Through the Sexual Looking Glass

By Carl Zimmer | March 17, 2010 1:00 pm

pipefish collage.001There was a time when seahorses meant little to me. They were pleasant to look at in an aquarium. They seemed to show up a lot on the walls of restaurants near beaches. But as is so often the case in nature, there’s bizarre biology lurking under the surface. Specifically, inside the male seahorses. When it’s time to make new seahorses, the male seahorses get pregnant.

Their pregnancy seems bizarre because it is rare. In most species that keep their young inside a parent, the job goes to the mother. But there is a deep symmetry to these two ways of reproducing. That’s a general rule when it comes to evolution: time and again, biologists find the same underlying principles driving the evolution of both the familiar and the bizarre.

The specifics of an animal’s sex life have their ultimate origin in the time and effort each sex have to put into reproducing. Very often, there’s a wild imbalance between the sexes. Just take a look at a human sperm and egg. One’s tiny and one’s big. Women may produce a few hundred viable eggs in a lifetime. Men make hundreds of new sperm a second.

The imbalance between the sexes means that they face different limits to how many offspring they can have. Females are not limited by a scarce supply of sperm. It would be possible, in theory, for every woman on Earth to have children fathered by a single man. Instead, what limits the reproductive success of females in many species is how many eggs they can successfully produce and rear to adulthood. Individuals that do better at that job will spread their genes over the generations. This selection drives females to put even more effort into rearing their young. Eggs can become enormous, for example–take the Kiwi bird, whose eggs can equal a quarter of the mother’s weight. Females typically put more effort into finding shelters for their young. In a number of species as varied as cockroaches and humans, females carry their young inside their body, where they can feed them and protect them at the same time.

For males, the limits to reproductive success are usually very different. They don’t have to worry about nurturing their sperm, since they’re so cheap to make. Instead, in many species, they are limited by the number of females they can mate with. The fact that females spend so much time provisioning their young makes this limit even more intense. And so in many species, males compete with one another for the opportunity to mate with females. In some cases, they fight over territory where the females will show up in search of food. In other cases, they show off to females with fancy songs or feathers. In the end, some males manage to mate with more females and have more offspring.

This arrangement gives females in some species the chance to be choosy about their mates. In many species, females will tend to mate with some males over others–in some species of fireflies, for example, the females prefer males with faster flashes over ones that flash slowly. But females face a quandary in making their choice. If they have the prospect of mating with one particular male today, who’s to say that they might not find a more attractive male tomorrow? If they fertilize their eggs with the sperm of today’s male, they won’t have the chance to upgrade later. And sometimes males make this quandary even worse, by guarding them so they can’t mate with other males.

So females in many species have evolved some elaborate systems to keep their options open. Female ducks, for example, have lots of little pouches along their reproductive tract where they may be able to store sperm from different males, selecting the sperm they want to use to fertilize their eggs. Hens will squeeze out the sperm from a previous mating if they see an attractive rooster.

Darwin first recognized what he dubbed sexual selection, and in the past couple decades scientists have expanded the theory and used it to make sense of the specific details of the sex lives of particular species. Sexual selection theory is not based on some mystical essence of being male or female, however. It simply takes into consideration the costs and benefits that each sex faces in a given species. Under some conditions, the benefit that males get from competing for lots of females may be offset by the need that their young have for care. In these cases, males that help provide for their offspring after they’re born may fare better than males that don’t.

As a result, there are some species in which both males and females provide care. And there are also some cases in which the common pattern is entirely reversed: the male does most of the work.

Such is the case with seahorses and their close relatives, pipefishes and seadragons. In all of these species males undergo a sort of pregnancy. When they mate, the female transfers unfertilized eggs to the male. The male stores the eggs, sometimes inside a fleshy pouch, where he fertilizes them with his sperm. While sperm in other animals may be heroic swimmers that can travel a female’s reproductive tract, the sperm of these fish barely move at all.

The eggs then develop in the male. The eggs get some of their energy from the yolk their mother provided them, but the males help out too. The pouch of some species of seahorses and their relatives changes shape, taking on a very complex anatomy. Each fish embryo ends up in intimate contact with the father’s blood supply, so that he can give them nutrients. Eventually the baby fish wiggle out of dad and are ready for life on their own.

