Three major beetle groups come up one testis short, CU researcher finds

By Sarah Yang and Susan S. Lang

A surprisingly large number of beetles are missing one of their testes, the male gonads of insects. As far as the researchers who discovered this can tell, the insects are not in any way impaired by this absence.

The discovery is striking because most animals are bilaterally symmetrical, which means the left and right sides of the body roughly mirror each other. This bilateralism extends to many internal organs, although some systems, such as the human heart and liver, develop or are positioned asymmetrically.

This Onypterigia tricolor beetle is a member of one of three beetle lineages that have only one testis instead of the typical pair. Photo by Kipling Will/UC-Berkeley

"The beetles with one testis are mating normally and doing their beetle thing," said James Liebherr, professor of entomology at Cornell. "It strikes me that carabid beetles are pretty well known to scientists, yet the loss of an entire organ across three major lineages was not fully comprehended until this study."

Lieherr and his co-authors, including first author Kipling Will, Cornell Ph.D. 2000, assistant professor of insect biology at University of California-Berkeley, suspect that this asymmetry in a bilateral organism might have evolved to make more room for the accessory glands, which are somewhat larger in the one-testis beetles than in two-testes beetles, the researchers found. These glands produce most of the seminal fluid.

The study will be published in the April print issue of the Journal of Morphology but is available now online at http://www3.interscience.wiley.com/cgi-bin/jissue/109771912.

"In other insects where these glands have been studied, accessory glands produce proteins that are passed to the female during mating," says Liebherr. "They're a nuptial gift, so to speak, that can be used during development of the female's eggs."

Will led a systematic survey of all major lineages of the beetle family Carabidae. The researchers said that field observations such as this provide valuable clues to beetle biology and evolution.

The one-testis phenomenon, or monorchy, was first noted in Harpalini carabid beetles in 1825. But it would take another 180 years before researchers discovered that two other major lineages also lack one testis.

The survey required detailed dissection and study of over 820 species, a representative sampling from the 37,000 species of carabid beetles estimated to exist. The researchers found 174 species, all members of the three lineages with only one testis. The researchers note that except for this one anatomical distinction, the one-testis beetles appear and behave no differently than their two-testes counterparts.

For reasons unknown, in almost all cases it is the left testis that has disappeared. In one case Will found, however, that the right testis was lost. While animals such as jellyfish and starfish are radially symmetrical, bilateral symmetry is, hands down, the dominant body shape in the animal world, thanks in part to the drive for forward motion.

That's not to say there is no precedent for such deviations from bilateralism. One well-known example is the male fiddler crab, which has an outsized claw on one side that is used to attract female crabs and fend off male competitors.

Still, the researchers said the complete absence of an organ, or absence asymmetry, is rare. "Evolution has predominantly favored bilateral symmetry in animals, so when we see that the rule is violated, as in the case with these beetles, it gets our attention," said Will.

When it does occur, there is likely a good reason for the organ loss. Snakes, for example, have one lung that is significantly reduced to accommodate a relatively extreme body shape. Most birds have only one functioning ovary, which some biologists believe helps optimize their bodies for flight.

"Male crickets will directly transfer fluid from their accessory glands to female crickets to provide nutrition to their eggs," said Liebherr. "It may be that the male beetles are similarly providing other things than sperm to the females. But it's a chicken-and-egg question. We don't know what came first. Was the testis lost first, leaving more space for the accessory glands to grow? Or did the testis lose out to make way for a larger accessory gland? That's a subject for further study."

Whatever the ultimate cause, something drove the evolution of this absence asymmetry.

"We found monorchy in three distantly related groups of carabid beetles -- Abacetini, Harpalini and Platynini -- indicating that the loss of the testis occurred at least three separate times in the evolution of the beetles," said Will. "It seems unlikely that it was completely random."

Based on the geographic distributions of the beetle groups involved, Liebherr estimates that the origins of monorchy in the beetles occurred 90 to 100 million years ago during the Cretaceous period. "That era witnessed a dramatic increase in the diversity of organisms," he said.

He added that these findings illustrate the value of basic natural history.

"So many of the scientific discoveries today seem to occur primarily on the molecular and genetic level, so findings such as this are remarkable," said Liebherr. "A lot of the ideas that come to the lab bench start in the field. We still have much to discover by looking at whole organisms."

Other co-authors are David Maddison at the University of Arizona and José Galián at the Departamento de Biologia Animal Facultad de Veterinaria in Murcia, Spain.

This research was funded by the National Science Foundation.