Saturday 26 March 2011

Churning out babies - pregnancy in the naked mole rat

By any standards, the naked mole rat (Heterocephalus glaber) has to be among the strangest of the placental mammals - and, to be honest, also one of the ugliest. It spends virtually its entire life underground, is hairless, apparently can't do the decent mammalian thing and control it's own body temperature, and may well be entirely blind. Perhaps even stranger, though, is its method of reproduction.

Remember the brown antechinus? Well, this is almost the exact opposite.

The mole rat family is itself a fairly strange group of animals, and actually more related to guinea pigs than they are to rats. The naked mole rat is almost certainly the best known member of the group, but there are several not-naked mole rats as well (I plan to discuss these in another post, coming up soon). In evolutionary terms, the naked species lies outside the main group, having diverged long before they did, and it's often given its own subfamily to highlight the differences between it and its furry kin.

Naked Mole      Other       Degus,       Guinea Pigs,
   Rat        Mole Rats      etc.           etc.
    |             ^            ^             ^
    |             |            |             |
    |             |            |             |
    ---------------            ---------------
           |                          |              Cane Rats,
           |                          |                 etc.
           ----------------------------                  ^
                       |                                 |
                       |                                 |

The naked mole rat lives in huge underground colonies, with anything up to 300 members, although around 80 is more common. What's particularly strange is that, out of all of the rats in the colony, only one of the females breeds. This, of course, is a pattern we often see in insects, with bees, ants, and termites all being good examples. In those insects, we have a single queen that lays all the eggs, tended to by hordes of sterile workers and a small number of reproductive males. Mammals don't work like that... but the naked mole rat comes remarkably close.

Just as with bees, all the breeding in a naked mole rat colony is performed by a single queen, and a slightly larger number of males. That the other males don't get a look in isn't so unusual; they have to wait until the dominant males die off, as happens with many other species of mammal. It's the fact that the other females don't reproduce, and are, effectively, sterile workers, that makes the naked mole rat so unusual. (Not absolutely unique, though, since at least one other mole rat species seems to do the same - it just hasn't been studied so thoroughly yet).

There are differences between naked mole rats and insects, of course. Most notably, the workers in insect colonies are permanently sterile, and completely incapable of breeding - the queen is born to her status. Among naked mole rats that isn't true, and any female can leave the colony to found her own, becoming fertile in the process. The same happens when an existing queen dies off, often after some vicious fighting between her potential replacements. Nonetheless, once fertile, the queen's appearance changes from that of her siblings. Her ovaries and uterus greatly enlarge as her body floods with the female hormone progesterone, and her back actually lengthens to accommodate her eventual pregnancy.

Pregnancy in naked mole rats is unusually long. It lasts 70 days, which may not sound like much, but is at least twice what you would expect compared with other rodents of similar size - they only weigh around 30 to 35 grams (just over one ounce). Small rodents generally breed rapidly, producing as many litters as possible in a short time, not least to compensate for the fact that a lot of them are going to get eaten. So why not this one? A recent study by Kathleen Roellig et al. may shed at least some light on what's going on.

The researchers established a captive colony of naked mole rats, and monitored the pregnancies of the queen, using ultrasound equipment much the same as that used for human pregnancies - albeit somewhat smaller. There are a couple of ways that mammals can extend their apparent period of pregnancy. Some, such as the silver-tipped myotis, seem to be able to store sperm in their reproductive tracts for a few months until the time is right to have children.

More common is delayed implantation, in which the egg is fertilised as normal, but, after dividing into a tiny ball of cells, then suddenly stops its development, and does nothing for a few months. Eventually, it attaches itself to the uterine wall, and begins to grow and develop again. This is especially useful to animals such as seals. Seals only come ashore to breed and give birth once a year, so their pregnancy has to last just under 12 months. Since it wouldn't take that long for a properly growing embryo to develop into a seal pup (seals, are, after all, not far off the size of a human) its obviously useful for that to be prolonged somehow. And, of course, it means they don't spend their entire adult life feeling the symptoms of pregnancy.

