Sunday 27 May 2012

Being a Little Bit Pregnant

Sun bear
In my ongoing series on the members of the weasel family, I have, on a number of occasions, referred to the concept of delayed implantation. A number of members of the weasel family exhibit this phenomenon, and they are far from alone among mammals.

To begin with, the egg cell starts to divide immediately after fertilisation. In most mammals, it then rapidly forms into a hollow ball of cells that move down through the reproductive tract into the womb. During this time, it really doesn't change much in size; the ball of cells, known as a blastocyst, is not much larger than the unfertilised egg, and the individual cells within it are much smaller.

Once it reaches the womb, the blastocyst attaches itself to the uterine lining and begins to send out tiny tendrils of cells that penetrate the wall in search of blood vessels. Once it finds them, the embryo can obtain nutrients from the mother, and starts to grow and develop. The side of the structure in contact with the uterine lining develops into the placenta, while the remainder forms the embryo proper, and the amniotic membranes surrounding it. This even occurs in marsupials, although, in their case, the placenta is primitive and short-lived, and, for that matter, there's something similar in some reptiles, such as sea snakes.

The process by which the blastocyst attaches to the lining of the womb is called implantation, and it's obviously a vital step in the development of the young - a number of pregnancies never get this far, and because the embryo is still microscopic at this stage, the mother will never even be aware that she has conceived if implantation fails.

In humans, implantation occurs about nine days after conception, and the story is generally not that different in other mammalian species. But, in some species, the blastocyst remains in the womb for an extended period, and does not attach itself to the wall - this is 'delayed implantation'. Unable to derive much in the way of nutrients, the blastocyst stops developing, and remains little more than a hollow ball of cells for weeks or months until implantation finally occurs and the regular pregnancy can begin.

There are generally two reasons why this can happen. In the case of seals and their relatives, the animals spend almost their entire lives at sea, coming ashore only to breed and to give birth. In order to avoid having to come ashore twice every year, mating occurs almost immediately after the young are born, so that the two events occur close together. In order for that to work, though, pregnancy has to last just under one year - regardless of the size of the species concerned, or any other factors that might otherwise affect it. Even in the largest of seals, it just doesn't take that long for an embryo to grow to term, so implantation is delayed for just long enough to get the timing right.

In other mammals, delayed implantation is usually associated with an environment where food is very scarce at certain times of the year, whether it be a dry season or a snowy winter. It often makes sense for breeding to occur when food is relatively plentiful, so that the animal doesn't have to spend too much time looking for it, and can concentrate on more important things. At the same time, it is useful for the young to be born when there is a lot of food around too, since they will be growing, and, initially, the mother needs to provide a lot of milk for them.

If the pregnancy is really short, as it is, for example, in mice, that may not be much of an issue, but in many mammals it's just long enough that, if they bred in the autumn, they would normally give birth in the dead of winter. Delayed implantation allows them to extend their pregnancy, so that the young can be born in the spring. This, for example, is what weasels do.

Those, at least, are the usual explanations. But there may be other advantages, too. Take bears, for example. It is generally said that all species of bear exhibit delayed implantation. In the case of the northern species - brown bears, polar bears, and the two species of black bear - breeding takes place in the late spring to early summer, followed by a lengthy period of delayed implantation. As winter approaches, the bears bulk up on food, putting on a considerable amount of fat, and then head of to a secluded den to hibernate. In fact, while they wake up to do it, the females give birth while they're hibernating, and the young cubs suckle from her as she snoozes, until the family is ready to emerge in the spring. Although they don't hibernate, and the period of delayed implantation appears to be somewhat shorter, the story is otherwise similar in pandas.

It has long been observed that, the fatter the mother is when she begins hibernation, not only the more likely is it that she will have cubs, but the larger they will be when they emerge in the spring. The obvious explanation for this is that larger mothers can give birth to larger cubs, and, perhaps more importantly, will be able to provide more milk for their young, allowing them to grow more rapidly, and thus be larger and fitter when it comes time for them to emerge from the den.

The obvious explanation is not always the correct one.

Charles Robbins of Washington State University, and colleagues, thought that there might be more to it than that, and that this might be related to another possible advantage of delayed implantation. The University has a number of brown bears (Ursus arctos) in captivity, making it possible to study them in a controlled environment, while allowing them access to a large exercise yard with grass and clover. In the study, each year for eleven years, the researchers put mated female bears on varying diets from August onwards, so that they could control how much weight they put on as they prepared for hibernation. Around late October, the bears stopped feeding and headed into their dens to hibernate and, eventually, to give birth.

The dens in question are artificial, and contain cameras and microphones, making it possible to monitor what happens inside. Since, much like human babies, newborn bear cubs do a lot of screaming, the researchers could work out, almost to the minute, exactly when they were born. Not long after, the mother rolls over onto her side, allowing the cubs to suckle, and goes back to sleep. However, bears don't sleep for the whole of their hibernation, so every now and then the mother took a wander outside for a short while, giving the researchers the opportunity to enter the den and weigh the cubs.

It wasn't possible to weigh the cubs at birth, because that would hardly be a good time to disturb the mother, but, by extrapolating backwards from the weights they did get, it was possible to determine that the cubs were usually all around the same weight at birth - around 650 grams (1.4 pounds). So larger mothers do not necessarily have larger cubs. However, over the following three months, the cubs of fatter mothers did, as expected, put on weight faster, presumably being able to obtain more, or higher quality, milk during this time.

