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Today we have a text-and-photo tale by Athayde Tonhasca Júnior on his favorite topic: pollination, but also on sex and gender in plants. You should be impressed at the cleverness of plants in having evolved to facilitate reproduction through pollinators.  Athayde’s narrative is indented, and you can enlarge the photos by clicking on them.

Nifty gender bias

Once upon a time in Ancient Greece, a young man was sauntering in the woods, enjoying the fine weather, unaware he was approaching a pond inhabited by the naiad Salmacis. Like all naiads, the minor deities that oversaw springs, wells and lakes, Salmacis had a weak spot for youthful, virile men. Awestruck by the lad’s beauty, Salmacis tried to seduce him. Her lascivious prattle only managed to alarm the visitor, so she pretended to give up and walked away. The young man, possibly flustered by the naiad’s unladylike harassment, decided to go for a dip in the pond. Beautiful he might have been, but not very smart: freshwater bodies were naiads’ territory. From behind a tree, Salmacis saw her chance. She leapt into the water to have another go at the shy looker, and the poet Ovid tells us what happened next: She poured herself all over the young man, and finally coiled herself right round him as he struggled against her and tried to slip out of her grasp. She was like a snake whom an eagle, the king of birds, snatches and holds up on high. (Metamorphoses, Book 4). Salmacis, who today would be on the Sex Offender Register, realised that her less than refined tactics were not working. In desperation, she begged the gods to let the two of them stay together forever. The gods complied, but interpreted the feisty naiad’s wishes literally. They merged Salmacis and her quarry in one body, creating a deity half man and half woman, with male and female parts. Perhaps an ironic destiny for a man whose name was also the product of a blend. A son of Hermes, the messenger of the gods, and Aphrodite, the goddess of love and beauty, the youth was called Hermaphroditus.

Salmacis making an inappropriate move on Hermaphroditus, by François-Joseph Navez (1787–1869) © Museum of Fine Arts Ghent, Wikimedia Commons.

To 18th century naturalists, who were well versed in the Classics, Hermaphroditus was an ideal trope for a biological phenomenon known from ancient times: the existence of plants and animals with male and female reproductive organs. As biology progressed, the term ‘hermaphrodite’ began to be applied to sexually reproducing organisms that produce male and female gametes. Roughly 5% of all animals, mostly invertebrates, fulfill the condition. Among vertebrates, hermaphrodism is found only in some fishes and frogs: the great majority of species are gonochoric, that is, either male or female; the rare instances of hermaphroditism are considered pathologies.

Hermaphroditism may be unusual among animals, but it’s the way of life for most flowering plants. About 90% of them are functionally hermaphrodites, either by having male and female reproductive parts in the same flower or having male and female flowers in the same plant (these are known as monoecious). Hermaphroditism opens the door for self-fertilization, a handy strategy when mates or pollinators are rare or absent. But this type of shortcut in the dating game has severe disadvantages: it reduces genetic diversity, leading to lower capacity to survive and reproduce, and to adapt to changing environments. So it is not surprising that many hermaphroditic plants have developed physical and genetic barriers to avoid or reduce the possibility of self-fertilisation. Some species inhibit the germination of their own pollen grains; for others, their sex bits are morphologically different, such as long stamens and short styles or vice-versa (herkogamy); some resort to temporal separation of male and female stages (dichogamy).

A hermaphrodite flower with male (pollen-producing) and female (ovule-producing) parts © Anjubaba, Wikimedia Commons.

 

If self-fertilisation was to be the norm among hermaphroditic plants, Charles Darwin’s evolutionary theory would be seriously dented because outcrossing (the interbreeding of unrelated individuals) sets the stage for adaptation by natural selection. Understandably, Darwin paid much attention to pollination mechanisms in his book about orchids (Darwin, 1862) that followed On the Origin of Species by Means of Natural Selection. His research and observations paid off: he closed his orchid book by stating it is hardly an exaggeration to say that Nature tells us, in the most emphatic manner, that she abhors perpetual self-fertilisation.

