Small and ugly? Phylogenetic analyses of the "selfing syndrome" reveal complex evolutionary fates of monomorphic primrose flowers

Evolution

Volumn 68, Issue 4, 2014, Pages 1042-1057

  de Vos, Jurriaan M ^a,b   Wüest, Rafael O ^a,c,d   Conti, Elena ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b BROWN UNIVERSITY   (United States)

^c SWISS FEDERAL RESEARCH INSTITUTE WSL   (Switzerland)

^d UNIVERSITÉ JOSEPH FOURIER   (France)

Author keywords

Breeding system; Floral evolution; Heterostyly; Homostyly; Phylogenetic comparative methods; Primula; Self incompatibility

Indexed keywords

AUTOGAMY; BAYESIAN ANALYSIS; COMPARATIVE STUDY; DICOTYLEDON; FLORAL TRAIT; MORPHOLOGY; PHYLOGENETICS; PHYLOGENY; REPRODUCTIVE STRATEGY; SELF INCOMPATIBILITY;

PRIMULA; PRIMULACEAE;

ANATOMY AND HISTOLOGY; BAYES THEOREM; EVOLUTION; FLOWER; GENETICS; PHYLOGENY; POPULATION GENETICS; PRIMULACEAE; REPRODUCTION; SELF-INCOMPATIBILITY (PLANT);

BAYES THEOREM; BIOLOGICAL EVOLUTION; FLOWERS; GENETICS, POPULATION; PHYLOGENY; PRIMULA; REPRODUCTION; SELF-INCOMPATIBILITY IN FLOWERING PLANTS;

EID: 84898057797     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12331     Document Type: Article

References (100)

