UMA REVISÃO SOBRE A SELEÇÃO SEXUAL EM PLANTAS

Authors

  • Cassio Augusto Patrocinio Toledo Universidade Estadual de Campinas
  • Narcísio Costa Bígio Universidade Federal de Rondônia
  • Joicelene Regina Lima da Paz Universidade Estadual de Feira de Santana

DOI:

https://doi.org/10.4257/oeco.2020.2401.03

Keywords:

Bateman’s principle, female choice, pollen competition, reproductive success, selective abortion

Abstract

A seleção sexual em plantas é um assunto que tem sido discutido recentemente na literatura, considerando que a origem do termo foi proposta por Darwin em 1871. A seleção sexual pode ser entendida como um mecanismo que age no sentido de conferir sucesso reprodutivo aos diferentes indivíduos envolvidos. Nestes casos, as principais relações envolvidas na seleção sexual em plantas incluem: (1) competição intrasexual por polinização e fertilização; (2) escolha da função feminina para que os melhores gametas masculinos tenham acesso aos óvulos e (3) aborto seletivo de sementes para garantir que embriões de qualidade se desenvolvam. De acordo com os resultados aqui apresentados, foi possível identificar mais de 161 espécies vegetais em que processos relacionados à seleção sexual foram demonstrados. A grande maioria dos trabalhos foi conduzida a partir de experimentos comparativos de remoção e deposição de pólen e produção de sementes com os atrativos florais, sendo embasados por testes estatísticos, mas um número considerável deles foi feito com base em experimentos genéticos e químicos, e alguns ainda com base exclusivamente teórica. A seleção sexual também tem sido entendida como um dos mecanismos responsáveis por mudanças evolutivas nas plantas, tais como a morfologia floral (e.g., tamanho das inflorescências, comprimento do estilete, receptividade do estigma) e evolução de sistemas sexuais (e.g., dioicia). Para estudos futuros, ressalta-se a necessidade de incluir uma variedade maior de grupos taxonômicos em trabalhos de seleção sexual, além de buscar entender como os mecanismos de aptidão dos grãos de pólen e escolha da fêmea funcionam em escala molecular. Este trabalho de revisão objetiva apresentar como a seleção sexual ocorre nas plantas e como os experimentos sobre esta temática têm sido conduzidos.

A REVISION OF SEXUAL SELECTION IN PLANTS. Sexual selection in plants has been discussed only recently in the literature, considering that the term was originally proposed by Darwin in 1871. Sexual selection can be understood as a mechanism that acts in order to ensure reproductive success to different individuals. In these cases, the main relations involved in the sexual selection in plants are: (1) intrasexual competition for pollination and fertilization; (2) female choice to guarantee that more vigorous male gametophytes fertilize the ovules; and (3) selective abortion of seeds so that only high-quality embryos develop. According to our revision, we found more than 161 plant species in which events related to sexual selection were identified. Most of these works have been conducted base on comparative experiments of pollen removal and deposition and seed production with floral attractiveness, corroborated by statistical tests, although a considerable number of studies has used genetic and chemical approaches, and a few are exclusively theoretical. Sexual selection has also been considered as one of the mechanisms that has driven evolutionary changes in plants, such as floral morphology (e.g., inflorescence size, style length, stigma receptivity) and the evolution of sexual systems (e.g., dioecy). For future studies, we stress the necessity to include more taxonomic groups in sexual selection experiments, as well as understand how the mechanisms of pollen ability and female choice operate in molecular scale. This revision aims to present how sexual selection occurs in plants and how experiments on this subject have been conducted.

References

Aagaard, J. E., George, R. D., Fishman, L., MacCoss, M. J., & Swanson, W. J. 2013. Selection on plant male function genes identifies candidates for reproductive isolation of yellow monkeyflowers. PLoS Genetics, 9(12), e1003965. DOI: 10.1371/journal.pgen.1003965

Andersson, S. 1991. Floral display and pollination success in Achillea ptarmica (Asteraceae). Holarctic Ecology, 14(3), 186–191. DOI: 10.1111/j.1600-0587.1991.tb00651.x

Arathi, H. S., Ganeshaiah, K. N., Shaanker, R. U., & Hegde, S. G. 1996. Factors affecting embryo abortion in Syzygium cuminii (L.) skeels (Myrtaceae). International Journal of Plant Sciences, 157(1), 49–52. DOI: 10.1086/297319

Arnold, S. J. 1994. Is there a unifying concept of sexual selection that applies to both plants and animals? American Naturalist, 144, S1–S12. DOI: 10.1086/285650

Banks, J. A. 1994. Sex-determining genes in the homosporous fern Ceratopteris. Development, 120, 1949–1958.

