The strange sex lives of bone-eating whaleworms

For at least 30 million years, bone-eating worms have been making their homes in the bodies of decomposing whales on the seabottom, but the rotting cetacean carcasses are not just food sources for the polychaetes.

The term "worm" immediately conjures up images of the red, squiggly things which crawl all over the sidewalk after it rains, but this imagery does not fit the boneworms of the genus Osedax. These worms start off life as sexless larvae, and the timing of their arrival at a whale corpse makes all the difference as to whether they will be male or female. If the larva lands on the bones of a whale first, it will grow into a large female which will digest the bone with the help of endosymbiotic bacteria which comes to live inside the worm. Once this starts to happen, the larvae which fall on the already-established females will have a different life history. They will become males and will remain tiny (0.2-1.0mm long) for the rest of their lives, accumulating in crowded harems inside the tube of the larger female and living off stored yolk from their younger days as they have no mouth or digestive tract to speak of.

But where are the larvae which become males coming from? As explained by researchers R.C. Vrijenhoek, B. Johnson, and G.W. Rouse in a 2008 Molecular Ecology study, there are three hypotheses. The first is that both males and females are coming from a common larval pool; sex differentiation is a luck-of-the-draw affair in which all individuals are derived from a large accumulation of larvae from multiple parents. This has been taken as the null hypothesis, yet observations in the lab have suggested that individuals which end up as males might also come from neighboring females, and a third possibility is that the males are born via parthenogenesis after the females grow large enough.

To find out which was the case, the researchers undertook genetic tests of Osedax rubiplumus worms recovered from whalefalls found in Monterey Bay, California, particularly looking at the level of relatedness between male and female worms. If the males had been born via parthenogenesis, for example, it would be expected that they would share much of the female's mitochondrial DNA, while males derived from a neighboring female would not be as genetically similar but would still retain markers of a recent common ancestry since many female worm neighbors are siblings. If the males were derived from a larger communal pool, by contrast, it would be expected that they would show a greater range of genetic variation. By comparing the genetic relatedness of males and females, the team could get some idea of where they had come from.

The results of the tests showed that the Osedax worms had a high level of genetic diversity, and in most cases the difference between male and female mitochondrial DNA allowed the idea of parthenogenesis to be rejected. (The few cases in which some males seemed closely related to females they attached to appear to be the result of chance.) Nor did there appear to be any close connection between males and neighboring females, and altogether the hypothesis that both males and females were drawn from a common larval pool remained the best explanation for the observed pattern. It appears that, over the life of the female, males from this large larval pool continue to accumulate in her tube, living off their ever-diminishing supply of yolk and producing sperm until they perish.

Just why male Osedax worms became dwarfed, however, is unknown. One popular hypothesis is that it had something to do with how these worms find and consume rare, ephemeral resources such as whalefalls. Rather than compete with females for resources, males have been adapted to simply latch themselves onto them and produce sperm until they run out of nourishment, a strategy which appears to work well when places to live and feed are hard to find. Many larvae may never make it, but more may have the chance to reproduce if all they have to do is fall on a female. Since these worms were only discovered by science in 2002, however, with new species being discovered all the time, there is still much we have to learn about them, and perhaps future studies will help explain the peculiarities of their evolution.

VRIJENHOEK, R., JOHNSON, S., & ROUSE, G. (2008). Bone-eating females and their 'harems' of dwarf males are recruited from a common larval pool
Molecular Ecology, 17 (20), 4535-4544 DOI: 10.1111/j.1365-294X.2008.03937.x

[Image from Vrijenhoek et al, 2008]