Is self-fertilization an evolutionary dead end?

New Phytologist

Volumn 198, Issue 2, 2013, Pages 386-397

  Igic, Boris ^a   Busch, Jeremiah W ^b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Diversification; Effective population size; Levels of selection; Mating system; Statistical inference

Indexed keywords

ADAPTATION; AUTOGAMY; EFFECTIVE POPULATION SIZE; EVOLUTIONARY BIOLOGY; OUTCROSSING; PHYLOGENETICS; REPRODUCTIVE STRATEGY; SEXUAL SELECTION;

ANGIOSPERM; BIOLOGICAL MODEL; CROSS BREEDING; EVOLUTION; PHYLOGENY; PHYSIOLOGY; REVIEW; SELF FERTILIZATION;

ANGIOSPERMS; BIOLOGICAL EVOLUTION; CROSSES, GENETIC; MODELS, BIOLOGICAL; PHYLOGENY; SELF-FERTILIZATION;

EID: 84875485255     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12182     Document Type: Review

References (123)

1. Anderson IA, Busch JW. 2006. Relaxed pollinator-mediated selection weakens floral integration in self-compatible taxa of Leavenworthia. American Journal of Botany 93: 860-867.
2. Armbruster WS, Mulder CPH, Baldwin BG, Kalisz S, Wessa B, Nute H. 2002. Comparative analysis of late floral development and mating-system evolution in tribe Collinsieae (Scrophulariaceae SL). American Journal of Botany 89: 37-49.
3. Bachtrog D, Charlesworth B. 2002. Reduced adaptation of a non-recombining neo-Y chromosome. Nature 416: 323-326.
4. Baker HG. 1959. Reproductive methods as a factor in speciation in flowering plants. Cold Spring Harbor Symposia on Quantitative Biology 24: 177-191.
5. Baldwin BG, Kalisz S, Armbruster WS. 2011. Phylogenetic perspectives on diversification, diversity, and phytogeography of Collinsia and Tonella (Plantaginaceae). American Journal of Botany 98: 731-753.
6. Barrett SCH. 2002. The evolution of plant sexual diversity. Nature Reviews Genetics 3: 274-284.
7. Barrett SCH, Eckert CG. 1990. Variation and evolution of mating systems in seed plants. In: Kawano S, ed. Biological approaches and evolutionary trends in plants. London, UK: Academic Press, 229-254.
8. Barrett SCH, Harder LD. 1996. Ecology and evolution of plant mating. Trends in Ecology and Evolution 11: A73-A79.
9. Bartkowska MP, Johnston MO. 2009. Quantitative genetic variation in populations of Amsinckia spectabilis that differ in rate of self-fertilization. Evolution 63: 1103-1117.
10. Bernacchi D, Tanksley SD. 1997. An interspecific backcross of Lycopersicon esculentum L. hirsutum: linkage analysis and a QTL study of sexual compatibility factors and floral traits. Genetics 147: 861-877.
11. Bixby PJ, Levin DA. 1996. Response to selection on autogamy in Phlox. Evolution 50: 892-899.
12. Bull J, Charnov EL. 1985. On irreversible evolution. Evolution 39: 1149-1155.
13. Busch JW, Delph LF. 2012. The relative importance of reproductive assurance and automatic selection as hypotheses for the evolution of self-fertilization. Annals of Botany 109: 553-562.
14. Busch JW, Joly S, Schoen DJ. 2011. Demographic signatures accompanying the evolution of selfing in Leavenworthia alabamica. Molecular Biology and Evolution 28: 1717-1729.
15. Bustamante CD, Nielsen R, Sawyer SA, Olsen KM, Purugganan MD, Hartl DL. 2002. The cost of inbreeding in Arabidopsis. Nature 416: 531-534.
16. Byers DL, Waller DM. 1999. Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annual Review of Ecology, Evolution and Systematics 30: 479-513.
17. Carneiro M, Albert FW, Melo-Ferreira J, Galtier N, Gayral P, Blanco-Aguilar JA, Villafuerte R, Nachman MW, Ferrand N. 2012. Evidence for widespread positive and purifying selection across the European rabbit (Oryctolagus cuniculus) genome. Molecular Biology and Evolution 29: 1837-1849.
18. Charlesworth D. 2003. Effects of inbreeding on the genetic diversity of populations. Philosophical Transactions of the Royal Society of London B 358: 1051-1070.
19. Charlesworth D, Charlesworth B. 1995. Quantitative genetics in plants - the effect of the breeding system on genetic variability. Evolution 49: 911-920.
20. Charlesworth D, Morgan MT, Charlesworth B. 1993. Mutation accumulation in finite outbreeding and inbreeding populations. Genetical Research 61: 39-56.
