–84
    [Google Scholar]
  95. Langerhans RB. 2018. Predictability and parallelism of multitrait adaptation. J. Hered. 109:59–70
    [Google Scholar]
  96. Langerhans RB, DeWitt T 2004. Shared and unique features of evolutionary diversification. Am. Nat. 164:335–49
    [Google Scholar]
  97. Langerhans RB, Knouft JH, Losos JB 2006. Shared and unique features of diversification in greater Antillean Anolis ecomorphs. Evolution 60:362–69
    [Google Scholar]
  98. Langerhans RB, Makowicz AM 2009. Shared and unique features of morphological differentiation between predator regimes in Gambusia caymanensis. J. Evol. Biol 22:2231–42
    [Google Scholar]
  99. Laporte M, Rogers SM, Dion-Cote AM, Normandeau E, Gagnaire PA et al. 2015. RAD-QTL mapping reveals both genome-level parallelism and different genetic architecture underlying the evolution of body shape in lake whitefish (Coregonus clupeaformis) species pairs. G3 5:1481–91
    [Google Scholar]
  100. Lauder GV. 1981. Form and function: structural analysis in evolutionary morphology. Paleobiology 7:430–42
    [Google Scholar]
  101. Le Moan A, Gagnaire P-A, Bonhomme F 2016. Parallel genetic divergence among coastal–marine ecotype pairs of European anchovy explained by differential introgression after secondary contact. Mol. Ecol. 25:3187–202
    [Google Scholar]
  102. Leal M, Knox AK, Losos JB 2002. Lack of convergence in aquatic Anolis lizards. Evolution 56:785–91
    [Google Scholar]
  103. Leger EA, Rice KJ 2007. Assessing the speed and predictability of local adaptation in invasive California poppies (Eschscholzia californica). J. Evol. Biol. 20:1090–103
    [Google Scholar]
  104. Leinonen T, McCairns RJ, Herczeg G, Merila J 2012. Multiple evolutionary pathways to decreased lateral plate coverage in freshwater threespine sticklebacks. Evolution 66:3866–75
    [Google Scholar]
  105. Lenormand T. 2002. Gene flow and the limits to natural selection. Trends Ecol. Evol. 17:183–89
    [Google Scholar]
  106. Lenski RE. 2017. Convergence and divergence in a long-term experiment with bacteria. Am. Nat. 190:S57–68
    [Google Scholar]
  107. Levy YY, Dean C 1998. Control of flowering time. Curr. Opin. Plant Biol. 1:49–54
    [Google Scholar]
  108. Lohman B, Berner D, Bolnick DI 2017. Clines arc through multivariate morphospace. Am. Nat. 189:354–67
    [Google Scholar]
  109. Losos JB. 2009. Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of Anoles Berkeley: Univ. Calif. Press
  110. Losos JB. 2011. Convergence, adaptation, and constraint. Evolution 65:1827–40
    [Google Scholar]
  111. Lucek K, Sivasundar A, Kristjánsson BK, Skúlason S, Seehausen O 2014. Quick divergence but slow convergence during ecotype formation in lake and stream stickleback pairs of variable age. J. Evol. Biol. 27:1878–92
    [Google Scholar]
  112. MacPherson A, Nuismer SL 2017. The probability of parallel genetic evolution from standing genetic variation. J. Evol. Biol. 30:326–37
    [Google Scholar]
  113. Mahler DL, Ingram T, Revell LJ, Losos JB 2013. Exceptional convergence on the macroevolutionary landscape in island lizard radiations. Science 341:292–95
    [Google Scholar]
  114. Manceau M, Domingues VS, Mallarino R, Hoekstra HE 2011. The developmental role of Agouti in color pattern evolution. Science 331:1062–65
    [Google Scholar]
  115. Manousaki T, Hull PM, Kusche H, Machado-Schiaffino G, Franchini P et al. 2013. Parsing parallel evolution: ecological divergence and differential gene expression in the adaptive radiations of thick-lipped Midas cichlid fishes from Nicaragua. Mol. Ecol. 22:650–69
