Key to metamorphosis evolution

It’s in the hormones

The next time you turn on a light and see a silverfish scampering away, be thankful evolution didn’t bestow it with the same development as some of its more advanced insect cousins.

James W. Truman and Lynn M. Riddiford, professors of zoology, with two of their research subjects, a tobacco hornworm and a cercrupia moth.

Four insect groups comprising beetles, bees and ants; moths and butterflies; and flies and mosquitoes make up nearly 60 percent of the more than 1 million known animal species. They are so prolific and exhibit great diversity because of metamorphosis, a process in which larval, pupal and adult stages differ greatly, allowing each to occupy a different habitat and consume different food sources.

Now two University of Washington zoology professors are proposing a novel hypothesis for how metamorphosis evolved. Their proposition suggests that a change in hormonal function during embryonic development led to the evolution of a unique larval stage, an innovation that allowed a virtual population explosion among these species in the last 250 million years.

“Metamorphosis really opened up niches that weren’t available to insects before that,” said UW zoologist James Truman, who along with UW zoologist Lynn Riddiford published their findings in today’s issue of Nature.

The earliest insects, which strongly resembled today’s silverfish, lacked metamorphosis and their juveniles looked very much like adults except that they didn’t have functioning genitalia. After the evolution of flight, more advanced species, such as cockroaches and grasshoppers, developed incomplete metamorphosis. Their immature stages, called nymphs, still resembled the adults except that they lacked genitalia and bore wing buds that only transformed into functional wings during the molt to the adult stage. In both cases, the insects molt, or shed their external skeletons, several times as they grow to adults.

The higher insects, species with complete metamorphosis, spend their juvenile life as larvae that bear no resemblance to the adults. What allows the change from, say, a caterpillar into a butterfly is the way a group of insect hormones, juvenile hormones and ecdysteroids interact during embryonic, larval and pupal stages, the researchers said.

Juvenile hormones suppress the development of adult structures. In insects with partial or no metamorphosis, the absence of juvenile hormones during embryo formation and development allows the embryo to become a miniature version of the adult. In embryos of insects with complete metamorphosis, Truman and Riddiford said, there is an early appearance of juvenile hormones that suppresses some of the adult-directed growth and promotes formation of the larval stage. Juvenile hormones remain as the larva grows, then disappear to allow growth of imaginal discs, which will give rise to specific adult structures. A complex interplay between these hormones and ecdysteroids then allows the larva to progress to a pupa, and finally ecdysteroids alone drive the transformation to adult.

Juvenile hormones play such an important role in the embryonic and larval development of metamorphosing insects that they have been used as the basis for insecticides. For instance, mimics of the hormones are used to treat ponds where mosquitoes breed, thereby blocking their metamorphosis. Such treatment also prevents eggs from hatching.

The four major insect groups with complete metamorphosis all are thought to descend from a common ancestor, so it appears the development of metamorphosis in the insect world has occurred only once. There are indications that another group, called thrips, has evolved toward complete metamorphosis but so far has fallen short, Truman and Riddiford said.

In insects with complete metamorphosis, the lack of competition between juveniles and adults for food is a major factor in their success and diversification, the husband-wife team said. Adults can feed on one source, such as nectar or blood, and only lay eggs when there is appropriate food for their young, such as dung, carcasses, fruit and other relatively temporary sources.

“The key to different types of development is timing, when certain kinds of proteins are made, how long they’re present, and so on,” Truman said. He believes metamorphosis will provide a valuable model for researchers to understand the molecular basis for how shifts in the timing of protein production can lead to the creation of different body forms. That, in turn, could shed greater light on how life patterns have evolved.

“Any innovation that helps you generate species that account for more than half of all living animals is not a trivial innovation,” he said. ¶

Vince Stricherz, News & Information