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January 19, 2015 | By:  Sedeer el-Showk
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For bone-eating worms, smaller is better

In 2002, researchers discovered a genus of quirky little deep-sea worms in Montery Bay, California. They named it Osedax, from the Latin for “bone-eating”, because the little critters grasp onto whale skeletons and bore through the bones with acid to get at the lovely nutrients within! Sara Mynott will tell you lots more about Osedax in an upcomping post on Saltwater Science, so I'm going to focus on the striking size difference between the males and females.

Osedax females are bigger than males. That's hardly remarkable in itself; sexual dimorphism is very common, and females are often the larger sex. What makes Osedax exceptional is the scale of the difference. Female Osedax aren't just larger than the males, they're thousands – even tens of thousands – of times larger. The females are so much bigger that they actually carry around a 'harem' of hundreds of males in their tube; the dwarf males never really develop beyond the larval stage and can't live on their own. It can be hard to imagine a 10,000-fold size difference, so I made a little graphic to help:

That shows the average size difference, which is around 30,000 times, but females can be anywhere from 1,500 to 100,000 times bigger than the males. According to Wolfram Alpha, humans average around 66 liters in volume, so that means women would be stuck with mates that would only fill half a teaspoon. (Osedax females are only a few millimeters in size, which means the males are incredibly tiny little things!)

What could possibly lead to such extreme size differences? One theory holds that male dwarfism is most likely to evolve in a species when: (1) males don't compete for access to females; (2) resources are limited; (3) individuals can't move about; and (4) finding a mate is hard. Under those conditions, it makes sense for males to become small to maximize their mate's success (if they're lucky enough to find one). Smaller males won't compete with their mate for the limited resources, so she can get bigger and produce more offspring. Sperm are pretty cheap compared to eggs, so it's better to give more energy to the partner doing most of the work, especially if the male doesn't need to compete with other males.

That's probably what happened during the evolution of Osedax. They fit all the criteria, so the males defer to the females instead of fighting with them over the limited sunken bones. By turning tiny and letting the females do all the work, the males maximized their odds of reproductive success. There's an exception, however, and while it doesn't quite prove the rule, it does lend some support. The size difference is quite a bit smaller in the newly-discovered species Osedax priapus. The males are much bigger than those of other species, and the females are much smaller, resulting in only a three-fold size difference. This graphic is drawn at the same scale as the one above, so you can get an idea of the size difference in O. priapus and also see how much bigger the males are than those of other species:

The males are about 70 times the size of an average Osedax male, though the males of some species are one-thousandth the size of O. priapus males. Likewise, O. priapus females are roughly 35 times smaller than average Osedax females, but 130 times smaller than those of some species. O. priapus aren't just bigger than other Osedax males; they're also free-living, feeding on bone beside their female counterparts – a unique arrangement for these worms.

One explanation for the reduced dimorphism in O. priapus is that the smaller size of the females effectively increases the resources available. Small females take up less space on the precious skeletons and require fewer resources, which makes room for the males to become larger and feed on the bones without putting pressure on the females. It's then in the males' best interest to grow a bit and become free-living again, so they can mate with several females, none of whom will be resource-limited. It's a nice story, but it's probably not the full explanation. Several other Osedax species have small females but haven't lost male dwarfism, so something else must have helped in the case of O. priapus. Perhaps O. priapus females don't live as long as other Osedax females, so there isn't enough time to recruit a harem (or maybe not enough value in being part of one). The truth is, we simply don't know enough about the ecology and life history of these creatures to offer a convincing explanation.

The most recent common ancestor of all Osedax species is thought to have had dwarfed males, and O. priapus is the only known species without male dwarfism. In other words, priapus isn't an evolutionary hold-out from an era where Osedax males and females were the same size. Instead, Osedax males have actually lost dwarfism during their evolution. It's a pretty remarkable reversal, because the males haven't just regained the ability to grow in size; they also mature into adults, which means they've reactivated a suite of genes inactive in other Osedax males. It's rare to see a complex trait get re-acquired during evolution, since the genes involved usually degrade by mutation during the generations when they're not being used. O. priapus is a remarkable evolutionary story, and one we still don't fully understand.

Rouse et al. A Dwarf Male Reversal in Bone-Eating Worms. Current Biology 25(2):236-241 (2015). doi: 10.1016/j.cub.2014.11.032

The O. rubiplumus image is by Robert C. Vrijenhoek, Shannon B. Johnson & Greg W. Rouse and is distributed by Wikipedia Commons under a CC-BY license. The remaining images are by Sedeer el-Showk.

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