Genome Evolution in Outcrossing Versus Selfing Versus Asexual Species

  • Sylvain Glémin
  • Nicolas GaltierEmail author
Part of the Methods in Molecular Biology book series (MIMB, volume 855)


A major current molecular evolution challenge is to link comparative genomic patterns to species’ biology and ecology. Breeding systems are pivotal because they affect many population genetic processes, and thus genome evolution. We review theoretical predictions and empirical evidence about molecular evolutionary processes under three distinct breeding systems—outcrossing, selfing, and asexuality. Breeding systems may have a profound impact on genome evolution, including molecular evolutionary rates, base composition, genomic conflict, and possibly genome size. However, while asexual species essentially conform to theoretical predictions, the situation is less simple in selfing species. We discuss the possible reasons to potentially explain this paradox. In reverse, comparative and population genomic data and approaches help revisiting old questions on the long-term evolution of breeding systems.

Key words

Breeding systems GC-biased gene conversion Genome evolution Genomic conflicts Selection Transposable elements 



We thank three anonymous reviewers for helpful comments to improve the manuscript. This work was supported by ARCAD, a flagship project of Agropolis Fondation, an ERC grant (PopPhyl) to N.G., and the CoGeBi program (grant number ANR-08-GENM-036-01). This publication is the contribution ISEM 2012-006 of the Institut des Sciences de l’Evolution de Montpellier (UMR 5554—CNRS).


  1. 1.
    Lynch M (2007) The origin of genome architecture. 1 edn. Sinauer, Sunderland.Google Scholar
  2. 2.
    Nikolaev SI, Montoya-Burgos JI, Popadin K, Parand L, Margulies EH, Antonarakis SE (2007) Life-history traits drive the evolutionary rates of mammalian coding and noncoding genomic elements. Proc Natl Acad Sci USA 104 (51):20443–20448.PubMedGoogle Scholar
  3. 3.
    Popadin K, Polishchuk LV, Mamirova L, Knorre D, Gunbin K (2007) Accumulation of slightly deleterious mutations in mitochondrial protein-coding genes of large versus small mammals. Proc Natl Acad Sci USA 104 (33):13390–13395.PubMedGoogle Scholar
  4. 4.
    Foltz DW (2003) Invertebrate species with nonpelagic larvae have elevated levels of nonsynonymous substitutions and reduced nucleotide diversities. J Mol Evol 57 (6):607–612.PubMedGoogle Scholar
  5. 5.
    Woolfit M, Bromham L (2005) Population size and molecular evolution on islands. Proc Biol Sci 272 (1578):2277–2282.PubMedGoogle Scholar
  6. 6.
    Jarne P, Auld JR (2006) Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals. Evolution 60 (9):1816–1824.PubMedGoogle Scholar
  7. 7.
    Vogler DW, Kaliz S (2001) Sex among the flowers: the distribution of plant mating systems. Evolution 55 (1):202–204.PubMedGoogle Scholar
  8. 8.
    Haldane JBS (1932) The causes of Evolution, vol 1. 1 edn. Princeton University Press, Princeton.Google Scholar
  9. 9.
    Balloux F, Lehmann L, de Meeus T (2003) The population genetics of clonal and partially clonal diploids. Genetics 164 (4):1635–1644.PubMedGoogle Scholar
  10. 10.
    Simon JC, Delmotte F, Rispe C, Crease TJ (2003) Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biol J Lin Soc 79:151–163.Google Scholar
  11. 11.
    Whitton J, Sears CJ, Baack EJ, Otto SP (2008) The dynamic nature of apomixis in the angiosperms. Int J Plant Sci 169 (1):169–182.Google Scholar
  12. 12.
    Maynard-Smith J (1978) The Evolution of Sex. Cambridge University Press, Cambridge.Google Scholar
  13. 13.
    Stebbins GL (1957) Self fertilization and population variability in higher plants. Am Nat 91:337–354.Google Scholar
  14. 14.
    Wright S, Ness RW, Foxe JP, Barrett SC (2008) Genomic consequences of outcrossing and selfing in plants. Int J Plant Sci 169 (1):105–118.Google Scholar
  15. 15.
