Mating with castrated males induces females to oviposit

As I was picking up rotting fruit from the ground, a woman walked by and told me “pick the nice ones from the tree, you are going to get sick”. I was amused by her concern and explained that indeed I was looking for the rotting fruit. I was searching for the fly maggots that infest oranges and mangoes.

The Mexican fruit fly is a pest that can cause devastating effects for both small fruit farmers and exporters. Most people think of fruit flies as those pesky small flies around our ripening bananas, but those in reality are in the Family Drosophilidae, the vinegar fruit flies. The pests that I was looking for are called the true fruit flies and belong to the Family Tephritidae. The reason for this distinction is that the true fruit flies lay their eggs in fruits when they are still green on the tree, while the vinegar flies lay their eggs in ripening or rotting fruit. The eggs of the true fruit flies develop into maggots (larval flies) which eventually leave the fruit when it falls from the tree. Once on the ground, the maggots burrow into the soil and form a cocoon known as a pupa. Some species even have an unusual behaviour in which the maggots can coil and jump from the fruit into the soil. A few weeks later the adult emerges from the pupa; eats and matures sexually; mates; and then lay eggs into the fruit.

Some species from the Tephritidae are worldwide pests that cause huge losses in agriculture and commerce. Because no one wants to eat fruit with maggots inside, scientists have developed various control measures against these flies. One of the most successful and environmentally friendly means of control is called the Sterile Insect Technique (SIT). This technique begins with mass-rearing of the insect in huge factories. Then the males are sterilized (so they cannot reproduce) and are released into the field where they will mate with the wild females. These mated females will not be able to lay fertile eggs in the fruit and so the number of flies in the next generation decreases. So SIT uses the pest as a type of its own “birth control” and reduces the use of harmful insecticides. By avoiding pesticide use, this method has the advantage of not targeting beneficial insects such as native bees.

For SIT to be effective, we need factory-produced males to be attractive to wild females and to successfully prevent the females from mating with other wild males that may be around. In my lab we are trying to understand how males that mate with females can cause the females to not mate with other males, and this has led us to studying the male ejaculate. It turns out that when males mate, they transfer to the female not just sperm, but a whole lot of other substances from the male accessory glands (MAGs). In many insects, these glands contain proteins that act as anti-aphrodisiacs, so that when females receive them after mating, they will not remate. The gland contents also stimulate the female of other species into laying more eggs. These are all very important behaviours when it comes to pests, as we do not want them to lay fertile eggs or mate again. The Mexican fruit fly has very complex male accessory glands, thus we are trying to find out what effect they have on the females. By injecting the contents of the MAGs into females, we observed that, contrary to what happens in other insects, they did not increase egg laying. So, the question still remains as to what the functions of Mexican fruit fly MAGs are.

Next, as the MAG contents do not increase egg laying, we wanted to find out about the whole ejaculate (MAG contents and sperm plus other components). Thus, we proceeded to cut the tip of the male penis (don´t worry they could still mate), so that they could not transfer any of their ejaculate. Surprisingly, we found that females that mated with these partially castrated males laid more eggs compared to virgin females that did not mate. This means that the internal and external aspects of the male copulatory courtship behavior that females receive during the mating is enough to stimulate them to lay eggs.

These results are important for two reasons: 1) studying MAGs can help us better develop control measures for these pests, with a better understanding on how mating affects female behaviour, and 2) we still know little about how various stimuli during mating affect female reproduction. As these are pests of economic importance to fruit growers, this knowledge will help us to further improve an environmentally friendly means of control.

–Diana Perez-Staples