Journal Number 90
March 2004

EDITORIAL

Floral Mimicry
By Ian St George

Perhaps 10,000 orchid species employ some form of mimicry. Mimicry is the resemblance of one organism to another, a resemblance that confers an adaptive advantage on at least one of the organisms. Darwin recognized it in the early days of evolutionary theory. The resemblance of some insects to leaves (mimetic camouflage) is a simple example of mimicry: carnivores ignore the insect because they don't like leaves. Mimicry may assist reproduction and it may involve any sensory mode - baby burrowing owls imitate the sound of rattlesnakes, and some Gastrodia "long column" have the scent of freesias. 

Mimicry has been most extensively studied in predation - when a tasty butterfly mimics a nasty-tasting butterfly in order to dupe the predator it is called Batesian mimicry (there is also Mullerian mimicry, where several nasty species adopt a common appearance). In Batesian mimicry there are thus three actors - the mimic, the model and the dupe. The mimic gains, while the model and the dupe lose. The mimic's success requires the dupe to (1) discriminate between prey that are tasty and nasty; (2) remember the nasty experience, and learn and remember the appearance of the nasty prey; (3) be deceived, so that having learned to avoid the nasty prey, it must at least sometimes be fooled by tasties that look like nasties.

Let's say the tasty mimic is so successful in imitating the model that it eventually outnumbers the model; and let's say the dupe is at times forgetful. He forgets prey that look like this are nasty, eats one, and (now that tasty mimics outnumber nasty models) is likely to find it tasty (in this way lapses in memory may favour his survival). He starts to eat prey that look like this, relishing the tastiness of most of them, until the nasty population again outnumbers the tasty population and he finds he is eating a lot of nasty-tasting prey, so stops. The tasty population, protected, takes off again..

The population of Batesian mimics thus follows a sine wave. The model is eaten sometimes, but cannot get rid of the mimic by changing its own appearance, because it is exactly that appearance that conferred survival advantage, and anyway the mimic would change just as quickly to resemble the new appearance - and probably does.

Batesian mimicry theory can be applied to floral mimicry and thus to orchids. In animals a tasty mimic obtains advantage by resembling a nasty model; in flowers a non-rewarding (to a pollinator) mimic obtains advantage by resembling a rewarding model; the evolutionary processes are the same.

For instance there is a suggestion that Thelymitra aff. longifolia (the mimic) looks like manuka (the model) in order to fool the pollinating native bee (the dupe) into "thinking" there is a nectar reward when there is none; this would similarly require the bee to be able to discriminate, learn, remember and be fooled (can a bee be so educated? Interestingly, most visitors to deceptive Batesian floral mimics in the Mediterranean region are solitary bees too). The process would provide an advantage to the orchid, and would cause the bee to expend fruitless energy. It also has the theoretical potential to harm the manuka if the orchids eventually outnumbered the manuka and the bees learned there was not much nectar to be had by visiting small white flowers with dark centres.

Pollinators will learn to differentiate the rewarding manuka from the nonrewarding Thelymitra of course, but there is another trick up the mimic's sleeve: if there is some variation in the appearance of the mimic, it is harder for the pollinator to learn which flowers are nonrewarding - i.e. one might expect many forms of T. aff. longifolia, and it is indeed polymorphic in the Far North.

Cryptostylis subulata exudes a pheromone that attracts male ichneumonid wasps, because they cannot distinguish it from the mating pheromones of female wasps. The orchid is the mimic, the female wasp the model, and the male wasp the dupe. The male wasps hatch a couple of weeks before the female wasps, and in that interval the orchid blooms and enjoys the undivided attention of the male wasps. Later, when the female wasps hatch, the males find them more attractive, and turn to them instead of the orchid. Who wins? The orchid - and perhaps the male wasp if he enjoys the orchid. Who loses? Well, nobody really - so is this truly Batesian? Or is it symbiosis?

Many other orchids mimic female insect models in their visible and tactile labellar decoration (e.g. Chiloglottis trapeziformis).

Mimicry between plants requires strongly overlapping distributions over enough time for co-evolution to have occurred, a significant overlap in flowering time, and sharing the same pollinator species. A disadvantage of mimicry between plants is improper pollen transfer (the deposition of pollen from one species onto another); orchids reduce the chances of this by aggregating pollen into pollinia, whose shape keys best into other flowers of the same species. Flower longevity also confers advantage, and colony-formation may reduce improper pollen transfer.

How does this evolution take place? how did Calochilus get to look like an insect if Calochilus evolved from Thelymitra?

Darwin favoured natural selection where individuals with particular features (within-species variation) proved most fit to reproduce, so were successful. Mutationists regarded natural selection as largely irrelevant, claiming evolution by way of mutations which, if successful, would favour the mutant individuals. The modern synthesists say that natural selection moulds organisms by sifting the raw material provided by genetic mutation. But then - how small or how large are the initial changes provided by mutation? You can't believe Thelymitra evolved into Calochilus in one massive mutation, and yet what advantage would lesser changes afford?

Well, first of all, it didn't. Thelymitra didn't evolve into Calochilus: it was some unknown ancestor
of both that evolved into each. That ancestor just may have looked like Calomitra, the manmade intergeneric hybrid between the two.

But second, the answer appears to be encapsulated in what is called the "two-phase theory": first,
a relatively large mutation establishes a rough resemblance to the model, altering the original pattern of the organism considerably but achieving only approximate mimicry; and then this rough resemblance is slowly improved by the selection of many modifier genes each of small effect, which may eventually produce very accurate mimicry.

Many specimens of the old Thelymitra and Calochilus ancestor got hit by cosmic rays, and many of them developed useless abnormalities that might have been inherited for a while but died out eventually (the curious exploded Pterostylis of Upper Morrison's Creek [J41 p2] is a modern example of a doomed mutation). Then one was hit, had a genetic change, and its offspring had such hairy labella that pollinating insects tried to mate with it, and in doing so they increased cross-pollination, which conferred an advantage on those carrying this inherited mutation.

The new orchid was successful, and gradually small improvements were made by the natural selection of favorable within-species variations. Perhaps, ages later, one of its descendants also got zapped by the raygun of the great genetic engineer in the sky and there was another big change. Eventually we got a Calochilus. By a similar process we got an ancestor of Thelymitra aff. longifolia, whose flowers underwent successive changes, keeping up with those of manuka flowers until the two look as alike as they do today - Ed.

See also Roy BA, Widmer A (1999). Floral mimicry: a fascinating yet poorly understood phenomenon. Trends in plant science. 4 (8): 325-340.