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The Sex Lives of Flies

In 1963 a pre-med undergraduate student at UH Manoa got a summer job washing test tubes. The student was Ken Kaneshiro and the job was for the new Hawaii Drosophila Project. Today, Dr. Ken Kaneshiro is an eminent evolutionary biologist. He built his world-renown scientific reputation by studying the sex lives of flies. Of course, these flies are no ordinary flies. They are uniquely Hawaiian flies with an evolutionary history that is unsurpassed in the animal kingdom; they have chromosomes made for laboratory study; and perform remarkably elaborate mating rituals. The Hawaiian Drosophila is one of our islands great evolutionary treasures.

The story of Hawaii’s Drosophila began several million years ago. Most likely, one solitary fertilized female, carried by wind for thousands of miles, landed safely somewhere in the Hawaiian archipelago. From that single, genetic ancestor, a population of flies evolved here that today numbers in the hundreds. Five hundred and eleven to be exact with another four or five hundred in collections waiting to be described and named. Dr. Kaneshiro and others believe that eventually there will be over one thousand species of Drosophila listed. From a single colonizing event, hundreds and hundreds of new species have derived. This type of speciation is known as adaptive radiation and the Hawaiian Drosophila are considered to be the world’s supreme example. If only for this amazing evolution, our Drosophila would be fascinating, but the story continues.

Photo by Bill Mull

Photo by Bill Mull

One of an estimated 1000 species of Hawaiian Drosophila pomace flies, many of which are undescribed and unnamed.

Drosophila are found throughout the world. All of them have within their saliva glands giant polytene chromosomes. These genetic strands are so large that it is relatively simple to view and study them. This feature coupled with the ease and success of rearing Drosophila in captivity has made these flies the workhorse of genetics over the past twenty to thirty years. The Hawaiian drosophilids, with their explosive speciation are even more attractive for study. By crossing closely related but geographically isolated species, biologists have, among other things, studied the sexual behavior of the flies. What they discovered were elaborate and bizarre mating rituals. Dr. Kaneshiro calls them “the birds-of-paradise of the insect world.” These rituals are most extreme within a group of the Hawaiian species known as the Picture-wing drosophilids.

The Picture-wing Drosophila are the world’s largest species of Drosophila and arguably the most beautiful. Their mating and courtship ritual is two-fold. First, the males stake out a mating territory, or lek, and defend it from other males of the same species. Lekking is seen in other species, though mostly mammals and birds. The males use different techniques to ward off their competitors. One species, D. heteroneura, butts heads like Bighorn sheep. Others grasp one another with legs and wings in a wrestling match-a kind of “King of the Leaf.” There is a Picture-wing that intimidates with noise, creating a buzzing roar with muscles from the abdomen. Imagine two flies standing head to head trying to make the loudest noise until the competitor gives up and flies away. Once the male has secured his lek, the hard work begins. Now he must perform for the females that visit his site with a detailed choreography of flirtations and foreplay. If he does not convey the right moves and messages, she leaves without mating. Each species has its own ritual, some include dancing around the female in some fashion, buzzing of wings at a specific pitch, placing the males head under the females wing, tongue-tasting, or dousing the female with pheromone which E.C. Zimmerman describes as a “shower of aphrodisiac perfume.” Just because one fly is the toughest guy on the block and secures a prime lek, it doesn’t mean he’ll be successful with the ladies. He may be able to box, but if he can’t dance the female flies away without mating. It is here that the Hawaiian Drosophila story converges upon genetics, evolution, sex, and Kaneshiro.

One thing that geneticists and evolutionary biologists try to do is figure out the evolutionary progression of speciation. How do different species arise? The Hawaiian Islands are one of the best places in the world to study this question and the Drosophila are the best tool. Dr. Kaneshiro took different but closely derived species and placed males of one with females of another together and observed. From genetic studies and estimated ages of the islands the scientists had some idea which species were ancestral and which were derived. The younger islands have flies whose closest relatives genetically are on the geologically older islands. The suspicion was that younger species derived from colonizers from the older islands. In the lab females of these ancestral stock rejected the courtship of the derived males, but, ancestral males were usually able to please the derived females. Kaneshiro also found that within a population males that had superior courtship abilities were very successful in mating with most females. Most of the females in the population were very choosy though there were always a small percentage of females that showed little discrimination. These females basically take whatever comes along. So what does this tell us about speciation?

Imagine a fertilized female from Kauai is blown to Niihau and with her newly hatched offspring colonizes that island. Now we have a tiny population with a small gene pool isolated from other individuals of the same species. Biologists call this a genetic bottleneck. Brothers and sisters are able to breed and the population survives and slowly builds up. With such a small gene pool and the intense inbreeding, genetic drift occurs resulting in changes within the group. Males born into this group may not have the right stuff to satisfy the females. Perhaps the population will die off from a lack of mating. But at this point, in the early stages of the founder event, the non-discriminating females save the day. They mate with the males despite their poor performance. Perhaps over time the male’s dance is simplified and the group has shifted to a larger percentage of females that are less discriminating. This explains how an ancestral male, with his elaborate moves, can satisfy a derived female who is less choosy and, how a derived male, with his simple skills, fails to woo the choosy ancestral stock.

Out of these conclusions came the Kaneshiro hypothesis. Basically it proposes that sexual selection, not the classic “survival of the fittest”, is the most important influence in the early stages of species creation. Kaneshiro states, “Changes within the sexual environment may be the entering ‘wedge’ for the speciation process.” When first published in 1976, Kaneshiro’s hypothesis was very controversial. Today it can be found in textbooks. There have been several lessons learned in Hawaii that have helped to change our fundamental understanding of life and its processes. This lesson came through the voyeuristic practices of entomologists in the lab.

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