Beautiful Contrivances

Runner-up National Bragg Prize for Science Writing 2016. Published in ‘The Best Australian Science Writing 2016’

‘An examination of their many beautiful contrivances will exalt the whole vegetable kingdom in most persons’ estimation.’ Charles Darwin 1877

A diminutive black insect patrols back and forth across a clearing between the trees. Not a fly, but a tiny wasp, and he is searching for a mate. He detects a scent, just a few molecules, and is drawn, as fish on a line, to the source. He zig-zags through the air, crossing and recrossing the stream of alluring perfume. Finally he sees his goal. Her delicate magenta body shivers as she broadcasts her availability to the morning breeze. Like a siren she entices him, but her song is her scent. Imperceptible to human senses, but irresistible to his. He darts down and aligns his body with hers, his abdomen curving under, while he grasps her body firmly with his forelegs. He mates for fully a minute, transferring his sperm, before, sated at last, finally pulling away and flying off, leaving his mate alone.

The year is 1927 and Edith Coleman has been following the wasp’s progress, watching closely, and noting his every move. She observes something astonishing, and wonders why. For Coleman sees that the wasp has been deceived, though he was probably unaware of it. What lures him, and what he mates with, is not the female wasp he desires, but the delicate pink flower of an orchid. The plant has exploited his need to mate, and during the process it has affixed a package of pollen onto his body to be carried off and delivered to the next orchid flower he visits.

It was probably Coleman’s destiny to make a ground-breaking discovery eventually, although there is no hint, in her first reports, of the excitement she must have been feeling. She writes not as a scientist, but as an informed and enthusiastic amateur, whose pure joy at what she sees in the natural world around her is foremost in her work. She wrote on all number of things that sparked her interest, faithfully recording the intimate details of the lives of the animals, plants and insects she observed in her garden and hills surrounding her Victorian home. She simply noticed things, and wondered, with inexhaustible curiosity, why is that? This, surely, is the premise upon which all science works and moves forward. Someone notices something unusual and asks why. She was a natural historian in the true sense of the words, a discipline that seems now to have gone out of fashion.

Her daughter, Dorothy, first brought the wasp’s peculiar behaviour to Coleman’s attention. This simple observation by Dorothy, and which Coleman described as ‘An interesting, but perplexing, problem…’, led to her discovery of a process that is a product of evolution which still astonishes and fascinates scientists and natural historians today.

What Coleman had observed was a male ichneumon wasp (Lissopimpla excelsa, but known during Coleman’s time as L. semipunctata) entering the flower of the small tongue orchid (Cryptostylis leptochila) backwards, and not head-first as would normally be seen with an insect searching for nectar or pollen. That the wasps were pollinating the flowers she could be sure, for she observed them carrying packets of pollen (called pollinia) to and from the flowers attached to the tips of their abdomens, as well as depositing them. She suspected something had to be attracting the wasps to the flowers, and that it wasn’t nectar. She knew that this species of orchid does not produce it, and the wasp is a species that normally hunts for caterpillars and other larvae, not nectar. Coleman wrote:

…all the visiting insects entered the flowers in a reverse manner from that of most nectar-feeding hymenoptera [bees, ants and wasps], and thus removed the pollen, not on the head, proboscis or back, but on the tip of the abdomen! It was soon clear that our wasps were seeking neither nectar nor edible tissue; and, as they were all males, there could be no question of egg-placing, either in any larvae hidden in the flower, or in the viscid matter of the stigma [Female part of the flower that becomes sticky (viscid) when receptive to pollen]. I could form only one conclusion…

Her surprise was self-evident, but her conclusion is stated, considering the era in which it was written, without a hint of coyness, ‘...they are answering to an irresistible sex-instinct…‘ Coleman’s observation wasn’t new. Others before her in France and North Africa had noticed and pondered on the strange behaviour, as well as Darwin fifty years before, but none had realised that pollination was being effected by the pseudocopulation (false mating) of the insect, or if they had made the connection, they had skirted the issue in print. Coleman reports, in her 1928 paper,

‘Even Darwin overlooked what now appears an obvious conclusion…’ Coleman was referring to a comment Darwin had made in his Fertilisation of Orchids, where he responds to a statement that, “Mr. Price has frequently witnessed attacks made upon the Bee Orchis by a bee.” Darwin writes, ‘What this sentence means I cannot conjecture.‘

Coleman became the first to observe, describe and collect empirical data on the behaviour in an Australian orchid. She devised meticulous experiments, including the use of photography, which proved beyond doubt that the wasps were, indeed, pollinating the orchids and not just visiting the plants.

