Smells like a new species: gene duplication at the periphery.

T he remarkable long-distance sexual communication system of moths has fascinated and puzzled biologists and chemists since bombykol was identified and the term “pheromone” was coined 51 years ago. The pheromone signal is a bouquet of volatile chemicals wafting through the night air, synthesized and released by the female’s pheromone gland and detected and decoded by the male’s antenna and central nervous system. The sensitivity and selectivity of this chemical code poses a dilemma in explaining how changes could evolve, because strong reciprocal stabilizing selection between signaler and responder would seem to allow little scope for change. The genetic study of Gould et al. in PNAS (1) shows the importance of gene duplication in generating the variation in peripheral sensory physiology that could enable a change in male preference from one species’ pheromone blend to another. This scenario fits satisfyingly into the “asymmetric tracking” hypothesis (2) of pheromone evolution, which posits weaker selection for signaling fidelity on the limiting sex, females, than on males. Some sort of saltational mechanism is assumed to produce initially random, nonadaptive variants in female pheromone production, which are then “tracked” by a subpopulation of males with “broadened tuning” of some of their olfactory receptor neurons (ORNs) (3). As the genes altering female signaling are likely different from those changing male response, it is still unclear what mechanism maintains an association between them in the early stages; and there is no general agreement as to whether this process can drive speciation or can only proceed once reproductive isolation due to other factors has already occurred (4). Heliothis virescens (Hv) and H. subflexa (Hs) serve as a useful model system for studying this process. Although distinct in many respects, the two species are similar enough so that laboratory hybrids may represent some features that were present in the early stages of divergence. Gould et al. sought to map QTL (quantitative trait loci) for the response to species-specific attractants, by marking all chromosomes and looking for correlations with male flight behavior in interspecific backcrosses. Both species produce the major component Z-11-hexadecenal (Z11-16:Ald). Hv also produces Z-9tetradecenal (Z9-14:Ald), which is critical to male Hv attraction; Hs instead produces Z-9-hexadecenal (Z9-16:Ald), Z-11hexadecenol (Z11-16:OH), and Z-11hexadecenyl acetate (Z11-16:OAc) which attract Hs males; the latter inhibits Hv males. The behavioral assay required presentation of the species-specific attractants in just the right ratios to elicit a stronger response from F1 males than Hv or Hs. Active flight was required to show that an intact signal-processing pathway capable of discriminating among pheromone blends was functional in hybrids. Gould et al. found that attraction to either Z9-14: