Disassortative mating, sexual specialization, and the evolution of gender dimorphism in heterodichogamous Acer opalus

Evolution

Volumn 62, Issue 7, 2008, Pages 1676-1688

  Gleiser, Gabriela ^a   Verdú, Miguel ^a   Segarra Moragues, José G ^a   González Martínez, Santiago C ^b   Pannell, John R ^c  

^a CDIS UV Generalitat Valenciana)   (Spain)

^b INIA   (Spain)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Acer; Gender specialization; Heterodichogamy; Intermorph mating; Paternity analysis; Sexual inconstancy

Indexed keywords

DECIDUOUS TREE; EVOLUTION; FITNESS; MATING BEHAVIOR; PATERNITY; POLYMORPHISM; REPRODUCTIVE SUCCESS; SEXUAL DIMORPHISM; SPECIALIZATION;

ACER; ARTICLE; BIOLOGICAL MODEL; COMPUTER SIMULATION; EVOLUTION; FLOWER; GENETIC SELECTION; PHYSIOLOGY; PLANT SEED; SEXUAL DEVELOPMENT; TIME;

ACER; COMPUTER SIMULATION; EVOLUTION; FLOWERS; MODELS, BIOLOGICAL; SEEDS; SELECTION (GENETICS); SEX CHARACTERISTICS; TIME FACTORS;

ACER; ACER OPALUS;

EID: 47349101483     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00394.x     Document Type: Article

References (77)

