Dichogamy, Protandry, Protogyny

dichogamy [ dahy-KOG–uh-mee ] noun:  relating to a flower in which the time gap between the release of pollen by the stamens and the receptivity to pollen of the stigma is such as to prevent self-pollination; the maturation of male and female reproductive organs of a flower at different times

protandry [ proh-TAN-drahy ] noun: relating to a flower in which the stamens release pollen prior to the stigmas being receptive; having male reproductive organs maturing before the female

protogyny [ proh-TOJ–uh-nee ] noun: relating to a flower in which the stamens release pollen after the stigma has stopped being receptive; having female reproductive organs maturing before the male

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In order for a plant to produce fruit it must be pollinated—either through cross-pollination or self-pollination. In cross-pollination, pollen grains are transferred from the stamens (the male reproductive organs) of one flower to the pistils (the female reproductive organs) of another flower on a different plant. In terms of evolution, cross-pollination has the advantage of producing genetically diverse offspring that are more likely to adapt to and survive in changing environments. 

Cross-pollination depends on vectors like wind, water, insects, birds, and bats; plants employ different strategies to ensure a vector’s success. One strategy that bisexual plants (those with flowers having both stamens and pistils) use is dichogamy, where the stamens and pistils of a flower mature at different times. This sequential hermaphroditism occurs in two phases—either as protandry, where the flowers in the first phase are functionally male and in the second phase functionally female, or in reverse as protogyny where the flowers are functionally female first and male second. Depending on the species, intervals between the first and second phases can range from hours to months. If there is no overlap between the phases, the dichogamy is complete. If phases overlap, the dichogamy is incomplete. Dichogamy is also characterized by the degree and nature of synchrony of the flowers on a plant as described below:

• asynchronous, the most common type, during which the flower phases in a given plant are not in sync with each other
• hemisynchronous, during which a portion of flowers or Inflorescences on a plant or part of an inflorescence are in the same phase 
• synchronous, during which all of the open flowers on the same plant or in an inflorescence are in the same phase and where the plant or inflorescence undergoes:
  • multiple consecutive phase cycles during a single flowering season, which is most common, or
  • duodichogamy, which is three synchronized phases in the sequence male → female → male (Renner et al. 2007), or
  • one cycle where all of the flowers on a plant are in the same phase, which is less common, in which case, other plants of that species are likely to be out of phase so that cross-breeding is possible, or
  • heterodichogamy, either in the order of presentation of pollen and stigmas or in the timing of the flower opening. For example, in some Juglans (walnut) and Acer (maple) species, one portion of the tree population is protandrous and the other protogynous at the same time (Lloyd & Webb 1986). In Persea americana (avocado), one group is female on the first morning and male the second afternoon and the other group is female on the first afternoon and male on the second morning (Solares et al. 2023).

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Protandry

Protandry is illustrated (above) by the bisexual flowers of native Geranium maculatum (wild geranium), which is gynodioecious, so it also has separate plants with just female flowers. Protandry is prevalent among flowering plants, including in much of the Asteraceae (aster family), Lamiaceae (mints), and Malvaceae (mallow family) and in varying degrees in the Campanulaceae (bellflower family) and Apiaceae (umbellifers or carrot family) (Willmer 2011). 

Protandry is more frequently associated with self-incompatibility (the inability of pollen grains to fertilize flowers of the same plant). It is more common among bee and fly pollinated flowers—although it “does not appear to be significantly more correlated with biotic pollination systems than all other breeding systems considered together” (Sargent & Otto 2004)—and racemose inflorescences (those that bloom from the bottom up). It has been observed that bees, in particular, forage upwards on an inflorescence. In a protandrous racemose inflorescence, the older flowers at the bottom that have reached the female phase present their stigmas to receive pollen the bees are carrying from other inflorescences. As the bees work their way up the inflorescence, they will visit last the younger flowers still in the male phase from which they will pick up new pollen grains to transport to other inflorescences and plants.

