Mating systems and selection efficacy: A test using chloroplastic sequence data in Angiosperms

Journal of Evolutionary Biology

Volumn 27, Issue 7, 2014, Pages 1386-1399

  Glemin S ^a   Muyle, A ^b  

^a INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^b LABORATOIRE DE BIOMÉTRIE ET BIOLOGIE EVOLUTIVE   (France)

Author keywords

Chloroplast; Deleterious mutations; dN dS ratio; Mating systems; Selection; Selfing

Indexed keywords

ANGIOSPERM; AUTOGAMY; CHLOROPLAST; EVOLUTIONARY BIOLOGY; EXTINCTION; FITNESS; GENOMICS; HYPOTHESIS TESTING; MUTATION; NATURAL SELECTION; OUTCROSSING; REPRODUCTIVE STRATEGY;

MAGNOLIOPHYTA;

ANGIOSPERM; ASEXUAL REPRODUCTION; CHLOROPLAST; COMPUTER SIMULATION; CROSS BREEDING; EVOLUTION; GENETIC SELECTION; GENETICS; MUTATION; PHYSIOLOGY;

ANGIOSPERMS; BIOLOGICAL EVOLUTION; CHLOROPLASTS; COMPUTER SIMULATION; CROSSES, GENETIC; MUTATION; REPRODUCTION, ASEXUAL; SELECTION, GENETIC;

EID: 84903442692     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12356     Document Type: Article

References (78)

