Australasian Science Magazine

Female Lake Eyre dragon lizards will flip over onto their backs to prevent males from mounting them.

By Devi Stuart-Fox

So much of our obsession with sex revolves around how to get it, and how often, but the females of many animal species have evolved remarkable adaptations to avoid it. Why?

In the animal world, females can go to impressive lengths to avoid sex. The explanation lies in a conflict of interest between males and females over how often to mate.

In general, males pass on more of their genes if they mate with as many different partners as possible, but that’s not the case for females, whose eggs are finite in number. This “battle of the sexes” over the frequency of mating has led to some remarkable male strategies to get sex – and female counter-strategies to avoid it.

Contrary to early beliefs, the females of many species benefit from mating with several different males. Even females in apparently monogamous partnerships may solicit covert sex with other males. Australian fairy wrens are the kings and queens of infidelity, with up to three-quarters of a female’s chicks fathered by a male who is not her social partner. In species that form pair bonds, infidelity is often rampant – and in species that don’t form pair bonds, mating with multiple partners tends to be the rule rather than the exception.

Females clearly don’t try to avoid sex altogether, but they do generally mate the minimum number of times necessary to fertilise all their eggs or to gain other benefits. For instance, many female insects mate with multiple males because the males bribe them with nutritious food or other gifts. Females may also gain genetic benefits for their offspring. By mating with additional males, they can ensure the best possible genetic father for at least some of their offspring.

Alternatively females may be employing a form of genetic “bet-hedging”. If offspring are genetically diverse, at least some are likely to survive in an unpredictable environment.

Given the benefits, why would females mate less often than males? The reason is that mating is often dangerous, especially for females.

The Cost of Sex

For the females of some species, sex isn’t fun or easy – it can be downright life-threatening. In the fighting frenzy of Australian Dawson’s bees over access to emerging females, the males bite each other to death until there’s ‘“one bee left standing” – and the females sometimes become collateral damage. Similarly, female northern elephant seals are sometimes inadvertently crushed to death by fighting males, which are more than three times their size.

The females of some species are even harmed directly during mating. Male bed-bugs pierce the body wall of females with a special needle-like structure, injecting sperm directly into the body cavity rather than into the reproductive tract. This is termed “traumatic insemination”. Likewise, giant squid inject sperm directly into the female’s tissue, anywhere on her body. The females are literally wounded in the process.

In other species, males benefit at the expense of females. The seminal fluid of various insects contains substances that harm sperm from other males, reduce the likelihood that females will mate again, or induce females to lay more often. Several studies have shown that females exposed to these substances die younger.

Female suffering is not confined to the act of mating. In some species, sexual harassment is rampant. Males may harass females until they mate, or punish females that persistently refuse to mate.

Females Retaliate

As in any arms race, females have evolved counter-strategies to reduce the costs of sex. To resist unwanted matings, females may employ a variety of strategies ranging from simply running away to vigorous pre-mating struggles, warning signals and specialised body parts.

A curious example is the Lake Eyre dragon lizard, which lives only on the barren salt crusts of dry lakes in Australia’s arid interior. During the breeding season, males persistently harass females and bite the female’s neck during mating, which can cause injury and even death. Females try to run away or aggressively display to harassing males but, as a last resort, flip over onto their backs (see image). Although it seems counter-intuitive that a female should flip over to avoid sex, this position prevents mating, which can only occur when males are mounted on the female’s back.

Female counter-strategies don’t just involve avoidance of males – they can literally involve armour. Female bed bugs have a specialised structure on their abdomen, the spermelage, through which males must pierce to inject sperm. The spermelage contains a high concentration of haemocytes, which are critical in their immunological defence against pathogens. In other words, females have special armour to minimise disease transfer from “shared needles” during traumatic insemination.