21. Charlesworth D, Wright SI. 2001. Breeding systems and genome evolution. Current Opinion in Genetics and Development 11: 685-690.
22. Cheptou PO, Schoen DJ. 2007. Combining population genetics and demographical approaches in evolutionary studies of plant mating systems. Oikos 116: 271-279.
23. Crnokrak P, Barrett SCH. 2002. Purging the genetic load: a review of the experimental evidence. Evolution 56: 2347-2358.
24. Cutter AD, Wasmuth JD, Washington NL. 2008. Patterns of molecular evolution in Caenorhabditis preclude ancient origins of selfing. Genetics 178: 2093-2104.
25. Darlington C. 1939. The evolution of genetic systems. Cambridge, UK: Cambridge University Press.
26. Dobzhansky T. 1950. Evolution in the tropics. American Scientist 38: 209-221.
27. Eckert CG, Herlihy CR. 2004. Using a cost-benefit approach to understand the evolution of self-fertilization in plants: the perplexing case of Aquilegia canadensis (Ranunculaceae). Plant Species Biology 19: 159-173.
28. Escobar J, Cenci A, Bolognini J, Haudry A, Laurent S, David J, Glémin S. 2010. An integrated test of the dead-end hypothesis of selfing evolution in Triticeae (Poaceae). Evolution 64: 2855-2872.
29. Etienne RS, Rosindell J. 2012. Prolonging the past counteracts the pull of the present: protracted speciation can explain observed slowdowns in diversification. Systematic Biology 61: 204-213.
30. Eyre-Walker A, Keightley PD. 2009. Estimating the rate of adaptive molecular evolution in the presence of slightly deleterious mutations and population size change. Molecular Biology and Evolution 26: 2097-2108.
31. Fisher RA. 1941. Average excess and average effect of a gene substitution. Annals of Eugenics 11: 53-63.
32. Fishman L, Kelly AJ, Willis JH. 2002. Minor quantitative trait loci underlie floral traits associated with mating system divergence in Mimulus. Evolution 56: 2138-2155.
33. Fishman L, Stratton DA. 2004. The genetics of floral divergence and postzygotic barriers between outcrossing and selfing populations of Arenaria uniflora (Caryophyllaceae). Evolution 58: 296-307.
34. FitzJohn RG. 2012. Diversitree: comparative phylogenetic analyses of diversification in R. Methods in Ecology and Evolution 3: 1084-1092.
35. FitzJohn RG, Maddison WP, Otto SP. 2009. Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. Systematic Biology 58: 595-611.
36. Foxe JP, Slotte T, Stahl EA, Neuffer B, Hurka H, Wright SI. 2009. Recent speciation associated with the evolution of selfing in Capsella. Proceedings of the National Academy of Sciences, USA 106: 5241-5245.
37. Georgiady MS, Whitkus RW, Lord EM. 2002. Genetic analysis of traits distinguishing outcrossing and self-pollinating forms of currant tomato, Lycopersicon pimpinellifolium (Jusl.) Mill. Genetics 161: 333-344.
38. Glémin S. 2003. How are deleterious mutations purged? Drift versus nonrandom mating. Genetics 57: 2678-2687.
39. Glémin S, Bazin E, Charlesworth D. 2006. Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proceedings of the Royal Society of London, Series B: Biological Sciences 273: 3011-3019.
40. Glémin S, Ronfort J. 2013. Adaptation and maladaptation in selfing and outcrossing species: new mutations versus standing variation. Evolution 67: 225-240.
41. Goldberg EE, Igic B. 2008. On phylogenetic tests of irreversible evolution. Evolution 62: 2727-2741.
42. Goldberg EE, Igic B. 2012. Tempo and mode in plant breeding system evolution. Evolution 66: 3701-3709.
43. Goldberg EE, Kohn JR, Lande R, Robertson KA, Smith SA. 2010. Species selection maintains self-incompatibility. Science 330: 493-495.
44. Goodwillie C. 1999. Multiple origins of self-compatibility in Linanthus section Leptosiphon (Polemoniaceae): phylogenetic evidence from internal-transcribed-spacer sequence data. Evolution 53: 1387-1395.
45. Goodwillie C, Kalisz S, Eckert CG. 2005. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology, Evolution and Systematics 11: 15-39.