1. Aarssen, L. W. 2000. Why are most selfers annuals? A new hypothesis for the fitness benefit of selfing. Oikos 89:606-612.
2. Anderson, I. A., and J. W. Busch 2006. Relaxed pollinator-mediated selection weakens floral integration in self-compatible taxa of Leavenworthia (Brassicaceae). Am. J. Bot. 93:860-867.
3. Angiosperm Phylogeny Group. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc. 161:105-121.
4. Baker, H. G. 1955. Self-compatibility and establishment after "long distance" dispersal. Evolution 9:347-348.
5. Barrett, S. C. H. 1992. Evolution and function of heterostyly. Springer-Verlag, Berlin, Germany.
6. Barrett, S. C. H. 2002. The evolution of plant sexual diversity. Nat. Rev. Genet. 3:274-284.
7. Barrett, S. C. H. 2003. Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond. Philos. Trans. R. Soc. Lond., Ser. B: Biol. Sci. 358:991-1004.
8. Barrett, S. C. H., and J. S. Shore 1987. Variation and evolution of breeding systems in the Turnera ulmifolia complex (Turneraceae). Evolution 41:340-354.
9. Barrett, S. C. H., and J. S. Shore 2008. New insights on heterostyly: comparative biology, ecology and genetics. Pp. 3-32 in V. Franklin-Tong, ed. Self-incompatibility in flowering plants: evolution, diversity and mechanisms. Springer-Verlag, Berlin, Germany.
10. Beaulieu, J. M., D.-C. Jhwueng, C. Boettiger, B. C. O'Meara 2012. Modeling stabilizing selection: expanding the Ornstein-Uhlenbeck model of adaptive evolution. Evolution 66:2369-2383.
11. Brunet, J. 1992. Sex allocation in hermaphrodite plants. Trends Ecol. Evol. 7:79-84
12. Burnham, K. P., and D. R. Anderson 2002. Model selection and multimodel inference: a practical information theoretic approach. Springer-Verlag, New York
13. Busch, J. W., and D. J. Schoen 2008. The evolution of self-incompatibility when mates are limiting. Trends Pl. Sci. 13:128-136.
14. Busch, J. W., and L. Urban 2011. Insights gained from 50 years of studying the evolution of self-compatibility in Leavenworthia (Brassicaceae). Evol. Biol. 38:15-27.
15. 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.
16. Butler, M. A., and A. A. King 2004. Phylogenetic comparative analysis: a modeling approach for adaptive evolution. Am. Nat. 164:683-695.
17. Carlson, M. L., S. D. Gisler, and S. Kelso 2008. The role of reproductive assurance in the arctic: a comparative study of a homostylous and distylous species pair. Arct. Antarct. Alp. Res. 40:39-47.
18. Charlesworth, B. 2009. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 10:195-205.
19. Chen, M. 2009. Comparative reproductive biology of Primula merrilliana Schltr. and P. cicutariifolia Pax. Plant Syst. Evol. 278:23-32.
20. Cohen, J. I. 2010. "A case to which no parallel exists": the influence of Darwin's different forms of flowers. Am. J. Bot. 97:701-716.
21. Cohen, J. I., and J. I. Davis 2012. Molecular phylogenetics, molecular evolution, and patterns of clade support in Lithospermum (Boraginaceae) and related taxa. Syst. Bot. 37:490-506.
22. Cresswell, J. E. 1998. Stabilizing selection and the structural variability of flowers within species. Ann. Bot. 81:463-473.
23. Cruden, R. W. 1977. Pollen-ovule ratios: a conservative index of breeding systems in flowering plants. Evolution 31:32-46.
24. Darwin, C. 1876. The effects of cross and self fertilization in the vegetable kingdom. John Murray, London.
25. de Vos, J. M., B. Keller, S. T. Isham, S. Kelso, and E. Conti 2012. Reproductive implications of floral variation in alpine Primroses: variation during anthesis and reproductive assurance in alpine environments. Funct. Ecol. 26:854-865.
26. Drummond, A. J., and A. Rambaut 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214.
27. Eckert, C. G., K. E. Samis, and S. Dart 2006. Reproductive assurance and the evolution of uniparental reproduction in flowering plants. in L. D. Harder and S. C. H. Barrett, eds. The ecology and evolution of flowers. Oxford Univ. Press, Oxford, U.K.
