Abstract
Pheromones are central to the mating systems of a wide range of organisms, and reproductive isolation between closely related species is often achieved by subtle differences in pheromone composition. In insects and moths in particular, the use of structurally similar components in different blend ratios is usually sufficient to impede gene flow between taxa. To date, the genetic changes associated with variation and divergence in pheromone signals remain largely unknown. Using the emerging model system Ostrinia, we show the functional consequences of mutations in the protein-coding region of the pheromone biosynthetic fatty-acyl reductase gene pgFAR. Heterologous expression confirmed that pgFAR orthologs encode enzymes exhibiting different substrate specificities that are the direct consequences of extensive nonsynonymous substitutions. When taking natural ratios of pheromone precursors into account, our data reveal that pgFAR substrate preference provides a good explanation of how species-specific ratios of pheromone components are obtained among Ostrinia species. Moreover, our data indicate that positive selection may have promoted the observed accumulation of nonsynonymous amino acid substitutions. Site-directed mutagenesis experiments substantiate the idea that amino acid polymorphisms underlie subtle or drastic changes in pgFAR substrate preference. Altogether, this study identifies the reduction step as a potential source of variation in pheromone signals in the moth genus Ostrinia and suggests that selection acting on particular mutations provides a mechanism allowing pheromone reductases to evolve new functional properties that may contribute to variation in the composition of pheromone signals.
Highlights
Pheromones are central to the mating systems of a wide range of organisms, and reproductive isolation between closely related species is often achieved by subtle differences in pheromone composition
When taking natural ratios of pheromone precursors into account, our data reveal that pgFAR substrate preference provides a good explanation of how species-specific ratios of pheromone components are obtained among Ostrinia species
Moth sex pheromones usually consist of a bouquet of structurally similar chemical components, and species specificity is in many cases achieved by the use of a narrow range of pheromone components combined in a specific ratio [1, 7, 8]
Summary
Pheromones are central to the mating systems of a wide range of organisms, and reproductive isolation between closely related species is often achieved by subtle differences in pheromone composition. Studies on intra- and interspecific differences among isolated taxa have the potential to reveal the causes of signal divergence that are associated with reproductive isolation [3] In this context, moths (Insecta: Lepidoptera), which represent one of the largest group of insects with ∼160,000 described species [6], provide highly relevant examples because subtle changes in their sex pheromone composition are often the initial trigger for population divergence and can lead to speciation [7, 8]. Earlier in vivo experiments demonstrated that the acetyltransferase, which is involved in the last step of the biosynthesis pathways leading to acetate pheromone components, has low substrate specificity in Ostrinia species [17,18,19] These results imply that pheromone blend ratio regulation occurs before the acetylation step.
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