The Dark Side of Love
Love isn't all rainbows and butterflies. Sure, in the beginning, everything is great. Everyone knows the age-old story: boy meets girl, boy courts girl, and if girl accepts then boy mates with girl. Life is good. Unfortunately, this honeymoon stage doesn't endure. Initially, the interests of the sexes are aligned because mating benefits both males and females. From an evolutionary perspective, these benefits are expressed in terms of number and quality of offspring produced. The name of the game is passing on genes to the next generation, and "success" is measured in offspring number. In this way, sexual reproduction is cooperation between males and females. Everyone is happy...until they are not.
After mating, things change. Conflict of interest arises when either the male or the female attempts to maximize their own reproductive success at the expense of the other- the schism in the once harmonious relationship. For example, one way for both sexes to potentially increase the quantity and/or quality of offspring they produce is to mate with other partners. However, as females produce a limited number of eggs, remating almost always results in a reduction in the number of offspring fathered by the first male in favour of the next male. Thus, female remating behaviour is under conflict as it would benefit the female but at a large cost to her previous male mate.
Sexual conflict theory suggests that males should develop tactics, which decreases the chances of their mates to commit infidelities thereby increasing the chances that they will produce their offspring. There are various examples of how males restrict the reproductive behaviour of the females they mated with, ranging from intensive physical guarding to the more hands-off approach of installing a mating plug within the female reproductive tract to block mating with a future mate. In some insect species, males use "chemical warfare" by transferring chemicals, called pheromones, to the female during copulation making her less attractive, and thus less likely to remate. Sexual conflict theory, however, also predicts that females should develop counter-tactics, for example removing the anti-aphrodisiac pheromones, to increase their post-mating attractiveness and increasing their chances of taking on new mates. Shockingly, no female mechanism of this sort has been identified; and so we decided to investigate it.
Chemical mate-guarding is arguably best understood in the fruit fly Drosophila melanogaster. That's right: attraction, sex, control, betrayal and infidelity are just a typical day in the love life of fruit flies. Males of this species produce at least two anti-aphrodisiac pheromones, which are transferred during mating and are found on the female directly after mating. One, 7-Tricosene a.k.a. 7-T, is produced on the outside of the male body, and is rubbed onto the female during the act. The other, cis-vaccenyl acetate a.k.a. cVA, is produced inside the male reproductive tract and is transferred to the female reproductive tract along with sperm. A recently mated female that receives both of these chemicals becomes less attractive.
We wondered, first, why are there two anti-aphrodisiac pheromones and not just one? Second, can the female remove them? And third, does removal result in increased attractiveness?
To tackle the first question we performed a series of experiments by which females with varying amounts of either one or both pheromones were presented to a male and his courtship was observed. We found that neither chemical alone caused a decrease in female attractiveness, but together they caused males to reduce their courtship behaviour. This suggest that the two chemicals interact together to decrease a female's post-mating attractiveness. This also suggests that if females are capable of removing at least one of the chemicals then they could potentially disrupt this relationship and increase their attractiveness.
Female fruit flies normally remove unused portions of the ejaculate from their reproductive tract a few hours after mating, termed sperm ejection. Since cVA is transferred alongside sperm we wondered if sperm ejection also removes cVA. By performing chemical analysis on virgin, recently mated, and recently mated but ejected females, as well as the "sperm mass" ejected from the female reproductive tract we found that females remove the cVA they gain during mating via sperm ejection. Interestingly, we found that after ejection, females regain their attractiveness and go on to not only to be more attractive but are more likely to remate than females that have not yet ejected. Finally, as we and others have determined that the timing of sperm ejection involves the female brain, the removal of cVA is likely an active process by which females control when they eject and therefore control their attractiveness.
The results from our experiments have illustrated two important principles. First, although males have evolved a mechanism to reduce female attractiveness, benefiting his own reproductive success, female behaviour can influence the effect or influence of these reproductive restrictions. And second, whoever said the way to a man's heart is through his stomach was wrong: it's through his nose.
Laturney M., Billeter J. Drosophila melanogaster females restore their attractiveness after mating by removing male anti-aphrodisiac pheromones. Nature Communications. 2016; 7:12322. doi:10.1038/ncomms12322.
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