Female reproductive success in gynodioecious Thymus vulgaris: Pollen versus nutrient limitation and pollinator foraging behaviour

Botanical Journal of the Linnean Society

Volumn 175, Issue 3, 2014, Pages 395-408

  Arnan, Xavier ^a,b   Escolà, Anna ^c   Rodrigo, Anselm ^a,c   Bosch, Jordi ^a  

^a CREAF   (Spain)

^b DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

'inbreeding depression hypothesis'; 'resource reallocation hypothesis'; Floral display; Pollinator constancy; Visitation rates

Indexed keywords

ANGIOSPERM; FEMALE; FORAGING BEHAVIOR; FRUIT SET; INBREEDING DEPRESSION; NECTAR; NUTRIENT LIMITATION; POLLEN; POLLINATOR; REPRODUCTIVE STRATEGY; REPRODUCTIVE SUCCESS; RESOURCE ALLOCATION; SEED PRODUCTION;

THYMUS VULGARIS;

EID: 84903740156     PISSN: 00244074     EISSN: 10958339     Source Type: Journal    
DOI: 10.1111/boj.12173     Document Type: Article

References (66)

1. Alonso C, Herrera CM. 2011. Back-and-forth hermaphroditism: phylogenetic context of reproductive system evolution in subdioecious Daphne laureola. Evolution 65: 1680-1692.
2. Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash M, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson W. 2004. Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85: 2408-2421.
3. Ashman TL, Shivitz S, Swetz J. 2000. Understanding the basis of pollinator selectivity in sexually dimorphic Fragaria virginiana. Oikos 90: 347-356.
4. Ashman TL, Stanton M. 1991. Seasonal variation in pollination dynamics of sexually dimorphic Sidalcea oregana ssp. spicata (Malvaceae). Ecology 72: 993-1003.
5. Asikainen E, Mutikainen P. 2005. Pollen and resource limitation in a gynodioecious species. American Journal of Botany 92: 487-494.
6. Assouad MW, Dommée B, Lumaret R, Valdeyron G. 1978. Reproductive capacities in the sexual forms of gynodioecious species Thymus vulgaris L. Biological Journal of the Linnean Society 77: 29-39.
7. Assouad W, Valdeyron G. 1975. Remarques sur la biologie du thym, Thymus vulgaris L. Bulletin de la Société Botanique de France 122: 21-34.
8. Atlan AP, Gouyon H, Fournial T, Pomente D, Couvet D. 1992. Sex allocation in an hermaphroditic plant: the case of gynodioecy in Thymus vulgaris L. Journal of Evolutionary Biology 5: 189-203.
9. Bell G. 1985. On the function of flowers. Proceedings of the Royal Society B: Biological Sciences 224: 223-265.
10. Bonnemaison R, Dommée B, Jacquard P. 1979. Etude expérimentale de la concurrence entre formes sexuelles chez le thym, Thymus vulgaris L. Oecologia Plantarum 14: 85-101.
11. Case AL, Ashman TL. 2009. Resources and pollinators contribute to population sex-ratio bias and pollen limitation in Fragaria virginiana (Rosaceae). Oikos 118: 1250-1260.
12. Charlesworth B, Charlesworth D. 1978. Model for evolution of dioecy and gynodioecy. The American Naturalist 112: 975-997.
13. Charlesworth D, Charlesworth B. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18: 237-268.
14. Couvet D, Bonnemaison F, Gouyon PH. 1986. The maintenance of female among hermaphrodites: the importance of nuclear-cytoplasmic interactions. Heredity 57: 325-330.
15. Couvet D, Henry JP, Gouyon PH. 1985. Sexual selection in hermaphroditic plants: the case of gynodioecy. The American Naturalist 126: 294-299.
16. Cuevas E, Abarca CA. 2006. Origen, mantenimiento y evolución del ginodioicismo. Boletín de la Sociedad Botánica de México 78: 33-42.
17. Dafni A. 1992. Pollination ecology. A practical approach. Oxford: Oxford University Press.
18. Darwin CR. 1877. The different forms of flowers on plants of the same species. London: University of Chicago Press.
19. Delph LF. 1996. Flower size dimorphism in plants with unisexual flowers. In: Lloyd DG, Barrett SCH, eds. Floral biology: studies on floral evolution in animal-pollinated plants. New York: Chapman & Hall, 217-237.