46. Goodwillie C, Ritland C, Ritland K. 2006. The genetic basis of floral traits associated with mating system evolution in Leptosiphon (Polemoniaceae): an analysis of quantitative trait loci. Evolution 60: 491-504.
47. Gossmann TI, Song BH, Windsor AJ, Mitchell-Olds T, Dixon CJ, Kapralov MV, Filatov DA, Eyre-Walker A. 2010. Genome wide analyses reveal little evidence for adaptive evolution in many plant species. Molecular Biology and Evolution 27: 1822-1832.
48. Gould SJ. 1982. Darwinism and the expansion of evolutionary theory. Science 216: 380-387.
49. Gould SJ. 2002. The structure of evolutionary theory. Cambridge, MA, USA: Harvard University Press.
50. Hartmann K, Wong D, Stadler T. 2012. Sampling trees from evolutionary models. Systematic Biology 59: 465-476.
51. Haudry A, Cenci A, Guilhaumon C, Paux E, Poirier S, Santoni S, David J, Glemin S. 2008. Mating system and recombination affect molecular evolution in four Triticeae species. Genetical Research 90: 97-109.
52. Heller R, Maynard Smith J. 1979. Does Muller's Ratchet work with selfing? Genetical Research 32: 289-293.
53. Herlihy CR, Eckert CG. 2002. Genetic cost of reproductive assurance in a self-fertilizing plant. Nature 416: 320-323.
54. Herlihy CR, Eckert CG. 2004. Experimental dissection of inbreeding and its adaptive significance in a flowering plant, Aquilegia canadensis (Ranunculaceae). Evolution 58: 2693-2703.
55. Herlihy CR, Eckert CG. 2007. Evolutionary analysis of a key floral trait in Aquilegia canadensis (Ranunculaceae): genetic variation in herkogamy and its effect on the mating system. Evolution 61: 1661-1674.
56. Holsinger KE. 1991. Mass-action models of plant mating systems: the evolutionary stability of mixed mating systems. American Naturalist 138: 606-622.
57. Holsinger KE. 2000. Reproductive systems and evolution in vascular plants. Proceedings of the National Academy of Sciences, USA 97: 7037-7042.
58. Igic B, Bohs L, Kohn JR. 2006. Ancient polymorphism reveals unidirectional breeding system shifts. Proceedings of the National Academy of Sciences, USA 103: 1359-1363.
59. Igic B, Kohn JR. 2006. The distribution of plant mating systems: study bias against obligately outcrossing species. Evolution 60: 1098-1103.
60. Igic B, Lande R, Kohn JR. 2008. Loss of self-incompatibility and its evolutionary consequences. International Journal of Plant Sciences 169: 93-104.
61. Ingvarsson PK. 2002. A metapopulation perspective on genetic diversity and differentiation in partially self-fertilizing plants. Evolution 56: 2368-2373.
62. Inoue K, Maki M, Masuda M. 1996. Evolution of Campanula flowers in relation to insect pollinators on islands. In: Lloyd DG, Barrett SCH, eds. Floral biology: studies of floral evolution in animal-pollinated plants. New York, NY, USA: Chapman and Hall, 377-401.
63. Jablonski D. 2008. Species selection: theory and data. Annual Review of Ecology, Evolution and Systematics 39: 501-524.
64. Jain SK. 1976. The evolution of inbreeding in plants. Annual Review of Ecology, Evolution and Systematics 7: 469-495.
65. Johnston MO, Porcher E, Cheptou PO, Eckert CG, Elle E, Geber MA, Kalisz S, Kelly JK, Moeller DA, Vallejo-Marin M et al. 2010. Correlations among fertility components can maintain mixed mating in plants. American Naturalist 173: 1-11.
66. Jordan CY, Otto SP. 2012. Functional pleiotropy and mating system evolution in plants: frequency-independent mating. Evolution 66: 957-972.
67. Kalisz S, Randle AM, Chaiffetz D, Faigeles M, Butera A, Beight C. 2012. Dichogamy correlates with outcrossing rate and defines the selfing syndrome in the mixed mating genus, Collinsia. Annals of Botany 109: 571-582.
68. Kalisz S, Vogler D, Hanley K. 2004. Context-dependent autonomous selfing yields reproductive assurance and adaptive mixed mating. Nature 430: 884-886.
69. Lande R, Schemske DW. 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39: 24-40.
70. Lewis PO. 2001. A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50: 913-925.
71. Lewontin RC. 1970. The units of selection. Annual Review of Ecology, Evolution and Systematics 1: 1-18.