    Nordborg M (2000) Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Genetics 154 (2):923–929.PubMedGoogle Scholar
  16. 16.
    Flint-Garcia SA, Thornsberry JM, Buckler ESt (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374.Google Scholar
  17. 17.
    Glémin S, Bazin E, Charlesworth D (2006) Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proc Biol Sci 273 (1604):3011–3019.PubMedGoogle Scholar
  18. 18.
    Pollak E (1987) On the theory of partially inbreeding finite populations. I. Partial selfing. Genetics 117 (2):353–360.Google Scholar
  19. 19.
    Haag CR, Roze D (2007) Genetic load in sexual and asexual diploids: segregation, dominance and genetic drift. Genetics 176 (3):1663–1678.PubMedGoogle Scholar
  20. 20.
    Schoen DJ, Brown AHD (1991) Intraspecific variation in population gene diversity and effective population size correlates with the mating system in plants. Proc Natl Acad Sci USA 88:4494–4497.PubMedGoogle Scholar
  21. 21.
    Haag CR, Ebert D (2004) A new hypothesis to explain geographic parthenogenesis. Ann Zool Fennici 41:539–544.Google Scholar
  22. 22.
    Ingvarsson PK (2002) A metapopulation perspective on genetic diversity and differentiation in partially self-fertilizing plants. Evolution 56 (12):2368–2373.PubMedGoogle Scholar
  23. 23.
    Gordo I, Charlesworth B (2001) Genetic linkage and molecular evolution. Curr Biol 11 (17):R684–686.PubMedGoogle Scholar
  24. 24.
    Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc Lond B Biol Sci 351 (1345):1291–1298.Google Scholar
  25. 25.
    Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13 (5):1143–1155.PubMedGoogle Scholar
  26. 26.
    Normark BB, Judson OP, Moran NA (2003) Genomic signatures of ancient asexual lineages. Biol J Lin Soc 79:69–84.Google Scholar
  27. 27.
    Lercher MJ, Hurst LD (2002) Human SNP variability and mutation rate are higher in regions of high recombination. Trends Genet 18 (7):337–340.PubMedGoogle Scholar
  28. 28.
    Hellmann I, Ebersberger I, Ptak SE, Paabo S, Przeworski M (2003) A neutral explanation for the correlation of diversity with recombination rates in humans. Am J Hum Genet 72 (6):1527–1535.PubMedGoogle Scholar
  29. 29.
    Longman-Jacobsen N, Williamson JF, Dawkins RL, Gaudieri S (2003) In polymorphic genomic regions indels cluster with nucleotide polymorphism: Quantum Genomics. Gene 312:257–261.PubMedGoogle Scholar
  30. 30.
    Tian D, Wang Q, Zhang P, Araki H, Yang S, Kreitman M, Nagylaki T, Hudson R, Bergelson J, Chen JQ (2008) Single-nucleotide mutation rate increases close to insertions/deletions in eukaryotes. Nature 455 (7209):105–108.PubMedGoogle Scholar
  31. 31.
    Hollister JD, Ross-Ibarra J, Gaut BS (2010) Indel-associated mutation rate varies with mating system in flowering plants. Mol Biol Evol 27 (2):409–416.Google Scholar
  32. 32.
    Kimura M (1962) On the probability of fixation of mutant genes in a population. Genetics 47:713–719.PubMedGoogle Scholar
  33. 33.
    Paland S, Lynch M (2006) Transitions to asexuality result in excess amino acid substitutions. Science 311 (5763):990–992.PubMedGoogle Scholar
  34. 34.
    Johnson SG, Howard RS (2007) Contrasting patterns of synonymous and nonsynonymous sequence evolution in asexual and sexual freshwater snail lineages. Evolution 61 (11):2728–2735.PubMedGoogle Scholar
  35. 35.
    Neiman M, Hehman G, Miller JT, Logsdon JM, Jr., Taylor DR (2010) Accelerated mutation accumulation in asexual lineages of a freshwater snail. Mol Biol Evol 27 (4):954–963.PubMedGoogle Scholar
  36. 36.
    Wright SI, Lauga B, Charlesworth D (2002) Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol Biol Evol 19 (9):1407–1420.PubMedGoogle Scholar
  37. 37.