20. Delph LF. 2009. Sex allocation: evolution to and from dioecy. Current Biology 19: R249-R251.
21. Delph LF, Lively CM. 1992. Pollinator visitation, floral display, and nectar production of the sexual morphs of a gynodioecious shrub. Oikos 63: 161-170.
22. Dommée B, Assouad MW, Valdeyron G. 1978. Natural selection and gynodioecy in Thymus vulgaris L. Biological Journal of the Linnean Society 77: 17-28.
23. Dufay M, Billard E. 2012. How much better are females? The occurrence of female advantage, its proximal causes and its variation within and among gynodioecious species. Annals of Botany 109: 505-519.
24. Eckhart VM. 1992. Resource compensation and the evolution of gynodioecy in Phacelia linearis (Hydrophyllaceae). Evolution 46: 1313-1328.
25. Eckhart VM. 1999. Sexual dimorphism in flowers and inflorescences. In: Geber MA, Dawson TE, Delph LF, eds. Gender and sexual dimorphism in flowering plants. Berlin: Springer-Verlag, 123-148.
26. Gegear RJ, Thomson JD. 2004. Does the flower constancy of bumblebees reflect foraging economics? Ethology 110: 793-805.
27. Gómez JM, Bosch J, Perfectti F, Fernández JD, Abdelaziz M, Camacho JPM. 2008. Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators. Proceedings of the Royal Society B: Biological Sciences 275: 2241-2249.
28. Haig D, Westoby M. 1988. On limits to seed production. The American Naturalist 131: 757-759.
29. Holland JN, Chamberlain SA. 2007. Ecological and evolutionary mechanisms resulting in low seed:ovule ratios: need for a more pluralistic approach? Ecology 88: 706-715.
30. Ishii HS, Harder LD. 2006. The size of individual Delphinium flowers and the opportunity for geitonogamous pollination. Functional Ecology 20: 1115-1123.
31. Kaczorowski RL, Gardener MC, Holtsford TP. 2005. Nectar traits in Nicotiana section alatae (Solanaceae) in relation to floral traits, pollinators, and mating system. American Journal of Botany 92: 1270-1283.
32. Kaul MLH. 1988. Male sterility in higher plants. Berlin: Springer-Verlag.
33. Klinkhamer PGL, de Jong TJ, Wesselingh RA. 1991. Implications of differences between hermaphrodite and female flowers for attractiveness to pollinators and seed production. Netherlands Journal of Zoology 41: 130-143.
34. Lewis D. 1941. Male sterility in natural populations of hermaphrodite plants. New Phytologist 40: 56-63.
35. Lloyd DG. 1975. The maintenance of gynodioecy and androdioecy in angiosperms. Genetica 45: 325-339.
36. Lloyd DG. 1976. The transmission of genes via pollen and ovules in gynodioecious angiosperms. Theoretical Population Biology 9: 299-316.
37. Manicacci D, Atlan A, Rossello JAE, Couvet D. 1998. Gynodioecy and reproductive trait variation in three Thymus species (Lamiaceae). International Journal of Plant Science 159: 948-957.
38. Martin NH. 2004. Flower size preferences of the honeybee (Apis mellifera) foraging on Mimulus guttatus (Scrophulariaceae). Evolutionary Ecology Research 6: 777-782.
39. McGinley MA, Temme DH, Geber MA. 1987. Parental investment in offspring in variable environments: theoretical and empirical considerations. The American Naturalist 130: 370-398.
40. Natalis LC, Wesselingh RA. 2012. Shared pollinators and pollen transfer dynamics in two hybridizing species, Rhinanthus minor and R.angustifolius. Oecologia 170: 709-721.
41. Perrot V, Dommée D, Jacquard P. 1982. Etude expérimentale de la concurrence entre individus issus d'autofécondation et d'allofécondation chez le thym (Thymus vulgaris L.). Oecologia Plantarum 3: 171-184.
42. Petterson MW. 1992. Advantages of being a specialist female in gynodioecious Silene vugaris s.l. (Caryophyllaceae). American Journal of Botany 79: 1389-1395.
43. Pohl NB, Van Wyk J, Campbell DR. 2011. Butterflies show flower color preferences but not constancy in foraging at four plant species. Ecological Entomology 36: 290-300.
