Apr. 1, 1998
DURHAM, N.C. -- Caterpillars treated to stunt the growth of their future hind wings develop into butterflies with abnormally large front wings, two Duke biologists have discovered. And scarab dung beetles treated to stunt the growth of their horns sprout larger eyes.
These peculiar discoveries represent more than biological curiosities, the biologists say, constituting the first clear demonstration that living organisms arise not only through the direct read-out of some genetic recipe, but also through more subtle and mysterious processes of competition between growing body parts for resources.
According to the scientists, this competition, first suggested almost 150 years ago by Charles Darwin in Origin of Species, offers a highly cautionary lesson for scientists and laypersons alike who believe that genes are the direct blueprint for all aspects of a living organism, whether it be dung beetles or humans.
Such competition or resource tradeoffs between growing parts, in fact, may make inherited changes in some traits or structures appear genetic when they are not, say the biologists.
The researchers, Professor of Zoology Fred Nijhout and postdoctoral fellow Douglas Emlen, published their findings in the March 31 issue of the Proceedings of the National Academy of Sciences. Their work was supported by the Duke University Morphometrics Laboratory and the National Science Foundation.
In their experiments with butterflies, the scientists performed tiny incisions in caterpillars to remove one or both of the small fleshy discs that would develop into the hind wings once the caterpillars underwent metamorphosis. When the butterflies emerged, they had abnormally enlarged front wings.
In one set of experiments with the scarab dung beetles, the researchers treated male beetle larvae with a hormone known to decrease size of the horns -- which grow on the back of their head and which males use for fighting. The resulting adult male beetles with reduced horn size had correspondingly enlarged compound eyes.
In another set of beetle experiments, the researchers selectively bred beetles that had either long or short horns. After seven generations of such selection, the biologists found that beetles bred to have abnormally long horns had abnormally small eyes, and those bred to have abnormally short horns had correspondingly larger eyes.
"These experiments represent the first direct demonstration that the control of how big an organ or tissue grows doesn't lie entirely within that organ or tissue," Nijhout said. "It has long been suspected that this is the case, but the evidence has been indirect. For example, your arm may grow to a certain length because of some genetic development program within that arm. But if you are malnourished as a child, your body would have been smaller and your arms proportionately shorter because of some communication between the arms and the body as a whole.
"While many developmental biologists, and certainly the lay public, haven't paid much attention to this phenomenon, we believe our experiments show that it is important and should be explored further as a fundamental mechanism of development beyond genetics."
Interestingly, said Nijhout, the new experiments resolve a conundrum that Charles Darwin identified in 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 one part owing to the excess growth in another and adjoining part."
According to Nijhout, the insects made good experimental animals for demonstrating such competition because during metamorphosis they were "closed systems." An insect pupa does not feed and instead contains a fat body that provides the only nutrition for the developing adult animal, making the results of competition far more clear-cut.
"Such competition would be more difficult to detect in organisms such as mammals that grow continuously with continuous feeding," he said. "In such cases, the organism can dynamically shunt food between one system and another to where it's needed."
Importantly, the phenomenon was demonstrated in two very different species, indicating that it is able to be generalized, Nijhout said. "Evolutionarily, butterflies and beetles are about as far apart as people and alligators," he said.
Particularly intriguing, Nijhout said, was that the butterfly and beetle experiments both showed that the experimental removal of one part affected only the size of one or two nearby parts, rather than the insect's growth as a whole. This effect may be because nutrients are somehow compartmentalized, with adjacent parts vying for the same pool; or that tissues that develop at the same time share resources; or that the fastest growing tissues -- including wings, horns and eyes -- are most limited by resources, the Duke biologists said.
Nijhout emphasized that, while he and Emlen began their experiments with a theory that competition for nutrients might be the basis for any observed changes in the insects, they still don't know what chemical communication takes place between the fore and hind butterfly wings, or between the beetle's horns and eyes. Either a hind wing may produce something that inhibits the fore wing, or it may consume something that the fore wing needs, he said.
"But whatever this mechanism is, it will show up in selection experiments as a genetic correlation," Nijhout said. "In other words, if you alter the genes that affect the size of the hind wing, you will alter the fore wing in the opposite direction, even though there are no shared genes between them. They are only linked through a common resource.
"So, these experiments show that what really is important is not so much which genes you share, but which processes." Thus, Nijhout said, the discovery is cautionary for biologists studying development.
"These experiments help bring back into focus a question that investigators were concerned about decades ago, but everybody decided would be a very difficult problem to tackle," Nijhout said. "The huge majority of developmental biologists are now exploring how genes are activated, and what their sequences and pathways are. And we've lost track of the fact there must be these larger-scale biochemical regulatory mechanisms that manage size regulation and proportional regulation among body parts.
"We hope that this paper will demonstrate that these are approachable systems, that the questions are still out there and are interesting and important."
Thus, the Duke biologists plan further experiments with both butterflies and dung beetles to explore the chemical regulation of development, including how organisms make fine size adjustments to their organs and tissues. The scientists said their hope is that the mechanisms they discover in insects will also teach lessons about development in higher animals, including mammals.
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