    Haudry A, Cenci A, Guilhaumon C, Paux E, Poirier S, Santoni S, David J, GlÕmin S (2008) Mating system and recombination affect molecular evolution in four Triticeae species. Genet Res 90 (1):97–109.Google Scholar
  38. 38.
    Escobar JS, Cenci A, Bolognini J, Haudry A, Laurent S, David J, Glemin S (2010) An integrative test of the dead-end hypothesis of selfing evolution in Triticeae (poaceae). Evolution 64 (10):2855–2872.Google Scholar
  39. 39.
    Cutter AD, Wasmuth JD, Washington NL (2008) Patterns of molecular evolution in Caenorhabditis preclude ancient origins of selfing. Genetics 178 (4):2093–2104.PubMedGoogle Scholar
  40. 40.
    Slotte T, Foxe JP, Hazzouri KM, Wright SI (2010) Genome-wide evidence for efficient positive and purifying selection in Capsella grandiflora, a plant species with a large effective population size. Mol Biol Evol 27 (8): 1813–1821.PubMedGoogle Scholar
  41. 41.
    Charlesworth D, Morgan MT, Charlesworth B (1993) Mutation accumulation in finite outbreeding and inbreeding populations. Genet Res 61:39–56.Google Scholar
  42. 42.
    Hill WG, Robertson AW (1966) The effect of genetic linkage on the limits to artificial selection. Genet Res 8:269–294.PubMedGoogle Scholar
  43. 43.
    Bullaughey K, Przeworski M, Coop G (2008) No effect of recombination on the efficacy of natural selection in primates. Genome Res 18 (4):544–554.PubMedGoogle Scholar
  44. 44.
    Haddrill PR, Halligan DL, Tomaras D, Charlesworth B (2007) Reduced efficacy of selection in regions of the Drosophila genome that lack crossing over. Genome Biol 8 (2):R18.PubMedGoogle Scholar
  45. 45.
    Charlesworth B (1992) Evolutionary rates in partially self-fertilizing species. Am Nat 140 (1):126–148.PubMedGoogle Scholar
  46. 46.
    Glémin S (2007) Mating systems and the efficacy of selection at the molecular level. Genetics 177 (2):905–916.PubMedGoogle Scholar
  47. 47.
    Charlesworth B, Charlesworth D (1997) Rapid fixation of deleterious alleles can be caused by Muller’s ratchet. Genet Res 70 (1):63–73.PubMedGoogle Scholar
  48. 48.
    Kirkpatrick M, Jenkins CD (1989) Genetic segregation and the maintenance of sexual reproduction. Nature 339 (6222):300–301.PubMedGoogle Scholar
  49. 49.
    Vicoso B, Charlesworth B (2006) Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet 7 (8):645–653.PubMedGoogle Scholar
  50. 50.
    Eyre-Walker A, Keightley PD (2009) Estimating the rate of adaptive molecular evolution in the presence of slightly deleterious mutations and population size change. Mol Biol Evol 26 (9):2097–2108.PubMedGoogle Scholar
  51. 51.
    Mandegar MA, Otto SP (2007) Mitotic recombination counteracts the benefits of genetic segregation. Proc Biol Sci 274 (1615):1301–1307.PubMedGoogle Scholar
  52. 52.
    Omilian AR, Cristescu ME, Dudycha JL, Lynch M (2006) Ameiotic recombination in asexual lineages of Daphnia. Proc Natl Acad Sci USA 103 (49):18638–18643.PubMedGoogle Scholar
  53. 53.
    Roze D, Lenormand T (2005) Self-fertilization and the evolution of recombination. Genetics 170:841–857.PubMedGoogle Scholar
  54. 54.
    Ross-Ibarra J (2007) Genome size and recombination in angiosperms: a second look. J Evol Biol 20 (2):800–806.PubMedGoogle Scholar
  55. 55.
    Dawson KJ (1998) Evolutionarily stable mutation rates. J Theor Biol 194 (1):143–157.PubMedGoogle Scholar
  56. 56.
