Tempo and mode of mating system evolution between incipient clarkia species

Evolution

Volumn 66, Issue 4, 2012, Pages 1210-1225

  Pettengill, James B ^a   Moeller, David A ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Coalescence; Divergence time; Incomplete lineage sorting; Phylogeography; Reproductive assurance; Self fertilization; Species delimitation

Indexed keywords

CHLOROPLAST DNA; MICROSATELLITE DNA; PLANT DNA;

AUTOGAMY; COALESCENCE; COMMON ANCESTRY; DIVERGENCE; EVOLUTIONARILY STABLE STRATEGY; HERB; LIFE HISTORY TRAIT; OUTCROSSING; PHYLOGENETICS; PHYLOGEOGRAPHY; SUBSPECIES;

ARTICLE; CELL NUCLEUS; CLARKIA; DNA SEQUENCE; EVOLUTION; GENETICS; GENOTYPE; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; REPRODUCTION; SELF FERTILIZATION;

BIOLOGICAL EVOLUTION; CELL NUCLEUS; CLARKIA; DNA, CHLOROPLAST; DNA, PLANT; EVOLUTION, MOLECULAR; GENOTYPE; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; REPRODUCTION; SELF-FERTILIZATION; SEQUENCE ANALYSIS, DNA;

CLARKIA; CLARKIA XANTIANA; MAGNOLIOPHYTA;

EID: 84859442132     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2011.01521.x     Document Type: Article

References (104)

