Dichogamy

Dichogamy is the separation in time of gender expression in a hermaphroditic organism, a characteristic of some fishes, gastropods, and most flowering plants.

In flowering plants

In the context of the flowering plants (angiosperms), there are two forms of dichogamy: "protogyny"—female function precedes male function—and "protandry"—male function precedes female function.

Historically, dichogamy has been regarded as a mechanism for reducing inbreeding (e.g., Darwin, 1862). However, a survey of the angiosperms found that self-incompatible (SI) plants, which are incapable of inbreeding, were as likely to be dichogamous as were self-compatible (SC) plants (Bertin, 1993). This finding led to a reinterpretation of dichogamy as a more general mechanism for reducing the impact of pollen-pistil interference on pollen import and export (reviewed in Lloyd & Webb, 1986; Barrett, 2002). Unlike the inbreeding-avoidance hypothesis, which focused on female function, this interference-avoidance hypothesis considers both gender functions.

In many hermaphroditic species, the close physical proximity of anthers and stigma makes interference unavoidable, either within a flower or between flowers on an inflorescence. Within-flower interference, which occurs when either the pistil interrupts pollen removal or the anthers prevent pollen deposition, can result in autonomous or facilitated self-pollination (Lloyd & Webb, 1986; Lloyd & Schoen, 1992). Between-flower interference results from similar mechanisms, except that the interfering structures occur on different flowers within the same inflorescence and it requires pollinator activity. This results in geitonogamous pollination, the transfer of pollen between flowers of the same individual (Lloyd & Schoen, 1992; de Jong et al., 1993). In contrast to within-flower interference, geitonogamy necessarily involves the same processes as outcrossing: pollinator attraction, reward provisioning, and pollen removal. Therefore, between-flower interference not only carries the cost of self-fertilization (inbreeding depression; Charlesworth & Charlesworth, 1987; Husband & Schemske, 1996), but also reduces the amount of pollen available for export (so-called "pollen discounting"; Harder & Wilson, 1998] ). Because pollen discounting diminishes outcross siring success, interference avoidance may be an important evolutionary force in floral biology (Harder & Barrett, 1995, 1996; Harder & Wilson, 1998; Barrett, 2002).

Dichogamy may reduce between-flower interference by minimizing the temporal overlap between stigma and anthers within an inflorescence. Large inflorescences attract more pollinators, potentially enhancing reproductive success by increasing pollen import and export (Schemske, 1980; Queller, 1983; Bell, 1985; Geber, 1985; Schmid-Hempel & Speiser, 1988; Klinkhamer & de Jong, 1990). However, large inflorescences also increase the opportunities for both geitonogamy and pollen discounting, so that the opportunity for between-flower interference increases with inflorescence size (Harder & Barrett, 1996). Consequently, the evolution of floral display size may represent a compromise between maximizing pollinator visitation and minimizing geitonogamy and pollen discounting (Klinkhamer & de Jong, 1993; Barrett et al, 1994; Holsinger, 1996; Snow et al., 1996).

Protandry may be particularly relevant to this compromise, because it often results in an inflorescence structure with female phase flowers positioned below male phase flowers (Bertin & Newman, 1993). Given the tendency of many insect pollinators to forage upwards through inflorescences (Galen & Plowright, 1988), protandry may enhance pollen export by reducing between-flower interference (Darwin, 1862; Harder et al, 2000). Furthermore, this enhanced pollen export should increase as floral display size increases, because between-flower interference should increase with floral display size. These effects of protandry on between-flower interference may decouple the benefits of large inflorescences from the consequences of geitonogamy and pollen discounting. Such a decoupling would provide a significant reproductive advantage through increased pollinator visitation and siring success.

Harder et al. (2000) demonstrated experimentally that dichogamy both reduced rates of self-fertilization and enhanced outcross siring success through reductions in geitonogamy and pollen discounting, respectively. Routley & Husband (2003)examined the influence of inflorescence size on this siring advantage and found a bimodal distribution with increased siring success with both small and large display sizes.

See also

*Plant sexuality
* [http://www.amjbot.org/cgi/content/abstract/87/9/1246 Griffin et al., (2000)] for an experimental test of the adaptive significance of protogyny.