    Kondrashov AS (1995) Modifiers of Mutation-Selection Balance – General-Approach and the Evolution of Mutation-Rates. Genet Res 66 (1):53–69.Google Scholar
  57. 57.
    Lynch M (2010) Evolution of the mutation rate. Trends Genet 26 (8):345–352.PubMedGoogle Scholar
  58. 58.
    Gladyshev E, Meselson M (2008) Extreme resistance of bdelloid rotifers to ionizing radiation. Proc Natl Acad Sci USA 105 (13):5139–5144.PubMedGoogle Scholar
  59. 59.
    Schoen DJ (2005) Deleterious mutation in related species of the plant genus Amsinckia with contrasting mating systems. Evolution 59 (11):2370–2377.PubMedGoogle Scholar
  60. 60.
    Baer CF, Joyner-Matos J, Ostrow D, Grigaltchik V, Salomon MP, Upadhyay A (2010) Rapid decline in fitness of mutation accumulation lines of gonochoristic (outcrossing) Caenorhabditis nematodes. Evolution 64 (11):3242–3253.PubMedGoogle Scholar
  61. 61.
    Brandvain Y, Haig D (2005) Divergent mating systems and parental conflict as a barrier to hybridization in flowering plants. Am Nat 166 (3):330–338.PubMedGoogle Scholar
  62. 62.
    Burt A, Trivers R (1998) Selfish DNA and breeding systems in plants. Proc R Soc Lond B 265:141–146.Google Scholar
  63. 63.
    Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3 (2):137–144.Google Scholar
  64. 64.
    Palopoli MF, Rockman MV, TinMaung A, Ramsay C, Curwen S, Aduna A, Laurita J, Kruglyak L (2008) Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans. Nature 454 (7207):1019–1022.PubMedGoogle Scholar
  65. 65.
    Cutter AD (2008) Reproductive evolution: symptom of a selfing syndrome. Curr Biol 18 (22):R1056–1058.PubMedGoogle Scholar
  66. 66.
    Spillane C, Schmid KJ, Laoueille-Duprat S, Pien S, Escobar-Restrepo JM, Baroux C, Gagliardini V, Page DR, Wolfe KH, Grossniklaus U (2007) Positive darwinian selection at the imprinted MEDEA locus in plants. Nature 448 (7151):349–352.PubMedGoogle Scholar
  67. 67.
    Kawabe A, Fujimoto R, Charlesworth D (2007) High diversity due to balancing selection in the promoter region of the Medea gene in Arabidopsis lyrata. Curr Biol 17 (21):1885–1889.PubMedGoogle Scholar
  68. 68.
    Budar F, Touzet P, De Paepe R (2003) The nucleo-mitochondrial conflict in cytoplasmic male sterilities revisited. Genetica 117 (1): 3–16.PubMedGoogle Scholar
  69. 69.
    Houliston GJ, Olson MS (2006) Nonneutral evolution of organelle genes in Silene vulgaris. Genetics 174 (4):1983–1994.PubMedGoogle Scholar
  70. 70.
    Ingvarsson PK, Taylor DR (2002) Genealogical evidence for epidemics of selfish genes. Proc Natl Acad Sci USA 99 (17):11265–11269.PubMedGoogle Scholar
  71. 71.
    Touzet P, Delph LF (2009) The effect of breeding system on polymorphism in mitochondrial genes of Silene. Genetics 181 (2): 631–644.PubMedGoogle Scholar
  72. 72.
    Foxe JP, Wright SI (2009) Signature of diversifying selection on members of the pentatricopeptide repeat protein family in Arabidopsis lyrata. Genetics 183 (2):663–672, 661SI-668SI.Google Scholar
  73. 73.
    Marais G (2003) Biased gene conversion: implications for genome and sex evolution. Trends Genet 19 (6):330–338.PubMedGoogle Scholar
  74. 74.
    Spencer CC, Deloukas P, Hunt S, Mullikin J, Myers S, Silverman B, Donnelly P, Bentley D, McVean G (2006) The influence of recombination on human genetic diversity. PLoS Genet 2 (9):e148.PubMedGoogle Scholar
  75. 75.
    Duret L, Galtier N (2009) Biased gene conversion and the evolution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet 10:285–311.PubMedGoogle Scholar
  76. 76.