Water-striders or pond skaters may seem like gentle creatures, gracefully skating across the surface of ponds and rivers, but their peaceful appearance belies some combative mating rituals. Males and females engage in violent pre-mating struggles in which the female tries to dislodge the male by repeatedly doing backwards somersaults while the male desperately tries to hang on. Males have evolved special elongated clasping genitalia to help grip the female, while females have evolved abdominal spines to make hanging on more difficult. These “claspers” and “anti-claspers” have become so elaborate in some species that water-striders have come to epitomise the battle of the sexes to evolutionary biologists.

Rejecting male advances can be hard work for females, and come at a cost. The costs are many and varied, including the energy demands of vigorous struggles (such as the repeated backwards somersaults of water-striders), potential injury, and increased risk of being attacked by a predator.

We might assume that there’s a simple economic equation where the costs of accepting a mating must be greater than the cost of rejecting it, but nature is never that simple. For example, it may be that a single act of resistance serves as a deterrent to other males, reducing future harassment. We do not know how the equation balances, or even if it balances at all.

Sometimes, females seem to accept many more copulations than might be optimal. In some situations, such as an extreme excess of males, it becomes simply too hard to keep resisting. In other situations, females may allow extra copulations to avoid punishment or to gain protection from males who guard their mates from other males.

For example, in social primates that live in groups containing several males (including chimpanzees, baboons and gorillas), males often hit or bite females that refuse to mate or that consort with other males. Females that are persistently intimidated or punished by aggressive males will often mate with that male more frequently – even though she avoids him if given the choice.

Playing Hard to Get – Can It Pay Off?

Apart from avoiding the dangers of mating, an intriguing possibility is that playing “hard to get” benefits females in other ways. Could female rejection of male advances be one way to screen males – a form of indirect mate choice?

By rejecting most males, females may choose only the largest or most persistent males. Females could benefit because they pass on the genes of these males to their offspring. Larger or more persistent males may be “higher quality” due to their “good genes”, or sons may inherit persistence from their fathers, which will give them a future advantage in securing mates.

The yellow dung fly, ubiquitous and abundant on cow and horse pats in the northern hemisphere, have become a model system for studying mating interactions. Female dung flies vigorously shake mounted males to attempt to dislodge them. Shaking off males serves two purposes: it prevents mating when females are unwilling to mate with any male, but when females do need to mate it allows them to choose the biggest and strongest males, who are the only ones that can manage to hang on. In yellow dung flies, female resistance pays off.

Sperm-Storing Females

Rejecting males can be hard work for females, but courting of females is hard work for males too. A phenomenon that has puzzled evolutionary biologists is persistent male harassment of females when they are not sexually receptive. If females are not receptive they are not ready to produce fertile eggs, so why would males waste time and a great deal of effort persistently courting and harassing unreceptive females – and even forcing copulations? This is a particularly pertinent question given that females are generally sexually receptive for relatively brief periods.

The answer could lie in the ability of the females of many species to store sperm. Although his sperm cannot be used to fertilise eggs straight away, a male could father a female’s offspring if she uses stored sperm. Hence for males it may be worth trying, and trying again, regardless of female receptivity.

Even if females use stored sperm, perhaps they are more likely to use “fresher” sperm from males they mate with when receptive. Could females control which sperm they use to father their offspring? Mounting evidence suggests that they can in a wide range of animals – from moths to lizards. For example, females of the humble yellow dung fly produce a kind of spermicide to selectively kill the sperm of some males.

If females can determine which sperm they use to fertilise their eggs, could this be one more way of fighting back? Could they reject the sperm from more coercive males?

If so, the battle of the sexes continues to be played out in the reproductive tract of females, long after the memory of mating has passed.

Conclusion

In sexually reproducing animals, sex shapes the course of evolution. Evolutionary biologists must tackle a number of fundamental questions about sex. What is the optimal mating frequency for males and females? What happens when they differ? Can conflicts of interest between the sexes ultimately lead to the generation of new species?

Understanding some of the remarkable ways in which animals try to obtain or avoid sex can give us insight into these questions and help us to understand the bizarre and beautiful natural world of which we are a part.