No such luck for the naked mole rat, though. In this study, once she'd settled down into the new colony, the queen rarely waited more than a couple of weeks after giving birth before getting pregnant again. The ultrasound showed that there was a delay in the womb, with implantation probably not happening until around the end of the second week, but that's not long enough to explain the whole of the longer pregnancy. From then on, the embryos kept growing.

We're talking quite a lot of embryos, too. On average, the queen gave birth to around eleven pups at a time, which is plenty, even for a rodent. But even that isn't really the full extent of her alteration into a baby-making machine. The first ultrasound scans were given at about 20 days, and, at that point, she had an average of just over thirteen embryos. On average, a couple of them died and disappeared before birth - assuming, of course, that none had already gone by 20 days. It's at least possible that this has something to do with being in captivity, but it might also be that naked mole rat queens can control the size of their litter. It could even be a bit of both - a tunnel system in a lab would naturally have a limited size, so having too many young would make things rather crowded.

On one occasion, the researchers took an infertile female away, and gave her her own colony. She developed into a queen, and became pregnant, but never gave birth. No miscarriages, either; the embryos just vanished (as they do if they die young enough). Of course, that could be due to illness of some kind, but it might be that she had the ability to cancel her own pregnancy if she didn't feel comfortable enough. A second attempt to found a new colony was more successful; although the two females placed in it fought viciously to the death, the survivor went on to become a queen and raise a litter of thirteen pups.

Like many other mammals, the young of many rodents are born relatively undeveloped - hairless, blind, and essentially helpless (quite unlike, for example, deer). Its hard to tell whether naked mole rats follow this pattern, since they're hairless and virtually blind even as adults, but they certainly aren't able to walk from birth, so greater development doesn't seem likely to be the whole story behind their longer pregnancy.

The researchers suggest that the real reason may be down the almost perpetual pregnancy required of an animal that's the sole source of babies for a colony. Because they mate again so soon after birth, if naked mole rats had a normal gestation period for their size, of around 30 days or so, their first batch of young would still be suckling when the second litter was born. Far better then, to have double-sized litters half as often, giving you enough time to raise them all, while still having the same number of children in the long run.

And how many children is that, anyway? The researchers also measured something called the "lifetime reproductive effort", which essentially compares the total mass of a female's offspring when they become independent with her own adult body mass. For most mammals, around 1.4 is quite normal, and its rarely higher than 2.2 in rodents. For the naked mole rat, the researchers calculated a value of - wait for it - 139.8.

That's what you get for being the only reproductive female in a colony of over a hundred adults.

[Picture from Wikimedia Commons. Cladogram adapted from Mikko's Phylogeny Archive and Deuve et al. 2008]

Sunday 20 March 2011

Why Are There Marsupials in America?

So, what exactly are marsupials?

If you answered "mammals where the female carries her young in a pouch," I'm afraid the big QI buzzer has just gone off. That's because, while its mostly true, there are, in fact, some marsupials that don't have pouches.

Along with the placental mammals, the marsupials represent one of the two main groups of mammals alive today - although there is of course, also a third, much smaller, group that includes the enigmatic platypus. The oldest known marsupial fossil, Sinodelphys, dates back to 125 million years ago, as does Eomaia, the oldest fossil on the line leading to placentals. Our best guess is that the two groups diverged not long before that, probably no more than 131 million years ago. But its worth pausing to consider how far back that is; its a little over half way through the age of dinosaurs, and long before such famous animals as Tyrannosaurus, Velociraptor, and Triceratops evolved. Indeed, its as far back from Tyrannosaurus as that animal is from us today - half the history of marsupial evolution occurred before dinosaurs went extinct.

Sunday 13 March 2011

How the horse began to run

Hyracotherium, a close relative of Arenahippus
One of the advantages of studying fossil mammals, compared with dinosaurs, is that there are many close parallels still alive today. There isn't anything remotely like a Tyrannosaurus stalking the plains of present-day Africa, but comparing sabre-tooth cats to animals such as tigers and leopards can tell us quite a lot, with rather less need for guesswork. Also, while complete mammal fossils are still quite rare, they are, nonetheless, more common than those of animals from the more distant past.