1. Bai, W.-N., Y.-F. Zeng, and D.-Y. Zhang. 2007. Matting patterns and pollen dispersal in a heterodichogamous tree, Juglans mandshurica (Juglandaceae). New Phytol. 176 : 699 707.
2. Baker, A. M., J. D. Thompson, and S. C. H. Barrett. 2000. Evolution and maintenance of stigma-height polymorphism in Narcissus. II. Fitness comparisons between style morphs. Heredity 84 : 514 524.
3. Barker, P. A., D. C. Freeman, and K. T. Harper. 1982. Variation in the breeding system of Acer grandidentatum. Forest Sci. 28 : 563 572.
4. Barrett, S. C. H. 1992. Evolution and function of heterostyly. Springer-Verlag, Berlin.
5. Barrett, S. C. H. 2002. The evolution of plant sexual diversity. Nat. Rev. Genet. 3 : 274 284.
6. Barrett, S. C. H., and L. D. Harder. 2005. The evolution of polymorphic sexual systems in daffodils (Narcissus). New Phytol. 165 : 45 53.
7. Barrett, S. C. H., and K. A. Hodgins. 2006. Floral design and the evolution of asymmetrical mating systems. Pp. 239 255 in L. D. Harder, and S. C. H. Barrett eds. Ecology and evolution of flowers. Oxford Univ. Press, Oxford.
8. Barrett, S. C. H., A. L. Case, and G. B. Peters. 1999. Gender modification and resource allocation in subdioecious Wurmbea dioica (Colchicaceae). J. Ecol. 87 : 123 137.
9. Barrett, S. C. H., L. K. Jesson, and A. M. Baker. 2000. The evolution and function of stylar polymorphisms in flowering plants. Ann. Bot. 85 : 253 265.
10. Baskin, C. C., and J. M. Baskin. 1998. Causes of within-species variation in seed dormancy and germination characteristics. Pp. 181 237 in C. C. Baskin and J. M. Baskin eds. Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic Press, San Diego.
11. Bawa, K. S., and J. H. Beach. 1981. Evolution of sexual systems in flowering plants. Ann. Mo. Bot. Gard. 68 : 254 274.
12. Castric, V., and X. Vekemans. 2004. Plant self-incompatibility in natural populations: a critical assessment of recent theoretical and empirical advances. Mol. Ecol. 13 : 2873 2889.
13. Clarke, A. E., and E. Newbigin. 1993. Molecular aspects of self-incompatibility in flowering plants. Annu. Rev. Genet. 27 : 257 279.
14. de Jong, P. C. 1976. Flowering and sex expression in Acer L: A biosystematic study. Mededelingen Landbouwhogeschool. Wageningen, The Nederlands.
15. Dommée B., J.-L. Bompar, and N. Denelle. 1990. Sexual tetramorphism in Thymelaea hirsuta (Thymelaeaceae): evidence of the pathway from heterodichogamy to dioecy at the intraspecific level. Am. J. Bot. 77 : 1449 1462.
16. Doyle, J. J., and J. L. Doyle. 1990. Isolation of plant DNA from fresh tissue. Focus 12 : 13 15.
17. Eckert, C. G., D. Manicacci, and S. C. H. Barrett. 1996. Frequency-dependent selection on morph ratios in tristylous Lythrum salicaria (Lythraceae). Heredity 77 : 581 588.
18. Elle, E., and T. R. Meagher. 2000. Sex allocation and reproductive success in the andromonoecious perennial Solanum carolinense (Solanaceae). II. Paternity and functional gender. Am. Nat. 156 : 622 636.
19. Fenster, C. B. 1995. Mirror image flowers and their effect on outcrossing rate in Chamaecrista fasciculata (Leguminosae). Am. J. Bot. 82 : 46 50.
20. Galil, J., and M. Zeroni. 1967. On the pollination of Zizyphus spina-christi (L.) Wild in Israel. Israel J. Bot. 16 : 71 77.
21. Gerber, S., S. Mariette, R. Streiff, C. Bodénès, and A. Kremer. 2000. Comparison of microsatellites and amplified fragment length polymorphism markers for parentage analysis. Mol. Ecol. 9 : 1037 1048.
22. Gerber, S., P. Chabrier, and A. Kremer. 2003. FAMOZ: a software for parentage analysis using dominant, codominant and uniparentally inherited markers. Mol. Ecol. Notes 3 : 479 481.
23. Gleeson, S. K. 1982. Heterodichogamy in walnuts: inheritance and stable ratios. Evolution 36 : 892 902.
24. Gleiser, G., and M. Verdú. 2005. Repeated evolution of dioecy from androdioecy in Acer. New Phytol. 165 : 633 640.
25. Gleiser, G., J. G. Segarra-Moragues, J. R. Pannell, and M. Verdú. In press. Siring success and paternal effects in heterodichogamous Acer opalus. Ann. Bot. doi :.
