Dichogamy

Historically, dichogamy has been interpreted as a mechanism for reducing inbreeding (e.g., Darwin, 1862). However, a survey of the angiosperms (Bertin, 1993) found that self-incompatible (SI) plants, which are incapable of inbreeding, were as likely to be dichogamous as were self-compatible (SC) plants. This led to the recent 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 stigmass 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 (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 stigmass 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 Griffin et al., (2000) for an experimental test of the adaptive significance of protogyny.

References

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Bertin R.I. & Newman C.M., 1993, Dichogamy in angiosperms. Bot. Rev. 59: 112–152.

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.

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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.