Still, when it comes to early mammals, complete skeletons are rare enough that finding one can provide a significant opportunity to learn more about them. Species are often described on the basis of their skulls alone, since skulls tend to be the most distinctive parts of the skeleton, and you can tell a lot just from that, but having the rest of the skeleton stll attached to the skull is obviously pretty useful.

A recent report in the Journal of Mammalian Evolution described a remarkably complete skeleton of the early horse Arenahippus, with the tail being almost the only part missing.

As a side note, exactly what this animal should be called is a matter of some controversy. When specimens of the species were first found, they were thought to belong to the genus Hyracotherium, which may (or may not) be an alternative name for Eohippus, the "dawn horse" that appears at the beginning of so many charts of the evolutionary history of horses you see in museums and the like. But its probably neither, so we'll stick with the name it was given in 2002, even though there are counter-arguments to that one, too.

At any rate, whatever its called, Arenahippus is one of the most primitive members of the horse family known. It lived in the early Eocene epoch, just ten million years after the extinction of the dinosaurs, when many of the modern groups of mammals were just getting started. We don't know that later horses evolved from it, because there were lots of species of early horse living alongside each other, and while one of them must have evolved into the later ones, there's no way to tell which it was - if its even we've found yet. Those step-wise evolutionary charts you see of horse evolution don't really show exactly what evolved from what, just general pictures of what horses at a particular point in time looked like.

In reality, like all evolutionary stories, that of horses is a branching tree, although its interesting to note that Arenahippus appears to branch off even before the more famous Eohippus did, putting it even closer to the origin of the horse family:

True Equines    Mesohippus     Eohippus
     ^              |             |
     |              |             |      Arenahippus
     |              |             |           |
     ----------------             |           |
            |                     |           |
         (3 toes)                 |           |
            |                     |           |
            -----------------------           |     Palaeotheres
                       |                      |          ^
                       |                      |          |
                       ------------------------          |
                                   |                     |
                            (First horses)               |
                                   |                     |

In fact, even the tree above is greatly simplified - there are a great many other fossils branching off in between the steps shown above. Nonetheless, we can see that Arenahippus diverged at a point when horses still had four toes on their front feet (although, like Eohippus, they only had three on the hind feet). In terms of its size, and to some extent, its shape, it looked more like a dog than like a modern horse.

So what can this new skeleton tell us about the life of these earliest horses? Perhaps the most obvious place to look is the legs, since the one-toed foot of modern horses is one of their most distinctive features. The tops of the thigh and upper foreleg bones are clearly rounded, with flexible hip and shoulder joints. This is quite different from modern horses, where the shape of the joints means that the limbs can only move forward and back, with very little flexibility in any other direction. The authors suggest that this would have helped in an environment more cluttered with bushes and other obstacles, rather than the open grassland that favours the gallop of modern horses. Since other evidence suggests that the area of Wyoming where the fossil was found was woodland with dense undergrowth, this makes sense.

Furthermore, the shape of the bones of the hind limb show the presence of powerful muscles, especially the calf muscle. Taking into account the shape of the knee and ankle joints, this indicates that the hind limbs would have been bent as the animal pushed itself forward and began to run - something you see in dogs, but not in horses, whose hind limbs are fairly stiff.

However, its not just the shape of the limbs that show us how the animal would have moved, but also the backbone. Reconstructions of early horses tend to show a straight backbone, as can be seen in the photograph at the top. This is how the backbone of modern horses look, and the way that the individual vertebrae lock together makes the whole structure quite rigid, a pattern also seen in other fast-running hooved animals, such as antelopes. But there haven't been many good fossils with intact backbones before, and, looking at this one, it seems the pattern isn't quite so simple.