What she had discovered was the pollination of an orchid flower by the pseudocopulation, or false mating, by its male insect pollinator. By mimicking the colour, shape and odour of a female wasp, the orchid, in effect, persuades the insect to try to mate with its flowers, during which process pollen is transferred to the insect’s body. Then, as the true scientist that she was, she set out to prove it. Over the course of the next decade she experimented and investigated, checking and re-checking that the act of copulation was indeed causing the pollinia to be deposited on the insect’s body, that these pollinia were then taken to another orchid and deposited on the stigma, that the orchid did become fertilised by this act and produced viable seed, and that it was the L. semipunctata wasp alone which was responsible for the transfer of the C. leptochila orchid’s pollen. Initially she published papers in the journal of the Field Naturalist’s Club of Victoria, The Victorian Naturalist, but her work soon became noticed by the Entomological Society of London and her discoveries were first published (albeit without her permission!) in their Transactions in 1928. Coleman covered every aspect of the pseudocopulation process in the small tongue orchid and others, becoming a renowned authority on the process. Scientists still cite her work today.

Coleman rightly suspected that the insects were attracted by a ‘cunning mimicry‘ of the orchid flower to a female wasp. The flower’s pale pink labellum (the modified, enlarged third petal) with its double row of luscious, shiny magenta dots surrounded by the absurdly thin sepals and petals, does, to human eyes at least, bear a superficial likeness to the female wasp. Coleman supposed that, ‘To the inferior eyesight of the insect...’ the slight resemblance would be more than enough to persuade it. She was on the right track, but what he sees is more than a slight resemblance. The delicate pinks and rich magenta colours that humans see and find so attractive are, in fact, almost invisible to the male wasp, which can hardly discern them from the green background. What he sees are colours identical to that of the female wasp, and, almost incredibly, they mimic the dimensions and shape of the female’s body. Like most insects he is also attracted to reflected ultraviolet (UV) and yellow wavelengths of the spectrum. We now know that the glistening magenta bumps on the labellum of tongue orchids reflect UV exactly like the wings of female L. excelsa wasps, the reflections also resembling the shape and size of the female’s abdomen. The vivid yellow pollinia may also play a part in beckoning him, and can be seen, even with human eyes, shining brightly in the depths of the flower.

Coleman suspected, however, that the story did not end there. Her experiments convinced her that there was more than just visual mimicry at work. She noticed how swiftly the male wasps discovered cut flowers, despite being in a location where the small tongue orchid did not normally grow. The insects even quickly found flowers that had been brought indoors:

Having occasion to leave the room, and not wishing the flowers to be pollinated in my absence, I closed the window. There were no wasps visible. Returning in a few moments, I found three on the window-pane and one inside! I had inadvertently left the window open less than an inch at one side.

After watching wasps ‘tacking’ or zig-zagging towards the flowers she concluded that they were attracted by scent, though she reported that she could perceive little, if any. She was quite correct, of course. While the flower’s resemblance to a wasp obviously plays a part in the deception it is the odour that attracts the insects from a distance and then convinces them to attempt to mate with the flower. As Coleman had noticed, this odour, while undetectable to humans, is irresistibly strong to the male wasp. However, little was she to realise that more than three quarters of a century later research showed just to what extreme extent the orchid goes to attract its suitor. The truth had to wait until the invention of two new technologies: gas chromatography, which enables identification of individual compounds in a chemical, and a quite remarkable process named electroantennal detection, which allows scientists to measure the electrical activity present in an insect’s antennae when exposed to a chemical compound. Finally, in 2004, Florian Schiestl and his team at the Australian National University put these two technologies together and were the first to discover that this odour exactly mimics the sex pheromone of the female wasp. Even more astonishing is that in some species the orchids have reproduced an identical single compound present in the pheromone of its specific pollinator. To all intents and purposes the compounds are one and the same. Experiments where drops of a Drakaea orchid pheromone mimic were placed on beads glued to the heads of pins not only attracted male wasps, but they even attempted to copulate with the beads, which bore no resemblance to either orchid or female wasp. Each species of orchid which practices sexual mimicry replicates exactly the correct pheromone of its insect pollinator, whether bee, wasp, fly, or ant.

But there is more. The orchid even has tactile features that either stimulate the male wasp into mating or guide his body into the correct position. As Coleman eloquently stated, ‘…and so, with a Machiavellian cunning almost beyond belief, the orchid lures the artless insect to its service.’ So, you can have some sympathy for the poor male wasp. If it looks like a female, feels like a female, and smells like a female, then, well, you can’t blame him for assuming it is a female!

