It's a first in the animal kingdom. Among a group of cave-dwelling Brazilian insects, the females use a specialized sex organ to penetrate the males. Scientists say that their lives challenge everything we thought we knew about sexual selection.
The insects are all members of the genus Neotrogla, whose four species all measure around a third of a centimeter long when fully grown. Several years ago, a Brazilian scientist named Rodrigo Ferreira sent a few specimens to a Swiss entomologist named Charles Lienhard, who identified the insects as belonging to an entirely new genus. Lienhard also noticed that the females had an erectile "penis-like structure," which they've called a "gynosome."
Above: The gynosome of Neotrogla aurora.
Neotrogla aren't the only creatures on the planet where the females have a "penis-like structure." So-called "pseudo-penises" are known in some other species, and they range from an enlarged clitoris in hyenas to enlarged labia in spider monkeys. But in each of those cases, the male must still penetrate the female during mating. In Neotrogla, the gynosome actually penetrates the male during sex — though the males still do the fertilizing.
A new study in the journal Current Biology, Ferreira and Leinhard describe the species with colleagues Japanese researchers Kazunori Yoshizawa and Yoshitaka Kamimura, making it a truly international research effort. The team wanted to understand the anatomy of Neotrogla genitalia in the context of its mating behaviors.
They discovered that when the insects have sex, the female's gynosome is inserted into the male after it becomes erect. Once the female has penetrated the male, her gynosome inflates, releasing a set of spines that can be used to keep the male from escaping. The sex lasts forty to seventy hours.
The researchers found the spines when they tried to physically separate two insects while they were copulating. "Pulling apart coupled specimens," they write, "led to separation of the male abdomen from the thorax without breaking the genital coupling." In other words, they tore the male right in half. It showed that the female can hold tightly onto the male. That's an important ability for insects that need to remain in coitus for as long as two or three days.
With the male firmly in place, the gynosome is ready to receive the sperm. But that's not all they get: the males also deliver what are called "seminal gifts," nourishing packets of nutrients that help the females survive in the food-deprived cave environment in which they live.
Taken together, it's clear that "the relative function and pattern of elaboration of male and female genitalia in Neotrogla are completely reversed relative to that generally observed." But why?
The researchers suspect that Neotrogla evolved this way because of a sort of "reversed" sexual selection, relative to most other species.
When we usually think of sexual selection, we think that members of one sex are picky about who they mate with because they put more energy or resources into reproduction. Sperm are cheap and eggs are expensive, not to mention the energy associated with parental care.
But Neotrogla evolved in a food-deprived environment. The primary food sources for the insects in their parched Brazilian caves are the carcasses of dead bats, along with bat guano. But bat carcasses are somewhat scarce. The females are in constant need of nutrition to support their reproduction, and they get that nutrition thanks to the "seminal gifts" from the males. They get sex and food, simultaneously. Suddenly, sperm aren't quite so cheap anymore.
In this environment, natural selection could have operated to reverse the usual patterns, making the female Neotrogla compete with each other for access to the males, who put quite a bit of their own energy into feeding the females thanks to their "seminal gifts." It would be the males, in that situation, who are the pickier sex.
At this point, it's still a hypothesis. The researchers call it the "most likely factor favoring the evolution of the gynosome," but they acknowledge that the evidence is "mostly circumstantial." There's lots more work to be done. But if it holds up to further scrutiny, it could result in a far more nuanced understanding of sexual selection and sex roles. It would suggest that what it means to be male or female is even more fluid than we thought.
The scientists hope to create laboratory-based colonies of the insects for further research. "Further controlled studies of the mating system of Neotrogla species…would provide an extremely rare opportunity to test the generality and relative importance of some hypotheses about sexual selection," they say.
[via Current Biology]
All images via Current Biology/Yoshizawa et al. (2014)