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 a tandem run in the lab. Credit: Okinawa Institute of Science and Technology

You wouldn't be able to tell the difference between opposite-sex and same-sex couples if you happened to see them. One of the termites in a same-sex couple acts like the opposite sex. The evolution and maintenance of same-sex pairs is dependent on sex role flexibility.

Scientists from the Okinawa Institute of Science and Technology (OIST) collaborated with the University of St.

Homosexual behavior in animals has always been a puzzle for scientists. Heterosexual behavior is thought to be caused by mistaken identity, with animals rushing to mate without checking the sex of their partner. Same-sex courting requires a change in behavior. It is no accident.

During a brief and frantic period of time once a year, Japanese termites can be found courting and mate-hunting. Thousands of individuals leave their nest and swarm into the air before landing on the ground. After rushing to find a partner, the two termites set off to find a new colony to live in. A tandem run is a type of courting behavior.

The run is very coordinated and each sex has a different behavior. The female and male are always following the same path. The female stops while the male searches for her.

Sometimes a male and female can't find each other. A same-sex nest is established by the termites instead of staying single.

Termites need to groom each other in order to remain healthy. Females can reproduce on their own, and males can wait and later invade another nest to mate with her. Finding a partner of the opposite sex can leave them vulnerable to attack. Same-sex pairs are a strategy for survival because they make the best of bad jobs.

The researchers looked at whether sex roles seen in tandem runs in opposite-sex couples were also seen in same-sex pairs.

Researchers found that termites in same-sex pairings acted in a similar way to termites in opposite-sex pairings when the termites were separated. Leaders paused while followers searched, regardless of whether the termite was female or male. Credit: Okinawa Institute of Science and Technology

They observed how the termites would pair up for tandem runs. Female-female tandems occurred less frequently than male-male tandems. All tandem pairs were the same in terms of speed and duration.

Pre-established female-male, female-female, and male-male termite pairs were put in their own petri dishes. The scientists took the leader or follower of the pair and watched how the other one reacted.

The dynamics of same-sex and opposite-sex pairs were the same after separation. The female "follower female" searched for the other female when they were separated. The leader male paused when males were separated. Same-sex pairs could re-encounter their partner just as effectively as heterosexual pairs.

The simulations were run to see what would happen if the same-sex couples couldn't switch roles. The scientists did simulations of both females pausing and males searching for female and male partners. They were either less likely to re-encounter each other or take a long time.

The next question for the researchers was how this sex role flexibility came about.

To answer this, the scientists searched through a lot of scientific records to find out if tandem runs were present during the courting process, and if females or males lead them.

The researchers found that some of the species of termites that were more distantly related had female-led tandem runs that could be led by either males or females.

It's possible that males and females of the past had the ability to lead and follow. It's possible that the potential for females and males to switch behaviors is still there.

The evolution of same-sex sexual behavior is aided by ancestral sex-role plasticity. 10.1073/pnas.

Journal information: Proceedings of the National Academy of Sciences