Do you ever think about plant sex? I still remember walking into the first class of my first ever plant biology course during my undergraduate degree and my professor introducing himself as just another botanist who is obsessed with plant sex. At the time I thought my professor was a quirky guy trying to get the students’ attention by talking about sex, but now that I am doing a Masters in Botany, it all makes sense – I have yet to meet a botanist who is not absolutely fascinated by the whys and hows and whos and wheres of plant sex. As a plant sex enthusiast myself, I would like to share with you some amazing examples of this ever-important mechanism in hopes of making you a convert, and I cannot think of a better group of plants to do this than the orchids. Have you ever wondered why orchids are all so different and funky looking? If so, you are not alone. Orchids are the second largest group of flowering plants in terms of number of species, and their immense diversity in appearance has been a source of wonder and speculation for centuries (APG 2009). Even Charles Darwin was so enthused by orchids that in a letter to a colleague he wrote, “I never was more interested in any subject in my life than in this of Orchids” (Roberts & Dixon 2008). Darwin was particularly interested in orchid sex and we shall see why he used their intimate relationships with insects as evidence to support his famous theory of evolution by natural selection (Darwin 1877; Micheneau et al. 2009).

In order to better understand the sophisticated reproduction of orchids, let us begin with a quick run-down of the basic mechanisms. Flowers are the reproductive parts of angiosperms (a.k.a flowering plants). Their reproduction cycle begins when a pollen grain produced by the anther (male organ) comes into contact with the stigma (female organ) of the same flower species. This transfer of pollen from male to female parts is called pollination. Fertilization occurs when sperm formed in pollen grains unite with the female ovule, developing into the seed and fruit. Most angiosperms have both male and female reproductive organs, meaning that they can self-pollinate and self-fertilize (a.k.a selfing). The main benefit of “selfers” is that they are guaranteed to find a mate (themselves!). On the downside, offspring inherit their parent’s exact genome, including any mutations that are present. This lack of genetic diversity and the potential accumulation of damaging mutations over time, reduce a plant’s “genetic arsenal” for adapting to changes in its environment – orchids resort to this strategy only in pollinator-poor communities (Roberts & Dixon 2008). It is thus not surprising that many angiosperms have evolved intricate mechanisms to avoid selfing and instead promote cross-pollination with other individuals of their kind. Vectors for pollen transfer include wind and water (abiotic), as well as animals and insects (biotic).

Angiosperms are attached to a substrate and unable to move freely, but many of the species that rely on biotic vectors have effectively gained mobility by manipulating the behavior of their pollinator – they “borrow” their wings, legs, or abdomens to transfer pollen. Pollination is not a deliberate event, but rather occurs by chance as insects reap the rewards offered by the flower, which may include nectar, pollen, fragrant compounds, and shelter. Orchids in particular, have developed exquisite pollination syndromes through their coevolution with their pollinators. By coevolution I mean that each party has helped shaped the other over time, resulting in both becoming increasingly specialized. Flowers can evolve features to attract, guide, and orient pollinators for efficient pollen transfer (pollen is energetically expensive to make!) Pollinator behavior and appearance can evolve to “fit” into the flowers they visit, as is beautifully shown by the Malagasy orchid Angraecum sesquipedale. The petals of Angraecum flowers are fused at the base, forming a slightly curved floral tube that can be over 40 cm long and is filled with nectar at the very bottom. Having seen only the flowers, Darwin predicted that giant moths with long tongues pollinated this plant; moths fitting Darwin’s description were in fact discovered four decades later (Rodriguez-Girones & Santamaria 2007; Nillson et al. 1985).

To understand how this all came to be, we have to think about Darwin’s theory of natural selection. Individuals that make up a population vary in the traits they possess. Some of these traits, such as size and shape, are heritable and affect an individual’s ability to survive and reproduce. Individuals with traits that are particularly well suited to an environment are more likely to survive and reproduce; natural selection occurs when individuals with certain traits produce more offspring than individuals without these traits. The frequency of “selected” traits thus increases from one generation to the next and leads to evolution – a change in the heritable characteristics of a population over time. In the case of Angraecum, deep floral tubes select for moths with the longest tongues as only they can access nectar situated deep in the floral tube, leaving individuals with shorter tongues at the disadvantage of having to look for an alternative food source or perish. At the same time, long tongues select for the deepest floral tubes because these flowers can achieve higher fertilization rates, making them more prevalent in the population than flowers with shorter tubes. Long floral tubes force moths to insert the entire length of their tongues in order to reach the nectar; the moth’s thrusting increases friction and its withdrawal after consuming all the nectar triggers a mechanism that attaches two sticky pollen clumps to the base of its tongue. Selfing is prevented as moths carrying pollen (attached only after tongue withdrawal) continue their search for nectar by moving on to a different flower in which they inadvertently deposit the pollen. (Nillson et al. 1985). As you can see, an evolutionary “arms race” between the floral tube and the moth’s tongue has resulted in the lengthening of the two organs over time as well as reducing the likelihood of self-pollination (Roberts & Dixon 2008).

