Development of Distylous Flowers and Investment of Biomass in Male and Female Function in Palicourea padifolia (Rubiaceae)

Abstract

Knowledge of developmental pathways for achieving differences in style and anther heights, in concert with those of ancillary features accompanied with data in regard to biomass investment to male and female function, provide an excellent opportunity for examining the developmental correlations between primary and ancillary floral traits so as to understand the evolution of heterostyly. The ontogenetic relationships between bud length and anther height and between bud length and style height, and between bud length versus bud width, anther length, and number of pollen grains per anther for long-styled (LS) and short-styled (SS) morphs of P. padifolia are described. We also described the ontogenetic biomass allocation to male and female function and to corolla with elongation of buds harvested at regular intervals. We observed an early termination of stylar growth in SS buds, whereas LS styles steadily increased in size. Morph differences for relative growth rates were significant for anther height, anther length, and pollen number but not for bud width. Bud width and anther length had a negative allometric relationship with bud elongation. The relationship between bud length and number of pollen grains per anther was positive and morph differences in pollen number were detected at later stages of development. An increase in corolla mass involved a disproportionate allocation to the female function in SS flowers and male allocation was similar for the two morphs over the course of development. Our results are consistent with theoretical and empirical data for distylous species with an approach herkogamous ancestor, and with the more general hypothesis of ontogenetic lability of heterostyly, in which morph differences in style and anther heights are achieved in various ways. Variations observed in sexual investment between floral morphs suggest differences in sex expression during flower development.

Palicourea padifolia - ancillary traits - distyly - male and female function - ontogenetic relationships - pollen production