Barrett, S. C. H., & Harder, L. D. 2017. The ecology of mating and its evolutionary consequences in seed plants. Annual Review of Ecology, Evolution, and Systematics, 48(1), 135–157. DOI: 10.1146/annurev-ecolsys-110316-023021

Barrett, S. C. H., & Hough, J. 2013. Sexual dimorphism in flowering plants. Journal of Experimental Botany, 64(1), 67–82. DOI: 10.1093/jxb/ers308

Bateman, A. J. 1948. Intra-sexual selection in Drosophila. Heredity, 2(3), 349–368.

Bawa, K. S. 1980a. Mimicry of male by female flowers and intrasexual competition for pollinators in Jacaratia dolichauda (D.Smith) Woodson (Caricaceae). Evolution, 34(3), 467–474. DOI: 10.1111/j.1558-5646.1980.tb04836.x

Bawa, K. S. 1980b. Evolution of dioecy in flowering plants. Annual Review of Ecology and Systematics, 11(1), 15–39.

Beekman, M., Nieuwenhuis, B., Ortiz-Barrientos, D., & Evans, J. P. 2016. Sexual selection in hermaphrodites, sperm and broadcast spawners, plants and fungi. Physiological Transactions B, 371, 20150541. DOI: 10.1098/rstb.2015.0541

Bell, G. 1985. On the function of flowers. Proceedings of the Royal Society of London B, 224(1235), 223–265. DOI: 10.1098/rspb.1985.0031

Bertin, R. I. 1988. Paternity in plants. In: J. L. Doust & L. L. Doust (Eds.), Plant reproductive ecology: patterns and strategies. pp. 30–59. New York: Oxford University Press.

Bertin, R. I. 1990. Effects of pollination intensity in Campsis radicans. American Journal of Botany, 77(2), 178–187. DOI: 10.1002/j.1537-2197.1990.tb13544.x

Biernaskie, J. M., & Elle, E. 2007. A theory for exaggerated secondary sexual traits in animal-pollinated plants. Evolutionary Ecology, 21(4), 459–472. DOI: 10.1007/s10682-006-9112-1

Björkman, T. 1995. The effect of pollen load and pollen grain competition on fertilization success and progeny performance in Fagopyrum esculentum. Euphytica, 83(1), 47–52. DOI: 10.1007/BF01677860

Bond, W. J., & Maze, K. E. 1999. Survival costs and reproductive benefits of floral display in a sexually dimorphic dioecious shrub, Leucadendron xanthoconus. Evolutionary Ecology, 13(1), 1–18. DOI: 10.1023/A:1006581412580

Bookman, S. S. 1984. Evidence for selective fruit production in Asplepias. Evolution, 38(1), 72–86. DOI: 10.1111/j.1558-5646.1984.tb00261.x

Brewbaker, J. L., & Majumder, S. K. 1961. Cultural studies of the pollen population effect and the self-incompatibility inhibition. American Journal of Botany, 48(6), 457–464. DOI: 10.1002/j.1537-2197.1961.tb11669.x

Buchholz, J. T., & Blakeslee, A. F. 1930. Pollen tube growth and control of gametophytic selection in cocklebur, a 25-chromosome Datura. Botanical Gazette, 90(4), 366–383. DOI: 10.1086/334110

Campbell, D. R. 1989. Measurements of selection in a hermaphroditic plant: variation in male and female pollination success. Evolution, 43(2), 318–34. DOI: 10.1111/j.1558-5646.1989.tb04230.x

Carlson, J. E. 2007. Male-biased nectar production in a protandrous herb matches predictions of sexual selection theory in plants. American Journal of Botany, 94(4), 674–682. DOI: 10.3732/ajb.94.4.674

Carlson, J. E., & Harms, K. E. 2006. The Evolution of gender-biased nectar production in hermaphroditic plants. Botanica Review 72(2), 179–205. DOI: 10.1663/0006-8101(2006)72[179:TEOGNP]2.0.CO;2

Casper, B. B. 1988. Evidence for selective embryo abortion in Cryptantha flava. American Naturalist, 132(3), 318–326. DOI: 10.1086/284855

Charlesworth, D., Charlesworth, B., & Marais, G. 2005. Steps in the evolution of heteromorphic sex chromosomes. Heredity, 95(2), 108–128.