    Galtier N, Duret L (2007) Adaptation or biased gene conversion? Extending the null hypothesis of molecular evolution. Trends Genet 23 (6):273–277.PubMedGoogle Scholar
  77. 77.
    Marais G, Mouchiroud D, Duret L (2001) Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proc Natl Acad Sci USA 98 (10):5688–5692.PubMedGoogle Scholar
  78. 78.
    Meunier J, Duret L (2004) Recombination drives the evolution of GC-content in the human genome. Mol Biol Evol 21 (6): 984–990.PubMedGoogle Scholar
  79. 79.
    Marais G, Charlesworth B, Wright SI (2004) Recombination and base composition: the case of the highly self-fertilizing plant Arabidopsis thaliana. Genome Biol 5 (7):R45.PubMedGoogle Scholar
  80. 80.
    Wright SI, Iorgovan G, Misra S, Mokhtari M (2007) Neutral evolution of synonymous base composition in the Brassicaceae. J Mol Evol 64 (1):136–141.PubMedGoogle Scholar
  81. 81.
    Carels N, Bernardi G (2000) Two classes of genes in plants. Genetics 154:1819–1825.PubMedGoogle Scholar
  82. 82.
    Wong GK, Wang J, Tao L, Tan J, Zhang J, Passey DA, Yu J (2002) Compositional gradients in Gramineae genes. Genome Res 12 (6):851–856.PubMedGoogle Scholar
  83. 83.
    Wang HC, Singer GA, Hickey DA (2004) Mutational bias affects protein evolution in flowering plants. Mol Biol Evol 21 (1):90–96.PubMedGoogle Scholar
  84. 84.
    Dolgin ES, Charlesworth B (2006) The fate of transposable elements in asexual populations. Genetics 174 (2):817–827.PubMedGoogle Scholar
  85. 85.
    Morgan MT (2001) Transposable element number in mixed mating populations. Genet Res 77 (3):261–275.PubMedGoogle Scholar
  86. 86.
    Zeyl C, Bell G, Green DM (1996) Sex and the spread of retrotransposon Ty3 in experimental populations of Saccharomyces cerevisiae. Genetics 143 (4):1567–1577.PubMedGoogle Scholar
  87. 87.
    Goddard MR, Greig D, Burt A (2001) Outcrossed sex allows a selfish gene to invade yeast populations. Proc Biol Sci 268 (1485): 2537–2542.PubMedGoogle Scholar
  88. 88.
    Sullender BW, Crease TJ (2001) The behavior of a Daphnia pulex transposable element in cyclically and obligately parthenogenetic populations. J Mol Evol 53 (1):63–69.PubMedGoogle Scholar
  89. 89.
    Valizadeh P, Crease TJ (2008) The association between breeding system and transposable element dynamics in Daphnia pulex. J Mol Evol 66 (6):643–654.PubMedGoogle Scholar
  90. 90.
    Schaack S, Pritham EJ, Wolf A, Lynch M (2010) DNA transposon dynamics in populations of Daphnia pulex with and without sex. P Roy Soc B-Biol Sci 277 (1692):2381–2387.Google Scholar
  91. 91.
    Arkhipova I, Meselson M (2000) Transposable elements in sexual and ancient asexual taxa. Proc Natl Acad Sci USA 97 (26): 14473–14477.PubMedGoogle Scholar
  92. 92.
    Arkhipova IR, Meselson M (2005) Diverse DNA transposons in rotifers of the class Bdelloidea. Proc Natl Acad Sci USA 102 (33):11781–11786.PubMedGoogle Scholar
  93. 93.
    Arkhipova I, Meselson M (2005) Deleterious transposable elements and the extinction of asexuals. Bioessays 27 (1):76–85.PubMedGoogle Scholar
  94. 94.
    Matzk F, Hammer K, Schubert I (2003) Coevolution of apomixis and genome size within the genus Hypericum. Sex Plant Reprod 16:51–58.Google Scholar
  95. 95.
    Wright SI, Schoen DJ (1999) Transposon dynamics and the breeding system. Genetica 107 (1–3):139–148.PubMedGoogle Scholar
  96. 96.
