Insect love potion: the anti-anti-aphrodisiac

Some insect species are “polyandrous” - that means they mate more than once and with multiple males. But if a female has already recently mated it’s in no one’s interest for her to mate again too soon, because sperm from different males would end up competing. So western tarnished plant bug males - and these are pests that devour strawberries and cotton crops - also transfer to the females when they mate anti-aphrodisiac chemicals. One is myristyl acetate and another is geranyl geranyl acetate. These temporarily warn other males to steer clear. But now Colin Brent has found that the females use an anti- anti-aphrodisiac to neutralise the effect so that they don’t end up off-limits for too long. Chris Smith hears how it works...

Colin: The male has this very large accessory glands within its abdomen. They're each about the same size of the gut within those abdomens. So they're very substantial organs and they transfer a lot of constituents into the female during mating. And then these are slowly released into the female or externalised from the female and so, some of these chemicals control her behaviour. They’ll actually reduce her interest in re-mating and other chemicals are being volatilised out into the world and new males will come along and attempt to court that female but if they detect the presence of some of these odours and particularly myristyl acetate, it serves as an anti-aphrodisiac. The males quickly lose any interest in courting those females.

Chris: Is the reason for that, that were they to court those females, their sperm would end up in competition with whoever has already mated with that female, but also, it would impair the ability of the female to get on with the job of laying fertilised eggs?

Colin: Yes. So, it negatively impacts both the female and the male, but it also has a positive impact. So, the males benefit by not wasting a tremendous amount of time trying to court a female which will quite likely not be receptive to their advances. Once a female has mated, there's usually a period of several days where she loses all interest in mating while she’s busy trying to ovi-posit. So if a male is constantly clinging along, harassing her, she loses out on opportunities to deposit her eggs. And also, the enhanced activity around that female heightens the chances that predators will notice her; the same thing for the males. So it’s to their mutual benefit to have a signalling system that says, “this isn’t really a viable mating opportunity.”

Chris: Equally though and I can see the merit in that, is there not a danger that the males could over supply some of these anti-aphrodisiac chemicals so that the female loses interest but actually regains her ability to reproduce again before she regains her interest. And therefore, a mating and a reproductive opportunity is potentially lost.

Colin: Yes and that was one of the questions that sort of drove this research in addition to trying to find mechanisms that we can use against these pest populations. We were interested in why this chemical system would evolve this particular way. If a male is recently mated, he’ll actually transfer relatively little of this anti-aphrodisiac to the female so she’ll become essentially attractive again to courting males, well before the time when she wants to be courted. On the other hand, if a male hasn’t mated in a long time has built up a great reserve of these anti-aphrodisiacs and transfers that to the female, she may have her capability of reproducing again or mating again, masked by this excessive quantity of anti-aphrodisiac. So it would behove them to have a signalling system that wasn’t just sort of a one-note system that basically was “yes” or “no”, and having a quantity that varied from animal to animal. It basically makes it unpredictable and unusable.

Chris: Is that what they’ve got? Is that what you found?

Colin: No. In fact, what we found was that the female takes one of the chemicals delivered by the male, geranyl geranyl acetate and converts it over to a third chemical geranyl geraniol. This geranyl geraniol can actually serve to counteract the anti-aphrodisiac effect. So it’s a chemical that’s converted over the course of time. There's more and more of this geranyl geraniol and decreasing amounts of geranyl geranyl acetate and slowly decreasing amounts of myristyl acetate, and that geranyl geraniol actually counteracts the negative effects on the female’s attractiveness. We can topically apply a mixture of these chemicals to the female and render her attractive or unattractive depending on what ratios we use.

Chris: So summarising that then, the male puts into the female myristyl acetate and that’s an anti-aphrodisiac. He also transfers geranyl geranyl acetate, and that, together with the myristyl acetate is an anti-aphrodisiac. But at the same time, that geranyl geranyl acetate is being converted into geranyl geraniol and that actually kills off some of the anti-aphrodisiac effect. So you must therefore have an anti-anti-aphrodisiac effect. Is that reasonable to say?

Colin: Yes, it is. So essentially, instead of having a system in which the absolute quantity determines how males will respond to the female’s odour, you have a system in which there's greater balance where the proportion of one is going to be dictated by the proportion of the other. And it’s measuring the relative proportions that gives the males a greater ability to accurately assess the female’s reproductive state.

Chris: Is this exclusive to this particular group of insects or do you think other polyandrous insects that mate with multiple male partners, do you think they're using a similar or even the same chemicals?

Colin: We’ve looked at a number of different species and we found that there are several that have these anti-aphrodisiacs. This is the first instance in which we’ve actually found an anti-anti-aphrodisiac. There is evidence in Drosophila – the fruit fly – that the females will actively expel the anti-aphrodisiacs that the males are delivering to them during mating. And so at least, that one species has this active process of countering the negative impacts that the males are having from this passive mate guarding system. I suspect however that because we didn’t know to look for it before that if we were to actually go through and examine a number of these species where anti-aphrodisiacs have been found, we very well may find that other chemical anti-anti-aphrodisiacs exist.