How Mothers Stop Their Daughters from Sleeping Around

Northern mole-vole (E. talpinus)

Generally speaking, mammals are equally likely to be born as either males or females. The exact proportion may vary a little, and it doesn't follow that both sexes form 50% of the adult population, because one or the other may be more likely to die young. It's even less the case that all males, or all females, are equally likely to pair up and have offspring of their own.

This disparity is known as reproductive skew, and it varies considerably between species, and sometimes even between populations of the same species. At one extreme, it's essentially zero. This happens if the species is basically monogamous, usually because child rearing is a sufficiently draining exercise that being able to share the duties between two individuals is really helpful. It can also happen for what might be regarded as the exact opposite reason - if the species is highly promiscuous so that the females will mate with absolutely anyone, once again, everyone's chances of reproducing are the same. There's just less of that courtship stuff to worry about, off-set by having a single-parent family once you're done.

At the opposite end of the spectrum, reproductive skew is very high if one individual monopolises all the breeding. Usually, they're going to be the male, gathering a harem of females about themselves and preventing subordinate males from getting a look-in - and frequently killing their young if they ever do. But it may also be skewed towards a small number of females, and there are at least a couple of ways that this can happen.

In many species, such as various kinds of rodent, but also golden lion tamarins, dominant males hang about with a family group for long enough that, eventually, a number of their associates are, in fact, their own daughters. These are reluctant to mate with their father (or, indeed, brothers, if they're still around), but have no opportunity to mate with anyone else, so only the older females get to have children - until, of course, the male dies, a new one comes in, and suddenly lots of females become pregnant at once.

Alternatively, the species might be polyandrous (the opposite of "polygynous") so that one female mates with all the males, and somehow prevents others from doing the same. The most extreme example of this is thought to be among naked mole-rats, although there are others.

How do we tease these possible explanations apart? Let's look at one particular example that has been the subject of a recent paper on the subject: the Zaisan mole-vole (Ellobius tancrei).

This is an interesting animal for a number of reasons. It lives in semi-arid regions of central Asia, from Uzbekistan and Afghanistan in the west, through Kazakhstan and Mongolia, to north-eastern China in the east. As its name suggests, while it is, in fact, a vole, it spends most of its life underground, only coming out at night on the rare instances when it emerges at all. Like mole-rats, it burrows with its large teeth, using its claws for assistance, and pushing the loosened soil out of the way with its head. It feeds, as one might expect, primarily on roots, and constructs quite extensive burrows, with multiple chambers for food storage and sleeping.

Each burrow complex is home to  family of mole-voles, which may have anything up to twenty members - clearly, some of them must leave home at some point to establish new colonies, but the details are unclear, and some individuals remain with their parents for years. Crucially, most females living with their parents do not breed, leading to a strong reproductive skew. Those that do breed -  estimates range from around a quarter to just under a half of the female population - are typically thought to have multiple male partners as a consequence.

Much of this, of course, is immediately reminiscent of naked mole-rats, which are not all that closely related but have a similar lifestyle and an even stronger polyandrous reproductive skew. Is there something about this particular way of living that promotes this unusual reproductive pattern?

But, before I look at that, I should turn to something that's perhaps even more bizarre about the sexual biology of the Zaisan mole-vole: it doesn't have a Y-chromosome. While this is not unique among mammals, it is to say, the least, rather strange, and isn't something that's true even of most other mole-voles.

It should be noted that the Y-chromosome, as it is usually described, is something that is only found among mammals. Other animals either use different methods to determine biological sex, or have something that, for convenience, is generally called a Y-chromosome, but that actually has no relation to the structure found in mammals. But in mammals, individual genetic oddities aside, the rule for the vast majority of species is that females are XX, and males are XY.

Not so the Zaisan mole-vole, which only ever has two X-chromosomes (XX), regardless of whether it's male or female. Now, it has to be said that the Y-chromosome doesn't actually contain most of the instructions for making an individual male, which lie elsewhere in the genome. What it does have (and I'm simplifying here) is the master switch that turns those instructions on. By default, mammalian embryos develop into females, but if that switch is present and working, they become male instead.

In Zaisan mole-voles that switch isn't hiding somewhere else on the genome, it's just not there at all. Even the regular instructions for making testes and so forth have a normally vital bit missing, and this may have something to do with what's going on. But, as today's current knowledge stands, we have absolutely no idea what determines whether a Zaisan mole-vole is born male or female.

But back to reproductive skew. To try and figure out what was going on, the researchers took mole-voles that had recently been weaned, and raised them either with their mother, or on their own. They then introduced these pairs or individuals to an unfamiliar, and unrelated male, and waited to see what happened. If dominant females somehow prevent subordinates from breeding, we should expect that the older mole-vole in the mother/daughter pairings to get pregnant, while the younger did not.

Ant that is essentially what happened; the mothers got pregnant again, while their virgin daughters mostly stayed that way. But it can't have been age alone that was the difference, because younger mole-voles did get pregnant if their mother wasn't around to stop them. The question, of course, is how the mother is actually doing this.

One explanation may be provided by the fact that, in two out of the eight mother-daughter pairings, the daughter turned up dead within a week of the pair meeting the male. In both cases, they showed signs of injury that suggested they had been on the losing end of a fight. Their autopsies demonstrated that they were still virgins when they died, but it would seem that their mothers were taking no chances and wanted to keep the male for themselves.

Indeed, even where the daughter did survive long enough for the mother to get pregnant, she often died later on. In these cases, there was no sign of violence on the bodies, but there was evidence that they had mated, but had failed to become pregnant. This likely rules out the possibility that males simply prefer sexually experienced partners, and ignore virginal females when they have an alternative. But it does suggest that dominant females may have more subtle means that mere violence to prevent younger competition from breeding.

It's probable that, in the wild, when daughters get frustrated by their mothers in this way, they either put up with it, or leave. In the captive situation of the experiment, sadly, the latter was not an option, and those who really wanted to leave home died as a result. Even then, it's worth noting that the virginal daughters introduced to a male without their mother being present took several more days to eventually mate, perhaps just due to inexperience on their part, but possibly also because the male was waiting in the hope that a partner with more experience of successfully rearing children turned up. In the wild, this, too, would presumably lead to older females having an advantage, and being the ones more likely to give birth before the short breeding/birthing season was over.

This is not, it should be noted, normal for all voles, even if they do live communally. Common voles (Microtus arvalis), for example, are perfectly capable of rearing children from multiple parents at the same time in the same colony. And they certainly don't go around killing their own daughters just to increase their own chance of mating again - the level of violence shown in this experiment was unexpected, and, now that we know about it, might limit the chances of it being repeated as is.

But common voles, of course, don't spend their lives underground. It could be that living in constrained subterranean colonies increases the risk of inbreeding, and that mothers are reluctant to share sexual partners with their daughters, because then their respective children will be too closely related. Better for the daughters, when they really want to mate, to leave home and raise their own children somewhere else entirely.

It may be the only way, if your mother is really going to be that overbearing.

[Photo by Mikhail Kolesnikov and Marina Korobchenko, from Wikimedia Commons.]