28. Ernst, A. 1938. Stammesgeschichtliche Untersuchungen zum Heterostylie-Problem. Untersuchungen an mono- und dimorphe Arten der Sektion Candelabra. Ber. Schweiz. Bot. Ges. 48:85-238.
29. Ernst, A. 1949. Addenda, Corrigenda und Desiderata zur Genetik des amphidiploiden Artbastardes Pr. kewensis. Arch. Julius Klaus Stift. Vererbungsforsch. Sozialanthropol. Rassenhyg. Zür. 24:17-104.
30. Ernst, A. 1953. Basic Numbers und Polyploidie und ihre Bedeutung für das Heterostylie-Problem. Arch. Julius Klaus Stift. Vererbungsforsch. Sozialanthropol. Rassenhyg. Zür. 28:1-159.
31. Ernst, A. 1955. Self-fertility in monomorphic Primulas. Genetica 27:391-448.
32. Ernst, A. 1956. Stammesgeschichtliche Untersuchungen zum Heterostylie-Problem. 4. Konvergenzen und Divergenzen in der Ausprägung der Heterostyly-Merkmale in Primula-Sektionen desselben Verbreitungsgebietes (Sektionen Muscarioides, Soldanelloideae und Capitatae). Arch. Julius Klaus Stift. Vererbungsforsch. Sozialanthropol. Rassenhyg. Zür. 31:129-247.
33. Ernst, A. 1959. Stammesgeschichtliche Untersuchungen zum Heterostylie-Problem. 5. Mono- und Dimorphismus in Primula-Sektion Sinenses Pax. Arch. Julius Klaus Stift. Vererbungsforsch. Sozialanthropol. Rassenhyg. Zür. 34:57-191.
34. Ernst, A. 1961. Stammesgeschichtliche Untersuchungen zum Heterostylie-Problem. 6. Obligater Blütendimorphismus in Primula-Sektion Sikkimensis Balf.f. Arch. Julius Klaus Stift. Vererbungsforsch. Sozialanthropol. Rassenhyg. Zür. 36:1-59.
35. Ernst, A. 1962. Stammesgeschichtliche Untersuchungen zum Heterostylie-Problem. 7. Stand des Nachweises monomorpher Arten, homostyler Sippen und anderer genetisch bedingter Abweichungen vom "klassischen" Blütendimorphismus in den Sektionen der Gattung Primula. Arch. Julius Klaus Stift. Vererbungsforsch. Sozialanthropol. Rassenhyg. Zür. 37:1-127.
36. Escobar, J. S., A. Cenci, J. Bolognini, A. Haudry, S. Laurent, J. David, and S. Glémin 2010. An integrative test of the dead-end hypothesis of selfing evolution in Triticeae (Poaceae). Evolution 64:2855-2872.
37. Fenster, C. B., and S. Martén-Rodríguez 2007. Reproductive assurance and the evolution of pollination specialization. Int. J. Plant Sci. 168:215-228.
38. Ferrer, M. M., and S. V. Good 2012. Self-sterility in flowering plants: preventing self-fertilization increases family diversification rates. Ann. Bot. 110:535-553.
39. FitzJohn, R. G. 2012. Diversitree: comparative phylogenetic analyses of diversification in R. Methods Ecol. Evol. 3:1084-1092.
40. 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. Natl. Acad. Sci. U.S.A. 106:5241-5245.
41. Ganders, F. R. 1979. The biology of heterostyly. N. Z. J. Bot. 17:607-635.
42. Glémin, S., and J. Ronfort 2013. Adaptation and maladaptation in selfing and outcrossing species: new mutations versus standing variation. Evolution 67:225-240.
43. Goldberg, E. E., J. R. Kohn, R. Lande, K. A. Robertson, S. A. Smith, and B. Igic 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., R. D. Sargent, C. G. Eckert, E. Elle, M. A. Geber, M. O. Johnston, S. Kalisz, D. A. Moeller, R. H. Ree, M. Vallejo-Marin, et al. 2010. Correlated evolution of mating system and floral display traits in flowering plants and its implications for the distribution of mating system variation. New Phytol. 185:311-321.
46. Graham, S. W., and S. C. H. Barrett 2004. Phylogenetic reconstruction of the evolution of stylar polymorphisms in Narcissus (Amaryllidaceae). Am. J. Bot. 91:1007-1021.
47. Grey-Wilson, C. 1989. The genus Dionysia. Alpine Garden Society, Woking, U.K.
48. Guerrant, E. O. 1989. Early maturity, small flowers and autogamy: a developmental connection? Pp. 61-84 in J. H. Bock and Y. B. Linhart, eds. The evolutionary ecology of plants. Westview Press, Boulder, CO.
