In order for aquatic organisms to have made the transition from living in water to surviving on land, mutations in several physiological processes needed to occur. For one sensory system, that of smell, olfactory brain structures that detect odors based on sensing air-borne, volatile and hydrophobic molecules evolved from structures that had the ability to detect aqueous hydrophilic solutions. The necessary evolutionary adaptations that occurred in the ancient insect nose are the focus of a recent paper by Christine Missbach, Steffen Harzsch and Bill S. Hansson from the Max-Planck-Institute, Germany, published in the journal of Arthropod Structure and Development.

Insects use their sense of smell for almost every aspect of survival, from mating, predator avoidance and communication, to finding food. The antennae house sensory neurons that send projections to the antennal lobe, deep in the insect brain. Hansson's team analyzed the antennal lobes of insects within the Order Archaeognatha, the wingless insects known as jumping bristletails. Because the Archaeognatha are considered the least evolutionarily changed insects, the team hypothesized that jumping bristletails would provide clues to the minimal changes within the olfactory system that allowed one of the oldest insect groups to evolve the ability to smell on land.

First, the team collected a colony of Lepismachilis y-signata (a representative of the Archaeognatha), from a forest in Germany. They set out to analyze the brain architecture of the olfactory system in L. y-signata by several techniques. To get a picture of the outermost structures, the group used scanning electron microscopy and closely examined the different types of antennal sensilla – hair-like structures on the antennae that insects use to detect odors. The team found the same types of sensilla covering the antennae of L. y-signata that have also been found in higher order insects, suggesting that the antennae, in part, may function as the main olfactory organ in these primitive insects too.

Next, Hansson and his group decided to find out whether these primitive insect brains are organized as they are in more modern insect species. Sensilla house the olfactory sensory neurons that send their projections into the antennal lobe, which is considered to be the primary olfactory brain center. Connections between the olfactory sensory neurons and antennal lobe occur in organized regions called glomeruli, where odor detection and discrimination are processed and where different smells are represented as a chemotopic map in the brain – such that different odors activate different glomeruli. Using histological section series to generate three-dimensional reconstructions of the brain, immunohistochemistry to label neurons and follow their projections in the brain, and antennal backfills to determine where the antennal nerve enters the brain, the team compared the structure of L. y-signata brains with the brains of other modern insects.

Interestingly, they found the glomeruli of L. y-signata differ in shape and possess far fewer glomeruli overall. Compared with almost all other insects that have been studied so far – and have been found to contain between 40 and 170 individual glomeruli – L. y-signata contain less than a dozen. Assuming that more glomeruli translates into a greater array of olfactory receptor proteins (and the ability to detect a wide range of odor molecules) expressed in distinct subpopulations of olfactory sensory neurons, Hansson's team suggest that Archaeognatha may represent a most primitive terrestrial and undifferentiated olfactory model, one with the lowest number of olfactory receptors found in any insect studied to date.

B. S.
New insights into an ancient insect nose: the olfactory pathway of Lepismachilis y-signata (Archaeognatha: Machilidae)
Arthropod Struct. Dev.