By Meredith Swett Walker
Humans are a species where males and females are pretty equal — at least numerically. The number of boys born is roughly equal to the number of girls — a ratio of 1:1. Even if you look at the entire population of humans, not just newborns, the sex ratio is still roughly 1:1. But while this may seem normal to us, it is not the norm in many other species — especially insects.
Sex ratios are skewed, meaning they diverge from 1:1 in many insect species for many different reasons. Different numbers of males and females are produced in eusocial insects like bees or ants. In some cases, parasites manipulate the sex of their insect host’s offspring to their own advantage. Sex ratios may also become skewed after birth (or hatch) if males and females are eaten by predators at different rates, or if one sex simply lives longer than the other. Insect sex ratios have been the subject of study for more than a century.
A new study, published this month in the journal Environmental Entomology, presents another example of an insect with a skewed sex ratio: a feather louse (Quadraceps aethereus) found on auklets, small seabirds that nest in large colonies on northern islands. And the proposed cause of this sex ratio skew is surprising: the citrus-scent of the louse’s avian host.
Dr. Hector Douglas of the University of Alaska, Fairbanks, has been studying crested auklets and their unusual citrus scent for more than 15 years. In his latest report, “An Extraordinary Host-Specific Sex Ratio in an Avian Louse (Phthiraptera: Insecta) — Chemical Distortion?” Douglas and his co-author, Dr. Jael Malenke of the University of Utah, compared feather louse populations on least auklets, which do not have a distinct scent, to populations of crested auklets, which do. Douglas and Malenke found that one species of louse had an extremely female-biased sex ratio on the crested auklet, but not on the least auklet.
Crested auklets are more gregarious, larger, and have showier plumage than least auklets. They also secrete a chemical odorant composed of saturated and mono-unsaturated aldehydes that make them smell like citrus fruit. This odorant is secreted from specialized feathers between the bird’s shoulders that function like wicks. It appears that the odorant has a function in the bird’s courtship rituals.
“Prospective mates anoint each other with these chemicals during courtship,” Douglas said. “It is as if they are trying to smear themselves with it.”
In contrast, least auklets do not secrete an odorant.
Douglas and Malenke captured crested and least auklets that were breeding in a mixed-species colony on St. Lawrence Island, Alaska. The lice on each bird were identified and counted, and the sex of adult lice was determined. Quadraceps aethereus, a generalist louse thought to occur all over the bird’s body, were found on both auklet species. Saemundssonia spp., lice that are thought to specialize on the head, were also found on both auklets. However, S. wumisuzume was found only on the crested auklet, while a louse called S. boschi occurred only on least auklets.
Saemundssonia lice had a male-biased sex ratio on both species of auklet, but Q. aethereus had an extremely female-biased sex ratio — 3 males: 207 females — on the crested auklets. This degree of skew is much larger than the range of skew one might expect to find, according to Douglas. So why are Q. aethereus female-biased on crested auklets but not on least auklets? Douglas and Malenke believe the skew is an indirect effect of the crested auklet’s odorant.
Previous work by Douglas demonstrated that the odorant’s chemical constituents have a paralytic or paralyzing effect on feather lice, slowing their movements. Male lice are smaller than females, so they may be more severely affected by the chemicals. Males also move around more on the auklet’s body, which makes them easier for the birds to find and remove when they preen their feathers. Since males that have been slowed down by the paralytic effects of the odorant are even more likely to get picked off, the sex ratio becomes female-biased because more males than females become separated from the host by preening and possibly by just losing their grip when the auklets dive under water.
Why didn’t the researchers see the same skewed sex ratio in Saemundssonia lice on crested auklets, given that they are also exposed to the odorant? Possibly because Saemundssonia spp. appear to specialize on the bird’s head, an area where the bird cannot preen itself. Male Saemundssonia may be slowed by the odorant chemicals, just like Q. aethereus males, but if the birds cannot reach them they will not be removed.
The exact mechanisms leading to the extremely female-biased sex ratio of Q. aethereus on crested auklets require further study, but it seems clear that this phenomenon is specific to the host. This makes it especially intriguing. The most notable example of insect sex ratios being skewed by another organism involves Wolbachia, a genus of bacteria that infects insects, especially their reproductive organs. In some host-parasite interactions, Wolbachia can only be passed on by females, so the bacteria may manipulate their hosts into producing more female offspring in order to enhance their own transmission.
However, in the case of Q. aethereus and the crested auklet, it seems that the host may be causing a skew in the sex ratio of its parasite.
“I think there are relatively few examples where it has been shown that the host has caused a significant skew in the sex ratio of its parasites, particularly in the case of vertebrates and their insect parasites,” Douglas said.
The auklets and their feather lice make for a fascinating (and fragrant) case study.
“There is a natural complexity in this system that could add to scientific knowledge of the causes and consequences of sex-ratio bias,” said Douglas.
This may turn out to be one of the first examples of a chemical produced by a host that affects the sex ratio of its parasite.
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Meredith Swett Walker is a former avian endocrinologist who now studies the development and behavior of two juvenile humans in the high desert of western Colorado. When she is not handling her research subjects, she writes about science and nature. You can read her work on her blogs http://picahudsonia.com and https://citizenbiologist.com or follow her on Twitter at @mswettwalker.