1. Akaike, H. 1974. New look at statistical model identification. IEEE T. Automat. Contr. 19:716-723.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Arunyawat, U., W. Stephan, and T. Städler 2007. Using multilocus sequence data to assess population structure, natural selection, and linkage disequilibrium in wild tomatoes. Mol. Biol. Evol. 24:2310-2322.
4. Baker, H. G. 1955. Self-compatibility and establishment after long-distance dispersal. Evolution 9:349-350.
5. Baker, H. G. 1967. Support for Baker's law-as a rule. Evolution 21:853-856.
6. Barrett, S. C. H. 2002. The evolution of plant sexual diversity. Nat. Rev. Genet. 3:274-284.
7. Baum, D. A., and K. L. Shaw 1995. Genealogical perspectives on the species problem. Pp. 289-303 in P. C. Hock and A. G. Stevenson, eds. Experimental and molecular approaches to plant biosystematics. Missouri Botanical Garden, St. Louis.
8. Bazinet, A. L., and M. P. Cummings 2008. The Lattice Project: a grid research and production environment combining multiple grid computing models in M. H. W. Weber, ed. Distributed & grid computing-science made transparent for everyone. Principles, applications and supporting communities. Tectum Publishing House, Marburg
9. Becquet, C., and M. Przeworski 2009. Learning about modes of speciation by computational approaches. Evolution 63:2547-2562.
10. Berry, P. E., W. J. Hahn, K. J. Systma, J. C. Hall, and A. R. Mast 2004. Phylogenetic relationships and biogeography of Fuchsia (Onagraceae) based on noncoding nuclear and chloroplast DNA data. Am. J. Bot. 91:601-614.
11. Busch, J. W. 2005. The evolution of self-compatibility in geographically peripheral populations of Leavenworthia alabamica (Brassicaceae). Am. J. Bot. 92:1503-1512.
12. Busch, J. W., S. Joly, and D. J. Schoen 2011. Demographic signatures accompanying the evolution of selfing in Leavenworthia alabamica. Mol. Biol. Evol. 28:1717-1729.
13. Charlesworth, B., D. Charlesworth, and N. H. Barton 2003. The effects of genetic and geographic structure on neutral variation. Annu. Rev. Ecol. Syst. 34:99-125.
14. Charlesworth, D., M. T. Morgan, and B. Charlesworth 1993. Mutation accumulation in finite outbreeding and inbreeding populations. Genet. Res. 61:39-56.
15. Charlesworth, D., and S. I. Wright 2001. Breeding systems and genome evolution. Curr. Opin. Genet. Dev. 11:685-690.
16. Cheptou, P. O. 2004. Allee effect and self-fertilization in hermaphrodites: reproductive assurance in demographically stable populations. Evolution 58:2613-2621.
17. Cochran, M. E., and S. Ellner 1992. Simple methods for calculating age-based life history parameters for stage-structured populations. Ecol. Monogr. 62:345-364.
18. Cummings, M. P., M. C. Neel, and K. L. Shaw 2008. A genealogical approach to quantifying lineage divergence. Evolution 62:2411-2422.
19. De, A., and R. Durrett 2007. Stepping-stone spatial structure causes slow decay of linkage disequilibrium and shifts the site frequency spectrum. Genetics 176:969-981.
20. Drummond, A. J., and A. Rambaut 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214.
21. Eckhart, V. M., and M. A. Geber 1999. Character variation and geographic distribution of Clarkia xantiana (Onagraceae): flowers and phenology distinguish two subspecies. Madroño 46:117-125.
22. Eckhart, V. M., M. A. Geber, W. F. Morris, E. S. Fabio, P. Tiffin, and D. A. Moeller 2011. The geography of demography: long-term demographic studies and species distribution models reveal a species border limited by adaptation. Am. Nat. 178:526-543.
23. Eckhart, V. M., N. S. Rushing, G. M. Hart, and J. D. Hansen 2006. Frequency-dependent pollinator foraging in polymorphic Clarkia xantiana ssp. xantiana populations: implications for flower colour evolution and pollinator interactions. Oikos 112:412-421.
24. Eckhart, V. M., I. Singh, A. M. Louthan, A. J. Keledjian, A. Chu, D. A. Moeller, and M. A. Geber 2010. Plant-soil water relations and species border of Clarkia xantiana ssp. xantiana (Onagraceae). Int. J. Plant Sci. 171:749-760.
25. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nuc. Acids Res. 32:1792-1797.
26. Elle, E., and R. Carney 2003. Reproductive assurance varies with flower size in Collinsia parviflora (Scrophulariaceae). Am. J. Bot. 90:888-896.
27. Escobar, J. S., A. Cenci, J. Bolognini, A. Haudry, S. Laurent, J. David, and S. Glemin 2010. An integrative test of the dead-end hypothesis of selfing evolution in Triticeae (Poaceae). Evolution 64:2855-2872.
28. Fausto, J. A., V. M. Eckhart, and M. A. Geber 2001. Reproductive assurance and the evolutionary ecology of self-pollination in Clarkia xantiana (Onagraceae). Am. J. Bot. 88:1794-1800.
29. Fisher, R. A. 1941. Average excess and average effect of an allelic substitution. Ann. Eugenics 11:53-63.
30. Foxe, J. P., T. Slotte, E. A. Stahl, B. Neuffer, H. Hurka, and S. I. Wright 2009. Recent speciation associated with the evolution of selfing in Capsella. Proc. Nat. Acad. Sci. USA 106:5241-5245.
31. Foxe, J. P., M. Stift, A. Tedder, A. Haudry, S. I. Wright, and B. K. Mable 2010. Reconstructing origins of loss of self-incompatibility and selfing in North American Arabidopsis lyrata: a population genetic context. Evolution 64:495-510.