References

• 1 Arroyo J., Dafni A.. Variation in habitat, season, flower traits and pollinators in dimorphic Narcissus tazatta L. (Amaryllidaceae) in Israel.  New Phytologist. (1995);  129 135-145
• 2 Barrett S. C. H.. Evolution and Function of Heterostyly. Berlin; Springer-Verlag (1992)
• 3 Barrett S. C. H., Cruzan M. B.. Incompatibility in heterostylous flowers. Williams, E. G., Knox, R. B., and Clarke, A. E., eds. Genetic Control of Self-Incompatibility and Reproductive Development. Dordrecht; Kluwer Academic (1994): 189-219
• 4 Barrett S. C. H., Jesson L. K., Bake A. M.. The evolution and function of stylar polymorphisms in flowering plants.  Annals of Botany. (2000);  85 253-265
• 5 Casper B. B.. The application of sex allocation theory to heterostylous plants. Barrett, S. C. H., ed. Evolution and Function of Heterostyly. Berlin; Springer-Verlag (1992): 209-223
• 6 Castillo-Campos G.. Vegetación y flora del Municipio de Xalapa, Veracruz. Xalapa; Instituto de Ecología, A.C. (1991)
• 7 Cesaro A. C., Barrett S. C. H., Maurice S., Vaissiere B. E., Thompson J. D.. An experimental evaluation of self-interference in Narcissus assoanus: functional and evolutionary implications.  Journal of Evolutionary Biology. (2004);  17 1367-1376
• 8 Charlesworth D.. Allocation to male and female function in hermaphrodites, in sexually polymorphic populations.  Journal of Theoretical Biology. (1989);  96 143-149
• 9 Charlesworth D., Charlesworth B.. A model for the evolution of distyly.  American Naturalist. (1979);  114 467-498
• 10 Charlesworth D., Charlesworth B.. The effect of investment in attractive structures on allocation to male and female functions in plants.  Evolution. (1987);  41 948-968
• 11 Contreras P. S., Ornelas J. F.. Reproductive conflicts of Palicourea padifolia (Rubiaceae) a distylous shrub of a tropical cloud forest in Mexico.  Plant Systematics and Evolution. (1999);  219 225-241
• 12 Darwin C.. The different forms of flowers on plants of the same species. London; Murray (1877)
• 13 Domínguez C. A., Ávila-Sakar G., Vázquez-Santana S., Márquez-Guzmán J.. Morph-biased male sterility in the tropical distylous shrub Erythroxylum havanense (Erythroxylaceae).  American Journal of Botany. (1997);  84 626-632
• 14 Dulberger R.. Floral polymorphism and their functional significance in the heterostylous syndrome. Barrett, S. C. H., ed. Evolution and Function of Heterostyly. Berlin; Springer-Verlag (1992): 40-84
• 15 Dulberger R., Ornduff R.. Stigma morphology in distylous and non-heterostylous species of Villarsia (Menyanthaceae).  Plant Systematics and Evolution. (2000);  225 171-184
• 16 Faivre A. E.. Ontogenetic differences in heterostylous plants and implications for development from a herkogamous ancestor.  Evolution. (2000);  54 847-858
• 17 Ganders F. R.. The biology of heterostyly.  New Zealand Journal of Botany. (1979);  17 607-635
• 18 González C., Ornelas J. F., Jiménez L.. Between-year changes in functional gender expression of Palicourea padifolia (Rubiaceae), a distylous, hummingbird-pollinated shrub.  Annals of Botany. (2005);  95 371-378
• 19 Hernández A., Ornelas J. F.. Correlación morfoespecífica en flores de Palicourea padifolia (Rubiaceae).  Boletín de la Sociedad Botánica de México. (2003);  73 35-41
• 20 Hernández A., Ornelas J. F.. Disassortative pollen transfer in distylous Palicourea padifolia (Rubiaceae), a hummingbird-pollinated shrub.  EcoScience. (2007);  14 8-16
• 21 Lloyd D. G., Webb C. J.. The evolution of heterostyly. Barrett, S. C. H., ed. Evolution and Function of Heterostyly. Berlin; Springer-Verlag (1992 a): 151-175
• 22 Lloyd D. G., Webb C. J.. The selection of heterostyly. Barrett, S. C. H., ed. Evolution and Function of Heterostyly. Berlin; Springer-Verlag (1992 b): 179-207
• 23 Muenchow G.. Ecological use of failure time analysis.  Ecology. (1986);  67 246-250
• 24 Naiki A., Kato M.. Pollination system and evolution of dioecy from distyly in Mussaenda parviflora (Rubiaceae).  Plant Species Biology. (1999);  14 217-227
• 25 Nishihiro J., Washitani I., Thomson J. D., Thomson B. A.. Patterns and consequences of stigma height variation in a natural population of a distylous plant, Primula sieboldii.  Functional Ecology. (2000);  14 502-512
• 26 Ornduff R.. Systematics and breeding system of Gelsemium (Loganiaceae).  Journal of the Arnold Arboretum. (1970);  51 1-17
• 27 Ornelas J. F., Jiménez L., González C., Hernandez A.. Reproductive ecology of distylous Palicourea padifolia (Rubiaceae) in a tropical montane cloud forest. I. Hummingbirds' effectiveness as pollen vectors.  American Journal of Botany. (2004 a);  91 1052-1060
• 28 Ornelas J. F., González C., Jiménez L., Lara C., Martínez A. J.. Reproductive ecology of distylous Palicourea padifolia (Rubiaceae) in a tropical montane cloud forest. II. Attracting and rewarding mutualistic and antagonistic visitors.  American Journal of Botany. (2004 b);  91 1061-1069
• 29 Pailler T., Thompson J. D.. Distyly and variation in heteromorphic incompatibility in Gaertnera vaginata (Rubiaceae) endemic to La Réunion Island.  American Journal of Botany. (1997);  84 315-327
• 30 Ree R. H.. Pollen flow, fecundity, and the adaptive significance of heterostyly in Palicourea padifolia (Rubiaceae).  Biotropica. (1997);  29 298-308
• 31 Richards J. H., Barrett S. C. H.. The development of heterostyly. Barrett, S. C. H, ed. Evolution and Function of Heterostyly. Berlin; Springer-Verlag (1992): 85-127
• 32 Richards J. H., Koptur S.. Floral variation and distyly in Guettarda scabra (Rubiaceae).  American Journal of Botany. (1993);  80 31-40
• 33 Riveros M., Barria O., Humaña P.. Self-incompatibility in distylous Hedyotis salzmannii (Rubiaceae).  Plant Systematics and Evolution. (1995);  194 1-8
• 34 Taylor C. M.. Revision of Palicourea (Rubiaceae) in Mexico and Central America.  Systematic Botanical Monographs. (1989);  26 1-102
• 35 Webb C., Lloyd D.. The avoidance of interference between the presentation of pollen and stigmas in angiosperms. II. Herkogamy.  New Zealand Journal of Botany. (1986);  24 163-178
• 36 Wolfe L. M.. Associations among multiple floral polymorphisms in Linum pubescens (Linaceae), a heterostylous plant.  International Journal of Plant Sciences. (2001);  162 335-342
• 37 Wolfe L. M., Barrett S. C. H.. Pollinator foraging behavior and pollen collection on the floral morphs of tristylous Pontederia cordata L.  Oecologia. (1987);  74 347-351
• 38 Wolfe L. M., Barrett S. C. H.. Patterns of pollen removal and deposition in tristylous Pontederia cordata L. (Pontederiaceae).  Biological Journal of the Linnean Society. (1989);  36 317-329

Editor: J. T. M. Elzenga