One third of all orchids have evolved features that are perceived as rewards by pollinators, but do not end up materializing (Roberts & Dixon 2008). Species from the Mediterranean group Ophrys use sexual deceit to achieve pollination by tricking the males of a specific type of bee (Schiestl et al. 1999). To the surprise and awe of countless naturalists, Ophrys flowers remarkably mimic the appearance of receptive female bees. In the species O. speculum, the flower’s top petal (called labellum) is enlarged and appears swollen; it is dark purple and has red bristles along its edges. During development, the stalk of the flower twists 180º so that the labellum ends up at the bottom, giving it the appearance of a female bee’s abdomen with its wings at rest. As if impersonation was not enough, Ophrys flowers emit an odour that is almost identical to that of the sex pheromone of mature female bees. These visual and olfactory floral cues prove irresistible to male bees and trigger “pseudocopulation”, whereby the bee mounts the flower in a very specific position, causing it to rub up against the anther which attaches two sticky clumps of pollen to the bee’s bum. Pseudocopulation elicits sexual behaviors in males but does not cause them to ejaculate. The quick habituation of males moderates their response to previously visited flowers, whereas flowers on other plants remain highly attractive to them due to subtle differences in appearance and odour. Once a male realizes that a flower is not good enough for him, it is already carrying the pollen that it will unknowingly deposit in the next flower it visits as his search for love continues (Nilsson 1992). Thus, this finely-tuned mechanism does an excellent job of promoting cross-pollination between different flowers of the same species.

The chemical compounds used for odour mimicry in Ophrys orchids initially had the sole purpose of contributing to the formation of a waxy leaf layer that prevents water loss. Genetic mutations causing changes to the relative proportions of these compounds occasionally resulted in the production of an odour blend that resembled that of the sex pheromone of a pollinator species. This would have led to an excited male bee pollinating the mutant plant. Over time, the process of natural selection favoured plants with the mutant odour trait as they likely attracted more pollinators –albeit by chance– than non-mutants (Schiestl et al. 1999). The same argument could be extended to explain how inadvertently, pollinators fueled the natural selection of mutant orchids displaying traits for visual and odour mimicry. Yet another factor driving the evolution of sexual deception in Orphys is that mutants could reduce the production of energetically costly attractants and rewards for pollinators. This gave them a reproductive advantage over non-mutants by allowing them to reallocate valuable resources to improve their vigor as well as that of their offspring (Schiestl et al. 1999).

Orchids in the Coryanthes group (a.k.a. bucket orchids) also rely on a suite of traits to obtain pollination from a specific group of male bees. Coryanthes species are epiphytic (they grow on top of other plants) and their fragrant flowers are some of the most complex among the orchids (Gerlach & Schill 1989). I will use the species C. speciosa to illustrate this. Male bees are attracted to the floral fragrance emitted by floral glands. The bee pokes around in search of the source of the smell, which causes fluid secreted by glands right above the bee’s head to dislodge. The drop of fluid washes the bee down to a petal that is shaped like a bucket and filled with gooey liquid. The only way out of this trap is a tube-like petal which forces the bee to rub against the anther. By the time the pollinator emerges with pollen stuck to its back, the flower is no longer emitting a fragrance and the bee flies away, effectively preventing the same bee from returning and self-pollinating the plant. Fragrance production is resumed the following day, in an attempt to attract a pollen-carrying male that will fall into the trap but this time when it escapes it will deposit pollen on the stigma, fertilizing the plant (Baker 1963; Gerlack & Schill 1989).