Charnov, E. L. 1982. The theory of sex allocation. Princeton, NJ: Princeton University Press: p. 355.

Cocucci, A. A., Marino, S., Baranzelli, M., Wiemer, A. P., & Sérsic, A. 2014. The buck in the milkweed: evidence of male-male interference among pollinaria on pollinators. New Phytologist, 203(1), 280–286. DOI: 10.1111/nph.12766

Crowe, L. K. 1971. The polygenic control of outbreeding in Borago officinalis. Heredity, 27(1), 111–118. DOI: 10.1038/hdy.1971.75

Dai, C., & Galloway, L. F. 2013. Sexual selection in a hermaphroditic plant through female reproductive success. Journal of Evolutionary Biology, 26(12), 2622–2632. DOI: 10.1111/jeb.12254

Dajoz, I., Till-Bottraud, I., & Gouyon, P.-H. 1991. Evolution of pollen morphology. Science, 253(5015), 66–68. DOI: 10.1126/science.253.5015.66

Darwin, C. 1859. The origin of species by means of natural selection. London: John Murray: p. 502

De Jong, T. J., Waser, N. M., & Klinkhamer, P. G. L. 1993. Geitonogamy: The neglected side of selfing. Tree, 8(9), 321–325. DOI: 10.1016/0169-5347(93)90239-L

Delph, L. F., & Meagher, T. R. 1995. Sexual dimorphism masks life history trade‐offs in the dioecious plant Silene latifolia. Ecology, 76(3), 775–785. DOI: 10.2307/1939343

Delph, L. F., Weinig, C., & Sullivan, K. 1998. Why fast-growing pollen tubes give rise to vigorous progeny: the test of a new mechanism. Proceedings of the Royal Society of London Series B: Biological Sciences, 265(1399), 935–939. DOI: 10.1098/rspb.1998.0381

Devlin, B., & Ellstrand, N. C. 1990. Male and female fertility variation in wild radish, a hermaphrodite. American Naturalist, 136(1), 86–107. DOI: 10.1086/285083

Dickmann, D. I, & Kozlowski, T. T. 1969. Seasonal growth patterns of ovulate strobili of Pinus resinosa in central Wisconsin. Canadian Journal of Botany, 47(6), 839–848. DOI: 10.1139/b69-121

Dorken, M. E., & Perry, L. E. 2017. Correlated paternity measures mate monopolization and scales with the magnitude of sexual selection. Journal of Evolutionary Biology, 30(2), 377–387. DOI: 10.1111/jeb.13013

Douglas, K. L., & Cruden, R. W. 1994. The reproductive biology of Anemone Canadensis (Ranunculaceae). American Journal of Botany, 81(3), 314–321. DOI: 10.1002/j.1537-2197.1994.tb15449.x

Elleman, C. J., & Dickison, H. G. 1994. Pollen-stigma interaction during sporophytic self-incompatibility in Brassica oleracea. In: E. G. Williams, A. E. Clarke & R. B. Knox (Eds.), Genetic control of self-incompatibility and reproductive development in flowering plants. Advances in cellular and molecular biology of plantas. pp. 67–87. Dordrecht: Springer-Science+Business Media. DOI: 10.1007/978-94-017-1669-7

Emms, S. K., Stratton, D. A., & Snow, A. A. 1997. The effect of inflorescence size on male fitness: experimental tests in the andromonoecious lily, Zigadenus paniculatus. Evolution, 51(5), 1481–1489. DOI: 10.1111/j.1558-5646.1997.tb01471.x

Fiebig, A., Kimport, R., & Preuss, D. 2004. Comparisons of pollen coat genes across Brassicaceae species reveal rapid evolution by repeat expansion and diversification. PNAS, 101(9), 3286–3291. DOI: 10.1073/pnas.0305448101

Gerald, J. N. F., Carlson, A. L., Smith, E., Maloof, J. N., Weigel, D., Chory, J., Borevitz, J. O., & Swanson, R. J. 2014. New Arabidopsis advanced intercross recombinant inbred lines reveal female control of nonrandom mating. Plant Physiology, 165(1), 175–185. DOI: 10.1104/pp.113.233213