49. Guggisberg, A., G. Mansion, S. Kelso, and E. Conti 2006. Evolution of biogeographic patterns, ploidy levels, and breeding systems in a diploid-polyploid species complex of Primula. New Phyt. 171:617-632.
50. Guggisberg, A., G. Mansion, and E. Conti 2009. Disentangling reticulate evolution in an arctic-alpine polyploid complex. Syst. Biol. 58:55-73.
51. 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. Natl. Acad. Sci. U.S.A. 106:5246-5251.
52. Hadfield, J. D. 2010. MCMC Methods for multi-response generalized linear mixed models: the MCMCglmm R Package. J. Stat. Softw. 33:1-22.
53. Haller, B. C., R. Mazzucco, and U. Dieckmann 2013. Evolutionary branching in complex landscapes. Am. Nat. 182:E127-E141.
54. Hamrick, J. L. M., and J. W. Godt 1996. Effects of life history traits on genetic diversity in plant species. Philos. Trans. R. Soc. Lond. Ser. B 351:1291-1298.
55. Hansen, T. F. 1997. Stabilizing selection and the comparative analysis of adaptation. Evolution 51:1341-1351.
56. Hansen, T. F., and E. P. Martins 1996. Translating between microevolutionary process and macroevolutionary patterns: the correlation structure of interspecific data. Evolution 50:1404-1417.
57. Herlihy, C. R., and C. G. Eckert 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.
58. Hu, C. M., and S. Kelso 1996. Primulaceae. Pp. 99-185 in Z. Y. Wu and P. H. Raven, eds. Flora of China, Vol. 15. Science Press, Bejing, China.
59. Huelsenbeck, J. P., R. Neilsen, and J. P. Bollback 2003. Stochastic mapping of morphological characters. Syst. Biol. 52:131-138.
60. Igic, B., R. Lande, and J. R. Kohn 2008. Loss of self-incompatibility and its evolutionary consequences. Int. J. Plant Sci. 169:93-104.
61. Karron, J. D., C. T. Ivey, R. J. Mitchell, M. R. Whitehead, R. Peakall, A. L. Case 2012. New perspectives on the evolution of plant mating systems Ann. Bot. 109:493-503.
62. Kohn, J. R., S. W. Graham, B. Morton, J. J. Doyle, and S. C. H. Barrett 1996. Reconstruction of the evolution of reproductive characters in Pontederiaceae using phylogenetic evidence from chloroplast DNA restriction-site variation. Evolution 50:1454-1469.
63. Lande, R. 1976. Natural selection and random genetic drift in phenotypic evolution. Evolution 30:314-334.
64. Lande, R. 1977. The influence of the mating system on the maintenance of genetic variability in polygenic characters. Genetics 86:485-498.
65. Levin, D. A. 1970. Developmental instability and evolution in peripheral isolates. Am. Nat. 104:343-353.
66. Lewis, D., and D. A. Jones 1992. The genetics of heterostyly. Pp. 129-150. in S. C. H. Barrett, ed. Evolution and function of heterostyly. Springer-Verlag, Berlin.
67. Lloyd, D. G. 1980. Demographic factors and mating patterns in angiosperms. Pp. 67-88 in O. T. Solbrig, ed. Botanical monographs. Vol. 15. Demography and evolution in plant populations. Blackwell Scientific Publications, Oxford, U.K.
68. Lynch, M., and W. G. Hill 1986. Phenotypic evolution by neutral mutation. Evolution 40:915-935.
69. Maddison, W. P., P. E. Midford, and S. P. Otto 2007. Estimating a binary character's effect on speciation and extinction. Syst. Biol. 56:701-710.
70. Mast, A. R., S. Kelso, A. J. Richards, D. L. Lang, and D. M. S. Feller, and E. Conti 2001. Phylogenetic relationships in Primula L. and related genera (Primulaceae) based on noncoding chloroplast DNA. Int. J. Plant Sci. 162:1381-1400.
71. Mast, A. R., D. M. S. Feller, S. Kelso, and E. Conti 2004. Buzz-pollinated Dodecatheon originated from within the heterostylous Primula subgenus Auriculastrum (Primulaceae): a seven-region cpDNA phylogeny and its implications for floral evolution. Am. J. Bot. 91:926-942.
72. Mast, A.R., D. Kelso, and E. Conti 2006. Are any primroses (Primula) primitively monomorphic? New Phytol. 171:605-616.
73. Münkemüller, T., S. Lavergne, B. Bzeznik, S. Dray, T. Jombart, K. Schiffers, W. Thuiller 2012. How to measure and test phylogenetic signal. Methods Ecol. Evol. 3:743-756.
