The emotions that other species summon up in the human brain are perplexing. A lion inspires awe and respect. It is the king of the jungle, a great name for a football team, a noble guardian of the entrance to the New York Public Library. A tapeworm, on the other hand, summons disgust mixed with a little contempt. You will never find yourself cheering for the Kansas City Tapeworms. But are these species really so different? Both animals get their nutrition from the bodies of other animals, and tapeworms are arguably more sophisticated in the way they get their food than a lion. Tapeworms escape our immune systems with ingenious biochemistry, and may even be able to eat our antibodies as food. Some species that live in fish make the fish leap around at the surface of the water so they are easier prey for birds, the final hosts of the tapeworm. And is it any less gruesome to be torn apart by a lion than to be host to a tapeworm? The best that a parasite can hope for, if a parasite could ever hope, would be to inspire fear. That's the fate of parasitoid wasps, which, as I mentioned in a previous post, are the inspiration for the monsters of the Alien series. The precision of their cruelty, the intimate ways in which they can use up their hosts, give us chills. Yet they remain truly alien--a malevolence that is separate from the rest of the natural world.
But parasitoids are very much a part of nature, and what they do is really one a variation on what many other organisms do. It helps, I'd argue, to think of parasitoids as hackers. They have hacked the living code of their hosts--the combination-locks of cell receptors, the wiring of metabolic circuits, the calendars of life history. But parasitoids, as living things, can be hacked as well. And among their hackers are organisms that few would consider malevolent or cunning: orchids.
Flowers and insects have had intimate relationships for tens of millions of years. Honeybees, for example, will travel from flower to flower to gather nectar for food, and accidentally pick up pollen grains along the way. Some of those pollen grains will wind up on another flower of the same species, and will fertilize its seeds. Flowers have adapted to take advantage of these insect couriers with bright petals and convenient landing strips. The easier they can make it for insects to carry their pollen, the more successful they'll be in the evolutionary sweepstakes.
Many orchids have evolved particularly elaborate contraptions for insect pollination. One species keeps its nectar at the bottom of a foot-deep tube, so that only a moth with a foot-long tongue can reach it (and press its face into the orchid's pollen). Another orchid has a spring-loaded catapult that slaps pollen onto the back of bees as they walk toward the flower's nectar. But most elaborate of all are the adaptations of certain orchids in Australia and Europe that offer the insects nothing at all.
Take the parasitoid wasp Neozeleboria cryptoides. The females lay their eggs in insects; the males that emerge from the host grow wings, while the wingless females crawl around on the ground and up various plant stems. The females produce a pheromone in order to attract males. It takes less than a billionth of a gram of the stuff to let a male N. cryptoides pick her out from wasps of other species. It's also enough to let him distinguish between virgin females and ones that have already known the pleasure of another male's company. The male homes in on a suitable female and they mate, whereupon he lifts her up and carries her from eucalyptus tree to eucalyptus tree so that she can drink the juices secreted by aphids. He finally leaves her near an inviting host, where she can lay her eggs.
Most of the time this arrangement works pretty well for the wasps, but every now and then a male will get a shock. He is flying along when he gets the unique whiff of a female seeking a mate. He cruises low to the ground, where the female should be waiting on a plant stem. As the smell of pheromones gets more intense, he see her long slender body hove into view. He lands on her and takes hold, only to find that he has not actually found a female wasp. Instead, he's fumbling around on the end of an orchid flower.
In Australia and Europe, some orchids use love-starved males to spread their pollen. They produce exquisite replicas of the pheromones made by a species of wasp, and they grow lobe-shaped wasp decoys. When a male wasp crashes into the orchid, it gets covered with orchid pollen. If it gets fooled again, it allows the pollen to fertilize another orchid.
The closest relatives of many of these sexual deceivers are deceivers of another sort--orchids that produce the aroma of nectar without the nectar. This kinship hints that some ancestral food deceiver underwent a mutation that made it produce an aroma that was vaguely sexy to some insects. Over time, more mutations helped them create the aroma of attraction instead of food. Some of the structures in the orchid flower began to swell, offering another illusion to the male wasps. The wasps themselves may well have driven the orchid's evolution as well. N. cryptoides. The orchid, like the wasp itself, is a parasite, demanding a toll from the wasps but offering nothing in exchange. Males learn to avoid orchid patches after getting tricked a few times, and any mutation that helps them to a better job of distinguishing between orchids and female wasps will give them an advantage over less discriminating suitors. In order to benefit from sexual deception, the orchids need to continually reinvent their perfumes, so that they are harder to tell apart from wasp pheromones. In the process, they lost the flowery aromas left over from their ancestors, until their odor was pure mimic.