Guerrant Jr, E. O. 1988. Heterochrony in plants. In: M. L. McKinney (Ed.), Heterochrony in evolution. pp. 111–133. Boston, MA: Springer. DOI: 10.1007/978-1-4899-0795-0_7

Harder, L. D., Aizen, M. A., & Richards, S. A. 2016a. The population ecology of male gametophytes: the link between pollination and seed production. Ecology Letters, 19(5), 497–509. DOI: 10.1111/ele.12596

Harder, L. D., Aizen, M. A., Richards, S. A., Joseph, M. A., & Busch, J. W. 2016b. Diverse ecological relations of male gametophyte populations in stylar environments. American Journal of Botany, 103(3), 484–497. DOI: 10.3732/ajb.1500269

Harder, L. D., & Johnson, S. 2008. Function and evolution of aggregated pollen in angiosperms. International Journal of Plant Sciences, 169(1), 59–78. DOI: 10.1086/523364

Havens, K., & Delph, L. F. 1996. Differential seed maturation uncouples fertilization and siring success in Oenothera organensis (Onagraceae). Heredity, 76, 623–632. DOI: 10.1038/hdy.1996.89

Herrero, M., & Hormoza, J. I. 1996. Pistil strategies controlling pollen tube growth. Sexual Plant Reproduction, 9(6), 343–347. DOI: 10.1007/BF02441953

Holm, S. O. 1994. Pollination density effects on pollen germination and pollen tube growth in Betula pubescens Ehrh. in northern Sweden. New Phytologist, 126(3), 541–547. DOI: 10.1111/j.1469-8137.1994.tb04253.x

Janzen, D. H. 1977. A note on optimal mate selection by plants. American Naturalist, 111(978), 365–371. DOI: 10.1086/283166

Johnson, L. A., Chan, L. M., Weese, T. L., Busby L. D., & McMurry, S. 2008. Nuclear and cpDNA sequences combined provide strong inference of higher phylogenetic relationships in the phlox family (Polemoniaceae). Molecular Phylogenetics and Evolution, 48(3), 997–1012. DOI: 10.1016/j.ympev.2008.05.036

Johnson, L. A., Schultz J. L., Soltis, D. E., & Soltis, P. S. 1996. Monophyly and generic relationships of Polemoniaceae based on matK sequences. American Journal of Botany, 83(9), 1207–1224. DOI: 10.2307/2446205

Kirkpatrick, M., & Ravigné, V. 2002. Speciation by natural and sexual selection: models and experiments. American Naturalist, 159(S3), 22–35. DOI: 10.1086/338370

Korpelainen, H. 1994. Growth, sex determination and reproduction of Dryopteris filix‐mas (L.) Schott gametophytes under varying nutritional conditions. Botanical Journal of the Linnean Society, 114(4), 357–366. DOI: 10.1111/j.1095-8339.1994.tb01840.x

Lande, R. 1980. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34(2), 292–305. DOI: 10.2307/2407393

Lankinen, A., & Green, K. K. 2015. Using theories of sexual selection and sexual conflict to improve our understanding of plant ecology and evolution. AoB Plants, 7(plv008), 1–18. DOI: 10.1093/aobpla/plv008

Lau, J. A., Miller, R. E., & Rausher, M. D. 2008. Selection through male function favors smaller floral display size in the common morning glory Ipomoea purpurea (Convolvulaceae). American Naturalist, 172(1), 63–74. DOI: 10.1086/588080

Lee, T. D. 1984. Patterns of fruits maturation: a gametophyte competition hypothesis. American Naturalist, 123(3), 427–432. DOI: 10.1086/284213

Lloyd, D. G., & Webb, C. J., 1977. Secondary sex characters in plants. Botanical Review, 43(2), 177–216. DOI: 10.1007/BF02860717

Lovett-Doust, J., & Harper, J. L. 1980. The resource costs of gender and maternal support in an andromonoecious umbellifer, Smyrnium olusatrum L. New Phytologyst, 85(2), 251-264. DOI: 10.1111/j.1469-8137.1980.tb04467.x-

Maan, M. E., & Seehausen, O. 2011. Ecology, sexual selection and speciation. Ecology Letters, 14(6), 591–602. DOI: 10.1111/j.1461-0248.2011.01606.x

