Image: DUKE UNIVERSITY
The moral of this bizarre finding is that genes are not a direct blueprint for building a living organism. "These experiments are the first demonstration that the control of how big an organ or tissue grows doesn't lie entirely within that organ or tissue," says Fred Nijhout, a professor of zoology at Duke University and the lead author of a paper describing the results in the March 31 issue of the Proceedings of the National Academy of Science. "It has long been suspected that this is the case, but the evidence has been indirect."
Charles Darwin first proposed that developing body parts might compete for resources almost 150 years ago in the Origin of Species, but no one tested the idea until Nijhout and postdoctoral fellow Douglas Emlen did so in two ways. First, they made tiny incisions in caterpillars to remove parts of the tissue that would ultimately develop into hind wings. When these caterpillars underwent metamorphosis, they emerged with abnormally large front wings.
Similarly, Nijhout and Emlen treated larvae of male scarab dung beetles with a hormone known to stunt the growth of their horns. (The beetles use these horns for fighting.) They found that after the larvae matured, the resulting beetles had particularly small horns but unexpectedly large eyes.
Next, the researchers went on to solve a puzzle Darwin put forth in the Origin of Species when he wrote, "I see hardly any way of distinguishing between the effects, on the one hand, of a part being largely developed through natural selection and another and adjoining part being reduced by this same process..., and on the other hand, the actual withdrawal of nutriment from on part owing to the excess growth in another adjoining part." Nijhout and Emlen selectively bred beetles having long or short horns for seven generations and found that the insects with the longest horns had the smallest eyes and vice versa.
Image: Duke University
Butterflies and beetles were particularly good models for demonstrating this sort of inter-organ competition because they are essentially "closed systems" during development: The pupa do not need to feed because they have a fixed reserve of built-in nutrition. In contrast, organisms such as mammals continually feed as they grow, making it easier to compensate for competition between body parts. As a result, the effects of competition are less apparent.
Still, it is reasonable to assume that such competition does take place in higher organisms, such as mammals. Nijhout notes that the process was shown to occur in two animals that are, evolutionarily speaking, very different and so it is probably common to many species. Also, the competition in the butterflies and beetles shared similar traits: In both cases, thwarting the growth of one body part affected only on one or two nearby parts, and not the whole insect.
Perhaps during development the same pool of nutrients is shared by nearby body parts or by parts developing at the same time. Or perhaps shared resources are fought over primarily by the parts that develop most quickly--such as wings, horns and eyes. Until the mechanism is worked out, the correct explanation will remain unknown. In the case of the butterflies, the hind wings may produce chemical messengers that limit the size of the fore wings, so that removing parts of the hind wings leaves the fore wings' growth unchecked. Or the hind wings may ordinarily consume something the fore wings need.
Nijhout and Emlen do plan to look into what chemicals play a part in this developmental show down. But the conclusion from their current findings is clear: inherited changes in traits and structure are not always genetic in nature. "The huge majority of developmental biologists are now exploring how genes are activated, and what their sequences and pathways are," Nijhout says. "And we've lost track of the fact that there must be these larger-scale biochemical regulatory mechanisms. We hope that this paper will demonstrate that these are approachable systems, that the questions are still out there and are interesting and important."