Changes in reciprocal herkogamy during the tristyly-distyly transition in Oxalis alpina increase efficiency in pollen transfer

Journal of Evolutionary Biology

Volumn 25, Issue 3, 2012, Pages 574-583

  Baena Diaz F ^a   Fornoni, J ^a   Sosenski, P ^a   Molina Freaner, F E ^b   Weller, S G ^c   Perez Ishiwara R ^a   Dominguez C A ^a  

^a INSTITUTO DE ECOLOGÍA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Evolutionary transition; Heterostyly; Natural selection; Oxalis alpina; Pollen flow

Indexed keywords

FLUORESCENT DYE;

ADAPTATION; BEE; DYE; FLOWER; HYPOTHESIS TESTING; MORPHOLOGY; NATURAL SELECTION; PROBABILITY; RECIPROCITY;

ADAPTATION; ANGIOSPERM; ANIMAL; ARTICLE; BEE; COMPARATIVE STUDY; FLOWER; HISTOLOGY; MEXICO; PHYSIOLOGY; POLLINATION;

ADAPTATION, BIOLOGICAL; ANGIOSPERMS; ANIMALS; BEES; FLOWERS; FLUORESCENT DYES; MEXICO; POLLINATION;

APOIDEA; HETEROSARUS; OXALIS; OXALIS ALPINA;

EID: 84857035919     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2012.02455.x     Document Type: Article

References (51)