72. Lin JZ, Ritland K. 1997. Quantitative trait loci differentiating the outbreeding Mimulus guttatus from the inbreeding Mimulus platycalyx. Genetics 146: 1115-1121.
73. Lloyd DG. 1979. Some reproductive factors affecting the selection of self-fertilization in plants. American Naturalist 113: 67-79.
74. Lloyd DG. 1992. Self-fertilization and cross-fertilization in plants. II. The selection of self-fertilization. International Journal of Plant Sciences 153: 370-380.
75. Lloyd DG, Schoen DJ. 1992. Self-fertilization and cross-fertilization in plants I. Functional dimensions. International Journal of Plant Sciences 153: 358-369.
76. Maddison WP. 2006. Confounding asymmetries in evolutionary diversification and character change. Evolution 60: 1743-1746.
77. Maddison WP, Midford PE, Otto SP. 2007. Estimating a binary character's effect on speciation and extinction. Systematic Biology 56: 701-710.
78. Magallon S, Sanderson MJ. 2001. Absolute diversification rates in angiosperm clades. Evolution 55: 1762-1780.
79. Mather K. 1943. Polygenic inheritance and natural selection. Biological Reviews 18: 32-64.
80. Morrell PL, Toleno DM, Lundy KE, Clegg MT. 2005. Low levels of linkage disequilibrium in wild barley (Hordeum vulgare ssp. spontaneum) despite high rates of self-fertilization. Proceedings of the National Academy of Sciences, USA 102: 2442-2447.
81. Nasrallah ME, Liu P, Sherman-Broyles S, Boggs NA, Nasrallah JB. 2004. Natural variation in expression of self-incompatibility in Arabidopsis thaliana: implications for the evolution of selfing. Proceedings of the National Academy of Sciences, USA 45: 16070-16074.
82. Ness RW, Wright SI, Barrett SCH. 2010. Mating-system variation, demographic history and patterns of nucleotide diversity in the tristylous plant Eichhornia paniculata. Genetics 184: 381-392.
83. Niklas K, Tiffney BH, Knoll AH. 1983. Patterns in land plant diversification. Nature 303: 614-616.
84. Nordborg M. 2000. Linkage disequilibrium, gene trees and selfing: ancestral recombination graph with partial self-fertilization. Genetics 154: 923-929.
85. Nosil P, Mooers AO. 2005. Testing hypotheses about ecological specialization using phylogenetic trees. Evolution 59: 2256-2263.
86. Okasha S. 2006. Evolution and the levels of selection. Oxford, UK: Oxford University Press.
87. Pagel M. 1994. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proceedings of the Royal Society B 255: 37-45.
88. Pagel M. 1999. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Systematic Biology 48: 612-622.
89. Pagel M, Meade A. 2006. Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. American Naturalist 167: 808-825.
90. Pettengill JB, Moeller DA. 2012. Tempo and mode of mating system evolution between incipient Clarkia species. Evolution 66: 1210-1225.
91. Pollak E. 1987. On the theory of partially inbreeding finite populations. I. Partial selfing. Genetics 117: 353-360.
92. Rabosky DL. 2010. Primary controls on species richness in higher taxa. Systematic Biology 59: 634-645.
93. Rabosky DL, McCune AR. 2010. Reinventing species selection with molecular phylogenies. Trends in Ecology and Evolution 25: 68-74.
94. R Development Core Team. 2012. R: a Language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
95. Robacker CD, Ascher PD. 1978. Restoration of pseudo-self-compatibility (PSC) in derivatives of a high-psc × no-psc cross in Nemesia strumosa Benth. Theoretical and Applied Genetics 53: 135-141.
96. Revell LJ, Harmon LJ, Glor RE. 2005. Underparameterized model of sequence evolution leads to bias in the estimation of diversification rates from molecular phylogenies. Systematic Biology 54: 973-983.
97. Roels SA, Kelly JK. 2011. Rapid evolution caused by pollinator loss in Mimulus guttatus. Evolution 65: 2541-2552.
98. Ross-Ibarra J. 2004. The evolution of recombination under domestication: a test of two hypotheses. American Naturalist 163: 105-112.
99. Runions CJ, Geber MA. 2000. Evolution of the self-pollinating flower in Clarkia xantiana (Onagraceae). I. Size and development of floral organs. American Journal of Botany 87: 1439-1451.
