Published online 17 March 2010 | Nature | doi:10.1038/news.2010.127

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Males show sexual selection before and after copulation.

Male pipefish are choosy mates — before and after copulation. N. Ratterman

In pipefish, pregnant males give birth to more young from attractive mates, new research shows.

Pipefish, sea horses, and sea dragons belong to a family in which the males get pregnant. In some of these species, the females court and compete for males. The pair then do a dance, which includes "twitching at each other and spiralling together, like a double helix", says lead author Kimberly Paczolt from Texas A&M University in College Station. As they spiral around each other, the female transfers the eggs into two rows along its mate's body. The male then fertilizes the eggs, and the brood pouch — which consists of two flaps — glues itself together in the middle. Weeks later, the seam breaks apart, tiny versions of the adults swim out, and the males are free to be impregnated again in as little as an hour.

The male's pouch protects the embryos and gives them oxygen and nutrients. But, Paczolt says, the male doesn't care for the babies with utter abandon. Rather, he tempers how much he invests in the eggs according to how large the female is.

Embryos develop in the pouches of male pipefish. K. Paczolt.

In their study, published in Nature today, Paczolt and her colleague Adam Jones mated 22 male Gulf pipefish (Syngnathus scovelli) with two females each, in separate broods1. They found that the males preferred to mate with larger females, and that these more 'attractive' females transfer more eggs to the male and more of her young survive (see Nature 's video).

They also found that if the males mate with larger females for his first brood, their second broods don't survive as well. Similarly, if a second brood does well, that means that the first brood probably wasn't mothered by a large female. "Males are making trade-offs; when they have limited resources, they have to invest in the smartest ways possible," says Paczolt.

Infanticide and cannibalism?

The researchers then showed that a male pipefish will absorb some of his developing offspring — effectively eating some of his unborn young. This highlights a conflict of interest between the two sexes: the females surrender their eggs to the males in the hope that they will all be supported, but the males instead may support only a fraction of the brood.

"This potential for both the 'give and take' of resources during male pregnancy has prompted a reconsideration of the costs and benefits of male mating decisions in this system," says evolutionary biologist Tony Wilson at the University of Zurich in Switzerland. If differences in offspring survival can be directly linked to males making choices after mating it would be a "truly outstanding example" of such 'cryptic' choices, he says.

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Jones devised a computer model to test when this sort of behaviour might be useful to males in nature. He created an 'electronic community' of pipefish in which he could vary the number of males and females, the size of the females and the smallest size of female with which a male would mate. Given the short supply of large females and the pickiness of the males, it is beneficial for a male to mate with a smaller female and raise at least some of that brood, according to the model. "And hopefully by the time those are born, he'll find a bigger female to mate with," Paczolt says.

The fact that male pipefish are selectively judging the fitness of their mate both before and after copulation is surprising because, in general, most animals judge the quality of their mates before sex or, in some species, after sex. "So rather than just be stuck with a female he doesn't like as much, he can invest only partially," Paczolt says.

"The suggestion that the brood pouch possibly evolved because it gives the males control to resolve the sexual conflict of interest between them and the females is very interesting indeed," says Axel Meyer from the University of Konstanz. It is possible that large females can manipulate males so that they give birth to their offspring, whereas males may have greater control over smaller females than they do over him, he says.