These orchids have not become a faithful replica of a female wasp, however. They offer an exaggerate set of the cues a male wasp relies on to recognize a female was. (It's a bit like the grotesque bust and rear of a woman in a soft-porn cartoon.) In this month's issue of the Journal of Evolutionary Biology, the Swiss biologist Florian Schiestl reports on what male wasps find sexy in an orchid. He was able to do this because earlier this year he isolated the orchid mimic of the N. cryptoides pheromone. Schiestl coated dummy wasps of different sizes with different amounts of synthetic pheromone. He then presented male wasps with pairs of the dummies and recorded which ones they chose.
He found that males prefer bigger females to smaller ones. Size is probably a good clue to the health of a female. The wasp-mimicking structures on the orchids are a third longer than the actual wasps and over five times wider, which just so happens to be the strongest preference of the male wasps. Anything larger was no more attractive than small sizes. In other words, the orchid is perfectly exaggerated. The fake wasp body is as big as it needs to be, without being bigger.
Meanwhile, the male wasps are attracted to stronger pheromone scents over weak ones. Schiestl found that orchids on average produce 10 times more pheromone than female wasps. The flower can pump out vast amounts of pheromones compared to the females, most likely because the females are working under some special constraints. Many predators and parasites use pheromones as signals of potential prey, and so the wasps could risk death if they were too loud in their calls. But these wasp enemies pose no threat to the plants, and so they can shout as loud as they want. And since wasps don't bump into orchids all that often, the louder the better. As a result, an orchid is actually more attractive to a male wasp than a female of his own species.
But even now, the orchids haven't finished hacking into the wasp life cycle. After female wasps mate and their eggs begin to develop, they stop producing pheromones. The developing eggs give off another chemical that male wasps can recognize and which tells them that this female is no longer a virgin. Schiestl has also found that after some sexually deceptive orchid flowers have been pollinated, they release the same postprandial chemicals. The male wasps are repelled--perhaps towards one of the other flowers on the same plant that are still releasing come-hither signals.
In the comments to my previous blog about parasitoids, Walt pointed out that the next move in the Alien series actually going to be a battle between the alien parasitoid and the dreadlocked beast from the Predator series. (Here's the preview.) Now, one of my fondest memories in childhood was watching the various face-offs between Godzilla, Mothra, and the rest. But if nature is our guide, the alien should really meet its match in the luxurious, baffling embrace of a flower.
Another nit-pick for you. Bees collect flower pollen as food, as well as nectar.
For people that are curious, here's some pictures of bee orchids (Ophrys apifera). I love mimics. Some recent cool ones that I've come across are the moth that looks like a hummingbird and the black-and-white catterpillar that looks like bird poop.
Did anyone else appreciate the tribute to nature's little tricksters in Master and Commander?
I suppose my "favorite" parasitoid is Toxoplasma gondii, which causes rats to lose their fear of cats and thereby be eaten, transporting T. gondii into the cat's gut, where it reproduces (without harming the cat); see http://www.microbe.org/news/Tgondii.asp. I think that the best a parasite can hope for is to inspire complacency ... and I might as well have been cheering for the Kansas City Tapeworms last Sunday, but that's another story entirely. ;)
Fascinating. I have been intensely interested in these behaviors and what analogies one can draw from them for other areas, particularly human and machine systems. For further reading, I would recommend the RAND study entitled Unweaving the Web: Deception and Adaptation in Future Urban Operations found at http://www.rand.org/publications/MR/MR1495/
Keep up the good work.
re: Toxoplasma gondii and cats.
Jay Manifold comments [Jan 15 2004] that T gondii reproduces without harming the cat. I am certain that is true in the majority of cases, but anyone who has been unfortunate to have a cat actually contract Toxoplasmosis could not agree. I had a cat develop Toxoplasmosis in 1993, [probably from a mouse or bird eaten outside] and, despite heroics in treatment, he died. The progression of symptoms was extremely distressing. Those of us who get pregnant ;) are a bit less fond of T. gondii, I suspect.
Please see Cornell University's info at
http://web.vet.cornell.edu/Public/FHC/toxo.html for the science.