You would have thought that, having attracted its hapless go between, the orchid, would just dust him with pollen much like any other flower, but this is wasteful, and there is no guarantee that it will be taken to the correct plant for cross-fertilisation to occur. Pollen is expensive for the flower to produce so she wants to ensure she can place it on his body in the exact place it needs to be where it will be taken up by the next plant he visits, and that the next plant is another orchid of the same species. So she persuades him to copulate with her, and it is the act of copulation that causes the pollinia to adhere to his body. In persuading the wasp to copulate with it’s flower the orchid ensures that the wasp will have time to fly to another plant before the impulse to mate returns, and the mimicry of both flower appearance and sex pheromone ensures that it will be an orchid of the same species that he visits. Not only that, but the orchid flower, once pollinated, no longer produces the sex pheromone that attracted him, ensuring that he will not return to that same flower, risking self-pollination. This orchid needs cross-fertilisation with another, different, plant for the production of viable seed. Coleman had already noticed that undisturbed insects remained in the flower for up to a minute before flying off, and showed no further interest in that flower.

That the male wasp truly believes he is mating with a female is in no doubt, for both Coleman, and other researchers since, have found wasp spermatozoa deposited within the flowers. Wrote Coleman, ‘Mark the cunning of the plant, which first manufactures the sticky substance, and then delays the insect long enough for the viscid disc [the pollinia are attached to the viscid disc] to adhere to its body!‘

Coleman also noticed that male wasps still seemed to prefer the orchid flowers even if there were receptive females present, something observed by more recent scientists. In 1965 F.M. Coate reported in The Orchadian:

I had brought home a spike of C. ovata to photograph and was carrying it outdoors to a sheltered spot when there was a flash past my face. An ichneumon wasp (Lissopimpla sp.) which was already joined with a mate, darted towards the flower, violently discarding his lady-love in mid air. He alighted and backed into the flower, utterly ignoring the lady who sat disconsolately beside him for a while before flying off.

The scoundrel!

The individual male wasps may benefit, yes, but is this a problem for the wasp species as a whole? If the wasps continue to prefer the orchid flowers over real females then the wasp species would eventually become extinct. This hasn’t happened, for a number of interesting reasons.

It puzzled scientists for decades, but recently A.C. Gaskett of Australia’s Macquarie University suggested that most male wasp pollinators do not actually encounter one of these deceitful orchids in the wild, as they are generally uncommon or do not flower regularly. The male wasp is genetically programmed to seek out and mate with as many females as possible, but not all are fooled into mating with an orchid even if they encounter one. Some wasps learn to avoid the sexually deceptive orchids, and researchers have found that it may be the newly hatched naive males that fall victim to the flowers’ charms.

Also, in order to persist, the wasp species does not need many males, anyway. Males can mate again and again, fertilising many females during their short lives, and each female wasp can lay many eggs from one mating. Now this is where things get tricky, but quite remarkable. The orchid exploits a peculiarity in the wasps’ reproductive system. L. excelsa is a haplodiploid species of wasp, which means that unmated females can produce male offspring from unfertilised eggs. So, if a female wasp does not get to mate, due to the available males preferring the orchid flowers, she will only produce males, which in turn increases the amount of males in the population, (good for the orchids and also good for the wasps) and a positive feedback loop ensues. It seems that the cost of the occasional copulation with an orchid flower is outweighed by the many more matings with real female wasps. And so the wasp species persists. A truly amazing example of the interconnectedness of life.

As for the orchid, its survival as a species does not depend on cross-fertilisation entirely. The Cryptostylis genus spread by underground rhizomes and only need to produce the viable seeds, which cross-fertilisation ensures, very occasionally. The orchid’s pollination system is so efficient that each orchid flower only needs one successful pseudocopulation by a wasp to transfer its pollen, and one to receive it. So this finely balanced system survives. The orchid’s shape, colour and scent are so perfectly adapted to the wasp’s needs that it cannot be pollinated by any other species of insect, or even a related species of wasp. Coleman noted, ‘As the flower matures, the curve taken by the labellum with its upright posterior margins, so exactly meets the needs of the wasp…’

Coleman’s curiosity was piqued still further by the fact that her orchids did not self-pollinate. Self-pollination is where the pollen from a flower is deposited on the same flower’s stigma. This is perfectly normal for some plants, even some orchid species, but not so for those of the Cryptostylis genus, which, as explained earlier, need cross-pollination to produce viable seed. During her experiments she wondered why the pollinia were not deposited on the stigma when the insect left the flower. By careful inspection of the blooms Coleman realised that its construction was such that the stigma could only receive the pollinia attached to the wasp’s abdomen on the way in to the flower and not on the way out. She explained:

With the effort needed to free itself, the wasp exerts pressure on the rostellum [structure which separates the pollen bearing anthers from the stigma]. This pressure opens the anther-cells and releases the pollinia… and these are withdrawn by the insect, adhering to the last segment of its abdomen. The curve of the abdomen ensures the withdrawal of the pollinia clear of the stigma, otherwise the purpose of the partnership would be defeated, and self-fertilisation would result.