    [Google Scholar]
  116. Martinez-Picado J, Frost SDW, Izquierdo N, Morales-Lopetegi K, Marfil S et al. 2002. Viral evolution during structured treatment interruptions in chronically human immunodeficiency virus-infected individuals. J. Virol. 76:12344–48
    [Google Scholar]
  117. Mazzarella AB, Voje KL, Hansson TH, Taugbøl A, Fischer B 2015. Strong and parallel salinity-induced phenotypic plasticity in one generation of threespine stickleback. J. Evol. Biol. 28:667–77
    [Google Scholar]
  118. McGee MD, Neches RY, Seehausen O 2016. Evaluating genomic divergence and parallelism in replicate ecomorphs from young and old cichlid adaptive radiations. Mol. Ecol. 25:260–68
    [Google Scholar]
  119. Meyer JR, Agrawal AA, Quick RT, Dobias DT, Schneider D, Lenski RE 2010. Parallel changes in host resistance to viral infection during 45,000 generations of relaxed selection. Evolution 64:3024–34
    [Google Scholar]
  120. Moore J-S, Gow JL, Taylor EB, Hendry AP 2007. Quantifying the constraining influence of gene flow on adaptive divergence in the lake-stream threespine stickleback system. Evolution 61:2015–26
    [Google Scholar]
  121. Muir F. 1924. Homoplasmy or convergent development in evolution. Proc. Hawaii. Entomol. Soc. 5:473–83
    [Google Scholar]
  122. Muller HJ. 1939. Reversibility in evolution considered from the standpoint of genetics. Biol. Rev. Camb. Philos. Soc. 14:261–80
    [Google Scholar]
  123. Nachman MW. 2002. Variation in recombination rate across the genome: evidence and implications. Curr. Opin. Genet. Dev. 12:657–63
    [Google Scholar]
  124. Nichols JT. 1916. On primarily unadaptive variants. Am. Nat. 50:565–74
    [Google Scholar]
  125. Nosil P, Crespi BJ 2004. Does gene flow constrain adaptive divergence or vice versa? A test using ecomorphology and sexual isolation in Timema cristinae walking sticks. Evolution 58:102–12
    [Google Scholar]
  126. Nowell PC. 1976. The clonal evolution of tumor cell populations. Science 194:23–28
    [Google Scholar]
  127. Oke KB, Bukhari M, Kaueffer R, Rolshausen G, Räsänen K et al. 2015. Plasticity enhances phenotypic parallelism: evidence from lake-stream stickleback. J. Evol. Biol. 29:126–43
    [Google Scholar]
  128. Oke KB, Rolshausen G, LeBlond C, Hendry AP 2017. How parallel is parallel evolution? A comparative analysis in fishes. Am. Nat. 190:1–16
    [Google Scholar]
  129. Ord TJ, Summers TC 2015. Repeated evolution and the impact of evolutionary history on adaptation. BMC Evol. Biol. 15:137
    [Google Scholar]
  130. Orr HA. 2005. The probability of parallel evolution. Evolution 59:216–20
    [Google Scholar]
  131. Osborn HF. 1900. The geological and faunal relations of Europe and America during the Tertiary period and the theory of the successive invasions of an African fauna. Science 11:561–74
    [Google Scholar]
  132. Otto SP. 2004. Two steps forward, one step back: the pleiotropic effects of favoured alleles. Proc. R. Soc. B 271:705–14
    [Google Scholar]
  133. Packard AS. 1898. The philosophical views of Agassiz. Am. Nat. 32:159–64
    [Google Scholar]
  134. Papakostas S, Vøllestad LA, Bruneaux M, Aykanat T, Vanoverbeke J et al. 2014. Gene pleiotropy constrains gene expression changes in fish adapted to different thermal conditions. Nat. Commun. 5:4071
    [Google Scholar]