Marshall, D. L. 1988. Postpollination effects on seed paternity: mechanisms in addition to microgametophyte competition operate in wild radish. Evolution, 42(6), 1256–1266. DOI: 10.1111/j.1558-5646.1988.tb04185.x

Marshall, D. L., & Whittaker, K. L. 1989. Effects of pollen donor identity on offspring quality in wild radish, Raphanus sativus. American Journal of Botany, 76(7), 1081–1088. DOI: 10.1002/j.1537-2197.1989.tb15089.x

Melser, C., & Klinkhamer, P. 2001. Selective seed abortion increases offspring survival in Cynoglossum officinale (Boraginaceae). American Journal of Botany, 88(6),1033–40. DOI: 10.2307/2657085

Mena-Alí, J. I., & Rocha, O. J. 2005. Selective seed abortion affects the performance of the offspring in Bauhinia ungulata. Annals of Botany, 95(6), 1017–1023. DOI: 10.1093/aob/mci109

Meyer, K. M., Soldaad, L. L., Suge, H., & Thulke, H. H. 2014. Adaptive and selective seed abortion reveals complex conditional decision making in plants. American Naturalist, 183(3), 376–383. DOI: 10.1086/675063

Mohan-Raju, B., Uma-Shaanker, R., & Ganeshaiah, K. N. 1996. Intra-fruit seed abortion in a wind dispersed tree, Dalbergia sissoo Roxb: proximate mechanisms. Sexual Plant Reproduction, 9(5), 273–278. DOI: 10.1007/BF02152702

Moore, J. C., & Pannell, J. R. 2011. Sexual selection in plants. Current Biology, 21(5), 176–182. DOI: 10.1016/j.cub.2010.12.035

Moré, M., Amorim, F. W., Benitez-vieyra, S., Medina, A. M., Sazima, M., & Cocucci, A. A. 2012. Armament imbalances: match and mismatch in plant pollinator traits of highly specialized long-spurred orchids. PLoS ONE, 7(7), 1–9. DOI: 10.1371/journal.pone.0041878

Morgan, M. T., & Schoen, D. J. 1997. Selection on reproductive characters: floral morphology in Asclepias syriaca. Heredity, 79, 433–41. DOI: 10.1038/hdy.1997.178

Mulcahy, D. L. 1971. A correlation between gametophytic and sporophytic characteristics in Zea mays L. Science, 171(3976), 1155–1156. DOI: 10.1126/science.171.3976.1155

Mulcahy, D. L. 1979. The rise of the angiosperms: a genecological factor. Science, 206(4414), 20–23. DOI: 10.1126/science.206.4414.20

Mulcahy, D. L., & Mulcahy, G. B. 1975. The influence of gametophytic competition on sporophytic quality in Dianthus chinensis. Theoretical and Applied Genetics, 46(6), 277–280. DOI: 10.1007/BF00281149

Mulcahy, D. L., & Mulcahy, G. B. 1987. The effects of pollen competition. American Scientist, 75(1), 44–50.

Nettancourt, D. 1977a. Incompatibility in angiosperms. Sex Plant Report, 10, 185–199.

Nettancourt, D. 1977b. Incompatibility in angiosperms. Berlin and New York: Springer-Verlarg: p. 230.

Pasonen, H. L., Pulkkinen, P., & Käpylä, M. 2001. Do pollen donors with fastest-growing pollen tubes sire the best offspring in an anemophilous tree, Betula pendula (Betulaceae)? American Journal of Botany, 88(5), 854–860. DOI: 10.2307/2657037

Pleasants, J. M., & Chaplin, S. J. 1983. Nectar production rates of Asclepias quadrifolia: causes and consequences of individual variation. Oecologia, 59(2–3), 232–238. DOI: 10.1007/BF00378842

Plitmann, R. D., & Levin, D. A. 1983. Pollen-pistil relationships in the Polemoniaceae. Evolution, 37(5), 957–967. DOI: 10.1111/j.1558-5646.1983.tb05624.x

Podolsky, R.D. 1992. Strange floral attractors: pollinator attraction and the evolution of plant sexual systems. Science, 258(5083), 791-793. DOI: 10.1126/science.258.5083.791

Porter J. M. 1996. Phylogeny of Polemoniaceae based on nuclear ribosomal internal transcribed spacer DNA sequences. Aliso, 15(1), 57–77. DOI: 10.5642/aliso.19961501.06