44. Proctor M, Yeo P, Lack AJ. 1996. The natural history of pollination. Portland, OR: Timber Press.
45. Puterbaugh MN, Wied A, Galen C. 1997. The functional ecology of gynodioecy in Eritrichum aretioides (Boraginaceae), the alpine forget-me-not. American Journal of Botany 84: 393-400.
46. R Development Core Team. 2010. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Available at: http://www.R-project.org
47. Ramsey M, Vaughton G. 2002. Maintenance of gynodioecy in Wurmbea biglandulosa (Colchicaceae): gender differences in seed production and progeny success. Plant Systematics and Evolution 232: 189-200.
48. Richards A. 1986. Plant breeding systems. Cambridge: Cambridge University Press.
49. Sakai AK, Weller SG, Chen ML, Chou SY, Tasanont C. 1997. Evolution of gynodioecy and maintenance of females: the role of inbreeding depression, outcrossing rates, and resource allocation in Schiedea adamantis (Caryophyllaceae). Evolution 51: 724-736.
50. Shykoff JA. 1992. Sex polymorphism in Silene acaulis (Caryophyllaceae) and the possible role of sexual selection in maintaining females. American Journal of Botany 79: 138-143.
51. Shykoff JA, Kolokotronis SO, Collin CL, López-Villavicencio M. 2003. Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis. Oecologia 135: 1-9.
52. Stanton ML, Snow AA, Handel SN. 1986. Floral evolution: attractiveness to pollinators increases male fitness. Science 232: 1625-1627.
53. Stephenson AG. 1981. Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology and Systematics 12: 253-279.
54. Sun M, Ganders FR. 1986. Female frequencies in gynodioecious populations correlated with selfing rates in hermaphrodites. American Journal of Botany 73: 1645-1648.
55. Thompson JD. 2002. Population structure and the spatial dynamics of genetic polymorphism in thyme. In: Letchamo W, Saez F, Stahl-Biskup E, eds. Medicinal and aromatic plants - industrial profiles: the genus Thymus. Amsterdam: Harwood Academic Publishers, 44-74.
56. Thompson JD, Rolland AG, Prugnolle F. 2002. Genetic variation for sexual dimorphism in flower size within and between populations of gynodioecious Thymus vulgaris. Journal of Evolutionary Biology 15: 362-372.
57. Thompson JD, Tarayre M. 2000. Exploring the genetic basis and causes of variation in female fertility advantage in gynodioecious Thymus vulgaris. Evolution 54: 1510-1520.
58. Thomson JD. 1986. Pollen transport and deposition by bumble bees in Erythronium: influences of floral nectar and bee grooming. Journal of Ecology 74: 329-341.
59. Thomson JD, Plowright RC. 1980. Pollen carryover, nectar rewards, and pollinator behaviour with special reference to Diervilla lonieera. Oecologia 46: 68-74.
60. Vaarama A, Jaaskeläinen O. 1967. Studies in gynodioecism in the Finnish populations of Geranium sylvaticum L. Annales Academiae Scientiarum Fennicae. Series A. IV. Biologica 108.
61. Valdeyron G, Dommée B, Vernet P. 1977. Self-fertilisation in male-fertile plants of a gynodioeceous species Thymus vulgaris L. Heredity 39: 243-249.
62. Waser NM. 1986. Flower constancy: definition, cause, and measurement. The American Naturalist 127: 593-603.
63. Wesselingh RA. 2007. Pollen limitation meets resource allocation: towards a comprehensive methodology. New Phytologist 174: 26-37.
64. Williams CF, Kuchenreuther MA, Drew A. 2000. Floral dimorphism, and self fertilization in gynodioecious Geranium richardsonii (Geraniaceae). American Journal of Botany 87: 661-666.
65. Zhang YW, Wang Y, Yu Q, Zhao JM. 2008. Sex expression, female frequency, and reproduction output in a gynodioecious clonal herb, Glechoma longiturba (Lamiaceae). Plant Ecology 199: 255-264.
66. Zimmerman M, Pyke GH. 1988. Reproduction in Polemonium: assessing the factors limiting seed set. The American Naturalist 131: 723-738.