Sunday, 12 August 2012

Mating in the Rain

Cairo spiny mouse, a related species
Humans have no defined breeding season, remaining sexually active throughout the year. This is relatively unusual among large mammal species, especially in temperate regions (although it's worth remembering that our species is originally from the tropics). That's at least partly because mating in humans also serves a social function, helping to bind individuals together. We see something very similar in bonobos, but most large mammal species do have a defined time of the year when the females come into heat, and mating begins.

The reason for this is to ensure that the young are born at an appropriate time of year, when food is most plentiful. That's particularly important in temperate regions, because there's inevitably going to be a shortage of food in the winter. However, the picture can become more blurred as we move towards the tropics, and when we look at smaller mammals.

The issue in the tropics is that there is no winter, and temperatures don't change radically throughout the year. However, due to the complex nature of climactic weather systems, even in the tropics, there is usually a rainy season and a dry season. While the jungles of Southeast Asia, for example, are never going to be as short on food in the dry season as Canada is in the depths of winter, there is still a notable difference. For example, flowers and fruit may be more available in the wet season, as may fresh growths of new plants. Even for carnivores, that's helpful, because the animals you're feeding on are plumper and more numerous when there's more tasty plants around. So, many species time their breeding so that births occur during the rainy season.

For smaller mammals, the issue can be that they don't tend to live very long. Since many don't live for more than a year or so (even if something doesn't eat them first), it can be important to breed whenever the opportunity arises, or miss your chance. That may well mean that the rainy season is the best time, and the fact that pregnancy is also very short in these animals does give them the advantage that they can tell immediately when the weather is suitable - if it's good now, it probably still will be by the time your young are born. However, it may also be that even brief spells of good weather might be adequate, or that, even if food isn't super-abundant, breeding now is better than waiting in the hope of it improving later.

We know quite a lot about the breeding habits of small mammals in temperate environments such as Europe and North America, and generally speaking, a fair amount about the breeding of large mammals across the world. Studies on small tropical or sub-tropical mammal, while not unknown, are less common.

The spiny mouse (Acomys spinosissimus) lives in eastern Africa, from northern South Africa to southern Tanzania, not far from the equator. It lives in rich savannah woodlands, sheltering in rocky outcrops or termite mounds close to rivers, and seems to mainly eat insects and other small invertebrates. It looks much like any other mouse, but, although it isn't truly spiny in the way that a hedgehog or porcupine is, it does have particularly stiff bristly hair over much of its body.

Unlike some other, very similar looking, 'mice', it is a true member of the mouse family - the largest of all mammalian families, with over 700 known species. Within that group, however, there is now fairly solid evidence that it is more related to gerbils than it is to familiar house mice. There are probably at least twenty species in the same genus as the spiny mouse, all of which tend to look very similar, and it is sometimes referred to as the 'South African spiny mouse' to distinguish it from these close relatives.

Spiny Mice     Link Rat     Brush-furred
    ^             |            Mice
    |             |              ^         Gerbils
    |             |              |            ^
    ---------------              |            |      'True' Mice
           |                     |            |        & Rats
           |                     |            |           ^
           -----------------------            |           |
                      |                       |           |
                      |                       |           |
                      -------------------------           |
                                  |                       |
                                  |                       |

The limited evidence available until recently suggested that spiny mice do have a distinct breeding season, timing their births to the rainy season, which broadly lasts through the southern hemisphere summer. However, given the sparse information, that doesn't necessarily reflect anything in the animal's biology. It could be that they can breed whenever they like, and simply do it more often when the weather is good. For example, a study on the four-striped grass mouse (a species of 'true', murine, mouse) in Cape Province, South Africa, showed exactly this. Crucially, the grass mice bred at different times of the year depending on how harsh the local winters were, and males, in particular, tried to breed all-year round, regardless of the weather, or of what the females thought of the matter.

Might spiny mice be the same? The first detailed study to look into this particular species was published in 2010, by Katarina Medger and co-workers. That looked at the females, determining, not only when they got pregnant, but at how their hormone levels varied throughout the year. The animals showed a distinct rise in progesterone between September and January, during the local rainy season. Progesterone is a female hormone produced when an animal ovulates, but normally drops again shortly afterwards. However, if she becomes pregnant, progesterone levels remain high until the birth.