  135. Pavey SA, Sevellec M, Adam W, Normandeau E, Lamaze FC et al. 2013. Nonparallelism in MHCIIβ diversity accompanies nonparallelism in pathogen infection of lake whitefish (Coregonus clupeaformis) species pairs as revealed by next-generation sequencing. Mol. Ecol. 22:3833–49
    [Google Scholar]
  136. Pérez-Pereira N, Quesada H, Caballero A 2017. Can parallel ecological speciation be detected with phylogenetic analyses. Mol. Phylogenetics Evol. 116:149–56
    [Google Scholar]
  137. Perreault-Payette A, Muir AM, Goetz F, Perrier C, Normandeau E et al. 2017. Investigating the extent of parallelism in morphological and genomic divergence among lake trout ecotypes in Lake Superior. Mol. Ecol. 26:1477–97
    [Google Scholar]
  138. Perrier C, Bourret V, Kent MP, Bernatchez L 2013. Parallel and nonparallel genome-wide divergence among replicate population pairs of freshwater and anadromous Atlantic salmon. Mol. Ecol. 22:5577–93
    [Google Scholar]
  139. Pfenninger M, Patel S, Arias-Rodriguez L, Feldmeyer B, Riesch R, Plath M 2015. Unique evolutionary trajectories in repeated adaptation to hydrogen sulphide-toxic habitats of a neotropical fish (Poecilia mexicana). Mol. Ecol. 24:5446–59
    [Google Scholar]
  140. Pujolar JM, Ferchaud AL, Bekkevold D, Hansen MM 2017. Non-parallel divergence across freshwater and marine three-spined stickleback Gasterosteus aculeatus populations. J. Fish Biol. 91:175–94
    [Google Scholar]
  141. Ramiro RS, Costa H, Gordo I 2016. Macrophage adaptation leads to parallel evolution of genetically diverse Escherichia coli small-colony variants with increased fitness in vivo and antibiotic collateral sensitivity. Evol. Appl. 9:994–1004
    [Google Scholar]
  142. Ravinet M, Westram A, Johannesson K, Butlin R, Andre C, Panova M 2016. Shared and nonshared genomic divergence in parallel ecotypes of Littorina saxatilis at a local scale. Mol. Ecol. 25:287–305
    [Google Scholar]
  143. Rensch B. 1939. Typen der Artbildung. Biol. Rev. 14:180–222
    [Google Scholar]
  144. Rinkevich B. 2005. Conservation of coral reefs through active restoration measures: recent approaches and last decade progress. Environ. Sci. Technol. 39:4333–42
    [Google Scholar]
  145. Roberge C. 2006. Rapid parallel evolutionary changes of gene transcription profiles in farmed Atlantic salmon. Mol. Ecol. 15:9–20
    [Google Scholar]
  146. Roda F, Walter GM, Nipper R, Ortiz-Barrientos D 2017. Genomic clustering of adaptive loci during parallel evolution of an Australian wildflower. Mol. Ecol. 14:3687–99
    [Google Scholar]
  147. Roesti M, Moser D, Berner D 2013. Recombination in the threespine stickleback genome–patterns and consequences. Mol. Ecol. 22:3014–27
    [Google Scholar]
  148. Rokas A, Carroll SB 2008. Frequent and widespread parallel evolution of protein sequences. Mol. Biol. Evol. 25:1943–53
    [Google Scholar]
  149. Rosenblum EB, Harmon LJ 2011. “Same same but different”: replicated ecological speciation at White Sands. Evolution 65:946–60
    [Google Scholar]
  150. Rosenblum EB, Parent CE, Brandt EE 2014. The molecular basis of phenotypic convergence. Annu. Rev. Ecol. Evol. Syst. 45:203–26
    [Google Scholar]
  151. Rosenblum EB, Römpler H, Schöneberg T, Hoekstra HE 2010. Molecular and functional basis of phenotypic convergence in white lizards at White Sands. PNAS 107:2113–17
    [Google Scholar]
  152. Sailer ZR, Harms MJ 2017. Molecular ensembles make evolution unpredictable. PNAS 114:11938–43
    [Google Scholar]
