Beetle horns and elk antlers are showy animal weapons that grow to outsized proportions: large beetles, for instance, have disproportionately larger horns than their smaller counterparts do. Although this phenomenon, known as hyperallometry, has been well-documented, the genetic basis for the evolution of hyperallometric traits remains incompletely understood.
Now, researchers at the Institut de Génétique Fonctionelle in Lyon, France, have discovered that the water strider Microvelia longipes’s massively exaggerated third legs, which males use to fight over access to females, are regulated by a gene called BMP11. That gene not only regulates both the size and the scaling pattern of the water strider’s weapon, but unexpectedly, is also involved in males’ fighting behavior, the researchers report in a study published today (May 11) in PLOS Biology.
“It’s one of the first studies to get at this question of what causes proportion—and how does proportion scale—at the genetic level,” says Kenneth McKenna, a postdoc at the University of California, San Diego, who studies scaling and growth in mice.
The fact that BMP11 regulates three interrelated traits is “kind of a blessing and a curse, from an evolvability point of view,” says Rajendhran Rajakumar, an evolutionary developmental biologist at the University of Ottawa. On the one hand, that gene can “essentially orchestrate the extreme covariation of body size, leg size, and behavior. On the other hand, if you were to select for a change in leg size but not on aggression or body size, it might actually be harder to do that, because BMP11 interlinks these three traits.”
Abderrahman Khila, the senior author of the study, first encountered these water striders while looking for other insects in French Guyana. He noticed the extremely exaggerated third legs of M. longipes gliding on the surfaces of shallow ephemeral puddles that were left behind after a rainfall, and he grabbed some of them to bring back to the lab.
In the wild, the males guard and fight over small, floating particles in the puddles upon which females lay their eggs. The males use their long third legs to kick other males away from the particle they are guarding. “There’s intense competition in these bugs, because they live in swarms in a very small space. So the males are always fighting,” Khila says.
To understand how those male legs got so long, Khila and his colleagues sequenced the transcriptomes of the legs of males and females. They used several different genetic lines of the water striders, including populations that were bred in the lab to have relatively short or long legs. By comparing the transcriptomes of the different lines, sexes, and the male third leg to the shorter first and second legs, the researchers identified about 30 candidate genes that seemed involved in the exaggerated growth of the limb.
They then used RNA interference to knock down the candidate genes one by one in Microvelia longipes and other closely related Microvelia species. Two of the genes had major effects on leg length: the HOX gene Ubx and the growth differentiation factor BMP11.
In M. longipes, the BMP11 knockdown produced the strongest change in phenotype: the third legs were shorter in altered males compared to males with their gene expression intact. The knockdown also reduced body size. In addition, the gene appeared to be a key regulator of the slope of the allometric scaling relationship between leg and body size. That scaling relationship mathematically describes how a change in leg length is linked to a change in body size. “When we knock [the gene] down, we reduce the slope dramatically in the males, but it does not affect slope in females,” Khila explains. The association between the growth of the leg and the growth of the body seems to be regulated by this single gene, BMP11.
What was most unexpected, though, was that the BMP11 knockdown males no longer showed any fighting behavior. “The males gather around the female, and they don’t pay attention to each other. You’ll have five or six males all trying to mate at the same time, and there is no fighting behavior,” Khila says.
This effect was specific to the M. longipes males. In M. longipes females and in males and females of other Microvelia species, BMP11 knockdown reduced body size but did not affect the scaling of the legs or fighting behavior.
“This is a really great example of how looking at different species within the same genus, you can get a really good idea about what’s happening in the focal species,” Rajakumar said.
This isn’t the first time BMP11 has garnered excitement in the biological community. About a decade ago, the gene was identified as a potential anti-aging factor—experiments in mice showed that connecting the circulatory systems of an old mouse and a young mouse could rejuvenate the old mouse, and BMP11 seemed to be involved in this effect. Now, it appears to have an entirely novel biological role.
“We have a gene that is involved in all three connected traits in the males: the increased size of the leg, the increased allometric slope, and the intensity of fighting behavior,” says Khila. “One of the conclusions of the paper is that pleiotropy—the fact that this one gene is controlling these interconnected traits at the same time—is going to promote the evolution of trait exaggeration, because all of these traits combined will increase mating success in the males,” he says.
W. Toubiana et al., “The growth factor BMP11 is required for the development and evolution of a male exaggerated weapon and its associated fighting behavior,” doi:10.1371/journal.pbio.3001157, PLOS Biol, 2021.