1. Abramowitz, M. & Stegun, I.A. 1970. Handbook of Mathematical Functions, 9th edn. Dover, New York.
2. Agrawal, A.F. & Lively, C.M. 2001. Parasites and the evolution of self-fertilization. Evolution 55: 869-879.
3. Agrawal, A.F. & Whitlock, M.C. 2012. Mutation load: the fitness of individuals in populations where deleterious alleles are abundant. Annu. Rev. Ecol. Evol. Syst. 43: 115-135.
4. Armbruster, W.S., Perez-Barrales, R., Arroyo, J., Edwards, M.E. & Vargas, P. 2006. Three-dimensional reciprocity of floral morphs in wild flax (Linum suffruticosum): a new twist on heterostyly. New Phytol. 171: 581-590.
5. Barraclough, T.G., Fontaneto, D., Ricci, C. & Herniou, E.A. 2007. Evidence for inefficient selection against deleterious mutations in cytochrome oxidase I of asexual bdelloid rotifers. Mol. Biol. Evol. 24: 1952-1962.
6. Barrett, S.C., Harder, L.D. & Worley, A.C. 1996. The comparative biology of pollination and mating in flowering plants. Philos. Trans. Roy. Soc. London B 351: 1271-1280.
7. Bechsgaard, J.S., Castric, V., Charlesworth, D., Vekemans, X. & Schierup, M.H. 2006. The transition to self-compatibility in Arabidopsis thaliana and evolution within S-haplotypes over 10 Myr. Mol. Biol. Evol. 23: 1741-1750.
8. Bena, G., Lejeune, B., Prosperi, J.M. & Olivieri, I. 1998. Molecular phylogenetic approach for studying life-history evolution: the ambiguous example of the genus Medicago L. Proc. Biol. Sci. 265: 1141-1151.
9. Billiard, S., Lopez-Villavicencio, M., Devier, B., Hood, M.E., Fairhead, C. & Giraud, T. 2011. Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types. Biol. Rev. Camb. Philos. Soc. 86: 421-442.
10. Brandvain, Y., Slotte, T., Hazzouri, K.M., Wright, S.I. & Coop, G. 2013. Genomic identification of founding haplotypes reveal the history of the selfing species Capsella rubella. PLoS Genet. 9: e1003754.
11. Caballero, A. & Hill, W.G. 1992. Effects of partial inbreeding on fixation rates and variation of mutant genes. Genetics 131: 493-507.
12. Charlesworth, B. 1992. Evolutionary rates in partially self-fertilizing species. Am. Nat. 140: 126-148.
13. Charlesworth, B., Morgan, M.T. & Charlesworth, D. 1993. The effect of deleterious mutations on neutral molecular variation. Genetics 134: 1289-1303.
14. Cutter, A.D. & Payseur, B.A. 2003. Selection at linked sites in the partial selfer Caenorhabditis elegans. Mol. Biol. Evol. 20: 665-673.
15. Cutter, A.D., Wasmuth, J.D. & Washington, N.L. 2008. Patterns of molecular evolution in Caenorhabditis preclude ancient origins of selfing. Genetics 178: 2093-2104.
16. Edgar, R.C. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
17. Escobar, J.S., Cenci, A., Bolognini, J., Haudry, A., Laurent, S., David, J. et al. 2010. An integrative test of the dead-end hypothesis of selfing evolution in Triticeae (poaceae). Evolution 64: 2855-2872.
18. Eyre-Walker, A., Woolfit, M. & Phelps, T. 2006. The distribution of fitness effects of new deleterious amino acid mutations in humans. Genetics 173: 891-900.
19. Ferrer, M.M. & Good-Avila, S.V. 2007. Macrophylogenetic analyses of the gain and loss of self-incompatibility in the Asteraceae. New Phytol. 173: 401-414.
20. Fiz, O., Vargas, P., Alarcon, M., Aedo, C., Garcia, J.L. & Aldasoro, J.J. 2008. Phylogeny and historical biogeography of Geraniaceae in relation to climate changes and pollination ecology. Syst. Bot. 33: 326-342.
21. Foxe, J.P., Dar, V.U., Zheng, H., Nordborg, M., Gaut, B.S. & Wright, S.I. 2008. Selection on amino acid substitutions in Arabidopsis. Mol. Biol. Evol. 25: 1375-1383.
22. Gioti, A., Mushegian, A.A., Strandberg, R., Stajich, J.E. & Johannesson, H. 2012. Unidirectional evolutionary transitions in fungal mating systems and the role of transposable elements. Mol. Biol. Evol. 29: 3215-3226.
23. Gioti, A., Stajich, J. & Johannesson, H. 2013. Neurospora and the dead-end hypothesis: genomic consequences of selfing in the model genus. Evolution 67: 3600-3616.
24. Glémin, S. 2007. Mating systems and the efficacy of selection at the molecular level. Genetics 177: 905-916.
25. Glémin, S. & Galtier, N. 2012. Genome evolution in outcrossing versus selfing versus asexual species. Methods Mol. Biol. 855: 311-335.
26. Glémin, S. & Ronfort, J. 2013. Adaptation and maladaptation in selfing and outcrossing species: new mutations versus standing variation. Evolution 67: 225-240.