    Tam SM, Causse M, Garchery C, Burck H, Mhiri C, Grandbastien MA (2007) The distribution of copia-type retrotransposons and the evolutionary history of tomato and related wild species. J Evol Biol 20 (3):1056–1072.PubMedGoogle Scholar
  97. 97.
    Wright SI, Le QH, Schoen DJ, Bureau TE (2001) Population dynamics of an Ac-like transposable element in self- and cross-pollinating arabidopsis. Genetics 158 (3): 1279–1288.PubMedGoogle Scholar
  98. 98.
    Trivers R, Burt A, Palestis BG (2004) B chromosomes and genome size in flowering plants. Genome 47 (1):1–8.PubMedGoogle Scholar
  99. 99.
    Whitney KD, Baack EJ, Hamrick JL, Godt MJ, Barringer BC, Bennett MD, Eckert CG, Goodwillie C, Kalisz S, Leitch IJ, Ross-Ibarra J (2010) A role for nonadaptive processes in plant genome size evolution? Evolution 64 (7):2097–2109.Google Scholar
  100. 100.
    Albach DC, Greilhuber J (2004) Genome size variation and evolution in Veronica. Ann Bot 94 (6):897–911.PubMedGoogle Scholar
  101. 101.
    Ritland K (2002) Extensions of models for the estimation of mating systems using n independent loci. Heredity 88 (4):221–228.PubMedGoogle Scholar
  102. 102.
    Ritland K, Jain S (1981) A Model for the Estimation of Outcrossing Rate and Gene-Frequencies Using N Independent Loci. Heredity 47 (Aug):35–52.Google Scholar
  103. 103.
    Nordborg MD, P. (1997) The coalescent process with selfing. Genetics 146 (3): 1185–1195.Google Scholar
  104. 104.
    Gao H, Williamson S, Bustamante CD (2007) A Markov chain Monte Carlo approach for joint inference of population structure and inbreeding rates from multilocus genotype data. Genetics 176 (3): 1635–1651.PubMedGoogle Scholar
  105. 105.
    Halkett F, Simon JC, Balloux F (2005) Tackling the population genetics of clonal and partially clonal organisms. Trends Ecol Evol 20 (4):194–201.PubMedGoogle Scholar
  106. 106.
    Bomblies K, Yant L, Laitinen RA, Kim ST, Hollister JD, Warthmann N, Fitz J, Weigel D (2010) Local-scale patterns of genetic variability, outcrossing, and spatial structure in natural stands of Arabidopsis thaliana. PLoS Genet 6 (3):e1000890.PubMedGoogle Scholar
  107. 107.
    Grimsley N, Pequin B, Bachy C, Moreau H, Piganeau G (2010) Cryptic sex in the smallest eukaryotic marine green alga. Mol Biol Evol 27 (1):47–54.PubMedGoogle Scholar
  108. 108.
    Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, Robbens S, Partensky F, Degroeve S, Echeynie S, Cooke R, Saeys Y, Wuyts J, Jabbari K, Bowler C, Panaud O, Piegu B, Ball SG, Ral JP, Bouget FY, Piganeau G, De Baets B, Picard A, Delseny M, Demaille J, Van de Peer Y, Moreau H (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103 (31): 11647–11652.PubMedGoogle Scholar
  109. 109.
    Takebayashi N, Morrell PL (2001) Is self-fertilization an evolutionary deed end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach. Am J Bot 88 (7):1143–1150.PubMedGoogle Scholar
  110. 110.
    Goldberg EE, Igic B (2008) On phylogenetic tests of irreversible evolution. Evolution 62 (11):2727–2741.PubMedGoogle Scholar
  111. 111.
    Welch DM, Meselson M (2000) Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288 (5469):1211–1215.Google Scholar
  112. 112.
    Schaefer I, Domes K, Heethoff M, Schneider K, Schon I, Norton RA, Scheu S, Maraun M (2006) No evidence for the ‘Meselson effect’ in parthenogenetic oribatid mites (Oribatida, Acari). J Evol Biol 19 (1):184–193.PubMedGoogle Scholar
  113. 113.
    Schon I, Martens K (2003) No slave to sex. Proc R Soc Lond B 270 (1517):827–833.Google Scholar
  114. 114.