While investigating the ways orchids avoid self-fertilisation, Darwin discovered a particularly clever instance involving the autumn lady’s-tresses orchid (Spiranthes spiralis, then known as S. autumnalis), and bumble bees (Bombus spp.), its main pollinators. This orchid produces an erect, unbranched flowering stalk, 7-20 cm tall. Flowers bloom from the bottom of the stalk to the top and are protandrous, a form of dichogamy where male reproductive organs mature before the female ones (studying botany is a sure way to improve your Scrabble scores). These traits are important for what Darwin observed in relation to the behaviour of visiting ‘humble bees’. In his own words: The bees always alighted at the bottom of the spike, and, crawling spirally up it, sucked one flower after the other. I believe humble-bees generally act thus when visiting a dense spike of flowers, as it is most convenient for them; in the same manner as a woodpecker always climbs up a tree in search of insects. This seems a most insignificant observation; but see the result. The result is thus: a bee alighting on the lowest flowers and making her way up may pick up some pollinia (sticky blobs of pollen grains typical of orchids) that may get transferred to apical flowers. However, this pollen will be wasted because upper flowers are functionally male; their pollen is ready to be taken away but their female parts are not yet mature. Bees that gather pollen from apical flowers fly away to the bottom of another stalk, where flowers are older and therefore receptive (functionally female). Thus, cross-fertilisation is assured. This setting has been labelled Darwin’s inflorescence configuration, a fitting tribute to his skills in observation, experimentation and deduction.

Darwin’s inflorescence configuration: a bee arrives to a flower at the bottom of a autumn lady’s-tresses stalk (A); she hops from flower to flower, picking up some pollinia on the way to the top (B); she moves to a bottom flower on another stalk, which, being older, is receptive to pollen (C) © bee image Jan Gillbank, flowers image BerndH, Wikimedia Commons.

 

Like the autumn lady’s-tresses, the rosebay willowherb (Chamaenerion angustifolium) is hermaphroditic, protandrous, has an inflorescence that blooms from bottom to top, and is pollinated by bees, mostly Western honey bees (Apis mellifera) and bumble bees. Rosebay willowherb too takes advantage of bees’ stereotypical foraging behaviour of moving up along erect inflorescences, but it goes one step further to encourage visitors to follow the script: flowers at the bottom of the inflorescence produce about 1.4 times more nectar than apical flowers (Antoń et al., 2017). Many bees and other pollinators visit flowers sequentially from the highest to the lowest quality, and stop inspecting those below a threshold (Carlson & Harms, 2006). This foraging strategy works to a T for the rosebay willowherb: a bee starts at the bottom where nectar is best, makes her way to less rewarding but pollen-bearing apical flowers, then flies away, hopefully taking some pollinia along.

A rosebay willowherb inflorescence: more nectar at the bottom encourages bees to climb up then fly away to another inflorescence © böhringer friedrich, Wikimedia Commons.

Functionally female or male flowers secreting more nectar than their counterparts is known as gender-biased nectar production. This phenomenon is relatively uncommon (although data are limited) but has been reported for a range of unrelated species, which suggests it evolved independently several times. Most known examples consist of biases towards functionally female flowers, just like the rosebay willowherb, and in most cases Darwin’s inflorescence configuration and bee pollination are involved (Strelin et al., 2025). We don’t know for sure whether gender-biased nectar production increases the probability of pollen transfer and promotes outcrossing, but it’s a reasonable assumption.

Common foxglove (Digitalis purpurea), another case of female-biased nectar production © Kurt Stüber, Wikimedia Commons.

Charles Darwin considered himself a mediocre botanist, even though eight of the ten books he published after On the Origin were about various aspects of plant biology, particularly reproduction (Barrett, 2010). The great naturalist was fascinated by flowers’ ‘beautiful contrivances’ that assured outcrossing and avoided the traps of inbreeding. When we look at the pas de deux performed by the autumn lady’s-tresses and rosebay willowherb with their pollinating bees to keep their hermaphrodite flowers on the straight and narrow towards cross-fertilisation, we can’t help but share Darwin’s fascination.

Darwin’s greenhouse at Down House where he conducted many of his experiments. I have found the study of Orchids eminently useful in showing me how nearly all parts of the flower are co-adapted for fertilisation by insects, and therefore the results of natural selection, – even the most trifling details of structure. Letter to Joseph Hooker, 1862 © Tony Corsini, Wikimedia Commons: