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Evolving Metamorphosis: A Hopeless Task

fruit fly

In Current Biology last month,1 Jason M. Tennessen and Carl S. Thummel from the University of Utah School of Medicine had a lot to say about the complex dance of signaling partners — hormones, receptors, organs, and genes — that guide a fruit fly through its stages of life. It’s pretty amazing stuff. How did it come to be? Well, the relevant subtopic in the article is titled, “An Evolutionarily Conserved Program to Coordinate Growth and Maturation.”
Conservatism in evolution is where something endures virtually unchanged even as, all around it, speciation and diversification yield endless forms most beautiful. It’s also known as “stasis” — something of a contradiction, you might think, for a scientific theory that posits continuous change at every level from gene to population.
Like a butterfly, a fruit fly undergoes four stages in its short life cycle, from egg to larva (analogous to the butterfly caterpillar), pupa (analogous to the butterfly chrysalis), followed by the remarkable resurrection from inert pupa to a flying adult capable of sexual reproduction. What is learned from the humble Drosophila is applicable, of course, to the understanding of butterfly metamorphosis as well.
To prepare for what Tennessen and Thummel are going to say about the evolution of metamorphosis, we need to set the stage by briefly summarizing what they wrote about the signaling network behind the fruit fly life cycle. As we already said, it’s quite amazing. Like us, flies have glands that produce hormones; they have genes; they have fat bodies (no offense); and they have numerous acceptors, promoters and receptors that turn genes on and off.
What’s interesting is that their life cycle is controlled by a sophisticated interplay among genes, hormones, environmental factors and checkpoints. For instance, a fly larva has to reach a critical size to pass one checkpoint for further development. Why? To survive the pupal stage, when it can’t eat, it needs a minimum supply of reserves on hand. Until it reaches that critical size, development is delayed till the food supply improves. Once past the checkpoint, though, it will enter the pupal stage — reserves or not — but will just end up being a smaller fly.
That’s just one protective measure built into the fly’s developmental program. There’s much, much more. Scientists understand the barest outlines. One specific vital hormone is released by a gland in the brain, and spreads throughout the fly’s body — but not in an activated form till it arrives at the organs that will respond to it. This provides another protection, like sending a laser through the mail without the batteries, as a safety precaution, to a destination where someone has the batteries and the know-how to install them. There are more protections in activators that turn genes on and those that turn them off; some of these switch places depending on hormones or environmental factors.
Its “fat body” is a surprisingly critical organ for a fruit fly. It stores reserves of food, but it also functions something like a combination liver and pancreas. It’s a place where certain genes are expressed. It can delay growth in bad times, such as when its amino acid stores are low (implying it has a way to monitor those levels via another signaling pathway), and it can affect the production of insulin-like hormones through feedback loops, or repress them by putting something like Denver boots on them. Lastly, the fat body is a soup kitchen in hard times if the larva is starving. The authors imply we still are learning about “the mechanisms by which the fat body can sense nutritional status and relay that information to control developmental growth.”
That’s enough to see that a lot is going on in that tiny fly as it prepares for its final act, metamorphosis: the stage magician entering a casket to come out something fully alive but completely different. As with butterfly caterpillars, at the onset of metamorphosis, the larva changes its behavior. It stops eating, starts wandering, becomes able to produce glue in its salivary glands, and starts using up its fat body reserves. Then it enters its pupa, appearing lifeless, meanwhile reconstructing itself silently inside.
Evolve that, guys! Here they go: “The regulation of steroid hormone activity to promote maturation appears to define an ancient regulatory pathway by which many animals control this key life history event.” Did we hear you right? “This common genetic architecture was first described in the context of the Caenorhabditis elegans (roundworm) life cycle, when the animal makes a decision, based on environmental factors, to either continue development to form a reproductive adult or enter a larval diapause state.” Excuse me, gentlemen, we’re confused. How did the roundworm get the program? They don’t say. All they said was that once roundworms got it, somehow, it was conserved.
Actually, they claim far less than that. The only thing that seems similar in roundworm development and fruit fly development is a go/no-go checkpoint involving three signaling pathways. Reading on, we look for any attempt to explain all the body-plan reorganization that goes on in the pupa, so nicely animated in the film Metamorphosis. But no; we just hear talk about the initiation of metamorphosis by a few hormone interactions. The rest of the explanation is left up to “future research.” How’s that for an escape hatch for your theory? We’ll figure it out later. Someday.
