Intercourse function flexibility is essential to evolution of gay partnerships in termites

Sex role flexibility is key to evolution of homosexual partnerships in termites

A female (leader) and male (follower) pair of Japanese termites perform a courtship ritual called tandem running in the laboratory. Photo credit: Okinawa Institute of Science and Technology

If you happen to see termites engaged in courtship rituals, you’ll find it hard to tell the difference between opposite-sex and same-sex couples. That’s because one of the termites in a same-sex pair changes behavior to behave like the opposite sex. This “gender role flexibility” is critical to the development and maintenance of same-sex couples, reports a new study published in PNAS Nov. 8, 2022.

The research, conducted by scientists from the Okinawa Institute of Science and Technology (OIST) in collaboration with the University of St. Andrews on the Japanese termite Reticulitermes speratus, also found that termites’ ability to switch sex roles during courtship , can be traced back to their distant termite ancestors.

“Gay behavior in animals has always been a mystery to scientists,” said Dr. Nobuaki Mizumoto, first author of the study and postdoctoral fellow in OIST’s Department of Evolutionary Genomics. “A prevailing theory holds that homosexual behavior stems from a mistaken identity, with animals rushing to mate without verifying their partner’s sex. But at least for termites, we have shown that same-sex courtship requires conscious behavioral modification. In other words, it’s not a coincidence.”

In Japanese termites, courtship and mate mating occurs once a year during a short and hectic period. Thousands of winged individuals scatter from their nests and swarm into the air before landing on the ground and shedding their wings. The termites then rush desperately to find a mate, and once they are together, the two termites set off to find a nesting site to start their new colony. They move together while performing a specific courtship behavior called tandem running.

“Tandem running is highly coordinated, with each sex exhibiting different behaviors,” explained Dr. Mizumoto. “The female termite always leads, and the male termite always follows closely behind. When separated, the female pauses while the male searches for her.”

However, sometimes a male termite may not find a female, or vice versa. In this case, termites choose to form male-male and female-female matings and construct a same-sex nest together rather than remain solitary.

“Termites need to groom each other to remove pathogens and stay healthy,” explained Dr. Mizumoto. “Then females can reproduce themselves through parthenogenesis, and males can wait and later invade another nest to mate with a female. Also, searching for a mate of the opposite sex for too long makes termites vulnerable to predators. So same-sex pairings are a survival strategy — they’re making the best of a bad job.”

In the latest study, researchers focused on whether gender-specific behavioral roles observed in tandem runs in opposite-sex couples were also reflected in same-sex pairings.

Researchers found that termites in same-sex matings behaved similarly to termites in opposite-sex matings when the termites were separated. The leaders paused while the followers searched, regardless of whether the termite was male or female. Photo credit: Okinawa Institute of Science and Technology

First, they observed termites mating in mixed or same-sex groups in tandem runs. They found that female-male tandems and male-male tandems were more common than female-female tandems. However, once formed, all tandem pairs were equally stable and maintained similar speeds and durations.

The researchers then transferred predetermined female-male, female-female, and male-male termite pairs to their own Petri dishes. Then, while the termites performed the tandem run, the scientists removed either the leader or follower of the pair and observed how the other termite reacted.

They found that same-sex termite matings exhibited similar dynamics to opposite-sex matings when they separated. When separating female termites, the “successor female” will search intensely for the other termite, although this is a typical male behavioral trait. When male and male termites were separated, the “leader male” paused, similar to heterosexual females. This allowed same-sex couples to meet their partners again just as easily as heterosexual couples.

The research team also ran computer simulations to see what would happen if the termites in same-sex pairs were unable to switch sex roles. In pairs of females and females, the scientists simulated both females pausing, and in pairs of males and males, they simulated both males foraging. The simulations showed that they were either less likely to meet again or it took much longer.

Since both female and male termites were able to display the behavior of both sexes, the next question the researchers had to solve was how this gender role flexibility came about.

To answer this, the scientists sifted through a trove of scientific records to determine, for as many termite species as possible, whether tandem runs were present during courtship and, if so, whether females or males led them.

The researchers found that while all termite species within the evolutionary group Neoisoptera, which includes the Japanese termite, had female-led tandem runs, termite species that were more distantly related had tandem runs that could be either male-led or female-led.

“This suggests that male and female termites, which were the ancestors of modern termites, likely had the ability to both lead and follow. That could be why the potential for female and male behaviors still exists in modern termites, allowing same-sex mating to evolve,” said Dr. Mizumoto.

More information:
Nobuaki Mizumoto et al., Ancestral sex-role plasticity facilitates the evolution of same-sex sexual behavior, Proceedings of the National Academy of Sciences (2022). DOI: 10.1073/pnas.2212401119

Provided by the Okinawa Institute of Science and Technology

Citation: Sex Role Flexibility is Key to Evolution of Homosexual Partnerships in Termites (2022, November 9), retrieved December 1, 2022 from evolution.html

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