On the Many Routes to Reproductive Success

From The Economist:

“BE FRUITFUL and multiply, and fill the Earth.” Taken as an evolutionary imperative, that seems straightforward enough. But in reality, identifying the best way of doing it can be difficult, whether for individuals seeking romance, or scientists studying reproductive behaviour.

The scientists, at least, have made demonstrable progress. Two studies published this week—one by Jonathan Evans, of the University of Western Australia, the other by Tom Tregenza of the University of Exeter, in England—show that in fish and insects there is more than one path to mating success, and that the biggest, flashiest males do not always do better than their less assuming brethren.

In their quest for mates, some guppy males are show-offs. They conduct a decorous courtship in which they parade before their chosen belles. If a show-off’s performance is sufficiently intense, his colour dramatic enough and his fins suitably ornamental, the female will welcome his advances—which explains the evolution of lavish tail fins and vivid, iridescent colouration. Other guppies, though, cannot be bothered with all this flummery. Instead, they go in for a copulatory ambush known as “sneaking”.

That is great for the sneak. Why, though, allow yourself to be ambushed if you are a female? Why mate with a second-class beau who cannot be bothered to bring you the fishy equivalent of roses and diamonds? The answer, as Dr Evans shows in the Proceedings of the Royal Society, is that sneaks are first-class in one particular department. Their sperm are much stronger swimmers than those of the show-offs. The energy that male fish expend on courtship comes at the expense of their semen.

For guppies, having vigorous sperm is valuable because females conduct multiple trysts. Sperm from several males must therefore compete to fertilise an egg. Dr Evans’s research suggests that male guppies invest selectively in one of two different stages of the sexual competition. Some try to outcourt other males for access to females. Others try to outrace their rivals’ sperm. The two strategies remain in equilibrium because, if one became rarer compared with the other, its practitioners would enjoy more individual success, passing their genes on preferentially and thus restoring the balance. Assuming, of course, that a preference for one strategy rather than another is inherited.

So the last part of Dr Evans’s study was to test whether the two strategies are, indeed, inherited. He found that they are. The sons of fertile, sneaky fathers do share these paternal traits, while sons of attractive fathers are equally appealing, but have similarly impoverished ejaculate.

The hunk and the troubadour

Dr Tregenza’s study, published in Science, illuminates the similarly diverse mating strategies of crickets. Like guppies, male crickets compete for female favour—though by virtuoso chirping, rather than visual displays. But because previous systematic knowledge of cricket behaviour has come from studies done in the laboratory (studies, indeed, like Dr Evans’s), some researchers have questioned whether this sort of behaviour actually contributes to reproductive success in the wild.

To address that point, Dr Tregenza and his colleagues exposed a group of wild crickets to the Big Brother treatment. They trained video cameras on to 64 cricket burrows. They then captured, marked, released and tracked hundreds of crickets, and used the footage from the cameras to observe courtship, copulation, cohabitation and fights for dominance.

In a heroic act of enlightened voyeurism, Dr Tregenza’s colleague Rolando Rodríguez-Muñoz watched and analysed the resulting epic—all 250,000 hours of it. (He had the tapes on fast-forward and scanned 16 monitors at a time, looking for signs of movement that might indicate something interesting was going on.) By combining this video trove with data about each specimen’s physical characteristics, genetics and offspring, the team then identified those traits that contribute to crickets’ mating and reproductive success in the wild.

Their results did indeed reinforce the established beauty standards for male crickets—“be large and be loud”—but with a twist. What they actually found was, “be large or be loud”. Small males, in other words, could overcome the handicap of their stature and win mates through prodigious chirping. Larger males, by contrast, gained no additional mates through song. Like the guppies, then, different strokes were best for different folks. Moreover, being a dominant male brought no reproductive advantage. Subordinates sired the same number of offspring as dominants—a fact the researchers were able to confirm by genetic analysis.

Once again, it looks as though two male strategies may be in equilibrium: the hunk and the troubadour, perhaps. What is clear from both studies, though, is that no matter how hard males compete, they will always be outwitted by the wiliest, most subversive competitors of all: females.


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