It's worth noting here that what mattered was how fat the mothers were, not necessarily how heavy they were. A lot of the weight of a bear comes from muscle and bone, so a bear can be quite large without having to be fat. But what caused the cubs to put on weight was the mother's body fat content - the ursine equivalent of a BMI - not her size alone.

So fatter mothers can afford to divert more of their reserves to milk production, and their cubs grow faster as a result. Case closed? Well, no, because it turns out that the difference in growth rates of the cubs wasn't enough to explain why the ones with fatter mothers were so much larger when they emerged from the den. That's because the fattest mothers gave birth up to two weeks earlier than their slimmer counterparts - indeed, those on the strictest diets didn't give birth at all, even though they would have mated long before starting the diet. So the cubs of fat mothers aren't just larger when they emerge from the den because they have grown faster - although they have - but because they're older.

This illustrates an advantage to delayed implantation not suggested in early studies on the subject: the mother has more control over when she gives birth. Bears bulk up considerably before hibernation, eating as much as a third of their own body weight every day, but sometimes there just isn't that much food available. It's really to her advantage to give birth as soon as possible, because the larger the cubs are when they're weaned, the more likely they are to survive.

But, if the mother hasn't been able to eat as much as she'd like, she may not have the fat reserves to provide milk for an extended period. If she can actually control when implantation occurs, she can set the date when she gives birth to her own best advantage. Indeed, if she's really short on fat reserves, she can stop implantation altogether, and just not give birth. That way, she has the chance to mate again the following spring, and try again next winter, instead of waiting for a couple of years, as bears normally do. An animal with regular, timed, implantation can't do that, or at least, not so easily. Since bears mate long before they know how much food they're going to find in the autumn, the ability to do that is particularly useful.

At least, it is if you're going to hibernate. Black, brown, and polar bears do, but there are species that don't. Pandas live in a rather harsh environment and, like their kin, have a strict mating season and delayed implantation. The other three species of bear all live in the tropics, and don't have a well-defined mating season, although two of them do seem to be more likely to mate at certain times of the year than at others, and it's generally believed that they all exhibit delayed implantation.

But do they? The sun bear (Helarctos malayanus) is the smallest living species of bear, living in the lowland jungles of Southeast Asia, where the climate is more uniform than it is further north. They don't appear to have any fixed breeding season, or even any particular preference as to when to breed, so are they really the same as other bears in this respect, or are they the only exception?

Brown bear   Polar bear    Black bears    Sun bear
    |             |             ^            |
    |             |             |            |
    |             |             |            |     Sloth bear
    ---------------             --------------          |
           |                           |                |
           |                           |                |
           -----------------------------                |
                        |                               |
                        |                               |

Living where they do, and not being especially numerous, we know relatively little about sun bears in comparison to other kinds of bear. So a study by Cheryl Frederick of the University of Washington (now at Unity College), and colleagues, looked at the eighteen members of the Bornean subspecies of sun bear then held in zoos in the United States. The study, or at least that part of it so far published, primarily focussed on the hormonal status of the bears, which can give clues to the details of their pregnancy and breeding habits.

They confirmed, firstly, that sun bears do, indeed, seem to come into heat throughout the year, with no particular preference for timing. However, births were more likely in autumn and winter, which might suggest a previously unsuspected preference for certain times of year, perhaps to concentrate births during the fertile Bornean wet season. According to records, pregnancy lasted between 96 and 105 days, also in line with previous, anecdotal, evidence.

That's remarkably short, compared with the nine months or more that a brown bear spends pregnant. Although we have no way of knowing for sure, estimates based on the size of sun bears, among other factors, suggest that it should take around 90 days for the embryo to develop to term. Furthermore, analysis of the mother's hormone levels showed a spike, normally associated with implantation, from two weeks to a month after mating. All of which suggests that, unlike every other bear we know of, sun bears do not exhibit delayed implantation - presumably, it's just not necessary in their relatively stable tropical habitat.

Oddly, though, that same hormone spike also occurred on schedule even when bears in heat had not been observed mating. In some cases, its possible that they had just done it when nobody was watching, and later had an early miscarriage that couldn't be detected. But on three occasion, there had not even been any males around when the female was on heat, so she can't possibly have been pregnant.

Yet, their bodies awash with hormones, these unmated bears proceeded to act just as if they were pregnant, setting up dens, and, in one case, even going so far as to start lactating. This is the phenomenon of pseudopregnancy, where the female acts pregnant, even though she isn't, and it's also observed in other bears.

There's not really any point in it, especially in a bear that can breed any time of year, because it prevents them from coming back into heat again for a while. It's not that they need a breather, because sun bears are apparently able to breed again almost immediately after giving birth, although they usually only do so if they lose the cubs. Interestingly, other bears can't do this, presumably because it would throw off the timing of the birth by too much if they did.

So why does it happen? The authors suggest that there may be no real answer to that. Sun bears appear to have evolved from black bears in the relatively recent past (during the Pliocene, to be precise), and all of their other relatives show delayed implantation, so perhaps they did too. Pseudopregnancy isn't a big deal in such animals, because that's how the body is supposed to react during delayed implantation, long before the embryo can send back any signals to show that it's there. It's a consequence of their reproductive system, and, since they can't mate again until the following year anyway, it's not much of a problem when it does occur.

Bears, like most animals, are likely to mate if the opportunity presents itself, so pseudopregnancy is probably quite rare in the wild. Maybe it's rare enough that sun bears just never got rid of it, leaving an evolutionary relict of a time when their ancestors weren't so different from their kin.

[Picture by Peter Halasz from Wikimedia Commons. Cladogram adapted from Krause et al, 2008]

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