She was clearly impressed by this, when she stated, ‘To follow closely the act of pollination increases one’s belief in the sagacity of plants.‘

Coleman’s sharp mind had noticed one more conundrum, however:

Having established the fact that both species of Cryptostylis [C. leptochila and C. subulata] are visited and pollinated by the same insect, it is surprising to find no hybrids between them. I have never seen a specimen which might even suggest hybridising.

So, why is this a puzzle? Take a step outside of the plant world for a moment and consider two other closely related species. Lions and tigers. They look very different, but are genetically very closely related. If they are put together they can, and do, breed, and produce viable and fertile offspring. The only reason they don’t do this in the wild is that they occur on different continents, and never encounter each other. The Cryptostylis orchids that Coleman describes also look very different, but they both use the same pollinating insect, the wasp L. excelsa, and therefore both mimic the same sex pheromone in order to attract it. They flower at the same time, and Coleman observed insects freely visiting both species of orchid in the same location ‘within the space of a few yards’. The placement of the pollinia on the insect’s body is slightly different, but, true to form, Coleman carried out experiments that showed these pollinia still struck the stigmas of the alternate orchid species. The two species should hybridise, but they don’t. Little did Coleman realise it would not be until the twenty-first century and the invention of DNA analysis technology that the puzzle would finally be solved. It is a pity that Coleman did not have access to the DNA analytical tools which scientists have at their disposal today. She would almost certainly have used them. One can only imagine her fascination and delight in the process. It turns out that Cryptostylis species differ in their numbers of chromosomes, so a possible explanation for the lack of hybridisation could be that even if one species receives the pollen of another species from their shared pollinator it is possible that no viable seed will be produced.

How this strange relationship between the orchid and its pollinator evolved, however, is something else again. Scientists have offered many possible explanations. One suggestion is that the evolution of pseudocopulation started as a strategy to prevent self-pollination by the pollinator re-visiting the same flower, a common practice in flowers that produce nectar. Self-pollination is also common in nectar producing flowers. Orchids that use pseudocopulation for pollination do not generally produce nectar. Once the wasp has ‘mated’ with the orchid flower there is no longer any attraction to the flower for him, as we have already seen. Self-pollination in these orchids, although possible, is very rare, as the wasps do not generally fly back to the same flower they have just left – there is no reason to, and the pollen is only transferred from an insect on the way in to a flower. So, self-pollination is avoided. Maybe we shall never know for sure how this peculiar phenomenon came to be.

The Cryptostylis species that Coleman studied were not the only Australian orchids to use this strange method of pollination. Australia has over 1300 named orchid species with several hundred more awaiting classification. They vary from the voluptuous blooms of the tropical epiphytics (tree dwelling) to the delicate and secretive terrestrial varieties, and many of those species are now known to practice sexual mimicry to effect pollination, although not all of those require pseudocopulation. Once an insect is lured by the sexual deceit, some orchids trap or hold it until a mechanism is triggered causing the flower to place its pollinia on the body or head of its pollinator. It is not only wasps that are deceived into providing this service, but ants, gnats, bees and flies are also employed.

This is an unusual case of co-evolution, as only one species has shown adaptation over time, and that is the orchid. No selection pressure seems to have been exerted on the wasp to change and adapt to the orchid’s deception. Neither is it a case of mutualism as the plants totally exploit the wasps for their pollination services, but give nothing back in return. It is a case of extreme exploitation, except that the unfortunate wasp is not harmed, but the orchids gain the cross-fertilisation needed to ensure the genetic diversity that is important for their species long-term survival.

And so, the final piece is laid upon the table and the picture is complete. What started as a simple observation of something unusual has taken almost a century to understand. Edith Coleman’s simple curiosity about the world around her, the attention to detail, meticulous experiments and data collection, but, above all, her body of written work stimulated many scientists over decades to try to unravel the orchids’ secrets, each contributing their own piece to the puzzle. Many breakthroughs had to wait until the invention of new technologies and processes. The research continues. There may yet be more surprises around the corner.

The orchid’s sexual deceit and the strategies it uses to ensure the transfer of its genes is so breathtaking in its level of detail and complexity that it is impossible to conceive the thousands upon thousands of individual random genetic mutations that had to occur, and be selected for, to achieve it. A wondrous process that man is only just beginning to understand. Charles Darwin expresses it beautifully, and Edith Coleman would surely have concurred:

The more I study nature, the more I become impressed with ever-increasing force, that the contrivances and beautiful adaptations slowly acquired through each part occasionally varying in a slight degree but in many ways, with the preservation of those variations which were beneficial to the organism under complex and ever-varying conditions of life, transcend in an incomparable manner the contrivances and adaptations which the most fertile imagination of man could invent.

‘The Best Australian Science Writing 2016’ , Published by New South Publishing, Sydney, NSW, Australia

ISBN:

9781742235035 (paperback) 

9781742242606 (ebook)

9781742248059 (epdf)