Potts, W. K., & Wakeland, E. K. 1993. Evolution of MHC genetic diversity: a tale of incest, pestilence and sexual preference. Trends in Genetics, 9(12), 408–412. DOI: 10.1016/0168-9525(93)90103-O

Prather, L. A., Ferguson C. J., & Jansen, R. K. 2000. Polemoniaceae phylogeny and classification: implications of sequence data from the chloroplast gene ndhF. American Journal of Botany, 87(9), 1300–1308. DOI: 10.2307/2656723

Queller, D. C. 1983. Sexual selection in a hermaphroditic plant. Nature, 305, 706–707. DOI: 10.1038/305706a0

Richards, A. J. 1997. Multi-allelic self-incompatibility. In: A. J. Richards (Ed.), Plant breeding systems. pp. 200–241. London: Chapman and Hall.

Rosas-Guerrero, V., Aguilar, R., Martén-Rodríguez, S., Ashworth, L., Lopezaraiza-Mikel, M., Bastida, J. M., & Quesada, M. 2014. A quantitative review of pollination syndromes: do floral traits predict effective pollinators? Ecology Letters, 17(3), 388–400. DOI: 10.1111/ele.12224

Schedlbauer, M. D. 1976. Fern gametophyte development: controls of dimorphism in Ceratopteris thalictroides. American Journal of Botany, 63(8), 1080–1087. DOI: 10.1002/j.1537-2197.1976.tb13192.x

Schlichting, C. D., Stephenson, A. G., & Small, L. E. 1990. Pollen loads and progeny vigor in Cucurbita pepo: the next generation. Evolution, 44(5), 1358–1372. DOI: 10.1111/j.1558-5646.1990.tb05238.x

Schemske, D. W., & Fenster, C. B. 1983. Pollen-grain interactions in a neotropical Costus: effects of clump size and competitors. In: D. L. Mulcahy & E. Ottaviano (Eds.), Pollen: biology and implications for plant breeding. pp. 405–410. New York: Elsevier.

Shaanker, R. U., & Ganeshaiah, K. N. 1997. Conflict between parent and offspring in plants: predictions, processes and evolutionary consequences. Current Science, 72(12), 932–939.

Skogsmyr, I., & Lankinen, A. 2000. Female assessment of good genes in stylar tissue. Evolutionary Ecology Research, 2, 965–979.

Skogsmyr, I., & Lankinen, A. 2002. Sexual selection: an evolutionary force in plants? Biological Reviews, 77(4), 537–562. DOI: 10.1017/S1464793102005973

Smith, C. A., & Evenson, W. E. 1978. Energy distribution in reproductive structures of Amaryllis. American Journal of Botany, 65(6), 714–716. DOI: 10.1002/j.1537-2197.1978.tb06128.x

Snow, A. A., & Spira, T. P. 1991. Differential pollen-tube growth rates and nonrandom fertilization in Hibiscus moscheutos (Malvaceae). American Journal of Botany, 78(10), 1419–1426. DOI: 10.1002/j.1537-2197.1991.tb12608.x

Sork, V. K., & Schemske, D. W. 1992. Fitness consequences of mixed-donor pollen loads in the annual legume Chamaecrista fasciculata. American Journal of Botany, 79(5), 508–515. DOI: 10.1002/j.1537-2197.1992.tb14586.x

Stanton, M. L., & Preston, R. E. 1988. Ecological consequences and phenotypic correlates of petal size variation in wild radish, Raphanus sativus (Brassicaceae). American Journal of Botany, 75(4), 68–76. DOI: 10.1002/j.1537-2197.1988.tb13471.x

Stanton, M. L., Snow, A. A., & Handel, S. N. 1986. Floral evolution: attractiveness to pollinators increases male fitness. Science, 232(4758), 1625–1627. DOI: 10.1126/science.232.4758.1625

Stanton, M. L., Snow, A. A., Handel, S. N., & Bereczky, J. 1989. The impact of a flower-color polymorphism on mating patterns in experimental population of wild radish (Raphanus raphanistrum L.) Evolution, 43(2), 335–346. DOI: 10.1111/j.1558-5646.1989.tb04231.x

Stephenson, A. G. 1980. Fruit reduction, and the fruiting strategy of Catalpa speciosa (Bignoniaceae). Ecology, 61(1), 57–64. DOI: 10.2307/1937155

Stephenson, A. G., & Bertin, R. I. 1983. Male competition, female choice and sexual selection in plants. In: L. Real (Ed.), Pollination biology. pp. 109–149. New York: Academic Press.