32. Gao, H., S. Williamson, and C. D. Bustamante 2007. A Markov Chain Monte Carlo approach for joint inference of population structure and inbreeding rates from multilocus genotype data. Genetics 176:1635-1651.
33. Geber, M. A., and V. M. Eckhart 2005. Experimental studies of adaptation in Clarkia xantiana. II. Fitness variation across a subspecies border. Evolution 59:521-531.
34. Glemin, S., E. Bazin, and D. Charlesworth 2006. Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proc. R. Soc. Lond. B. 273:3011-3019.
35. Goldberg, E. E., and B. Igic 2008. On phylogenetic tests of irreversible evolution. Evolution 62:2727-2741.
36. 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.
37. Goodwillie, C., S. Kalisz, and C. G. Eckert 2005. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annu. Rev. Ecol. Evol. Syst. 36:47-79.
38. Goudet, J. 1995. FSTAT v1.2: a computer program to calculate F- statistics. J. Hered. 86:485-486.
39. Guo, Y. L., J. S. Bechsgaard, T. Slotte, B. Neuffer, M. Lascoux, D. Weigel, and M. H. Schierup 2009. Recent speciation of Capsella rubella from Capsella grandiflora, associated with loss of self-incompatibility and an extreme bottleneck. Proc. Nat. Acad. Sci. USA 106:5246-5251.
40. Hamrick, J. L, and M. J. W. Godt 1996. Effects of life history traits on genetic diversity in plant species. Philos. Trans. R. Soc. Lond. B. 351:1291-1298.
41. Hasegawa, M., H. Kishino, and T. Yano 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22:160-174.
42. Heled, J., and A. J. Drummond 2010. Bayesian inference of species trees from multilocus data. Mol. Biol. Evol. 27:570-580.
43. Herlihy, C. R., and C. G. Eckert 2002. Genetic cost of reproductive assurance in a self-fertilizing plant. Nature 416:320-323.
44. Hey, J., and R. Nielsen 2004. Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747-760.
45. Hey, J., and R. Nielsen 2007. Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc. Nat. Acad. Sci. USA 104:2785-2790.
46. Hey, J., and J. Wakeley 1997. A coalescent estimator of the population recombination rate. Genetics 145:833-846.
47. Holsinger, K. E. 2000. Reproductive systems and evolution in vascular plants. Proc. Nat. Acad. Sci. USA 97:7037-7042.
48. Hudson, R. R., and J. A. Coyne 2002. Mathematical consequences of the genealogical species concept. Evolution 56:1557-1565.
49. Huelsenbeck, J. P., and F. Ronquist 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755.
50. Hudson, R. R., M. Slatkin and W. P. Maddison 1992. Estimation of levels of gene flow from DNA sequence data. Genetics 132:583-589.
51. Huson, D. H., and D. Bryant 2006. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23:254-267.
52. Igic, B., L. Bohs, and J. R. Kohn 2006. Ancient polymorphism reveals unidirectional breeding system transitions. Proc. Nat. Acad. Sci. USA 103:1359-1363.
53. Igic, B., R. Lande, and J. R. Kohn 2008. Loss of self-incompatibility and its evolutionary consequences. Int. J. Plant Sci. 169:93-104.
54. Jain, S. K. 1976. Evolution of inbreeding in plants. Annu. Rev. Ecol. Syst. 7:469-495.
55. Kalisz, S., D. W. Vogler, and K. M. Hanley 2004. Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 430:884-887.
56. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
57. Koch, M., B. Haubold, and T. Mitchell-Olds 2001. Molecular systematics of the Brassicaceae: evidence from coding plastidic matK and nuclear Chs sequences. Am. J. Bot. 88:534-544.
58. Kress, J. W., and D. L. Erickson 2007. A two-locus global DNA barcode for land plants: the coding rbcL gene complements the non-coding trnH-psbA spacer region. PLoS ONE 2:e560.
59. Librado, P., and Rozas, J. 2009. DNASP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452.
60. Lloyd, D. G. 1979. Some reproductive factors affecting the selection of self-fertilization in plants. Am. Nat. 113:67-79.
61. Lloyd, D. G. 1992. Self- and cross-fertilization in plants. II. The selection of self-fertilization. Int. J. Plant Sci. 153:370-380.
62. Mallett, J. 1995. A species definition for the Modern Synthesis. Trends Ecol. Evol. 10:294-299.
63. Meirmans, P. G., and P. H. Van Tienderen 2004. GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol. Ecol. Notes 4:792-794.
64. Moeller, D. A. 2005. Pollinator community structure and sources of spatial variation in plant-pollinator interactions in Clarkia xantiana ssp. xantiana. Oecologia 142:28-37.
65. Moeller, D. A. 2006. Geographic structure of pollinator communities, reproductive assurance, and the evolution of self-pollination. Ecology 87:1510-1522.
66. Moeller, D. A., and M. A. Geber 2005. Ecological context of the evolution of self-pollination in Clarkia xantiana: population size, plant communities, and reproductive assurance. Evolution 59:786-799.
67. Moeller, D. A., M. I. Tenaillon, and P. Tiffin 2007. Population structure and its effects on patterns of nucleotide polymorphism in teosinte (Zea mays ssp. parviglumis). Genetics 176:1799-1809.
68. Moeller, D. A., M. A. Geber, and P. Tiffin 2011. Population genetics and the evolution of geographic range limits in an annual plant. Am. Nat. 178:S44-S61.
69. Moeller, D. A., M. A. Geber, V. M. Eckhart, and P. Tiffin 2012. Reduced pollinator service and elevated pollen limitation at the geographic range limit of an annual plant. Ecology: In press
70. Morgan, M. T., and W. G. Wilson 2005. Self-fertilization and the escape from pollen limitation in variable pollination environments. Evolution 59:1143-1148.
71. Ness, R. W., S. I. Wright, and S. C. H. Barrett 2010. Mating-system variation, demographic history and patterns of nucleotide diversity in the tristylous plant Eichhornia paniculata. Genetics 184:381-392.
72. Nordborg, M. 2000. Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Genetics 154:923-929.
73. Nybom, H. 2004. Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol. Ecol. 13:1143-1155.
74. Pannell, J. R., and S. C. H. Barrett 1998. Baker's law revisited: reproductive assurance in a metapopulation. Evolution 52:657-668.
75. Pool, J. E., and C. F. Aquadro 2006. History and structure of sub-Saharan populations of Drosophila melanogaster. Genetics 174:915-929.
76. Posada, D., and K. A. Crandall 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
77. Ptak, S. E., and M. Przeworski 2002. Evidence for population growth in humans is confounded by fine-scale population structure. Trends. Genet. 18:559-563.
78. Rambaut, A., and A. J. Drummond 2009. TRACER. Available at University of Edinburgh, Edinburgh, U.K.
79. Richards, A. 1999. Plant breeding systems. Chapman and Hall, London, U.K.
80. Ronquist, F., and J. P. Huelsenbeck 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
81. Rosenberg, N. A. 2003. The shapes of neutral gene genealogies in two species: probabilities of monophyly, paraphyly, and polyphyly in a coalescent model. Evolution 57:1465-1477.
82. Runions, C. J., and M. A. Geber 2000. Evolution of the self-pollinating flower in Clarkia xantiana (Onagraceae). I. Size and development of floral organs. Am. J. Bot. 67:1439-1450.
83. Schoen, D. J., M. O. Johnston, A. L'Heureux, and J. V. Marsolais 1997. Evolutionary history of the mating system in Amsinckia (Boraginaceae). Evolution 51:1090-1099.
84. Schoen, D. J., M. T. Morgan, and T. Bataillon 1996. How does self-pollination evolve? Inferences from floral ecology and molecular genetic variation. Philos. Trans. R. Soc. Lond. B. 351:1281-1290.
85. Shaw, J., E. B. Lickey, J. T. Beck, S. B. Farmer, W. S. Liu, J. Miller, K. C. Siripun, C. T. Winder, E. E. Schilling, and R. L. Small 2005. The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am. J. Bot. 92:142-166.
86. Stadler, T., B. Haubold, C. Merino, W. Stephan, and P. Pfaffelhuber 2009. The impact of sampling schemes on the site frequency spectrum in nonequilibrium subdivided populations. Genetics 182:205-216.
87. Stebbins, G. L. 1957. Self-fertilization and population variability in the higher plants. Am. Nat. 91:337-354.
88. Stebbins, G. L. 1974. Flowering plants: evolution above the species level. Harvard Univ. Press, Cambridge, MA
89. Stephens, M., and P. Donnelly 2003. A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am. J. Hum. Genet. 73:1162-1169.
90. Stephens, M., N. Smith, and P. Donnelly 2001. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 68:978-989.
91. Strasburg, J. L., and L. H. Rieseberg 2009. How robust are "Isolation with Migration" analyses to violations of the IM model? A simulation study. Mol. Biol. Evol. 27:297- 310.
92. Sweigart, A. L., and J. H. Willis 2003. Patterns of nucleotide diversity are affected by mating system and asymmetric introgression in two species of Mimulus. Evolution 57:2490-2506.
93. Swofford, D. L. 2003. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0. Sinauer Associates, Sunderland
94. Taberlet, P., L. Gielly, G. Pautou, and J. Bouvet 1991. Universal primers for amplification of three noncoding regions of chloroplast DNA. Plant Mol. Biol. 17:1105-1109.
95. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
96. Takebayashi, N., and P. L. Morrell 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.
97. Tang, C., C. Toomajian, S. Sherman-Broyles, V. Plagnol, Y. L. Guo, T. T. Hu, R. M. Clark, J. B. Nasrallah, D. Weigel, and M. Nordborg 2007. The evolution of selfing in Arabidopsis thaliana. Science 317:1070-1072.
98. Thuillet, A. C., D. Bru, J. David, P. Roumet, S. Santoni, P. Sourdille, and T. Bataillon 2002. Direct estimation of mutation rate for 10 microsatellite loci in durum wheat, Triticum turgidum (L.) Thell. ssp durum desf. Mol. Biol. Evol. 19:122-125.
99. Uyenoyama, M. K., K. E. Holsinger, and D. M. Waller 1993. Ecological and genetic factors directing the evolution of self-fertilization. Oxford Surv. Evol. Biol. 9:327-381.
100. Watterson, G. A. 1975. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7:256-275.
101. Weir, B. S., and C. C. Cockerham 1984. Estimating F-statistics for the analysis of population structure. Evolution 38:1358-1370.
102. Wright, S. I., and B. S. Gaut 2005. Molecular population genetics and the search for adaptive evolution in plants. Mol. Biol. Evol. 22:506-519.
103. Woerner, A. E., M. P. Cox, and M. F. Hammer 2007. Recombination-filtered genomic datasets by information maximization. Bioinformatics 23:1851-1853.
104. Zwickl, D. J. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. diss., The University of Texas at Austin.