Evolution of moth sex pheromones via ancestral genes

Abstract

Mate finding in most moth species involves long-distance signaling via female-emitted sex pheromones. There is a great diversity of pheromone structures used throughout the Lepidoptera, even among closely related species. The conundrum is how signal divergence has occurred. With strong normalizing selection pressure on blend composition and response preferences, it is improbable that shifts to pheromones of diverse structures occur through adaptive changes in small steps. Here, we present data supporting the hypothesis that a major shift in the pheromone of an Ostrinia species occurred by activation of a nonfunctional desaturase gene transcript present in the pheromone gland. We also demonstrate the existence of rare males that respond to the new pheromone blend. Their presence would allow for asymmetric tracking of male response to the new blend and, thus, evolution of an Ostrinia species with structurally different sex pheromone components.M ate finding in most moth species involves the use of long-distance sex pheromones, which are emitted by females (Arn, H. The Pherolist, www.nysaes.cornell.edu͞fst͞ faculty͞acree͞pheronet͞index.html). These chemical communication systems are highly canalized, with strong selection pressure against novel blends and response preferences. Thus, it is unlikely that shifts to pheromones of diverse structures occur through adaptive changes in small steps (1); rather, structural changes in the signaling system may require a major shift. In moth species studied to date, pheromone production (female) and response (male) are not genetically linked (2), but a model for the evolution of new pheromones based on asymmetric tracking (3, 4) predicts that a large mutational effect in female pheromone production can subsequently be tracked by male response. This model can explain how the Asian corn borer (ACB), Ostrinia furnacalis, evolved to use (Z)-and (E)-12-tetradecenyl acetate (Z͞E12-14:OAc) pheromone components (5), whereas all other analyzed Ostrinia species use Z͞E11-14:OAcs (6) (Fig. 1). What has been difficult to understand is how a major shift in a pheromone blend like this could occur.Moth sex pheromones are produced in specialized female abdominal glands, generally via unsaturated fatty-acid precursors produced by desaturases that exhibit a range of stereo-and regiospecificities (7). In an attempt to understand how these diverse desaturases evolved, we have characterized desaturase genes from various moth species. These include genes for desaturases producing Z9-(8-12), Z10-(10), Z11-(11-13), and E11-isomers (9, 12) of C14 and C16 unsaturated acids. In the course of these studies, we discovered that, in female European corn borer (ECB), O. nubilalis, the pheromone gland contains three different transcripts (cDNA) of desaturase genes, only one of which appears to result in a functional protein product. The functional transcript in ECB is for a ⌬11-desaturase used for production of its pheromone components. One of the nonfunctional transcripts is for a ⌬14-desaturase, which is use...

On the scent of speciation: the chemosensory system and its role in premating isolation

“…In this case, divergence in olfactory signals results from the inactivation of a desaturase enzyme. Research on the desaturases in various moth species revealed that another way to produce a change in pheromone blend is by activation of a non-functional desaturase gene transcript present in the pheromone gland (Roelofs and Rooney, 2003): for instance, pheromonal differences between O. nubilalis and its Asian relative Ostrinia furnacalis result from the activation of an ancestral desaturase gene in O. furnacalis, found to be inactivated in all other Ostrinia species (Roelofs et al, 2002). From these examples on destaturases, it is clear that the change occurred in a single step whereas large differences that map to a single locus, but have not been characterized at the molecular level, could, in principle, have accumulated by a series of substitutions of small effect.…”

Identification of quantitative trait loci function through analysis of multiple cuticular hydrocarbons differing between Drosophila simulans and Drosophila sechellia females

“…The second cluster of four genes fell between MtnA and slo; one or more of these elongases is likely to be important in the difference between D. simulans and D. sechellia. Most of the literature discussing genetic control of pheromonal differences among species has focused on the role of desaturases (e.g., Coyne et al, 1999;Rosenfield et al, 2001;Fang et al, 2002;Roelofs et al, 2002;Greenberg et al, 2003;Roelofs and Rooney, 2003;Coyne and Elwyn, 2006;Legendre et al, 2008). Although a desaturase has been implicated for 3L, there is at least an equal role in CHC for elongases in the difference between D. simulans and D. sechellia.…”

“…A change in the expression of a single desaturase in the Asian Corn Borer results in a novel pheromonal blend compared with the European Corn Borer (Roelofs et al, 2002), and there is evidence for a single gene change in sibling species of Helicoverpa moths resulting in a pheromonal blend change (Wang et al, 2008). Although in both of these cases single genes are implicated, the allelic difference between species results in a change in the blend of compounds, not just a single pheromone.…”

Beyond species recognition: somatic state affects long-distance sex pheromone communication

“…This early classical view had arisen because receivers often seem to be highly sensitive and narrowly tuned to the conspecific pheromone blend, and a slight change in the blend would thus result in a fitness loss of the signaller and therefore selected against (e.g. [18,19]). Nevertheless, various studies found considerable interindividual variation in the amount and ratio of pheromone components [20].…”