Fly vs. fly

July 29, 1999

Researchers at the University of Chicago have discovered two offensive mechanisms male fruit flies use to ensure that more of their genes get passed on to the next generation--displacement and incapacitation of a previous male's sperm.

In most insect species, the second male to copulate with a female sires most of her offspring. Scientists have long puzzled over this strange phenomenon, also seen in birds and some arachnids.

Female fruit flies mate with multiple males, storing the sperm in three specialized storage organs (the long, tubular seminal receptacle and two mushroom-shaped spermatheace) and using it as needed to fertilize eggs. However, the odds of becoming a father aren't equal for all the males. The last fruit fly to mate with the female tends to sire the most offspring.

"Not only are the flies in competition with each other to mate with a female, but their sperm are in competition to fertilize the eggs once inside the female," says Catherine Price, PhD, first author of the July 29, 1999 Nature paper. "This leads us to believe that the males have evolved mechanisms for encouraging females to use their sperm, and females may have evolved means of mediating competition between sperm from different males."

Price and Jerry Coyne, PhD, professor of ecology and evolution at the University of Chicago and an author of the paper, concentrated on mechanisms the male uses for ensuring paternity, focusing on the apparent displacement and incapacitation of stored sperm by the ejaculate of later-mating males.

The researchers obtained male fruit flies whose sperm had been labeled with green fluorescent protein (GFP), enabling them for the first time to distinguish first from second male sperm in the female's reproductive tract.

When they mated females to males with the GFP-labeled sperm, and then to males without the label, they counted far less fluorescent sperm in the seminal receptacle than if the female hadn't been re-mated.

"The first male's sperm seems to have been physically displaced here, but where it goes remains somewhat of a mystery," says Coyne. The displacement occurred shortly after mating, but only if the second male had viable sperm. Seminal fluid alone could not cause displacement of stored sperm.

Coyne and Price also noticed that the number of stored first male sperm used to fertilize eggs dropped considerably after the female was re-mated. This "sperm incapacitation" effect became much stronger as more time passed between the first and second matings.

When the second mating was allowed to take place two days after the first, the female produced less offspring using first male sperm because of its loss from the seminal receptacle. After seven days between matings, the loss of first male offspring is more severe, due to both incapacitation of first male sperm as well as displacement.

The researchers were able to rule out the possibility that all the first male's sperm had been used up by using males with GFP-labeled sperm for the first mating. "There were just as many first male sperm stored as we would expect after seven days," says Coyne. The same incapacitation effect was observed even when the second male delivered seminal fluid alone.

"As the sperm sit in the female's storage organs, they must undergo some change that makes them more susceptible to damage by something in the second male's seminal fluid."

"Previous research has shown that a fly can incapacitate and displace his own sperm if he mates with the same female twice. So we know that second male sperm precedence does not rest on a genetic difference between the sperm of the first and second male," says Coyne.

The evolutionary underpinnings of second male sperm precedence are still unclear, especially since the reproductive interests of the male and female are different. "It may be in the female's best interest to get rid of old sperm because it could get damaged if its stored for too long," says Price. But for the male, the truth is in the numbers. It is to his evolutionary advantage to fertilize as many eggs as possible and to prevent the fertilization of as many eggs as possible by his competitors. "The mystery is why the second male nearly always defeats the first male," Price says.

Some species have evolved infinitely more elaborate means of ousting sperm from the female than the fruit fly. In rove beetles, the male deposits a sperm packet that expands inside the female like a balloon, literally pushing the first male's sperm out. The female then uses a specialized tooth to pop the packet and release the new sperm. In crickets, any remaining first male sperm gets eaten before the female is inseminated again.

"Second male precedence is so common that we're really interested to learn that there are multiple complex mechanisms behind it, even within a single species," says Price. "By studying the balance between cooperation and antagonism between males and females, we may gain a greater understanding of what happens in a fertilized female."

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