So now think about how this system can drive the evolution of the fish. The females still produce the eggs, but they don’t have to put the time and effort into rearing them. Sexual selection theory suggests that they would be better off looking for lots of males to take their eggs. And with all those females swimming around in search of males, they’re going to face some fierce competition.

Adam Jones of Texas A & M University and his colleagues have studied Gulf Pipefish to see whether this in fact occurs. (The picture above is of a male [left] and female Gulf Pipefish.) In one experiment, they found that most females failed to find any mates at all, while a small proportion of the females managed to mate with four males. Most of the males in that experiment, on the other hand, mated once. The pattern, in other words, is flipped from what you’d normally expect.

Because males can’t mate and run, they are not limited by the number of females they can fertilize. As a result, there’s less of a benefit to making lots of sperm. And that explains the remarkably scant supply of sperm these fish produce. Instead of making millions of sperm every day, a male seahorse’s testes may carry just 150 sperm in total.

The competition of females opens up the opportunity for males to be picky, rather than the females. And Jones and other scientists have found that, indeed, the females that mate the most have certain traits in common. They tend to be bigger than other females, and they have fancier fins and brighter color patterns. It’s no surprise, then, that female Gulf Pipefish females are bigger than males.

But why do the males go for the big flashy females? Today in Nature, Jones and his colleagues have published an experiment that offers some answers. Big females transfer more eggs into the pouches of males than small females. And the bigger the female, the more likely each egg was to survive. By being picky, males can have more kids.

But the reversal does not stop there. Jones and his colleagues wondered if males controlled the amount of investment they put into rearing eggs from different females. They had males mate one female, and then another. They discovered that the survival of the second brood depended on the first. If the first brood came from a big female, fewer of the eggs from the second brood survived. The opposite also held true. Jones and his colleagues concluded that the males are likely giving more resources to the eggs from big females, leaving less for small females they might later encounter. And they do end up mating with smaller females, they give the eggs fewer resources, so that they’re in a better position should they encounter a big female next time around.

I had left seahorses and their kin out of the sex chapter in The Tangled Bank, but when it comes time to update it, they will definitely be making a cameo appearance. Their mirror-image sex life has turned out to be just too amazing to ignore.

“Post-copulatory sexual selection and sexual conflict in the evolution of male pregnancy.” Kimberly A. Paczolt1 & Adam G. Jones. Nature, http://dx.doi.org/10.1038/nature08861

[Image: Nick Ratterman, Texas A & M]

CATEGORIZED UNDER: Evolution, The Tangled Bank

Comments (5)

  1. Thanny

    Polyandry with male parental investment is also practiced among some birds (such as Phalaropes) and a few mammals (some types of marmosets are all I can think of right now).

    But it’s hard to beat what the seahorses do. It makes one wonder just how it got started, given the obvious tendency for polygyny to dominate.

  2. This is really fascinating. I think I knew that male seahorses kept the eggs, but hadn’t thought of the bigger implications of how it affects the dynamics of mating.

    Nature has a couple relevant episodes out that can be watched online:

    What Females Want

    What Males Will Do

    I only made it part of the way through the first one and need to go back again to finish watching, but already I learned there about how some supposedly monogamous “mate for life” species aren’t as they appear (and true monogamy is even rarer than thought). Apparently, some females will pair with a good nurturing male but go off to have their eggs fertilized by a more aggressive male. It’s easy to see the benefits for her in this infidelity. Her male offspring should get the best of both worlds: a good provider to help raise the more aggressive genes. It probably goes some way to explaining too why some human women seem to be more sexually attracted to the “bad boys” who treat them so poorly.

  3. G

    A picture of a seahorse and not a pipefish would be nice.

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The Loom

A blog about life, past and future. Written by DISCOVER contributing editor and columnist Carl Zimmer.

About Carl Zimmer

Carl Zimmer writes about science regularly for The New York Times and magazines such as DISCOVER, which also hosts his blog, The LoomHe is the author of 12 books, the most recent of which is Science Ink: Tattoos of the Science Obsessed.

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