  153. Samuk K, Owens GL, Delmore KE, Miller SE, Rennison DJ, Schluter D 2017. Gene flow and selection interact to promote adaptive divergence in regions of low recombination. Mol. Ecol. 26:4378–90
    [Google Scholar]
  154. Schmutz J, McClean PE, Mamidi S, Wu GA, Cannon SB et al. 2014. A reference genome for common bean and genome-wide analysis of dual domestications. Nat. Genet. 46:707–13
    [Google Scholar]
  155. Scotland RW. 2011. What is parallelism. Evol. Dev. 13:214–27
    [Google Scholar]
  156. Shindo C, Aranzana MJ, Lister C, Baxter C, Nicholls C et al. 2005. Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol 138:1163–73
    [Google Scholar]
  157. Shpak M, Lu J 2016. An evolutionary genetic perspective on cancer biology. Annu. Rev. Ecol. Evol. Syst. 47:25–49
    [Google Scholar]
  158. Siepielski AM, DiBattista JD, Carlson SM 2009. It's about time: the temporal dynamics of phenotypic selection in the wild. Ecol. Lett. 12:1261–76
    [Google Scholar]
  159. Simpson GG. 1953. The Major Features of Evolution New York: Columbia Univ. Press
  160. Simpson GG. 1961. Principles of Animal Taxonomy New York: Columbia Univ. Press
  161. Siwertsson A, Knudsen R, Adams CE, Praebel K, Amundsen PA 2013. Parallel and non-parallel morphological divergence among foraging specialists in European whitefish (Coregonus lavaretus). Ecol. Evol. 3:1590–602
    [Google Scholar]
  162. Slatkin M. 1985. Gene flow in natural populations. Annu. Rev. Ecol. Syst. 16:393–430
    [Google Scholar]
  163. Speed MP, Arbuckle K 2017. Quantification provides a conceptual basis for convergent evolution. Biol. Rev. 92:815–29
    [Google Scholar]
  164. Stayton CT. 2008. Is convergence surprising? An examination of the frequency of convergence in simulated datasets. J. Theor. Biol. 252:1–14
    [Google Scholar]
  165. Stockwell CA, Hendry AP, Kinnison MT 2003. Contemporary evolution meets conservation biology. Trends Ecol. Evol. 18:94–101
    [Google Scholar]
  166. Storz JF. 2016. Causes of molecular convergence and parallelism in protein evolution. Nat. Rev. Genet. 17:239–50
    [Google Scholar]
  167. Stuart YE, Veen T, Weber JN, Hanson D, Lohman BK et al. 2017. Contrasting effects of environment and genetics generate a continuum of parallel evolution. Nat. Ecol. Evol. 1:158
    [Google Scholar]
  168. Sturm RA, Duffy DL 2012. Human pigmentation genes under environmental selection. Genome Biol 13:248
    [Google Scholar]
  169. Swanton C. 2014. Cancer evolution: the final frontier of precision medicine. Ann. Oncol. 25:549–51
    [Google Scholar]
  170. Szendro IG, Franke J, de Visser JAGM, Krug J 2013. Predictability of evolution depends nonmonotonically on population size. PNAS 110:571–76
    [Google Scholar]
  171. Takahashi K, Kohno T, Matsumoto S, Nakanishi Y, Arai Y et al. 2007. Clonal and parallel evolution of primary lung cancers and their metastases revealed by molecular dissection of cancer cells. Hum. Cancer Biol. 13:111–20
    [Google Scholar]
  172. Takuno S, Ralph P, Swarts K, Elshire RJ, Glaubitz JC et al. 2015. Independent molecular basis of convergent highland adaptation in maize. Genetics 207:1297–312
    [Google Scholar]
  173. Tegze B, Szállási Z, Haltrich I, Pénzváltó Z, Tóth Z et al. 2012. Parallel evolution under chemotherapy pressure in 29 breast cancer cell lines results in dissimilar mechanisms of resistance. PLOS ONE 7:e30804
    [Google Scholar]
  174. Tellier A, Brown JK 2007. Polymorphism in multilocus host parasite coevolutionary interactions. Genetics 177:1777–90
    [Google Scholar]
