Herkogamy and mate diversity in the wild daffodil Narcissus longispathus: Beyond the selfing-outcrossing paradigm in the evolution of mixed mating

Plant Biology

Volumn 14, Issue 5, 2012, Pages 801-810

  Medrano, M ^a   Requerey, R ^a   Karron, J D ^b   Herrera, C M ^a  

^a DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^b UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

Amaryllidaceae; Anther stigma separation; Correlated paternity; Mixed mating system; Multiple paternity; Outcrossing rate; Style length

Indexed keywords

ADAPTATION; ANGIOSPERM; AUTOGAMY; FERTILIZATION (REPRODUCTION); MATING BEHAVIOR; MONOCOTYLEDON; OUTCROSSING; PARADIGM SHIFT; PATERNITY; POPULATION DISTRIBUTION; POPULATION STRUCTURE; REPRODUCTIVE STATUS; SPECIES DIVERSITY; WILD POPULATION;

AMARYLLIDACEAE; NARCISSUS; NARCISSUS LONGISPATHUS; NARCISSUS PSEUDONARCISSUS;

ANATOMY AND HISTOLOGY; CROSS BREEDING; EVOLUTION; FLOWER; GENE LOCUS; NARCISSUS; PHENOTYPE; PHYSIOLOGY; QUANTITATIVE TRAIT; REPRODUCTION; SELF FERTILIZATION; STATISTICAL MODEL;

BIOLOGICAL EVOLUTION; CROSSES, GENETIC; FLOWERS; GENETIC LOCI; LINEAR MODELS; NARCISSUS; PHENOTYPE; QUANTITATIVE TRAIT, HERITABLE; REPRODUCTION; SELF-FERTILIZATION;

EID: 84864781033     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/j.1438-8677.2012.00569.x     Document Type: Article

References (70)