26. Gómez-Aparicio, L. 2004. Papel de la heterogeneidad en la regeneración del Acer opalus subsp. granatense en la montaña mediterránea: implicaciones para la conservación y restauración de sus poblaciones. Ph.D. thesis. Univ. of Granada. Granada, Spain.
27. Gómez-Aparicio, L., R. Zamora, and J. M. Gómez. 2005. The regeneration status of the endangered species Acer opalus subsp. granatense throughout its geographical distribution in the Iberian Peninsula. Biol. Conserv. 121 : 195 206.
28. Hibbs D. E., and B. C. Fischer. 1979. Sexual and vegetative reproduction of striped maple (Acer pensylvanicum L.). Bull Torrey Bot. Club 106 : 222 227.
29. Jesson, L. K., and S. C. H. Barrett. 2002. Solving the puzzle of mirror-image flowers. Nature 417 : 707 707.
30. Jones, R. H., B. P. Allen, and R. R. Sharitz. 1997. Why do early-emergent tree seedlings have survival advantage? A test using Acer rubrum (Aceraceae). Am. J. Bot 84 : 1714 1718.
31. Klinkhamer, P. G. L., T. J. de Jong, and H. Metz. 1997. Sex and size in cosexual plants. Trends Ecol. Evol. 12 : 260 265.
32. Kubitzki, K., and H. Kurz. 1984. Synchronized dichogamy and dioecy in Neotropical Lauraceae. Pl. Syst. Evol. 147 : 253 266.
33. Laguna, E., and M. García. 1988. El parque natural del carrascal de la Font Roja. Vida Silvestre 63 : 42 48.
34. Lawrence, M. J. 2000. Population genetics of the homomorphic self-incompatibility polymorphisms in flowering plants. Ann. Bot. 85 : 221 226.
35. Leishman, M. R., I. J. Wright, A. T. Moles, and M. Westoby. 2000. The evolutionary ecology of seed size. Pp. 31 57 in M. Fenner ed. Seeds: the ecology of regeneration in plants communities. CABI Publishing, Oxon.
36. Leishman, M. L. 2001. Does the seed size/number trade-off model determine plant community structure? An assessment of the model mechanisms and their generality. Oikos 93 : 294 302.
37. Li, Q.-J., Z.-F. Xu, W. J. Kress, Y.-M. Xia, L. Zhang, X.-B. Deng, J.-Y. Gao, and Z.-L. Bai. 2001. Flexible style that encourages outcrossing. Nature 410 : 432.
38. Lloyd, D. G. 1979. Evolution towards dioecy in heterostylous populations. Plant Syst. Evol. 131 : 71 80.
39. Lloyd, D. G. 1980. Sexual strategies in plants. III. A quantitative method for describing the gender of plants. NZ. J. Bot. 18 : 103 108.
40. Lloyd, D. G., and K. S. Bawa. 1984. Modification of the gender of seed plants in varying conditions. Evol. Biol. 17 : 255 388.
41. Marshall, T. C., J. Slate, L. E. B. Kruuk, and J. M. Pemberton. 1998. Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7 : 639 655.
42. Matsui, K. 1995. Sex expression, sex change and fruiting habit in an Acer rufinerve population. Ecol. Res. 10 : 65 74.
43. Meagher, T. R. 1986. Analysis of paternity within a natural population of Chamaelirium luteum. 1. Identification of most-likely male parents. Am. Nat. 128 : 199 215.
44. Morgan, M. T., and J. K. Conner. 2001. Using genetic markers to directly estimate male selection gradients. Evolution 55 : 272 281.
45. Muenchow, G. E., and M. Grebus. 1989. The evolution of dioecy from distyly: reevaluation of the hypothesis of the loss of long-tongued pollinators. Am. Nat. 133 : 149 156.
46. Nielsen, R., D. K. Mattila, P. J. Clapham, and P. J. Pasbøll. 2001. Statistical approaches to paternity analysis in natural populations and applications to the Northern humpback whale. Genetics 157 : 1673 1682.
47. Ornduff, R., and R. Dulberger. 1978. Floral enantiomorphy and the reproductive system of Wachendorfia paniculata (Haemodoraceae). New Phytol. 80 : 427 434.
48. Pandey, M, O. Gailing, D. Fischer, H. H. Hattemer, and R. Finkeldey. 2004. Characterisation of microsatellite markers in sycamore (Acer pseudoplatanus L.). Mol. Ecol. Notes 4 : 253 255.
49. Pannell, J. R., and M. Verdú. 2006. The evolution of gender specialization from dimorphic hermaphroditism: paths from heterodichogamy to gynodioecy and androdioecy. Evolution 60 : 660 673.
50. Pannell, J. R., M. E. Dorken, and S. M. Eppley. 2005. "Haldane's sieve" in a metapopulation: sifting through plant reproductive polymorphisms. Trends Ecol. Evol. 20 : 374 379.
51. Pendleton, R. L., E. D. McArthur, D. C. Freeman, and A. C. Blauer. 1988. Heterodichogamy in Grayia brandegei (Chenopodiaceae): report from a new family. Am. J. Bot. 75 : 267 274.