1. Adler, L. & Irwin, R. 2006. Comparison of pollen transfer dynamics by multiple floral visitors: experiment with pollen and fluorescent dye. Ann. Bot. 97: 141-150.
2. Armbruster, W.S., Hansen, T.F., Pélabon, C., Pérez-Barrales, R. & Maad, J. 2009. The adaptive accuracy of flowers: measurement and microevolutionary patterns. Ann. Bot. 103: 1529-1545.
3. Barrett, S.C.H. 2002. The evolution of plant sexual diversity. Nat. Rev. 3: 274-284.
4. Barrett, S.C.H. & Glover, D.E. 1985. On the Darwinian hypothesis of the adaptive significance of tristyly. Evolution 39: 766-774.
5. Barrett, S.C.H. & Husband, B.C. 1990. Variation in outcrossing rates in Eichornia paniculata: the role of demographic and reproductive factors. Plant Species Biol. 5: 41-55.
6. Barrett, S.C.H. & Shore, J.S. 2008. New insights on heterostyly: comparative biology, ecology and genetics. In: Self-Incompatibility in Flowering Plants (V.E. Franklin-Tong, ed.), pp. 3-32. Springer, Berlin, Heidelberg.
7. Barrett, S.C.H., Jesson, L.K. & Baker, A.M. 2000. The evolution and function of stylar polymorphisms in flowering plants. Ann. Bot. 85: 253-265.
8. Barrett, S.C.H., Harder, L.D. & Cole, W.W. 2004. Correlated evolution of floral morphology and mating-type frequencies in a sexually polymorphic plant. Evolution 58: 964-975.
9. Bell, G. 1985. On the function of flowers. Proc. R. Soc. Lond. B 224: 223-265.
10. Castillo, R.A., Cordero, C. & Domínguez, C.A. 2002. Are reward polymorphisms subject to frequency-and density-dependent selection? Evidence from a monoecious species pollinated by deceit. J. Evol. Biol. 15: 544-552.
11. Cesaro, A.C., Barrett, S.C.H., Maurice, S., Vaissiere, B.E. & Thompson, J.D. 2004. An experimental evaluation of self-interference in Narcissus assoanus: functional and evolutionary implications. J. Evol. Biol. 17: 1367-1376.
12. Charlesworth, D. 1979. The evolution and breakdown of tristyly. Evolution 33: 486-498.
13. Dai, D. & Galloway, L.F. 2011. Do dichogamy and herkogamy reduce sexual interference in a self-incompatible species? Funct. Ecol. 25: 271-278.
14. Darwin, C. 1877. The Different Forms of Flowers of Plants of the Same Species. Murray, London.
15. Eckert, C.G. & Mavraganis, K. 1996. Evolutionary consequences of extensive morph loss in tristylous Decodon verticillatus (Lythraceae): a shift from tristyly to distyly? Am. J. Bot. 83: 1024-1032.
16. Ferrero, V., Chapela, I., Arroyo, J. & Navarro, L. 2011. Reciprocal style polymorphisms are not easily categorised: the case of heterostyly in Lithodora and Glandora (Boraginaceae). Plant Biol. 13: 7-18.
17. Fisher, R.A. 1941. The theoretical consequences of polyploidy inheritance for the mid style form of Lythrum salicaria. Ann. Hum. Genet., 11: 31-38.
18. Ganders, F.G. 1975. Fecundity in distylous and self-incompatible homostylous plants of Mitchella repens (Rubiaceae). Evolution 29: 186-188.
19. Ganders, F.R. 1979. The biology of heterostyly. N. Z. J. Bot. 17: 607-635.
20. Glover, D.E. & Barrett, S.C.H. 1983. Trimorphic incompatibility in Mexican populations of Pontederia sagittata Presl. (Pontederiaceae). New Phytol. 95: 439-455.
21. Harder, L.D. & Barrett, S.C.H. 2006. Ecology and Evolution of Flowers. Oxford University Press, Oxford, UK.
22. Jersakova, J. & Johnson, S.D. 2007. Protandry promotes male pollination success in a moth-pollinated orchid. Funct. Ecol. 21: 496-504.
23. Kutaka, J., Weller, S.G., Domínguez, C.A., Sakai, A.K., Molina-Freaner, F.E., Sosenski, P. et al. 2011. Female and male mediation of incompatibility modifications during the tristyly-distyly transition in Oxalis alpina. Int. J. Plant Sci. 172: 644-654.
24. Lau, P. & Bosque, C. 2003. Pollen flow in the distylous Palicourea fendleri (Rubiaceae): an experimental test of the disassortative pollen flow hypothesis. Oecologia 135: 593-600.
25. Lewis, D. & Rao, A.N. 1971. Evolution of dimorphism and population polymorphism in Pemphis acidula Forst. Proc. Roy. Soc. Lond. 178: 79-94.
26. Lloyd, D.G. & Webb, C.J. 1986. The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dicogamy. N. Z. J. Bot. 24: 135-162.
27. Lloyd, D.G. & Webb, C.J. 1992. The evolution of heterostyly. In: Evolution and Function of Heterostylv (S.C.H. Barrett, ed.), pp. 151-178. Springer Verlag, Berlin.
28. Medrano, M., Herrera, C.M. & Barrett, S.C.H. 2005. Herkogamy and mating patterns in the self-compatible daffodil Narcissus longispathus. Ann. Bot. 95: 1105-1111.
29. 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). Am. J. Bot. 87: 339-347.
30. Mulcahy, D. 1964. The reproductive biology of Oxalis priceae. Am. J. Bot. 51: 1045-1050.
31. Mulcahy, D.L. 1979. The rise of the angiosperm: a genecological factor. Science 206: 20-23.
32. Nishihiro, J., Washitani, I., Thompson, J.D. & Thompson, B.A. 2000. Patterns and consequences of stigma height variation in a natural population of a distylous plant, Primula sieboldii. Funct. Ecol. 14: 502-512.
33. O'Neil, P. 1992. Variation in male and female reproductive success among floral morphs in the tristylous plant Lythrum salicaria (Lythraceae). Am. J. Bot. 79: 1024-1030.
34. Ordano, M., Fornoni, J., Boege, K. & Dominguez, C.A. 2008. The adaptive value of phenotypic floral integration. New Phytol. 179: 1183-1192.
35. Pérez-Alquicira, J., Molina-Freaner, F.E., Piñero, Weller, S.G., D., Martínez-Meyer, E., Rozas, J. et al. 2010. The role of historical factors and natural selection in the evolution of breeding systems of Oxalis alpina in the Sonoran desert 'Sky Islands'. J. Evol. Biol. 23: 2163-2175.
36. Pérez-Barrales, R. & Arroyo, J. 2010. Pollinator shifts and the loss of style polymorphism in Narcissus papyraceus (Amaryllidaceae). J. Evol. Biol. 23: 1117-1128.
37. R Development Core Team 2008. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
38. Richards, J.H. & Barrett, S.C.H. 1992. The development of heterostyly. In: The Evolution and Function of Heterostyly (S.C.H. Barrett, ed.), pp. 279. Theor. Appl. Genet. 15, Springer-Verlag, Heidlberg.
39. SAS Institute. 1999. SAS/STAT Software, Version 8. SAS Institute, Cary, NC, USA.
40. Sosenski, P., Fornoni, J., Molina-Freaner, F.E., Weller, S.G. & Domínguez, C.A. 2010. Changes in sexual organ reciprocity and phenotypic floral integration during the tristyly distyly transition in Oxalis alpina. New Phytol. 185: 829-840.
41. Stebbins, L. 1970. Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Ann. Rev. Ecol. Syst. 1: 307-326.
42. Swamy, R.N. & Bahadur, B. 1984. Pollen flow in dimorphic Turnera subulata (Turneraceae). New Phytol. 98: 205-209.
43. Torres, C. 2000. Pollen size evolution: correlation between pollen volume and pistil length in Asteraceae. Sex. Plant Reprod. 12: 365-370.
44. Webb, C.J. & Lloyd, D. 1986. The avoidance of interference between the presentation of pollen and stigmas in angiosperms II. Herkogamy. N. Z. J. Bot. 24: 163-178.
45. Weller, S.G. 1979. Variation in heterostylous reproductive systems among populations of Oxalis alpina in southeastern Arizona. Syst. Bot. 4: 57-71.
46. Weller, S.G. 1980. Pollen flow and fecundity in populations of Lithospermum caroliniense. Am. J. Bot. 67: 1334-1341.
47. Weller, S.G. 1981. Pollination biology of heteromorphic populations of Oxalis alpina (Rose) Kunth (Oxalidaceae) in south-eastern Arizona. Bot. J. Linn. Soc. 83: 189-198.
48. Weller, S.G. 1986. Factors influencing frequency of the mid-styled morph in tristylous populations of Oxalis alpina. Evolution 40: 279-289.
49. Weller, S.G. 1992. Evolutionary modifications of tristylous breeding systems. In: Evolution and Function of Heterostyly (S. C. H. Barrett, ed.), pp. 247-272. Springer-Verlag, Berlin.
50. Weller, S.G. 2009. The different forms of flowers - what have we learned since Darwin? Bot. J. Linn. Soc. 160: 249-261.
51. Weller, S.G., Domínguez, C.A., Molina-Freaner, F.E., Fornoni, J. & LeBuhn, G. 2007. The Evolution of distyly from tristyly in populations of Oxalis alpina (Oxalidaceae) in the Sky Islands of the Sonoran Desert. Am. J. Bot. 94: 972-985.