1. Armbruster W.S., Rogers D.G. (2004) Does pollen competition reduce the cost of inbreeding? American Journal of Botany, 91, 1939-1943.
2. Armbruster W.S., Debevec E.M., Willson M.F. (2002) The evolution of syncarpy in angiosperms: theoretical and phylogenetic analyses of the effects of carpel fusion on offspring quantity and quality. Journal of Evolutionary Biology, 15, 657-672.
3. Barrett S.C.H. (2003) Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond. Philosophical Transactions of the Royal Society of London B, 358, 991-1004.
4. Barrett S.C.H., Cole W.W., Herrera C.M. (2004) Mating patterns and genetic diversity in the wild daffodil Narcissus longispathus (Amaryllidaceae). Heredity, 92, 459-465.
5. Belaoussoff S., Shore J.S. (1995) Floral correlates and fitness consequences of mating system variation in Turnera ulmifolia. Evolution, 49, 545-556.
6. Bernasconi G. (2004) Seed paternity in flowering plants: an evolutionary perspective. Perspectives in Plant Ecology, Evolution and Systematics, 6, 149-158.
7. Bernasconi G., Ashman T.-L., Birkhead T.R., Bishop J., Grossniklaus U., Kubli E., Marshall D.L., Schmid B., Skogsmyr I., Snook R.R., Taylor D.R., Till-Bottraud I., Ward P., Zeh D., Hellriegel B. (2004) Evolutionary ecology of the pre-zygotic stage. Science, 303, 971-974.
8. Bernasconi G., Lang D.J., Schmid B. (2007) Microgametophyte population sizes and plant reproductive output in the insect-pollinated Prunella grandiflora (Lamiaceae). New Phytologist, 173, 393-400.
9. Brown A.H.D., Allard R.W. (1970) Estimation of the mating system in open-pollinated maize populations using isozyme polymorphisms. Genetics, 66, 133-145.
10. Brunet J., Eckert C.G. (1998) Effects of floral morphology and display on outcrossing in blue columbine, Aquilegia caerulea (Ranunculaceae). Functional Ecology, 12, 596-606.
11. Brunet J., Sweet H.R. (2006) Impact of insect pollinator group and floral display size on outcrossing rate. Evolution, 60, 234-246.
12. Conner J.K., Sahli H.F., Karoly K. (2009) Tests of adaptation: functional studies of pollen removal and estimates of natural selection on anther position in wild radish. Annals of Botany, 103, 1547-1556.
13. Cruzan M.B. (1998) Genetic markers in plant evolutionary ecology. Ecology, 79, 400-412.
14. Cruzan M.B., Arnold M.L. (1994) Assortative mating and natural selection in an Iris hybrid zone. Evolution, 48, 1946-1958.
15. Darwin C. (1862) The various contrivances by which British and foreign orchids are fertilised by insects. John Murray, London, UK.
16. Darwin C. (1876) The effects of cross- and self-fertilisation in the vegetable kingdom. John Murray, London, UK.
17. Darwin C. (1877) The different forms of flowers on plants of the same species. John Murray, London, UK.
18. Dudash M.R., Ritland K. (1991) Multiple paternity and self-fertilization in relation to floral age in Mimulus guttatus (Scrophulariaceae). American Journal of Botany, 78, 1746-1753.
19. Eckert C.G., Barrett S.C.H. (1994) Inbreeding depression in partially self-fertilizing Decodon verticillatus (Lythraceae): population-genetic and experimental analyses. Evolution, 48, 952-964.
20. Eckert C.G., Ozimec B., Herlihy C.R., Griffin C.A., Routley M.B. (2009) Floral morphology mediates temporal variation in the mating system of a self-compatible plant. Ecology, 90, 1540-1548.
21. Falconer D.S. (1981) Introduction to quantitative genetics. Longman, New York, USA.
22. Fenster C.B., Armbruster W.S., Wilson P., Dudash M.R., Thomson J.D. (2004) Pollination syndromes and floral specialization. Annual Review of Ecology and Systematics, 35, 375-403.
23. Fetscher A.E. (2001) Resolution of male-female conflict in an hermaphrodite flower. Proceedings of the Royal Society Series B, Biological Sciences, 268, 525-529.
24. Forrest J.R.K., Ogilvie J.E., Gorischek A.E., Thomson J.D. (2011) Seasonal change in a pollinator community and the maintenance of style length variation in Mertensia fusiformis (Boraginaceae). Annals of Botany, 108, 1-12.
25. Galen C., Rotenberry J.T. (1988) Variance in pollen carryover in animal-pollinated plants: implications for mate choice. Journal of Theoretical Biology, 135, 419-439.
26. Harder L.D., Barrett S.C.H. (1993) Pollen removal from tristylous Pontederia cordata: effects of anther position and pollinator specialization. Ecology, 74, 1059-1072.
27. Harder L.D., Barrett S.C.H. (2006) Ecology and evolution of flowers. Oxford University Press, Oxford, UK.
28. Hardy O.J., González-Martínez S.C., Colas B., Freville H., Mignot A., Olivieri I. (2004) Fine-scale genetic structure and gene dispersal in Centaurea corymbosa (Asteraceae). II. Correlated paternity within and among sibships. Genetics, 168, 1601-1614.
29. Herlihy C.R., Eckert C.G. (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.
30. Herrera C.M. (1995) Floral biology, microclimate, and pollination by ectothermic bees in an early-blooming herb. Ecology, 76, 218-228.
31. Herrera C.M. (2011) Complex implications around a simple trait: ecological context determines the fecundity effects of corolla marcescence. American Journal of Botany, 98, 812-818.
32. Holtsford T.P., Ellstrand N.C. (1992) Genetic and environmental variation in floral traits affecting outcrossing rate in Clarkia tembloriensis (Onagraceae). Evolution, 46, 216-225.
33. Ivey C.T., Wyatt R. (1999) Family outcrossing rates and neighborhood floral density in natural populations of swamp milkweed (Asclepias incarnata): potential statistical artifacts. Theoretical and Applied Genetics, 98, 1063-1071.
34. Kalisz S., Vogler D.W., Hanley K.M. (2004) Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature, 430, 884-887.
35. Karron J.D., Marshall D.L. (1993) Effects of environmental variation on fitness of singly and multiply sired progenies of Raphanus sativus (Brassicaceae). American Journal of Botany, 80, 1407-1412.
36. Karron J.D., Jackson R.T., Thumser N.N., Schlicht S.L. (1997) Outcrossing rates of individual Mimulus ringens genets are correlated with anther-stigma separation. Heredity, 79, 365-370.
