In the stalk-eyed fly world, it’s the males with longer eyestalks that get the females. Not only do the females prefer males with longer antennae dotted eye-stalks, but other males are also less likely to fight with these more well-endowed flies.
However, some males will always have short eyestalks due to a copy of the X chromosome that causes the eyestalks to be smaller. While investigating why this genetic mutation hasn’t disappeared–despite generations of sexual selection–a team of scientists found that the flies might be compensating for their shorter eyestalks with more aggression. The findings are detailed in a study published October 21 in the journal Frontiers in Ethology.
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“These driving X chromosomes are pretty interesting because they are an example of how parts of our genetic code aren’t necessarily working together, but have their own selfish interests,” study co-author and State University of New York–Geneseo biologist Josephine Reinhardt said in a statement. “This is an extreme example, but simply carrying one of these selfish chromosomes impacts so many parts of these animals’ biology, even their behavior.”
Gene drives and dueling flies
Stalk-eyed flies is a catchall term for the insects in the fly family Diopsidae and order Diptera. They are typically found among low-lying vegetation in humid areas, generally near rivers and streams. They are only about a centimeter long and feed on decaying animals and plants.
Two types of X chromones are present in stalk-eyed flies. The one carrying the mutation for short eyestalks is a driving X chromosome, or more specifically, a meiotic driver. This means that it carries alleles which are over-represented in a male’s sperm, so it is much more likely to be passed on to the next generation.
“The driving X chromosome has a huge natural advantage because it passes itself on more than the fair 50-50 ‘coin flip’ rule of genetics that most of us learned in high school biology,” said Reinhardt. “Up to 100% of a male’s offspring end up inheriting the X and therefore are female. Because of this, we might assume the X will keep increasing in the population and even cause extinction. Since that hasn’t happened, we’re interested in understanding what other traits could counteract that advantage.”
To defend their access to mates, male stalk-eyed flies generally use intimidating physical displays and fighting. They will also display more aggression against other flies with similarly-sized eyestalks
As a way to test whether the flies carrying the driving X are more aggressive, the team on this study used populations of flies carrying either type of X chromosome–the one that always results in flies with shorter eye stalks and the one that does not. They also matched up competitors with similar eyestalks, recorded their contests, and analyzed their behavior.
The fighting behaviors were more common when the two flies had more closely matched eyestalk sizes. These aggressive actions were also seen more often in male flies with the driving X. The males that deployed more of these fighting behaviors were also more likely to win in these contests. Males with the driving X chromosome were also more likely to come out victorious when they engaged in more fighting than displaying.
“When fighters are mismatched, fights tend to end quickly, with the smaller male retreating,” Reinhardt said. “When a male with the driving X chromosome is fighting a male with similar-sized eyestalks, he is more aggressive. But because driving X males are on average smaller, it is likely still a disadvantage.”
Mating opportunities
According to the team, this feisty behavior might explain why the flies with short eyestalks were able to mate. Since longer eyestalks signal a larger body size and potentially more dangerous foe, the flies with shorter eyestalks will typically retreat from contests with these bigger flies.
However, if males with the driving X chromosome are more aggressive or fail to accurately assess the threat from other males, they might choose to compete with males with longer eyestalks. This then brings them into contact with the females that are initially attracted to their opponent.
While this extra aggression is potentially dangerous, it may also give the flies access to mating opportunities that they otherwise wouldn’t. Still, this can’t fully counterbalance sexual selection. The team’s modeling of the spread of the driving X suggests it might explain why the shorter eyestalks haven’t taken over. The females still prefer males with longer eyestalks, keeping the variant’s frequency low.
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“I would say that this study is an initial finding,” said Reinhardt. “A larger study might be done in which we specifically test for the increase in high-intensity behavior that we saw here in a larger sample. In addition, this is a laboratory study, so it is not totally clear how well it would apply to field behavior.”
The study also didn’t test female flies. If the driving X chromosome is what directly increases aggression, it might impact females. However, if it’s an indirect effect to do with the eyestalk size, the driving X chromosome might not affect the females.