27. Glémin, S., Bazin, E. & Charlesworth, D. 2006. Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proc. Biol. Sci. 273: 3011-3019.
28. Goldberg, E.E. & Igic, B. 2012. Tempo and mode in plant breeding system evolution. Evolution 66: 3701-3709.
29. Goldberg, E.E., Kohn, J.R., Lande, R., Robertson, K.A., Smith, S.A. & Igic, B. 2010. Species selection maintains self-incompatibility. Science 330: 493-495.
30. Gossmann, T.I., Song, B.H., Windsor, A.J., Mitchell-Olds, T., Dixon, C.J., Kapralov, M.V. et al. 2010. Genome wide analyses reveal little evidence for adaptive evolution in many plant species. Mol. Biol. Evol. 27: 1822-1832.
31. Haudry, A., Cenci, A., Guilhaumon, C., Paux, E., Poirier, S., Santoni, S. et al. 2008. Mating system and recombination affect molecular evolution in four Triticeae species. Genet. Res. 90: 97-109.
32. Hazzouri, K.M., Escobar, J.S., Ness, R.W., Killian Newman, L., Randle, A.M., Kalisz, S. et al. 2013. Comparative population genomics in Collinsia sister species reveals evidence for reduced effective population size, relaxed selection, and evolution of biased gene conversion with an ongoing mating system shift. Evolution 67: 1263-1278.
33. Henry, L., Schwander, T. & Crespi, B.J. 2012. Deleterious mutation accumulation in asexual Timema stick insects. Mol. Biol. Evol. 29: 401-408.
34. Hersch-Green, E.I., Myburg, H. & Johnson, M.T. 2012. Adaptive molecular evolution of a defence gene in sexual but not functionally asexual evening primroses. J. Evol. Biol. 25: 1576-1586.
35. Hudson, R.R. & Kaplan, N.L. 1995. Deleterious background selection with recombination. Genetics 141: 1605-1617.
36. Igic, B. & Busch, J.W. 2013. Is self-fertilization an evolutionary dead end? New Phytol. 198: 386-397.
37. Igic, B., Bohs, L. & Kohn, J.R. 2006. Ancient polymorphism reveals unidirectional breeding system shifts. Proc. Natl. Acad. Sci. USA 103: 1359-1363.
38. Igic, B., Lande, R. & Kohn, J.R. 2008. Loss of self-incompatibility and its evolutionary consequences. Int. J. Plant Sci. 169: 93-104.
39. Ingvarsson, P.K. 2002. A metapopulation perspective on genetic diversity and differentiation in partially self-fertilizing plants. Evolution: Int. J. Org. Evolution 56: 2368-2373.
40. Jarne, P. & Auld, J.R. 2006. Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals. Evolution: Int. J. Org. Evolution 60: 1816-1824.
41. Johnson, S.G. & Howard, R.S. 2007. Contrasting patterns of synonymous and nonsynonymous sequence evolution in asexual and sexual freshwater snail lineages. Evolution: Int. J. Org. Evolution 61: 2728-2735.
42. Kapralov, M.V. & Filatov, D.A. 2007. Widespread positive selection in the photosynthetic Rubisco enzyme. BMC Evol. Biol. 7: 73.
43. Kissling, J. & Barrett, S.C. 2013. Variation and evolution of herkogamy in Exochaenium (Gentianaceae): implications for the evolution of distyly. Ann. Bot. 112: 95-102.
44. Kohn, J.R., Graham, S.W., Morton, B., Doyle, J.J. & Barrett, S.C.H. 1996. Reconstruction of the evolution of reproductive characters in Pontederiaceae using phylogenetic evidence from chloroplast DNA restriction-site variation. Evolution 50: 1454-1469.
45. Lande, R. 1994. Risk of population extinction from fixation of new deleterious mutations. Evolution 48: 1460-1469.
46. Lynch, M., Conery, J. & Bürger, R. 1995. Mutational meltdowns in sexual populations. Evolution 49: 1067-1080.
47. Mark Welch, D.B. & Meselson, M.S. 2001. Rates of nucleotide substitution in sexual and anciently asexual rotifers. Proc. Natl. Acad. Sci. USA 98: 6720-6724.
48. Mast, A.R., Kelso, S. & Conti, E. 2006. Are any primroses (Primula) primitively monomorphic? New Phytol. 171: 605-616.
49. Maynard-Smith, J. & Haigh, D. 1974. The hitch-hiking effect of a favourable gene. Genet. Res. 23: 23-35.
50. Morran, L.T., Schmidt, O.G., Gelarden, I.A., Parrish, R.C. & Lively, C.M. 2011. Running with the Red Queen: host-parasite coevolution selects for biparental sex. Science 333: 216-218.
51. Muller, K. & Albach, D.C. 2010. Evolutionary rates in Veronica L. (Plantaginaceae): disentangling the influence of life history and breeding system. J. Mol. Evol. 70: 44-56.
52. Neiman, M., Hehman, G., Miller, J.T., Logsdon, J.M. Jr & Taylor, D.R. 2010. Accelerated mutation accumulation in asexual lineages of a freshwater snail. Mol. Biol. Evol. 27: 954-963.