The population density of epiphytic orchids is usually quite low, so highly specialized pollination systems are essential for effective cross-pollination between individuals (Gravendeel et al. 2004). Research comparing the reproduction of orchids offering nectar rewards with orchids offering fragrance rewards shows that the former are more successful. Without the genetic capacity to produce nectar, Coryanthes rely solely on their flowers and fragrance. The Coryanthes flowers that happen to inherit the most attractive fragrances and complex flowers will have the highest pollinator visitation frequency and fertilization rates, which over time will increase the number of individuals in the population displaying these traits. Through natural selection, Coryanthes have evolved to become the nectar-less tropical orchids with the highest reproductive success (Neiland & Wilcock 1998).

It would be impossible to discuss all modes of orchid pollination in this short paper (entire books have been devoted to this topic!), so may aim was merely to illustrate just how diverse, intricate, and flat-out beautiful these mechanisms can be. The effect of natural selection on orchids is so powerful that sometimes I cannot help but think of them as organisms with personalities and the intelligence to manipulate those around them. Their intimate and specialized relationships with their pollinators are a remarkable example for the study of coevolution, but also raise issues about their conservation.      Just like Darwin asserted that the extinction of Angraecum orchids would be imminent should their long-tongued moth pollinators disappear, the same argument could be made for most orchids species as they rely on only one or very few types of pollinators (Micheneau et al. 2009). Mounting evidence showing a worldwide decline in pollinators, including those of orchids, shows how vulnerable to extinction these plants are (Zayed et al. 2004; Swarts & Dixon 2009; Vereecken et al. 2010). The economic importance of orchids in the horticultural trade poses yet another challenge for their conservation as collectors pay big bucks to acquire the rarest of specimens, creating incentives for illegal poaching even though many species are now protected under the Convention on International Trade in Endangered Species. Hopefully I have shown in this paper that the study of orchids can provide many insights into our understanding of how life on Earth was shaped by natural selection and evolution. For this reason, if not only for their intrinsic value, biologists should be thinking very seriously about the design and implementation of strategies for the conservation of this fascinating group of plants.

Cited Literature

An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. 2009. Bot. J. Linn. Soc. 161: 105-121.

Baker, H. G. 1963. Evolutionary Mechanisms in Pollination Biology. Science.  139:877-883

Darwin, C. 1892. The various contrivances by which orchids are fertilized by insects. 2nd ed. rev. (1st ed. 1862). New York: Appleton.

Freeman, S., M. Harrington, J. Sharp. 2011. Biological Science.

Gerlach, G. and R. Schill. 1989. Fragrance analyses, an aid to taxonomic relationships of the genus Coryanthes (Orchidaceae). Pl. Syst. Evol. 168: 159-165.

Gravendeel, B., A. Smithson, F. J. W. Slik, A. Schuiteman. 2004. Epiphytism and pollinator specialization: drivers for orchid diversity? Phil. Trans. R. Soc. Lond. B. 329: 1523-1535.

Micheneau, C., S. D. Johnson, M. F. Fay. 2009. Orchid pollination: from Darwin to present day. Bot. J. Linn. Soc. 161(1):1-19.

Neiland, M. R. M. and C. C. Wilcock. 1998. Fruit set, nectar reward, and parity in the Orchidaceae. Am. J. Bot. 85(12): 1657-1671.

Nillson, L. A., L. Jonsson, L. Rason, E. Randrianjohany. 1985. Monophily and pollination mechanisms in Angraecum arachnites Schltr. (Orchidaceae) in a guild of long-tongued hawk-moths (Sphingidae) in Madagascar. Biol. J. Linn. Soc. 26:1-19.

Nillson, L. A. 1992. Orchid pollination biology. Trends in ecology & evolution. 7(8):255-259

Roberts, D.L. and K.W. Dixon. 2008. Orchids. Current Biology 18(8): R325-R329.

Swarts, N. D. and K. W. Dixon. 2009. Terrestrial orchid conservation in the age of extinction. Ann. Bot. 104: 543-556.

Vereecken, N. J., A. Dafni, S. Cozzolino. 2010. Pollination syndromes in Mediterranean orchids – implications for speciation, taxonomy, and conservation. Bot. Rev. 76: 220-240.

Zayed, A., D. W. Roubik, L. Parker. 2004. Use of diploid male frequency data as an indicator of pollinator decline. Proceedings: Biological Sciences 271(3): S9-S12.