74. Naiki, A. 2012. Heterostyly and the possibility of its breakdown by polyploidization. Plant Species Biol. 27:3-29.
75. O'Meara, B. C., C. Ane, M. J. Sanderson, and P. C. Wainwright 2006. Testing for different rates of continuous trait evolution. Evolution 60:922-933.
76. Ornduff, R. 1969. Reproductive biology in relation to systematics. Taxon 18:121-133.
77. Pagel, M. 1999. Inferring the historical patterns of biological evolution. Nature 401:877-884.
78. Piper, J. G., B. Charlesworth, and D. C. Charlesworth 1984. A high rate of self-fertilization and increased seed fertility of homostyle Primroses. Nature 310:50-51.
79. Price, S. A., J. J. Tavera, T. J. Near, and P. C. Wainwright 2013. Elevated rates of morphological and functional diversification in reef-dwelling Haemulid fishes. Evolution 67:417-428.
80. Raduski, A. R., E. B. Haney, and B. Igic 2012. The expression of self-incompatibility in angiosperms is bimodal. Evolution 66:1275-1283.
81. Reveal, J. L. 2009. Dodecatheon. Fl. N. Amer. 8:268-286.
82. Revell, L. J. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3:217-223.
83. Richards, A. J. 2003. Primula. 2nd ed. Batsford, London.
84. Ritland, C., and K. Ritland 1989. Variation of sex allocation among eight taxa of the Mimulus guttatus species complex (Scrophulariaceae). Am. J. Bot. 76:1731-1739.
85. Rosas-Guerrero, V., M. Quesada, W. S. Armbruster, R. Pérez-Barrales, and S. D. Smith 2011. Influence of pollination specialization and breeding system on floral integration and phenotypic variation in Ipomoea. Evolution 65:350-364.
86. Schoen, D. J., M. O. Johnston, A.-M. L'Heureux, and J. V. Marsolais 1997. Evolutionary history of the mating system in Amsinckia (Boraginaceae). Evolution 51:1090-1099.
87. Scott, J. 1865. Observations on the structure and function of the reproductive organs of the Primulaceae. J. Linn. Soc., Bot. 8:78-126.
88. Sicard, A., and M. Lenhard 2011. The selfing syndrome: a model for studying the genetic and evolutionary basis of morphological adaptation in plants. Ann. Bot. 107:1433-1443.
89. Sicard, A., N. Stacey, K. Hermann, J. Dessoly, B. Neuffer, and M. Lenhard 2011. Genetics, evolution, and adaptive significance of the selfing syndrome in the genus Capsella. Plant Cell 23:3156-3171.
90. Slotte, T., J. P. Foxe, K. M. Hazzouri, and S. I. Wright 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.
91. Slotte, T., K. M. Hazzouri, D. Stern, P. Andolfatto, and S. I. Wright 2012. Genetic architecture and adaptive significance of the selfing syndrome in Capsella. Evolution 66:1360-1374.
92. Stebbins, G. L. 1950. Variation and evolution in plants. Columbia Univ. Press, New York.
93. Stebbins, G. L. 1970. Adaptive radiation of reproductive characteristics in angiosperms. I: Pollination mechanisms. Annu. Rev. Ecol. Syst. 1:307-326.
94. 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.
95. Tippery, N. P., and D. H. Les 2011. Phylogenetic relationships and morphological evolution in Nymphoides (Menyanthaceae). Syst. Bot. 36:1101-1113.
96. Truyens, S., M. M. Arbo, and J. S. Shore 2005. Phylogenetic relationships, chromosome and breeding system evolution in Turnera (Turneraceae): inferences from ITS sequence data. Am. J. Bot. 92:1749-1758.
97. Vallejo-Marín, M., and S. C. H. Barrett 2009. Modification of flower architecture during early stages in the evolution of self-fertilization. Ann. Bot. 103:951-962.
98. Washitani, I., R. Osawa, H. Namai, and M. Niwa 1994. Patterns of female fertility in heterostylous Primula sieboldii under severe pollinator limitation. J. Ecol. 82:571-579.
99. Wedderburn, F. M., and A. J. Richards 1992. Secondary homostyly in Primula L.; evidence for the model of the 'S' supergene. New Phytol. 121:649-655.
100. Wright, S. I., R. W. Ness, J. P. Foxe, and S. C. H. Barrett 2008. Genomic consequences of outcrossing and selfing in plants. Int. J. Plant Sci. 169:105-118.