Protogyny

Protogyny is less common than protandry and occurs in families like Ranunculaceae (buttercups) and Brassicaceae (crucifers) and in grasses and alpine species. It is more commonly associated with self-compatibility as the flowers can resort to self-pollination if the pistil has not been fertilized before the anthers dehisce (Barrett 2003). It is also more likely to occur in wind- or beetle-pollinated flowers. “The dichogamy type with an unusual pollination mode is protogyny (and perhaps heterodichogamy), which differs from all other forms in being commonly (but not predominantly) found in wind-pollinated systems” (Sargent & Otto 2004).

Protogyny is illustrated (above) by the bisexual flowers of Plantago lanceolata (English plantain or rib-grass). Each flower opens sequentially from the base to the top of the spike. The stigma protrudes first and becomes receptive. As the female phase wanes, the male phase follows characterized by open sepals and petals and four strongly exerted stamens that release the pollen. Even though Plantago lanceolata is considered a wind-pollinated plant, honey bees have been reported on the flowering spikes crawling among the anthers collecting pollen up to the level with receptive stigmas (Clifford 1962).

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Although dichogamy was first described in the late 1700s, there has been comparatively little study of it since Darwin’s time. Research has been largely qualitative, identifying traits that are associated or may correlate with protandry or protogyny and offering numerous hypotheses. For example, scientists are still trying to explain why a species would employ two different mechanisms—dichogamy and self-incompatibility—to prevent self-pollination.

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References

Barrett SCH. June 29, 2003. Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond. Philos Trans R Soc Lond B Biol Sci.; 358(1434): 991–1004. doi: 10.1098/rstb.2003.1301 PMCID: PMC1693196.

Clifford H. 1962. Insect Pollination of Plantago lanceolata L.. Nature 193:196. doi: 10.1038/193196a0

David G. Lloyd & C. J. Webb (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dichogamy, New Zealand Journal of Botany, 24:1, 135-162, DOI: 10.1080/0028825X.1986.10409725

Edited by Harder LD. Barrett SCH. 2006. Ecology and Evolution of Flowers. Oxford University Press.

Narbona E, Ortiz PL, Arista M. 2011. Linking self-incompatibility, dichogamy, and flowering synchrony in two Euphorbia species: alternative mechanisms for avoiding self-fertilization? PLoS One. 6(6): e20668. doi: 10.1371/journal.pone.0020668. Epub 2011 Jun 2. PMID: 21674062; PMCID: PMC3107240.

Reardon W. Fitzpatrick DA, Fares MA, Nugent JM. 2009. Evolution of flower shape in Plantago lanceolata. Plant Mol Biol. 71: 241–250 DOI: 10.1007/s11103-009-9520-z

Renner SS, Beenken L, Grimm GW, Kocyan A, Ricklefs RE. 2007. The Evolution of Dioecy, Heterodichogamy, and Labile Sex Expression in Acer. Technical Comment. Evolution 61(11): 2701–2719. doi: 10.1111/j.1558-5646.2007.00221.x.

Ruan C-J. 2010. Review and Advances in Style Curvature for the Malvaceae. International Journal of Plant Developmental Biology. 4 (Special Issue 1): 98-111.

Sargent RD, Otto SP.  2004. A phylogenetic analysis of pollination mode and the evolution of dichogamy in angiosperms. Evolutionary Ecology Research. 6: 1183–1199.

Solares E, Morales-Cruz A, Balderas RF, Focht E, Ashworth VETM, Wyant S, Minio A, Cantu D, Arpaia ML, Gaut BS. February 2023. Insights into the domestication of avocado and potential genetic contributors to heterodichogamy, G3 Genes|Genomes|Genetics, 13(2). doi: 10.1093/g3journal/jkac323

Stout, A. B. (1928). Dichogamy in Flowering Plants. Bulletin of the Torrey Botanical Club, 55(3), 141–153.

Van Etten ML, Chang S-M. December 2014. Frequency-dependent pollinator discrimination acts against female plants in the gynodioecious Geranium maculatum. Annals of Botany. 114(8): 1769–1778. doi: 10.1093/aob/mcu204

Willmer P. 2011. Pollination and Floral Ecology. United Kingdom: Princeton University Press.