Progesterone is responsible, among other things, for maintaining a thick lining to the womb, able to support and cushion growing young. The sudden fall in progesterone levels that occurs in the absence of pregnancy is the immediate cause of menstruation in primates (such as humans), although other mammals are generally less messy. High levels of progesterone suggest that the animal is sexually fertile, and ready to produce young; if progesterone levels are continuously low, the animal just can't get pregnant - she won't be producing any eggs at all.

So, this suggests that spiny mice are, indeed, truly seasonal breeders. They actually can't breed during the dry season, even if they want to. But that could be just due to the weather; when the mother is going hungry, her body shuts down the functions necessary for her to get pregnant, ensuring no expensive and unwanted young. But, as was noted in the four-striped grass mouse, the male might have different ideas, and be ready to mate whenever he gets the chance.

After all, while female mammals are only capable of getting pregnant when they are in heat, or otherwise at the fertile point in their cycle, males are able to produce fertile sperm constantly, which makes their perspective rather different. For that matter, at least in non-monogamous animals, it really makes no difference to the male if the female struggles to look after her young - he can just have another go with somebody else later.

So, in the second part of the study, published this year, the researchers looked at male spiny mice. Again, they looked at hormone levels, in this case, testosterone, and also at how the animals' anatomy changed through the year.

Because humans breed year round, and even when the female isn't fertile, the anatomy of our males doesn't change much with the seasons. This, however, is unusual for mammals. The production of sperm is not as taxing on a male as pregnancy is on a female, but it still uses up some calories you could be using for something else. Therefore, in mammals with a biologically enforced breeding season, the male often stops producing sperm at times of the year when he doesn't need it.

It's possible to see this by examining slices of tissue under the microscope, but it's often also apparent just be looking at the animal. In seasonally breeding mammals, the testicles shrink, often dramatically, outside the mating season. Often, they disappear into the animal's abdomen, so that a true scrotum is only present at certain times of the year.

 It turns our that this is exactly what we see in male spiny mice. Between September and January, when the females are fertile, the male's testicles are sixteen times larger than they are in March and April. Indeed, at their maximum, they accounted for over 1% of the male's total body mass, and were highly active producing sperm. If 1% doesn't sound much, consider that, for humans, that would be well over a pound for most of us!

So, male spiny mice time their reproductive fitness for the same parts of the year as the females do. But this is a study from only one part of the world. Since they are experiencing the same climate, might the sudden growth in testicular size also be due to the change in the weather? That's an improvement over the four-striped grass mice, but it might still be that male fertility is signalled by how much food they've been getting, rather than something deeper in their biology. If so, it would obviously be different in parts of the world where the climate is also different.

That may still be the case, but there is reason to suppose it's not what's going on in South Africa, where the study was performed. That's because of the way that the testosterone levels changed. Testosterone is the hormone generally responsible for male sexual activity, and has numerous other effects on the body, bulking up muscle and producing sperm. It doesn't change much through the year for humans, but it certainly does in animals with breeding seasons.

In the male spiny mice, testosterone levels began to rise, not in September, but two months earlier, in July. Examination of tissue samples showed that, at that time, it was already doing it's job of increasing sperm production. That's important, because it's still during the dry season - it can't be a signal to there suddenly being more food around, because there isn't. Instead, the male mice are getting themselves ready for the breeding season to come, ensuring that their testicles are bulked up and their sperm is ready to go as soon as the females are ready to mate.

There still has to be some sort of cue to start this off, and if it isn't the weather and food availability, it's probably the changing day length, with testosterone levels starting to rise as days start to lengthen just after the winter solstice. That may, of course, be different in those spiny mice living just south of the equator in Tanzania and Malawi, but, if studies on South African rodents are relatively uncommon, they are even more so elsewhere in Africa.

Nonetheless, from studies like this one, we can deduce that, even in the absence of a snowy, leafless winter, some animals still have strictly biological breeding seasons that suit their local climate.

[Picture by Olaf Leillinger, from Wikimedia Commons. Cladogram adapted from Steppan et al, 2004]

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