    Bechsgaard JS, Castric V, Charlesworth D, Vekemans X, Schierup MH (2006) The transition to self-compatibility in Arabidopsis thaliana and evolution within S-haplotypes over 10 Myr. Mol Biol Evol 23 (9): 1741–1750.PubMedGoogle Scholar
  115. 115.
    Tang C, Toomajian C, Sherman-Broyles S, Plagnol V, Guo YL, Hu TT, Clark RM, Nasrallah JB, Weigel D, Nordborg M (2007) The evolution of selfing in Arabidopsis thaliana. Science 317 (5841):1070–1072.PubMedGoogle Scholar
  116. 116.
    Foxe JP, Slotte T, Stahl EA, Neuffer B, Hurka H, Wright SI (2009) Recent speciation associated with the evolution of selfing in Capsella. Proc Natl Acad Sci USA 106 (13):5241–5245.PubMedGoogle Scholar
  117. 117.
    Guo YL, Bechsgaard JS, Slotte T, Neuffer B, Lascoux M, Weigel D, Schierup MH (2009) Recent speciation of Capsella rubella from Capsella grandiflora, associated with loss of self-incompatibility and an extreme bottleneck. Proc Natl Acad Sci USA 106 (13):5246–5251.PubMedGoogle Scholar
  118. 118.
    Judson OP, Normark BB (1996) Ancient asexual scandals. Trends Ecol Evol 11 (2):41–46.PubMedGoogle Scholar
  119. 119.
    Igic B, Bohs L, Kohn JR (2006) Ancient polymorphism reveals unidirectional breeding system shifts. Proc Natl Acad Sci USA 103 (5):1359–1363.PubMedGoogle Scholar
  120. 120.
    Ferrer MM, Good-Avila SV (2007) Macrophylogenetic analyses of the gain and loss of self-incompatibility in the Asteraceae. New Phytol 173 (2):401–414.PubMedGoogle Scholar
  121. 121.
    Goldberg EE, Kohn JR, Lande R, Robertson KA, Smith SA, Igic B (2010) Species selection maintains self-incompatibility. Science 330 (6003):493–495.PubMedGoogle Scholar
  122. 122.
    Fitzjohn RG, Maddison WP, Otto SP (2009) Estimating Trait-Dependent Speciation and Extinction Rates from Incompletely Resolved Phylogenies. Syst Biol 58 (6):595–611.PubMedGoogle Scholar
  123. 123.
    Maddison WP, Midford PE, Otto SP (2007) Estimating a binary character’s effect on speciation and extinction. Syst Biol 56 (5): 701–710.PubMedGoogle Scholar
  124. 124.
    Glémin S (2003) How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57 (12):2678–2687.PubMedGoogle Scholar
  125. 125.
    Richards AJ (1997) Plant breeding systems. 2 edn. Chapman & Hall Ltd, London.Google Scholar
  126. 126.
    Igic B, Kohn JR (2006) The distribution of plant mating systems: study bias against obligately outcrossing species. Evolution 60 (5): 1098–1103.PubMedGoogle Scholar
  127. 127.
    Orr HA, Unckless RL (2008) Population extinction and the genetics of adaptation. Am Nat 172 (2):160–169.PubMedGoogle Scholar
  128. 128.
    Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268.Google Scholar
  129. 129.
    Glémin S (2010) Surprising fitness consequences of GC-biased gene conversion: I. Mutation load and inbreeding depression. Genetics 185 (3):939–959.Google Scholar
  130. 130.
    Mark Welch DB, Meselson MS (2001) Rates of nucleotide substitution in sexual and anciently asexual rotifers. Proc Natl Acad Sci USA 98, 6720–6724PubMedGoogle Scholar
  131. 131.
    Barraclough TG, Fontaneto D, Ricci C, Herniou EA (2007) Evidence for inefficient selection against deleterious mutations in cytochrome oxidase I of asexual bdelloid rotifers. Mol Biol Evol 24, 1952–1962PubMedGoogle Scholar

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© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Institut des Sciences de l’Evolution, UMR5554Université Montpellier IIMontpellierFrance

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