A new study published today says that ozone, a common air pollutant, can cause male flies to emit less pheromones, making them less attractive to females and leading to males courting other males. The study highlights the impact of pollution on insect populations and their ability to reproduce.
The successful mating of insects is heavily dependent on chemical signals called pheromones. These chemical attractants allow male and female insects of the same species to recognize each other and mate. These sex pheromones are unique to each species, making it impossible for males and females of different species to mate.
Even slight variations in pheromones, as seen in the evolution of new species, can cause males and females to no longer recognize each other, resulting in failed mating attempts.
Unfortunately, insect pheromones are vulnerable to the damaging effects of air pollution. Most of these pheromones are made up of carbon-carbon double bonds, which are easily destroyed by ozone. This can lead to a significant reduction in the ability of insects to find and mate with their conspecifics, ultimately affecting the population dynamics of these species.
“We already knew that environmental pollutants such as ozone and nitric oxide degrade floral scents, making flowers less attractive to their pollinators,” explains lead author Mrkus Knaden.
“Since compounds with carbon double bonds are particularly sensitive to ozone degradation, and almost all insect sex pheromones carry such double bonds, we wondered whether air pollution also affects how well insect females and males find and identify each other during mating.”
In order to investigate how ozone impacts the mating behavior of the model fly Drosophila melanogaster, the team devised an ozone exposure system specifically designed for these flies. The system was intended to replicate ozone levels found in the air during the summer in urban areas.
To accurately simulate ozone levels in the system, the scientists had to create a continuous airstream that precisely measured the levels of the unstable chemical compound. However, the challenges of working with ozone did not stop there, as the compound is also known for its tendency to decompose easily.
Moreover, the researchers also had to account for the fact that flies generally produce only small amounts of pheromones, even in normal conditions. Despite these difficulties, scientists developed an innovative ozone exposure system that could prove instrumental in uncovering the effects of this environmental pollutant on Drosophila melanogaster’s mating behavior.
“We therefore needed a technique that would allow us to measure even tiny amounts of pheromones on individual flies that had either been exposed to ozone or not prior to the measurements,” remarks first author Nanji Jiang.
“To do this, we used what is known as a thermal desorption unit coupled to a gas chromatograph/mass spectrometer, which allowed us to measure tiny amounts of odors emitted by individual flies.”
The trials subjected male flies to slightly higher ozone concentrations. After then, the researchers examined whether or not the flies continued to release their pheromone. When the flies were exposed to 100 ppb (parts per billion, which is a concentration of 10–9) of ozone for two hours, the pheromone levels dropped significantly compared to a control group that had only been exposed to normal air. The researchers tested not only males of the model fly Drosophila melanogaster, but also males of eight related species of the genus Drosophila. Just one species, Drosophila busckii, demonstrated that the production of certain male pheromones was unaffected by ozone exposure; however, these molecules also lack carbon-carbon double bonds and do not react with ozone very readily.
Next, the team analyzed the attraction of male flies to their own species. They made troubling observations, which may have been primarily influenced by the function of the various pheromones. In Drosophila species, they are released by males to woo potential mates. Although the male’s pheromone is effective in luring females, it drives away other males. Males provide their pheromone to females during mating. During the following several hours, other males are not attracted to newly mated females who still smell like the pheromone. Hence, increased ozone levels not only made women less interested in men, but made ozonated men more appealing to other men. The oxidation of carbon double bonds, and consequently pheromones, is a well-established chemical process, so they knew that increased ozone levels may have an effect on insect mating systems.
Yet they were surprised that even a little increase in ozone concentrations had such a big impact on fly behavior.
“Actually, we initially wanted to focus on the interactions between males and females. We could explain that males started courting each other after a short ozone exposure, because they obviously could not distinguish ozonated males from females. However, we had not thought about this before. Therefore, we were quite puzzled by the behavior of the ozone-exposed males, which lined up in long courtship chains,” the authors write.
The study group also noticed changes in other Drosophila species’ mating habits as a result of elevated ozone levels in the atmosphere. Ozone does not affect the pheromone that has been reported as being released by Drosophila busckii males, however even these males had reduced success mating after being exposed to ozone. But other chemical compounds that are sensitive to ozone but haven’t been found yet may also play a role in their mating behavior. Odd courting behavior between ozone-exposed males was seen in eight of the nine species tested. D. suzukii, a species that does not produce pheromones but instead relies on visual cues to attract a mate, showed no ill effects from the elevated ozone levels.
The majority of insect pheromones include carbon-carbon double bonds. As a result, ozone is considered to disrupt sexual communication in many insect species.
“Insects and their pheromones have evolved over millions of years. In contrast, the concentration of air pollutants has only increased dramatically since industrialization,” comments Bill Hansson, head of the Evolutionary Neuroethology Department and co-founder of the Max Planck Center next Generation Insect Chemical Ecology (nGICE).
“It is unlikely that the communication systems of insects, which have evolved over the course of evolution, will be able to adapt to new conditions within a short period of time if pheromones are suddenly no longer there. The only solution to this dilemma is to immediately reduce pollutants in the atmosphere.”
The majority of insect pheromones include carbon-carbon double bonds. As a result, ozone is considered to disrupt sexual communication in many insect species.
“Through millions of years, pheromones produced by insects have changed. On the other hand, since industrialisation, the concentration of air contaminants has only substantially grown “says Bill Hansson, co-founder of the Max Planck Institute for Next Generation Insect Chemical Ecology and chairman of the Evolutionary Neuroethology Department (nGICE).
“If pheromones suddenly disappear, it is doubtful that insects’ communication systems, which have changed over the course of evolution, would be able to quickly adjust to new circumstances. Reducing air pollution right now is the only way to resolve this conundrum.”
The study focuses on the consequences of human climate change on insect ecosystem services, invasive insect species outbreaks, and disease vector dissemination across Europe.
Jena researchers aim to investigate the impact of ozone on a larger variety of insects, including moths, which often follow pheromone plumes across vast distances. Insects rely heavily on pheromones to differentiate between conspecifics and closely related species.
Excessive ozone levels also affect humans. The cost of industrialized countries’ existing lifestyles on the ecology and climate is quite expensive; many indirect impacts are still unknown.
In addition to pesticide use and habitat destruction, the latest research offers a third reason for why insect populations are dropping sharply around the world. Pollutants in the air may prevent chemical communication, which prevents them from reproducing at a sufficient pace.
Many pollinators, including bees and butterflies, may potentially be impacted by this. If we do not succeed in dramatically lowering air pollution, it is evident what magnitude this issue may take in the future given that 80% of our crops need insect pollination.
Source: 10.1038/s41467-023-36534-9
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