The great sperm race

A sperm's job is to fight it out with other sperm and take the ultimate prize, the egg. But competition in the mating game goes much further than that, says Simon Hadlington

Prudent ejaculation. Now there's a phrase to ponder. It would appear something of a contradiction, but scientists are discovering that both male and female animals are capable of subtle tricks in the mating game to increase the chances that only the fittest will thrive. And yes, prudent ejaculation is one such strategy.

The key to this particular aspect of Darwinian evolution is sperm competition: how the sex cells of several males slug it out within the reproductive tract of the female with whom all have mated. The winner takes the ultimate prize - fusion of sperm with egg and propagation of his genes for another generation.

Dr Matthew Gage, a Royal Society research fellow in the School of Biological Sciences at the University of East Anglia, is an expert in the rapidly advancing field of evolutionary biology. "Sperm competition is an area where all the forces that Darwin recognised are acting at a level that we did not previously appreciate," he says. "It had always been assumed that once a male had succeeded in mating with a female, the battle had largely been won. In fact, it is becoming clear that what goes on after mating has a big influence if females mate with more than one male."

Evolutionary biologists want to understand the mechanisms that underlie sperm competition: what makes a sperm more likely to succeed, how males allocate precious resources to producing sperm, and how females influence sperm competition. "These are areas of fundamental evolution and adaptation that have largely gone unrecognised in the past," Gage says.

First, it is necessary to understand how organisms evolved sexual reproduction in the first place. The current thinking runs along these lines. Asexual reproduction - where the mother cell produces daughter cells without any exchange of genetic material - is efficient but has pitfalls. Any genetic mutation in the mother will be passed straight to the daughter, and given that most mutations are deleterious, this could have poor consequences for future generations.

The beauty of sexual reproduction is that when the male and female sex cells - or gametes - fuse (creating a zygote), each brings something to the party. If one set of genes carries a disadvantageous mutation, it can be masked by the other set; there is more mixing of genetic material, increasing the chance of producing a new generation whose genetic make-up is more suited to its environment. Organisms taking genes from a wider pool through sexual reproduction can out-evolvesimpler clones.

So, in the primeval soup where life evolved, natural selection in theory should have favoured sexual reproduction. But how did the two sexes with two different gametes (a phenomenon called anisogamy) evolve? Why do males produce numerous tiny sperm and females produce a smaller number of large eggs?

"Before anisogamy, organisms would probably have produced 'proto-gametes' of a similar size," Gage says. "For sexual reproduction to occur, two gametes need to meet and fuse together to form the zygote. So there is a pressure to make as many gametes as possible to increase the chances of an encounter." But the zygote must be equipped with sufficient energy resources to enable it to grow after fertilisation. It must, fundamentally, be large.

So there are two opposing pressures: numerous gametes to maximise fusions, and large gametes to maximise zygote survival. These pressures led to the evolution of anisogamy, or sperm and eggs. On this principle, all males should produce as many sperm as possible, which would be as small as possible.

Up to a point. It is here that sperm competition begins to affect things. Many females receive the sperm of several males, and these sperm need to compete to fertilise the egg. And it is becoming clear that sperm competition is not discouraged by females. In several species, females have evolved mating patterns that receive sperm from more males than necessary simply for fertilisation. She is, in effect, saying: "May the best sperm win." Not only must the male win the right to mate with her, but its representatives in the reproductive tract, its sperm cells, must continue the competition.

Males are then forced to adapt their own reproductive apparatus. "Across mammals, birds, fishes and insects, we know that the level of sperm competition generated by females affects the size of the male testis and the volume of ejaculate," Gage says. "Like an arms race, sperm competition drives males to invest more in the tissue of their gonads and in the production of sperm." So the male must adapt to ensure that he invests wisely to ensure a maximum chance of success in the great sperm race.

It is here that prudent ejaculation makes an appearance. Gage's laboratory has examined how insects and other organisms modulate the amount of sperm they produce during mating, depending on whether they are competing with another male or not. "You mate males either in the presence or absence of a rival male, and after mating, count how many sperm have been deposited," he says. "When a rival is present, males produce about twice as much sperm as when they are alone. It looks as though males are sensitive to sperm competition and allocate sperm prudently."

One of Gage's colleagues, Nick Pound, has shown that lab rats allocate sperm depending on whether a rival is present. When a male is with a female and another male, and both males are allowed to mate, the males produces 40 per cent more sperm. Also, there is evidence that some invertebrates will ejaculate more sperm into larger - presumably more fertile - females.

Gage is currently interested in why sperm size varies so much across species. According to the anisogamy theory, it might be predicted that smaller, more numerous sperm are the way to successful sperm competition. Gage and his colleague Ted Morrow showed that a population of male crickets could be divided into those that produced shorter sperm cells and those that produced longer cells. Each population was allowed to mate with females to see which sperm would win the competition.

"On the face of it, you might expect the bigger, more powerful sperm to win, but we found completely the opposite," Gage says. "Males producing both more numerous and smaller sperm were more successful in mating. This provides quite nice evidence that sperm competition in this species selects for numerous, tiny sperm, rather than fewer larger sperm, and that sperm competition was partly responsible for the evolution of anisogamy, which is fundamental to all sexual species."

However, things are not quite so simple. Sperm size varies hugely across species. One type of fruit fly, for example, has sperm that are almost six centimetres long when uncoiled, sacrificing quantity for quality. Precisely why some animals produce very large sperm is a mystery. The most likely explanation is that it is a question of horses for courses: the competition the sperm encounters dictates the evolution of its form and function. In salmon, for example, sperm competition follows the scenario of a race where the fastest sperm win fertilisations. "Which is probably why salmon sperm swim very fast for a very short period and the whole thing is over in a matter of seconds," Gage says.

"In butterflies, by contrast, we know that the length of the female reproductive tract correlates with sperm size, so it looks as though females are setting out the playing field in which the males' sperm have to compete. If the female can use sperm competition success as a useful indicator of male quality, then it pays females to make the playing field very testing - to sort out the men from the boys, as it were."