  175. Tenaillon O, Barrick J, Ribeck N, Deatherage DE, Blanchard JL et al. 2016. Tempo and mode of genome evolution in a 50,000-generation experiment. Nature 536:165–70
    [Google Scholar]
  176. Terekhanova NV, Logacheva MD, Penin AA, Neretina TV, Barmintseva AE et al. 2014. Fast evolution from precast bricks: genomics of young freshwater populations of threespine stickleback Gasterosteus aculeatus. PLOS Genet 10:e1004696
    [Google Scholar]
  177. Thompson C, Ahmed N, Veen T, Peichel CL, Hendry AP et al. 2017. Many-to-one form-to-function mapping weakens parallel morphological evolution. Evolution 71:2738–49
    [Google Scholar]
  178. Thompson CE, Taylor EB, McPhail JD 1997. Parallel evolution of lake-stream pairs of threespine sticklebacks (Gasterosteus) inferred from mitochondrial DNA variation. Evolution 51:1955–65
    [Google Scholar]
  179. Torriani SFF, Brunner PC, McDonald BA, Sierotzki H 2008. QoI resistance emerged independently at least 4 times in European populations of Mycosphaerella graminicola. Pest Manag. Sci. 65:155–62
    [Google Scholar]
  180. Vavilov NI. 1922. The law of homologous series in variation. J. Genet. 12:47–89
    [Google Scholar]
  181. Velotta JP, Wegrzyn JL, Ginzburg S, Kang L, Czesny S et al. 2017. Transcriptomic imprints of adaptation to fresh water: parallel evolution of osmoregulatory gene expression in the Alewife. Mol. Ecol. 26:831–48
    [Google Scholar]
  182. Vogwill T, Kohadinovic M, Furió V, MacLean RC 2014. Testing the role of genetic background in parallel evolution using the comparative experimental evolution of antibiotic resistance. Mol. Biol. Evol. 31:3314–23
    [Google Scholar]
  183. Wainwright PC. 1996. Ecological explanation through functional morphology: the feeding biology of sunfishes. Ecology 77:1336–43
    [Google Scholar]
  184. Wainwright PC, Alfaro M, Bolnick DI, Hulsey CD 2005. Many-to-one mapping of form to function: a general principle in organismal design. Integr. Comp. Biol. 45:256–62
    [Google Scholar]
  185. Wake DB. 1999. Homoplasy, homology and the problem of ‘sameness’ in biology. Homology GR Bock, G Cardew 24–46 New York: Wiley
    [Google Scholar]
  186. Wake DB, Wake MH, Specht CD 2011. Homoplasy: from detecting pattern to determining process and mechanism of evolution. Science 331:1032–35
    [Google Scholar]
  187. Walker JA. 2007. A general model of functional constraints on phenotypic evolution. Am. Nat. 170:681–89
    [Google Scholar]
  188. Westram AM, Galindo J, Rosenblad MA, Grahame JW, Panova M, Butlin RK 2014. Do the same genes underlie parallel phenotypic divergence in different Littorina saxatilis populations. Mol. Ecol. 23:4603–16
    [Google Scholar]
  189. Whitlock MC, Gomulkiewicz R 2005. Probability of fixation in a heterogeneous environment. Genetics 171:1407–17
    [Google Scholar]
  190. Wichman HA, Badgett MR, Scott LA, Boulianne CM, Bull JJ 1999. Divergent trajectories of parallel evolution during viral adaptation. Science 285:422–24
    [Google Scholar]
  191. Wilson HV. 1941. The recapitulation theory or biogenetic law in embryology. Am. Nat. 75:20–30
    [Google Scholar]
  192. Yeaman S, Hodgins KA, Lotterhos KE, Suren H, Nadeau S et al. 2016. Convergent local adaptation to climate in distantly related conifers. Science 353:1431–33
    [Google Scholar]
/content/journals/10.1146/annurev-ecolsys-110617-062240
Loading
/content/journals/10.1146/annurev-ecolsys-110617-062240
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error