Back flexed, legs pushing towards the midline
The vertebrae at the far end of the back, just before it joins the pelvis, were, indeed, rigid, with processes that would have locked them tightly together. But just before this was a more flexible region where the bones would have prevented the back from twisting, or from bending upwards, but would not have prevented it from bending downwards. Thus, unlike modern horses, Arenahippus could have arched its back, and most likely did so just as it began to run.

All in all, Arenahippus seems to have been a more flexible animal than a modern horse, or even than its more horse-like later relatives, such as Mesohippus. That may be partly because the later animals were bigger, and a more stable body would have made them more energy efficient while running. Arenahippus's movable knees, strong calf muscles, and flexible hips would have enabled it to push off the ground with some force, while the arching back ensured its centre of mass stayed in line. Still, it does seem to have been more rigid than, say, a modern dog and was, perhaps, just beginning on a path that would lead its later relatives (if not, necessarily, its literal descendants) to their fast-running lifestyle.

That leaves aside the question of why later horses became larger at all, requiring the change to the more familiar shape and posture we see today. That may be due to the changing climate of the time, and the spread of grasslands. Arenahippus, like other very early horses, mainly ate herbs, and perhaps fruit, browsing on low-lying vegetation, while later horses grazed on grasses. Grass is harder to digest than herbs, so that a longer digestive tract is needed if you're going to eat it. One way to increase the length of the digestive system is to increase the size of the animal its inside, and its at least possible that this was a major reason for the change. The more open environment of grasslands may also have meant that the longer stride that the size and body shape of later horses promotes would have been more useful for them than for something living among dense undergrowth.

[Pictures from Wikimedia Commons, cladogram adapted from Mikko's Phylogeny Archive]

Sunday 6 March 2011

Cultural Traditions of the Spider Monkey

One of the distinguishing features of humanity is the great cultural variation that we exhibit across the globe. The traditions and practices of, say, the Masai of Africa, are quite different from those of western Europeans. In animals, by contrast, behaviour tends to be firmly dictated by genetics. Even where there is clear learning, with mothers teaching their offspring to hunt, for example, the end results of that learning are often fairly similar across a given species.

But, as is so often the case, the dividing line between humans and our closest relatives is not so clear as that broad generalisation would imply. Traditions have been observed in other animals, even including some that aren't primates, such as dolphins and killer whales. When we talk about 'traditions' in these animals, we are referring to behaviours exhibited by some populations of a species that are, for no obvious reason, not seen among other populations. The behaviours are obviously not genetic, or everyone would perform them, but on the other hand, neither are they simply the result of some lucky discovery by a single individual that was never passed on to their peers.

Most research on such traditions has been carried out on chimpanzees, and has tended to focus on the way that they use tools. This has obvious relevance to our own origins, as well as having the advantage of being easily identifiable. Chimpanzees do seem to learn at least some of their behaviour by copying others in their local cultural environment, and this sort of learning may extend quite a way back in our evolutionary family tree, since such tool-using cultural traditions have also been seen in orangutans.

But tools do nor represent the entirety of culture. To look further back into the origins of traditions, it may be useful to look at our more distant relatives, and to consider behaviour that is more relevant to the way they live their lives. Geoffroy's spider monkey (Ateles geoffroyi) is native to the Americas, placing it firmly on a branch of monkey evolution entirely separate from that which eventually gave rise to humans in Africa. They appear to be remarkably intelligent animals - perhaps even more so than gorillas - but they don't have opposable thumbs, and since the main thing they want to do in life is pick fruit off trees, they really don't need much in the way of tools, anyway.

 Spider        Woolly      Howler
 monkeys       monkeys     monkeys
    ^             ^           ^
    |             |           |
    |             |           |      Other American
    ---------------           |         monkeys
           |                  |            ^
           |                  |            |
           --------------------            |       Apes & Old
                    |                      |      World monkeys
                    |                      |            ^
                    ------------------------            |
                               |                        |
                               |                        |

They also have a relatively unusual social structure among mammals. They live in groups, but individuals often wander about different groups, and the groups themselves are always merging and splitting. In contrast, most group-living mammals tend to stick to herds where the females stay with their relatives and the males wander off to find and dominate new groups elsewhere, and then stick with them. The more complex arrangement among spider monkeys means that it will be relatively common for individuals to encounter past 'friends' that they haven't seen in a long time, and perhaps to develop their own greeting rituals for that purpose. It's worth noting that, although they belong to a different part of the primate family tree, chimpanzees are among the few other mammals to live like this (along with humans, of course).

