The wonderfully strange sensory world of silkmoths

In the realm of scent perception, humans and silkmoths are very different. Humans of both genders share a similar level of olfactory development.

While women possess a marginally higher count of olfactory neurons, granting them a slightly keener sense of smell, both men and women generally perceive the same odors.

This contrasts starkly with the world of silkmoths, where males and females inhabit vastly different olfactory universes.

Specialized ‘nose’ of male silkmoths

Male silkmoths possess antennae that act as a highly specialized ‘nose’, fine-tuned to detect female sex pheromones. Conversely, female silkmoths lack the ability to smell their own pheromones.

These antennae are adorned with thousands of sensilla, hair-like structures that are categorized into distinct morphological and functional groups.

In male moths, the most prevalent sensilla are elongated, housing two sensory neurons. One neuron is adept at detecting bombykol, the female’s sex pheromone.

The other is responsive to bombykal, a compound found in the pheromones of other moth species. Intriguingly, bombykol is an attractant for male silkmoths, whereas bombykal acts as a deterrent.

Female silkmoths: A different sensory role

“Because female silkmoths cannot smell their own pheromone, it was long thought that their long sensilla also have a very specific function that is only found in females,” explains Sonja Bisch-Knaden, leader of a project group at the Max Planck Institute for Chemical Ecology’s Department of Evolutionary Neuroethology.

“After mating, the female’s only task is to find a suitable plant on which to lay her eggs. It has therefore been suggested that the long sensilla of females are specialized to detect the attractive odor of mulberry trees. We wanted to test this assumption.”

Innovative research and surprising discoveries

The team employed electrophysiological methods like single-sensillum recording to measure silkmoth scent and individual sensilla activity.

Their research extended beyond isolated odors to encompass natural odor mixtures, including those from mulberry leaves, caterpillar droppings, moth body odor, and meconium, a secretion emitted by moths upon hatching.

These odors, integral to the silkmoth’s ecological landscape, had been comprehensively collected. The researchers successfully correlated the expression of olfactory receptors with specific types of sensilla.

“We were surprised to find that neurons in the long sensilla of female silkmoths were not specialized to detect the odor of the host plant, as expected, but that one of the two neurons in the long sensilla is very sensitive to odors such as isovaleric acid and benzaldehyde. The detection of the odor of the mulberry leaf itself is carried out by neurons in medium-length sensilla,” summarizes Sonja Bisch-Knaden.

Studying silkmoth scent behavior

A simple Y-maze test, which offers a choice between a scent and clean air, revealed intriguing differences in the responses of virgin and mated female silkmoths.

Virgin females showed no specific reaction to odors associated with caterpillar droppings. However, these same odors repelled mated females.

This suggests that the scent of feces may guide females away from mulberry trees already hosting silkworms, ensuring a better environment for laying eggs.

Since the discovery of bombykol, the female silkmoth pheromone, in 1959, the elusive counterpart in male silkmoths has remained unidentified. The current study provides insights but stops short of revealing a male pheromone.

“The second neuron in the females’ long sensilla is highly specific for (+)-linalool, an odor already identified as a component of the male pheromone in other butterfly species. However, no linalool could be found in the body odor of male silkmoths, and (+)-linalool alone had neither an attractive nor a repellent effect on female silkmoths in behavioral experiments,” notes Sonja Bisch-Knaden.

Olfactory receptors: Silkmoths’ complex system

A noteworthy aspect of the study is the discovery of the spatial organization of silkmoth olfactory receptors.

Silkmoths possess two families of receptors: ionotropic receptors (IRs), primarily detecting acids, and odorant receptors (ORs), responsive to a variety of chemical compounds.

Contrary to previous beliefs based on studies of the model fly Drosophila melanogaster, silkmoths have neurons in their long sensilla that co-express both IRs and ORs.

This unique co-expression broadens the chemical sensitivity of the sensory neurons, allowing for the combined processing and transmission of odors detected by both receptor types. This could be vital for the clear detection of ecologically significant odor mixtures.

“It is amazing that research on insect olfaction continues to produce surprising results. Our study shows that it is important to study more than just one model,” says Bill Hansson, head of the Department of Evolutionary Neuroethology.

Interestingly, this co-expression of receptor types is also found in the long sensilla of male silkmoths, hinting that acid detection might be ecologically significant for them as well. Future research aims to explore this further.

In summary, this research challenges long-held assumptions about the sensory capabilities of silkmoths and improves our understanding of the complex interplay between organisms and their environments.

The full study was published in the journal Proceedings of the Royal Society B Biological Sciences.

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