37. Karron J.D., Mitchell R.J., Bell J.M. (2006) Multiple pollinator visits to Mimulus ringens (Phrymaceae) flowers increase mate number and seed set within fruits. American Journal of Botany, 93, 1306-1312.
38. Kubota S., Kameyama Y., Hirao A.S., Ohara M. (2008) Adaptive significance of self-fertilization in a hermaphroditic perennial, Trillium camschatcense (Melanthiaceae). American Journal of Botany, 95, 482-489.
39. Kudo G. (2003) Anther arrangement influences pollen deposition and removal in hermaphrodite flowers. Functional Ecology, 17, 349-355.
40. Kulbaba M.W., Worley A.C. (2008) Floral design in Polemonium brandegei (Polemoniaceae): genetic and phenotypic variation under hawkmoth and hummingbird pollination. International Journal of Plant Sciences, 169, 509-522.
41. Lankinen Å., Madjidian J.A. (2011) Enhancing pollen competition by delaying stigma receptivity: pollen deposition schedules affect siring ability, paternal diversity, and seed production in Collinsia heterophylla (Plantaginaceae). American Journal of Botany, 98, 1191-1200.
42. Lankinen Å., Skogsmyr I. (2001) Evolution of pistil length as a choice mechanism for pollen quality. Oikos, 92, 81-90.
43. Leege L.M., Wolfe L.M. (2002) Do floral herbivores respond to variation in flower characteristics in Gelsemium sempervirens (Loganiaceae), a distylous vine? American Journal of Botany, 89, 1270-1274.
44. Marshall D.L., Avritt J.J., Maliakal-Witt S., Medeiros J.S., Shaner M.G.M. (2010) The impact of plant and flower age on mating patterns. Annals of Botany, 105, 7-22.
45. Medrano M., Herrera C.M. (2008) Geographical structuring of genetic diversity across the whole distribution range of Narcissus longispathus, a habitat-specialist, Mediterranean narrow endemic. Annals of Botany, 102, 183-194.
46. Medrano M., Herrera C.M., Barrett S.C.H. (2005) Herkogamy and mating patterns in the self-compatible daffodil Narcissus longispathus. Annals of Botany, 95, 1105-1111.
47. Mitchell R.J. (1997a) Effects of pollen quantity on progeny vigor: evidence from Lesquerella fendleri. Evolution, 51, 1679-1684.
48. Mitchell R.J. (1997b) Effects of pollination intensity on Lesquerella fendleri seed set: variation among plants. Oecologia, 109, 382-388.
49. Mitchell R.J., Karron J.D., Holmquist K.G., Bell J.M. (2005) Patterns of multiple paternity in fruits of Mimulus ringens (Phrymaceae). American Journal of Botany, 5, 885-890.
50. Morgan M.T., Barrett S.C.H. (1990) Outcrossing rates and correlated mating within a population of Eichhornia paniculata (Pontederiaceae). Heredity, 64, 271-280.
51. Motten A.F., Stone J.L. (2000) Heritability of stigma position and the effect of stigma-anther separation on outcrossing in a predominantly self-fertilizing weed, Datura stramonium (Solanaceae). American Journal of Botany, 87, 339-347.
52. Navarro F.B. (2009) Narcissus L. In: Blanca G., Cabezudo B., Cueto M., Fernández López C., Morales Torres C. (Eds), Flora vascular de Andalucía oriental, Volume 1. Consejería de Medio Ambiente, Junta de Andalucía, Sevilla, Spain, pp 182-186.
53. Nishihiro J., Washitani I., Thomson J.D., Thomson B.A. (2000) Patterns and consequences of stigma height variation in a natural population of a distylous plant, Primula sieboldii. Functional Ecology, 14, 502-512.
54. Quesada-Aguilar A., Kalisz S., Ashman T.-L. (2008) Flower morphology and pollinator dynamics in Solanum carolinense (Solanaceae): implications for the evolution of andromonoecy. American Journal of Botany, 95, 974-984.
55. Ritland K.. (1996) MLTR: multilocus mating system program (version 1.1). Available from (accessed 8 February 2012).
56. Ritland K. (2002) Extensions of models for the estimation of mating systems using n independent loci. Heredity, 88, 221-228.
57. Ritland K., Jain S. (1981) A model for the estimation of outcrossing rate and gene frequencies using n independent loci. Heredity, 47, 35-52.
58. Routley M.B., Husband B.C. (2006) Sexual interference within flowers of Chamerion angustifolium. Evolutionary Ecology, 20, 331-343.
59. Ruane L.G. (2009) Post-pollination processes and non-random mating among compatible mates. Evolutionary Ecology Research, 11, 1031-1051.
60. SAS Institute (2005) SAS/STAT version 9.1.3. SAS Institute, Cary, NC, USA.
61. Schultz B.B. (1985) Levene's test for relative variation. Systematic Zoology, 34, 449-456.
62. Shaner M.G.M., Marshall D.L. (2003) Under how wide a set of conditions will nonrandom mating occur in Raphanus sativus (Brassicaceae)? American Journal of Botany, 90, 1604-1611.
63. Shaner M.G.M., Marshall D.L. (2007) How robust is nonrandom mating in wild radish: do small pollen loads coupled with more competing pollen donors lead to random mating? American Journal of Botany, 94, 266-273.
64. Snow A.A., Spira T.P., Liu H. (2000) Effects of sequential pollination on the success of 'fast' and 'slow' pollen donors in Hibiscus moscheutos (Malvaceae). American Journal of Botany, 87, 1656-1659.
65. Spira T.P., Snow A.A., Puterbaugh M.N. (1996) The timing and effectiveness of sequential pollinations in Hibiscus moscheutos. Oecologia, 105, 230-235.
66. Sun M., Ritland K. (1998) Mating system of yellow starthistle (Centaurea solstitialis), a successful colonizer in North America. Heredity, 80, 225-232.
67. Takebayashi N., Wolf D.E., Delph L.F. (2006) Effect of variation in herkogamy on outcrossing within a population of Gilia achilleifolia. Heredity, 96, 159-165.
68. Teixeira S., Bernasconi G. (2007) High prevalence of multiple paternity within fruits in natural populations of Silene latifolia, as revealed by microsatellite DNA analysis. Molecular Ecology, 16, 4370-4379.
69. Webb C.J., Lloyd D.G. (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms. II. Herkogamy. New Zealand Journal of Botany, 24, 163-178.
70. Willson M.F., Burley N. (1983) Mate choice in plants: tactics, mechanisms, and consequences. Princeton University Press, Princeton, NJ, USA.