It can be difficult to demonstrate that particular behaviours are not genetic in origin, since even within a species, there could well be genetic differences we are not aware of. However, the usual way of looking for cultural traditions, as used for chimpanzees and orang utans, is to examine the behaviour of animals in different locations, and see how much it differs. This was recently performed for an array of 62 different types of behaviour in Geoffroy's spider monkeys in Costa Rica, Panama, Belize, and Mexico.

Most of the behaviours turned out not to fit the definition of a 'tradition'. Around 20 were performed by monkeys in all the study sites, making it difficult to rule out these being genetically programmed habits. Others were very rare, suggesting that even if one animal had learned that this was a useful thing to do, it never (or at least, hadn't yet) passed the information on to its fellows. For a few, there were obvious reasons why the behaviour couldn't be carried out just anywhere - for example, its difficult to eat the fruit of cohune palms if there aren't any where you live.

But that still left 22 behaviours that just didn't fit the obvious pattern. Some of these were related to the choice of foods. In two sites, almost all the monkeys were seen happily eating the fruit of the elephant ear tree (which, despite being a tree, is also a really big legume). Yet, in the others, they never touched the plant, apparently not realising it was edible, even though there were plenty around. One Costa Rican population had even figured out that they could eat mushrooms, something not normally associated with this fruit-eating species.

Other behaviours, however, were more complex. In some areas, monkeys would climb onto the shoulders of their fellows in piggy-back style in order to appear larger and more threatening to an intruder, while in others it never seemed to occur to them to do this. The monkeys in Panama were often seen to walk upright on their hind legs, something that the monkeys in Belize never did, and was quite rare elsewhere.

As predicted, many of these more social behaviours were related with greeting outsiders, perhaps to determine whether they were long lost friends who shared the same traditions. These included various forms of scent marking, and whether or not they rubbed fig roots on their bodies (presumably to give themselves a distinctive smell). Although all of the groups greeted outsiders in the usual manner for their species - which includes a lot of embracing each other - some of them also kissed each other lightly on the cheeks. Yet the Panamanian monkeys, while they would blow kisses at each other from a distance, never actually kissed each other directly.

The same Costa Rican population that ate mushrooms also had an unusual habit of sometimes climbing to the tops of tall trees and facing into the wind with their mouths open. Presumably this felt pleasant, and probably helped them cool down, but again, its significant that none of the monkeys elsewhere did this, despite the obvious opportunity to do so.

All in all, there was significant variation among the different populations in terms of which practices they performed and which they didn't. Every population had at least some unusual practice that at least one other didn't possess. It's hard, as I mentioned earlier, to be sure that none of these are due to some minor genetic difference, especially since the communities are isolated from each other by the increasing fragmentation of Central American jungles (which has led, sadly, to the species becoming endangered). But that also reduces the chance for cultural communication across large distances, allowing particular traditions to develop and survive in isolated areas. That there was no pattern to which behaviours were exhibited where also tends to count against the genetic theory. If that were the case, then, since one might expect monkeys closer together geographically to be more related, one would also expect them to have more habits in common, and they don't.

Culture and learning are things that humans have developed far beyond any other species on Earth. But we are not entirely separate from the rest of the animal kingdom. The brains of our closest relatives are not simply hard-wired with everything they need to know, and sometimes animals can discover a way of doing something that other members of their species elsewhere have not. When they do, at least some of the time, they can pass this information on to their relatives and neighbours, something that requires the sort of cognitive powers that we tend to think are purely human.

Humans are animals, and the line between us and 'them' is sometimes a very blurred one.

[Picture from Wikimedia Commons]