52. Policansky, D. 1981. Sex choice and the size advantage model in Jack in-the-pulpit (Arisaema triphyllum). Proc. Natl. Acad. Sci. USA 78 : 1306 1308.
53. Posada, D., and T. R. Buckley. 2004. Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst. Biol. 53 : 793 808.
54. Primack, R. B., and C. McCall. 1986. Gender variation in a red maple population (Acer rubrum; Aceraceae); a seven-year study of a "polygamodioecious" species. Am. J. Bot. 73 : 1239 1248.
55. R Development Core Team 2007. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.
56. Raymond, M., and F. Rousset. 1995. GENEPOP (version 1.2). Population genetics software for exact tests and ecumenicism. J. Hered. 86 : 248 249.
57. Renner, S. S. 2001. How common is heterodichogamy? Trends Ecol. Evol. 16 : 595 597.
58. Renner, S. S., L. Beenken, G. W. Grimm, A. Kocyan, and R. E. Ricklefs. 2007. The evolution of dioecy, heterodichogamy, and labile sex expression in Acer. Evolution 61 : 2701 2719.
59. Ritland, K. 2002. Extensions of models for the estimation of mating systems using n independent loci. Heredity 88 : 221 228.
60. Sakai, A. K. 1990. Sex ratios of red maple (Acer rubrum) populations in northern lower Michigan. Ecology 71 : 571 580.
61. Sarkissian, T. S., S. C. H. Barrett, and L. D. Harder. 2001. Gender variation in Sagittaria latifolia (Alismataceae): is size all that matters? Ecology 82 : 360 373.
62. Sato, T. 2002. Phenology of sex expression and gender variation in a heterodichogamous maple, Acer japonicum. Ecology 83 : 1226 1238.
63. Schlessman, M. A. 1988. Gender diphasy ("sex choice"). Pp. 139 153 in J. Lovett Doust, and L. Lovett Doust, eds. Plant reproductive ecology: patterns and strategies. Oxford Univ. Press, New York.
64. Segarra-Moragues, J. M., G. Gleiser, and F. González-Candelas. In press. Isolation and characterization of microsatellite loci in Acer opalus (Aceraceae), a sexually-polymorphic tree, through an enriched genomic library. Conserv. Genet. doi :.
65. Signorovitch, J., and R. Nielsen. 2002. PATRI - paternity inference using genetic data. Bioinformatics 18 : 341 342.
66. Silva, N. F., and D. R. Goring. 2001. Mechanisms of self-incompatibility in flowering plants. Cell. Mol. Life Sci. 58 : 1988 2007.
67. Smouse, P. E., T. R. Meagher, and C. J. Kobak. 1999. Parentage analysis in Chamaelirium luteum (L.) Gray (Liliaceae): why do some males have higher reproductive contributions? J. Evol. Biol. 12 : 1069 1077.
68. Stanton, M. L. 1984. Seed variation in wild radish: effect of seed size on components of seedling and adult fitness. Ecology 65 : 1105 1112.
69. Thompson, T. E., and L. D. Romberg. 1985. Inheritance of heterodichogamy in pecan. J. Hered. 76 : 456 458.
70. Thompson, J. D., S. C. H. Barrett, and A. M. Baker. 2003. Frequency-dependent variation in reproductive success in Narcissus: implications for the maintenance of stigma-height dimorphism. Proc. R. Soc. Lond. B. 270 : 949 953.
71. Vassiliadis, C., P. Saumitou-Laprade, J. Lepart, and F. Viard. 2002. High male reproductive success of hermaphrodites in the androdioecious Phillyrea angustifolia. Evolution 56 : 1362 1373.
72. Verdú, M., P. García-Fayos, and G. Gleiser. 2004. Mites attack males of the sexually polymorphic tree Acer opalus more harmfully and more often. Funct. Ecol. 18 : 592 597.
73. Verdú, M., and A. Traveset. 2005. Early emergence enhances plant fitness: a phylogenetically controlled meta-analysis. Ecology 86 : 1385 1394.
74. Verdú, M., S. C. González-Martínez, A. I. Montilla, I. Mateu, and J. R. Pannell. 2006. Ovule discounting in an outcrossing, cryptically dioecious tree. Evolution 60 : 2056 2063.
75. Webb, C. J., and D. G. Lloyd. 1986. The avoidance of interference between the presentation of pollen and stigmas in angiosperms. II. Herkogamy. NZ. J. Bot. 24 : 163 178.
76. Wolfe, L. M., and A. Shmida. 1997. The ecology of sex expression in a gynodioecious Israeli desert shrub (Ochradenus baccatus). Ecology 78 : 101 110.
77. Wright, S. I., and S. C. H. Barrett. 1999. Size-dependent gender modification in a hermaphroditic perennial herb. Proc. R. Soc. Lond. B 266 : 225 232.