Internal fight settles size of body parts

Most animals compete fiercely for limited resources, as the phrase "survival of the fittest" suggests. An unusual new study showing that the absence of one growing organ or tissue allows another to become larger now hints that a similar competition exists internally as animals develop.

 The experiments -- in which butterflies grew large front wings in response to missing hind wings and male beetles deprived of their characteristic horns developed big eyes -- address the intriguing biological question of what determines how large various body parts become.

 While much of the information seems hardwired into an animal's genes, the new results indicate that to some extent, growing body parts directly influence each other's ultimate size. "Each tissue or organ isn't just running on its own genetic program and knows how big it's supposed to get," says H. Fred Nijhout of Duke University in Durham, N.C.

 Nijhout and his colleague Douglas J. Emlen, now at the University of Montana in Missoula, describe their manipulation of insect development in the March 31 Proceedings of the National Academy of Sciences.

"This is an absolutely delightful paper and really original. My bet is it's going to be a landmark," says Sean Carroll of the University of Wisconsin-Madison.

"It's pretty amazing work," agrees Rudolf A. Raff of Indiana University in Bloomington. "Here's a situation in animals where you can see competition, developmentally, between parts of the body."

 More than a century ago, in his book The Origin of Species, Charles Darwin pondered whether developing body parts clash with each other for nutrients. Until now, investigators had never found a way to view such conflict.

 Nijhout and Emlen approached the issue by working with holometabolous insects. In their larval stage, these insects stop feeding just before most adult structures form, providing a closed system in which the developing organisms have a finite supply of nutrients and other resources.

 In the case of the butterfly Precis coenia, the scientists removed from caterpillars the tissues that give rise to the adult's hind wings. After the caterpillars metamorphosed, the butterflies had larger front wings than butterflies from untreated caterpillars. The size increase was greater if larval tissue for both hind wings, rather than just one, had been removed.

 As for the beetle Onthophagus taurus, whose males sport horns that they use to fight for females, the investigators treated larvae with a hormone known to stunt the horns' growth. The beetles that emerged from this treatment had short horns, or none at all, and had larger eyes than untreated beetles of the same size.

 To examine whether the hormone was causing the larger eyes, the scientists gave it to female beetles, who have no horns. Their eyes remained the normal size.

 In neither species did shrinking or removing a body part spur widespread changes in the developing insect, notes Nijhout; rather, it increased the size only of body parts growing near the treated area. He plans to study why the response is localized and whether it stems from reallocating scarce resources, such as nutrients, or from the removal of growth inhibitors that one developing body part directs at others.