Even more astonishing, they claim this irreducibly complex software that somehow magically appeared in roundworms hasn’t evolved ever since, down to and including human beings: “It is interesting to note that a few studies in humans suggest that this pathway is conserved through evolution.”
Finally, in the paper, they get to “Generating an Adult Body.” This should be good. As in the film, we hear about imaginal tissues (ITs). Check. We read about the signals that turn them on. Check. “Moreover, communication is maintained between IT growth and maturation to ensure that these tissues are ready for their terminal differentiation during pupal stages.” This all sounds like intelligent design so far. When does Darwin come on the scene?
Continuing on, we learn that the pupa can survive X-rays and apoptosis (programmed cell death) through other pathways that delay maturation till the damage is repaired. OK. Tell us, Drs. Tennessen and Thummel, how evolution explains the processes that recycle larval tissues, and out of them build compound eyes, articulated legs, sex organs, the proboscis, wings and the muscles that power them, a new gut, and all the other organs that weren’t present in the larva? This section of their paper is remarkably silent about evolution.
They do tell us that mutations disrupt the program; but that’s still no help to Darwin. Once again, answers are shuffled off to the future: “Development and metabolism, therefore, are inseparably linked, and current studies are focused on better defining the mechanisms that underlie this interaction.”
In fact, they never return to how all this evolved. They just go on to discuss more wonders. One of the key hormones is a multitasking whiz kid: it “initiates distinct metabolic programs at the onset of metamorphosis that are directed toward utilizing stored forms of energy to allow proper growth and development during the non-feeding pupal stages.” It switches on the eating of reserves in the fat body; it switches on cell division where needed, and more. Amazing. Find something in the chemistry lab that can do all that.
We give them one last chance to vindicate Darwin. In “Perspectives and Future Directions,” they begin, “The discovery that evolutionarily conserved signaling systems regulate larval growth and development establish Drosophila as an ideal platform for exploring the basic principles of animal maturation.” Once again, they push off any answers to future research. Ma�ana, ma�ana. Then they do a bait-and-switch: “These findings, combined with the observation that the fat body plays a central role in sensing nutrients and coordinating organismal growth, have emerged at a time when childhood obesity is increasing at an alarming rate.” What? What’s childhood obesity got to do with the evolution of metamorphosis? No kidding; they talk about it for a whole paragraph.
Winding things up, the authors discuss more topics that are “poorly understood” or “largely unknown.” We don’t want to be too hard on them. Their paper is valuable; they did a good job of describing what is known about the interactions of multiple signals in development of fruit flies. And they could argue that evolution was not the main subject of their paper. But they had a golden opportunity to tell us how metamorphosis evolved, and they couldn’t do it — other than to say that something emerged in a roundworm that has been “evolutionarily conserved” all the way to us. If you’ve watched the film Metamorphosis, or read the companion e-book Metamorphosis: The Case for Intelligent Design in a Chrysalis, you know that Darwin has much, much more left to explain than interactions between a few hormones.
In fact, we might even claim that the fruit fly provides an even more spectacular example of design than do butterflies. Fruit flies aren’t as pretty, but look how tiny they are. Most of the same processes we see in butterfly metamorphosis occur in these minuscule insects as well. Arguably, miniaturization makes the case for intelligent design even more impressive. Think about how most of the power of your old desktop computer can now fit in the palm of your hand as a smart phone. Consider, too, that there are insects even smaller than fruit flies. Have you ever watched a gnat and considered the hardware and software required to make something that tiny fly? The design argument stands, despite hollow attempts to tell us how wonders like metamorphosis “evolved.” Conservation is the opposite of evolution.
References Cited
(1) Jason M. Tennessen and Carl S. Thummel, “Coordinating Growth and Maturation — Insights from Drosophila.” Current Biology, Volume 21, Issue 18 (27 September 2011), pages R750-R757. DOI: 10.1016/j.cub.2011.06.033.

Thumbnail image for metamorphosis-bluray.jpgTo learn more about butterflies and the evidence they reveal for intelligent design, visit Metamorphosisthefilm.com, where you can watch the trailer and order this outstanding film, now available in both DVD and Blu-Ray formats. While there, be sure to download the free companion e-book, Metamorphosis: The Case for Intelligent Design in a Chrysalis, edited by David Klinghoffer — a beautiful and informative resource to enhance your appreciation of butterflies.