Your Friday Dose of Weird: Male pipefish show the dark side of male pregnancy

At almost every aquarium I have ever visited with a seahorse exhibit, the plaque in front of the tank says the same thing: in seahorses and their relatives, males, not females, carry the babies. It is always interesting to watch the reactions of visitors to this curious fact. Adult men, for instance, sometimes seem unsettled by the thought of male pregnancy, but the reproductive reversal among the fish is often seen as kinda cute ("How sweet. A fishy dad taking care of his kids!"). As shown by a study by Kimberly Paczolt and Adam Jones published this week in Nature, however, there can be a dark side to male pregnancy.

Male seahorses, pipefish, and seadragons (collectively members of the Syngnathidae) expend a lot of energy caring for their offspring. For these fish, mating involves the female depositing her eggs inside an expandable brood pouch on the underside of the male which both houses and provides resources (such as food) for the developing young. As noted by Paczolt and Jones, this means that the males may be able to modulate the resources they put into raising young, perhaps withholding resources during some pregnancies to invest them in later broods, and to test this hypothesis the scientists looked at the reproductive behavior of Gulf pipefish (Syngnathus scovelli).

The experimental setup was fairly simple. The scientists mated several pairs of pipefish, allowed the male to bring the offspring to parturition, and then mated the same male to a different female. Since the brood pouches of the male pipefish were clear, photographs of the brood taken shortly after egg transfer, in the middle of the pregnancy, and before birth provided measures of health and mortality, and by recording these patterns the scientists hoped to detect whether males were investing differently in their broods.

Before all of this could happen, of course, the scientists had to get the pipefish to mate, and it seemed that males preferred to mate with larger females. This was not especially surprising since this pipefish species is sexually dimorphic (and so it was expected that males would prefer females that were bigger and showed more secondary sexual characteristics), but what was especially interesting was how these preferences influenced reproduction. The larger females typically transferred more eggs to males than smaller ones, and more offspring from larger females survived than those of smaller females.

These preferences can greatly affect the success of a female's eggs. As the researchers found, if the last brood a male carried came from a large female (as he would prefer), and then he was mated to a small female, the current brood fared worse. The reason why is that males may withhold some of their investment from a brood that comes after a particularly numerous one. While it is possible that there is something about larger females that triggers males to take better care of their offspring, the authors suggest that it is more likely that males are saving some of their available resources for the next big female that comes along. If you are a small female pipefish looking for a mate, both pre- and post-copulatory factors set the odds against you having a successful brood.

But this is not just about male investment. Males also get resources from their eggs, particularly amino acids that become incorporated into his body. A big brood from a large female would be more beneficial for him to carry than a smaller one from a comparatively tiny female. Yet large females are relatively rare. Many males simply will not have the opportunity to mate with the most desirable females, and so in circumstances in which they mate with smaller females males seem to hold some of their resources in reserve for when the next opportunity comes around.

The upshot of all this is that sexual selection is not just about how animals compete for desirable mates. Members of the sex which provide most of the resources and care for the young during early development (usually females, but in this case males) may have mechanisms to make "cryptic choices" about those offspring. The ornaments of selection that inspired Darwin, from flashy colors to large canine teeth, are just part of the story, and scientists are just beginning to uncover the larger picture of how sexual selection works.

For another take on this research, see Ed Yong's post at Not Exactly Rocket Science.

Paczolt, K., & Jones, A. (2010). Post-copulatory sexual selection and sexual conflict in the evolution of male pregnancy Nature, 464 (7287), 401-404 DOI: 10.1038/nature08861