53. Ness, R.W., Siol, M. & Barrett, S.C. 2012. Genomic consequences of transitions from cross- to self-fertilization on the efficacy of selection in three independently derived selfing plants. BMC Genomics 13: 611.
54. Nordborg, M.D.P. 1997. The coalescent process with selfing. Genetics 146: 1185-1195.
55. Nordborg, M. 2000. Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Genetics 154: 923-929.
56. Nygren, K., Strandberg, R., Wallberg, A., Nabholz, B., Gustafsson, T., Garcia, D. et al. 2011. A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi. Mol. Phylogenet. Evol. 59: 649-663.
57. Ollivier, M., Gabaldon, T., Poulain, J., Gavory, F., Leterme, N., Gauthier, J.P. et al. 2012. Comparison of gene repertoires and patterns of evolutionary rates in eight aphid species that differ by reproductive mode. Genome Biol. Evol. 4: 155-167.
58. Paland, S. & Lynch, M. 2006. Transitions to asexuality result in excess amino acid substitutions. Science 311: 990-992.
59. Pollak, E. 1987. On the theory of partially inbreeding finite populations. I. Partial selfing. Genetics 117: 353-360.
60. Pollak, E. & Sabran, M. 1992. On the theory of partially inbreeding finite populations. III. Fixation probabilities under partial selfing when heterozygotes are intermediate in viability. Genetics 131: 979-985.
61. Qiu, S., Zeng, K., Slotte, T., Wright, S. & Charlesworth, D. 2011. Reduced efficacy of natural selection on codon usage bias in selfing Arabidopsis and Capsella species. Genome Biol. Evol. 3: 868-880.
62. Sakai, S. & Wright, S.J. 2008. Reproductive ecology of 21 coexisting Psychotria species (Rubiaceae): when is heterostyly lost? Biol. J. Linn. Soc. 93: 125-134.
63. Sakai, A.K., Weller, S.G., Wagner, W.L., Nepokroeff, M. & Culley, T.M. 2006. Adaptive radiation and evolution of breeding systems in Schiedea (Caryophyllaceae), an endemic Hawaiian genus. Ann. Mo. Bot. Gard. 93: 49-63.
64. Schoen, D.J. & Brown, A.H.D. 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.
65. Schultz, S.T. & Lynch, M. 1997. Mutation and extinction: the role of variable mutational effects, synergistic epistasis, beneficial mutations, and degree of outcrossing. Evolution 51: 1363-1371.
66. Slotte, T., Foxe, J.P., Hazzouri, K.M. & Wright, S.I. 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: 1813-1821.
67. Slotte, T., Hazzouri, K.M., Agren, J.A., Koenig, D., Maumus, F., Guo, Y.L. et al. 2013. The Capsella rubella genome and the genomic consequences of rapid mating system evolution. Nat. Genet. 45: 831-835.
68. Stebbins, G.L. 1957. Self fertilization and population variability in higher plants. Am. Nat. 91: 337-354.
69. Takebayashi, N. & Morrell, P.L. 2001. Is self-fertilization an evolutionary dead end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach. Am. J. Bot. 88: 1143-1150.
70. Tang, C., Toomajian, C., Sherman-Broyles, S., Plagnol, V., Guo, Y.L., Hu, T.T. et al. 2007. The evolution of selfing in Arabidopsis thaliana. Science 317: 1070-1072.
71. Tucker, A.E., Ackerman, M.S., Eads, B.D., Xu, S. & Lynch, M. 2013. Population-genomic insights into the evolutionary origin and fate of obligately asexual Daphnia pulex. Proc. Natl. Acad. Sci. USA, 39: 15740-15745.
72. Welch, J.J., Eyre-Walker, A. & Waxman, D. 2008. Divergence and polymorphism under the nearly neutral theory of molecular evolution. J. Mol. Evol. 67: 418-426.
73. Whittle, C.A., Sun, Y. & Johannesson, H. 2011. Evolution of synonymous codon usage in Neurospora tetrasperma and Neurospora discreta. Genome Biol. Evol. 3: 332-343.
74. Wright, S.I., Lauga, B. & Charlesworth, D. 2002. Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol. Biol. Evol. 19: 1407-1420.
75. Wright, S.I., Iorgovan, G., Misra, S. & Mokhtari, M. 2007. Neutral evolution of synonymous base composition in the Brassicaceae. J. Mol. Evol. 64: 136-141.
76. Wright, S.I., Nano, N., Foxe, J.P. & Dar, V.U. 2008. Effective population size and tests of neutrality at cytoplasmic genes in Arabidopsis. Genet. Res. (Camb) 90: 119-128.
77. Wright, S.I., Kalisz, S. & Slotte, T. 2013. Evolutionary consequences of self-fertilization in plants. Proc. Biol. Sci. 280: 20130133.
78. Yang, Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24: 1586-1591.