100. Schemske DW, Lande R. 1985. The evolution of self-fertilization and inbreeding depression in plants. II. Empirical observations. Evolution 39: 41-52.
101. Schluter D, Price TD, Mooers AØ, Ludwig D. 1997. Likelihood of ancestor states in adaptive radiation. Evolution 51: 1699-1711.
102. Schoen DJ, Brown AHD. 1991. Intraspecific variation in population gene diversity and effective population size correlates with the mating system in plants. Proceedings of the National Academy of Sciences, USA 88: 4494-4497.
103. Schoen DJ, Busch JW. 2008. On the evolution of self-fertilization in a metapopulation. International Journal of Plant Sciences 169: 119-127.
104. Schoen DJ, Morgan MT, Bataillon T. 1996. How does self-pollination evolve? Inferences from floral ecology and molecular genetic variation. Philosophical Transactions of the Royal Society B 351: 1281-1290.
105. Schultz ST, Lynch M. 1997. Mutation and extinction: the role of variable mutational effects, synergistic epistasis, and degree of outcrossing. Evolution 51: 1363-1371.
106. Sicard A, Lenhard M. 2011. The selfing syndrome: a model for studying the genetic and evolutionary basis of morphological adaptation in plants. Annals of Botany 107: 1433-1443.
107. 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. Molecular Biology and Evolution 27: 1813-1821.
108. Slotte T, Hazzouri KM, Stern D, Andolfatto P, Wright SI. 2012. Genetic architecture and adaptive significance of the selfing syndrome in Capsella. Evolution 66: 1360-1374.
109. Stanley SM. 1976. A theory of evolution above the species level. Proceedings of the National Academy of Sciences, USA 72: 646-650.
110. Stebbins GL. 1957. Self-fertilization and population variability in the higher plants. American Naturalist 91: 337-354.
111. Stebbins GL. 1974. Flowering plants: evolution above the species level. Cambridge, MA, USA: Harvard University.
112. Steinbachs JE, Holsinger KE. 2002. S-RNase-mediated gametophytic self-incompatibility is ancestral in eudicots. Molecular Biology and Evolution 19: 825-829.
113. Stephenson AG, Vogler DW, Good SV. 2000. Interrelationships among inbreeding depression, plasticity in the self-incompatibility system, and the mating system of Campanula rapunculoides L (Campanulaceae). Annals of Botany 85: 211-219.
114. Takebayashi N, Morrell PL. 2001. Is self-fertilization an evolutionary dead end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach. American Journal of Botany 88: 1143-1150.
115. Tsuchimatsu T, Kaiser P, Yew C-L, Bachelier JB, Shimizu K. 2012. Recent loss of self-incompatibility by degradation of the male component in allotetraploid Arabidopsis kamchatica. PLoS Genetics 8: e1002838.
116. Vallejo-Marin M, Barrett SCH. 2009. Modification of flower architecture during early stages in the evolution of self-fertilization. Annals of Botany 103: 951-962.
117. Van Valen L. 1973. A new evolutionary law. Evolutionary Theory 1: 1-30.
118. Williams GC. 1992. Natural selection: domains, levels, and challenges. New York, NY, USA: Oxford University Press.
119. Winn AA, Elle E, Kalisz S, Cheptou PO, Eckert CG, Goodwillie C, Johnston MO, Moeller DA, Ree RH, Sargent RD et al. 2011. Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating. Evolution 65: 3339-3359.
120. Wright SI, Andolfatto P. 2008. The impact of natural selection on the genome: emerging patterns in Drosophila and Arabidopsis. Annual Review of Ecology, Evolution, and Systematics 39: 193-213.
121. Wright SI, Lauga B, Charlesworth D. 2002. Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Molecular Biology and Evolution 19: 1407-1420.
122. Wright SI, Ness RW, Foxe JP, Barrett SCH. 2008. Genomic consequences of evolutionary transitions in plant reproductive systems. International Journal of Plant Sciences 169: 105-118.
123. Yang JY, Hodges SA. 2010. Early inbreeding depression selects for high outcrossing rates in Aquilegia formosa and Aquilegia pubescens. International Journal of Plant Sciences 171: 860-871.