Sunday, 14 August 2011

Sex Without Pregnancy: how female macaques get what they want

Tibetan macaque (Macaca thibetana)
The females of most mammal species have some means of signalling to males that they are sexually fertile, and able to become pregnant. There is often some sort of breeding season, timed so that birth is likely to happen at a point in the year when food is abundant - spring, the rainy season, or whatever. But the cycles of female hormones mean that the female is only actually capable of becoming pregnant for periods of a few days, or even hours, during that season. Essentially, she comes into heat, and the males get excited.

That's the usual pattern. But there are some mammals that don't seem to do this. While they may not bother to mate outside of a mating season, they don't seem to be indicating to males when, within that season, they are likely to become pregnant. But is that really the case?

Among Old World monkeys - the type of monkeys to which we ourselves are most closely related - the females are often sexually promiscuous, mating with a number of different males. Although, in general, it tends to be males that sleep around, so that they can have as many children as possible, that's not relevant to females, who can have only one child (or litter) at a time. There are, however, some possible benefits for female promiscuity, which I have alluded to before, when discussing the common yellow-toothed cavy.

By mating with lots of males, you can increase the chance that the fittest one becomes the father of your children, whether that fitness is indicated by physical bulk or, as in the case of those cavies, sexual prowess. Even so, while they may want to give others a chance, just in case, female Old World monkeys normally have some way of indicating when they are most likely to become pregnant, allowing the largest male to drive off rivals around that time. For example, they may make specific calls, or have visible genital swellings during their peak of fertility.

The Assamese macaque (Macaca assamensis) is one of the exceptions - others include the Tibetan macaque, shown in the picture above. The macaques are a relatively large group of monkeys, found across southern and eastern Asia, and they include such well known species as the rhesus monkey. Perhaps more surprisingly, they also include the Barbary "ape" of north Africa and Gibraltar, although the Assamese macaque of south-east Asia is much more closely related to more typical species in southern India and China.

  Assamese         Rhesus       Lion-tailed
Macaque, etc.   Monkey, etc.   Macaque, etc.
     ^               ^               ^
     |               |               |        Barbary
     |               |               |        Macaque
     -----------------               |           |
             |                       |           |      Baboons,
             |                       |           |        etc.
             -------------------------           |         ^
                         |                       |         |
                         |                       |         |
                         -------------------------         |
                                     |                     |
                                 (Macaques)                |
                                     |                     |
                                     -----------------------
                                                |
                                                |

Over the last fifteen to twenty years, there has been some debate over the relationships among the twenty-two species of macaque. However, there does seem to be broad agreement that the Barbary macaque is out on its own (as might be expected, given that it's the only one not found in Asia), and that all the others fall into at least three general groups. I have used here the most up-to-date classification I could find.

The breeding season for Assamese macaques lasts a full four months, from mid October to mid February, resulting in the birth of a single infant after a pregnancy of around 164 days. Although the females do show some degree of genital swelling during the breeding season, this is not noticeably different when they are actually fertile than at any other time during the four month period. Since they don't seem to behave any differently during these times, there does not seem to be any obvious way for the males to tell when the females are fertile.

Of course, just because its not obvious to us, doesn't mean that it isn't obvious to the monkeys concerned. Perhaps, for example, they smell different, or there's something subtle in the way that they act which we humans have missed. Ines F├╝rtbauer and colleagues, of G├Âttingen University, recently published a study that took a closer look at the sex lives of female Assamese macaques to find out what they're really doing, and why.

They did this by watching the sexual activity of wild Assamese macaques in Thailand throughout their breeding season, and analysing their dung to find out when the females were fertile - a completely non-invasive way of assessing their hormonal status. Perhaps the first thing that was obvious was that the monkeys were mating quite a lot - pretty much every day, even assuming they never managed to hide from the researchers. Nor did the females much care who they mated with; on average each one mated with at least 80% of the available males at one time or another.

What's more, on a whopping 94% of occasions, the females mated when they were not fertile. Indeed, they carried on mating for at least two months after they became pregnant. Now, like other macaques, these monkeys have a strong social hierarchy, with a few powerful alpha males and a number of younger, smaller, subordinate males. Sometimes these alpha males would monopolise particular females for weeks at a time, protecting them as male mammals often do when they want to ensure any resulting child is going to be their own. The thing is, they were just as likely to do this whether or not the female was fertile, and whether or not they had even the slightest chance of getting her pregnant.

Which would suggest that they really didn't know.

So, if the females aren't giving their partners any clues as to when they're fertile, why not? The answer probably lies in an ugly fact of life as a monkey: infanticide. Dominant males, in particular, are quite likely to kill the offspring of other males to ensure that their own are the ones that survive to adulthood. But you can't do that if you don't know which ones they are. If you've mated with all of the females, and can't tell which ones you got pregnant, any child might be your own.

Infanticide is obviously bad news for the infant, but its also bad news for the mother, who invests a lot of time and energy in raising her young. So it may be in her interest to keep the males in the dark, and sexual promiscuity is one way to do that. That's not to say that there aren't advantages to monogamy too, or to mating only with the fittest and strongest males, but, in this species, that doesn't seem to be the way that the balance has swung. This would be an advantage if, for example, alpha males don't last very long so that they won't be much good at protecting you in the future.

However, while they would mate with just about any male, the females did seem to have preferred partners. That is, 30-40% of their matings would be with just one individual, even if they weren't exactly faithful to them. That these partners were as likely to be subordinate as alpha males would suggest that it's probably the females doing the choosing, although there's no way to know for sure. Again, if the alpha males don't last long, today's subordinate will be tomorrow's alpha, so you aren't necessarily losing much.

Indeed, there may well be some advantage to having a particular "boyfriend", even if you don't stay faithful. Humans, after all, tend to have a preferred partner, and to mate with them even when they won't get pregnant. Aside from the obvious, in evolutionary terms, this creates a social bond that comes in useful when you need to raise your children, and it may be that the Assamese macaques are doing something similar. There is some evidence that males help the females to raise their young, and a strong social bond, engendered at least partly through regular sex, may make them more likely to do that.

Besides, while you might not want to risk killing off the young of other females you've mated with, that of your own partner has at least a fair chance of being your own. If you're going to put any effort into being a father at all, you might as well do it for that one.

When we see rutting stags or powerful bull seals, it's easy to think that, at least among non-human mammals, male sexuality is all that really matters. But, for a number of species, females sexuality is at least as important, and they can use it to get exactly what they want.

[Picture from Wikimedia Commons. Cladogram adapted from Li et al, 2009.]

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