References

*Barrett, S.C.H. 2002. Sexual interference of the floral kind. "Heredity", 88(2): 154-9. [http://www.hubmed.org/display.cgi?issn=0018067X&uids=11932774 abstract] .
* Barrett, S.C.H., L. D. Harder, W. W. Cole. 1994. Effects of Flower Number and Position on Self-Fertilization in Experimental Populations of "Eichhornia paniculata" (Pontederiaceae). "Functional Ecology", 8(4): 526-535. [http://links.jstor.org/sici?sici=0269-8463%28199408%298%3A4%3C526%3AEOFNAP%3E2.0.CO%3B2-2 abstract] .
* Bell G., 1985. On the function of flowers. Proc. R. Soc. Lond. B 224: 223–265.
* Bertin, R.I. 1993. Incidence of monoecy and dichogamy in relation to self-fertilization in angiosperms. "Amer. J. Bot., 80(5): 557-560. [http://links.jstor.org/sici?sici=0002-9122%28199305%2980%3A5%3C557%3AIOMADI%3E2.0.CO%3B2-V abstract] .
* Bertin R.I. & Newman C.M. 1993. Dichogamy in angiosperms. "Bot. Rev.", 59: 112–152.
* Darwin, Charles. 1862. [http://pages.britishlibrary.net/charles.darwin3/orchids/orchids_fm.htm On the various contrivances by which British and foreign orchids are fertilized by insects, and on the good effects of intercrossing] . John Murray, London.
* Charlesworth, D. and B. Charlesworth. 1987. Inbreeding Depression and its Evolutionary Consequences. "Annual Review of Ecology and Systematics", 18: 237-268. [http://links.jstor.org/sici?sici=0066-4162%281987%2918%3C237%3AIDAIEC%3E2.0.CO%3B2-8 abstract]
* de Jong T.J., Waser N.M. & Klinkhamer P.G.L., 1993, Geitonogamy: the neglected side of selfing. "Trends Ecol. Evol.", 8: 321–325.
* Galen C. & Plowright R.C., 1988, Contrasting movement patterns of nectar-collecting and pollen-collecting bumble bees ("Bombus terricola") on fireweed ("Chamaenerion angustifolium") inflorescences. "Ecol. Entomol.", 10: 9–17.
* Geber, M. 1985. The Relationship of Plant Size to Self-Pollination in "Mertensia ciliata". "Ecology", 66(3): 762-772. [http://links.jstor.org/sici?sici=0012-9658%28198506%2966%3A3%3C762%3ATROPST%3E2.0.CO%3B2-0 abstract]
* [http://www.nature.com/cgi-taf/DynaPage.taf?file=/nature/journal/v373/n6514/abs/373512a0.html Harder & Barrett, 1995]
* Harder L.D. & Barrett S.C.H., 1996. Pollen dispersal and mating patterns in animal-pollinated plants. In: Floral Biology: Studies on Floral Evolution in Animal-Pollinated Plants (D.G. Lloyd & S.C.H. Barrett, eds.), Chapman and Hall, New York. pp. 140–190.
* [http://links.jstor.org/sici?sici=0003-0147%28199811%29152%3A5%3C684%3AACOPDA%3E2.0.CO%3B2-0 Harder & Wilson, 1998] .
* [http://www.hubmed.org/display.cgi?issn=09628452&uids=10722210 Harder et al, 2000] .
* Holsinger K.E., 1996, Pollination biology and the evolution of mating systems in flowering plants. In: Evolutionary Biology (M.K. Hecht, ed.), Plenum Press, New York, pp. 107–149.
* [http://links.jstor.org/sici?sici=0014-3820%28199602%2950%3A1%3C54%3AEOTMAT%3E2.0.CO%3B2-9 Husband & Schemske, 1996] .
* Klinkhamer P.G.L. & de Jong T.J., 1990, Effects of plant size, plant density and sex differential nectar reward on pollinator visitation in the protandrous "Echium vulgare". "Oikos" 57: 399–405.

* Klinkhamer P.G.L. & de Jong T.J., 1993, Attractiveness to pollinators: a plant’s dilemma. Oikos 66: 180–184.

* Lloyd D.G. & Webb C.J., 1986, The avoidance of interference between the presentation of pollen and stigmas in angiosperms: I. Dichogamy. New Zeal. J. Bot. 24: 135–162.
* [http://links.jstor.org/sici?sici=1058-5893%28199209%29153%3A3%3C358%3ASACIPI%3E2.0.CO%3B2-R Lloyd & Schoen, 1992] .

* Queller D.C., 1983, Sexual selection in a hermaphroditic plant. "Nature" 305: 706–707.
* Routley, M.B. & B.C. Husband. 2003. The effect of protandry on siring success in "Chamerion angustifolium" (Onagraceae) with different inflorence sizes. "Evolution Int. J. Org. Evolution", 57(2): 240-248 [http://www.hubmed.org/display.cgi?issn=00143820&uids=12683521 abstract]
* Schemske D.W., 1980, Evolution of floral display in the orchid Brassavola nodosa. Evolution 34: 489–491.

* Schmid-Hempel P. & Speiser B., 1988, Effects of inflorescence size on pollination in Epilobium angustifolium. "Oikos" 53: 98–104.

* Snow A.A., Spira T.P., Simpson R. & Klips R.A., 1996, The ecology of geitonogamous pollination. In: Floral Biology: Studies on Floral Evolution in Animal-Pollinated Plants (D.G. Lloyd & S.C.H. Barrett, eds.), Chapman and Hall, New York, New York, USA, pp. 191–216.