Stephenson, A. G., Johnson, R. S., & Winsor, J. A. 1988. Effects of competition on the growth of Lotus corniculatus L. seedlings produced by random and natural patterns of fruit abortion. American Midland Naturalist, 120(1), 102–10. DOI: 10.2307/2425890

Stone, S. L., Arnoldo, M., & Goring, D. R. 1999. A breakdown of Brassica self-incompatibility in ARC1 antisense transgenic plants. Science, 286(5445), 1729–1731. DOI: 10.1126/science.286.5445.1729

Stpiczyńska, M., Nepi, M., & Zyck, M. 2015. Nectaries and male-biased nectar production in protandrous flowers of perennial umbellifer Angelica sylvestris L. (Apiaceae). Plant System and Evolution, 301(4), 1099–1113. DOI: 10.1007/s00606-014-1152-3

Sweet, G. B. 1973. Shedding of reproductive structures in forest trees. In: T. T. Kozlowski (Ed.), Shedding of plant parts. pp. 341–382. New York: Academic Press.

Takayama, S., & Isogai, A. 2005. Self-incompatibility in plants. Annual Review of Plant Biology, 56(1), 467–489. DOI: 10.1146/annurev.arplant.56.032604.144249

Varga, S., Nuortila, C., & Kytöviita, M-M. 2013. Nectar sugar production across floral phases in the gynodioecious protandrous plant Geranium sylvaticum. PLoS One, 8(4), e62575. DOI: 10.1371/journal.pone.0062575

Vaughton, G., & Ramsey, M. 1998. Floral display, pollinator visitation and reproductive success in the dioecious perennial herb Wurmbea dioica (Liliaceae). Oecologia, 115(1–2), 93–101. DOI: 10.1007/s004420050495

Waser, N. M, & Price, M. V. 1991. Reproductive costs of self-pollination in Ipomopsis aggregata (Polemoniaceae): are ovules usurped. American Journal of Botany, 78(8), 1036–1046. DOI: 10.2307/2444892

Willson, M. F. 1979. Sexual selection in plants. American Naturalist 113(6), 777–790. DOI: 10.1086/283437

Willson, M. F. 1990. Sexual selection in plants and animals. Tree, 5(7), 210–214. DOI: 10.1016/0169-5347(90)90133-X

Willson, M. F. 1994. Sexual selection in plants: perspective and overview. American Naturalist, 144(1), 13–39. DOI: 10.1086/285651

Willson, M. F., & Price, P. W. 1977. The evolution of inflorescence size in Asclepias (Asclepiadaceae). Evolution, 31(3), 495–511. DOI: 10.1111/j.1558-5646.1977.tb01040.x

Willson, M. F., & Rathcke, B. J. 1974. Adaptative design of the floral display in Asclepias syriaca L. American Midland Naturalist, 92(1), 47–57.

Wilson, P., Thomson, J. D., Stanton, M. L., & Rigney, L. P. 1994. Beyond floral batemania: gender biases in selection for pollination success. American Naturalist, 143(2), 283–296. DOI: 10.1086/285604

Wolfe, L. M. 1987. Inflorescence size and pollinaria removal in Asclepias curassavica and Epidendrum radicans. Biotropica, 19(1), 86–89. DOI: 10.2307/2388464

Yang, C. F., Sun, S. G., & Guo, Y. H. 2005. Resource limitation and pollen source (self and outcross) affecting seed production in two louseworts, Pedicularis siphonantha and P. longiflora (Orobanchaceae). Botanical Journal of the Linnean Society, 147(1), 83–89. DOI: 10.1111/j.1095-8339.2005.00363.x

Yang, C. F., & Wang, Q. F. 2015. Nectarless flowers with deep corolla tubes in Pedicularis: does long pistil length provide an arena for male competition? Botanical Journal of the Linnean Society, 179(3), 526–532. DOI: 10.1111/boj.12331

Zhang, C., Tateishi, N., & Tanabe, K. 2010. Pollen density on the stigma affects endogenous gibberellin metabolism, seed and fruit set, and fruit quality in Pyrus pyrifolia. Journal of Experimental Botany, 61(15), 4291–4302. DOI: 10.1093/jxb/erq232

Published

2020-03-16