Evolution of Pheromone Reception In Spodoptera Moths – PRISM

The sex pheromone communication system of moths stands as a relevant model to investigate mechanisms responsible for the evolution of reproductive isolation. In those nocturnal animals, mate recognition largely depends on highly specific bouquets of air-borne chemicals called pheromones. These chemicals are synthesized in the pheromone gland of females, thanks to a variety of pheromone biosynthetic enzymes. In males, antennae usually bear thousands of sensory neurons that detect the different components of the pheromone blend with high sensitivity and specificity, which avoids cross-species mating and maintains reproductive isolation. This detection is mediated by membrane receptors belonging to the olfactory receptor family, and called pheromone receptors. As the sex pheromone system is fine-tuned and thus under a strong stabilizing selection, understanding how it can evolve and participate in reproductive isolation remains a conundrum. Which mechanisms allow for concomitant shifts in the signal emitted by females and in male preference, whereas the slightest change is supposed to be counter-selected? To fully answer this question, it is necessary to investigate the evolution of multigene families involved in both the biosynthesis and the detection of pheromones.

This is what we propose here, using crop pest moths of the genus Spodoptera as a model. In two sister species that live in parapatry, S. littoralis and S. litura, females synthesize an unusual compound that is the major component of the pheromone blend and is absent in other Spodoptera species, some of which living in sympatry with S. littoralis and S. litura. In S. littoralis, the presence of this component in the blend results from the activity of two previously identified fatty acid desaturases that introduce double bounds at specific positions. Interestingly, we recently discovered in S. littoralis males the receptor that specifically detects the major pheromone component and it is not a “classical” moth pheromone receptor but rather belongs to another lineage of olfactory receptors. Building on these results, we will reconstruct a comprehensive evolutionary history of desaturases and of the new lineage of pheromone receptors in the genus Spodoptera. This will shed light on evolutionary events that allowed the emergence of a new pheromone communication channel in the common ancestor of S. littoralis and S. litura, and likely to be involved in reproductive isolation between sympatric populations.

Thanks to already available genomic data, we will identify the entire repertoires of these genes in four Spodoptera species and will study the evolution of their coding sequence, their regulatory sequences, their expression pattern and their function using heterologous expression of relevant candidate genes. In addition to fundamental knowledge on evolution, studying a new lineage of pheromone receptors in crop pest moths will foster the development of novel strategies of bio-control based on agonists or antagonists of these receptors.