In the sex-pheromone communication systems of moths, odorant receptor (Or) specificity as well as higher olfactory information processing in males should be finely tuned to the pheromone of conspecific females. Accordingly, male sex-pheromone preference should have diversified along with the diversification of female sex pheromones; however, the genetic mechanisms that facilitated the diversification of male preference are not well understood. Here, we explored the mechanisms involved in a drastic shift in sex-pheromone preference in the silkmoth Bombyx mori using spli mutants in which the genomic structure of the gene Bmacj6, which encodes a class IV POU domain transcription factor, is disrupted or its expression is repressed. B. mori females secrete an ∼11:1 mixture of bombykol and bombykal. Bombykol alone elicits full male courtship behavior, whereas bombykal alone shows no apparent activity. In the spli mutants, the behavioral responsiveness of males to bombykol was markedly reduced, whereas bombykal alone evoked full courtship behavior. The reduced response of spli males to bombykol was explained by the paucity of bombykol receptors on the male antennae. It was also found that, in the spli males, neurons projecting into the toroid, a compartment in the brain where bombykol receptor neurons normally project, responded strongly to bombykal. The present study highlights a POU domain transcription factor, Bmacj6, which may have caused a shift of sex-pheromone preference in B. mori through Or gene choice and/or axon targeting.
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"Analyses of silkmoths with a null mutation in Bmacj6, a homolog of D. melanogaster abnormal chemosensory jump6 (acj6) that encodes a class IV POU domain transcription factor, have provided insight into the genetic mechanisms that may modify pheromone specificity at the behavioral level in moths (Fujii et al., 2011). In D. melanogaster, the acj6 mutant displays abnormal olfactory behavior (Ayer and Carlson, 1991), and genetic and electrophysiological analyses have suggested that acj6 determines the OR gene choice and axon targeting of ORNs (Clyne et al., 1999; Komiyama et al., 2004). "
[Show abstract][Hide abstract] ABSTRACT: Male moths locate their mates using species-specific sex pheromones emitted by conspecific females. One striking feature of sex pheromone recognition in males is the high degree of specificity and sensitivity at all levels, from the primary sensory processes to behavior. The silkmoth Bombyx mori is an excellent model insect in which to decipher the underlying mechanisms of sex pheromone recognition due to its simple sex pheromone communication system, where a single pheromone component, bombykol, elicits the full sexual behavior of male moths. Various technical advancements that cover all levels of analysis from molecular to behavioral also allow the systematic analysis of pheromone recognition mechanisms. Sex pheromone signals are detected by pheromone receptors expressed in olfactory receptor neurons in the pheromone-sensitive sensilla trichodea on male antennae. The signals are transmitted to the first olfactory processing center, the antennal lobe (AL), and then are processed further in the higher centers (mushroom body and lateral protocerebrum) to elicit orientation behavior toward females. In recent years, significant progress has been made elucidating the molecular mechanisms underlying the detection of sex pheromones. In addition, extensive studies of the AL and higher centers have provided insights into the neural basis of pheromone processing in the silkmoth brain. This review describes these latest advances, and discusses what these advances have revealed about the mechanisms underlying the specific and sensitive recognition of sex pheromones in the silkmoth.
Frontiers in Physiology 03/2014; 5:125. DOI:10.3389/fphys.2014.00125 · 3.53 Impact Factor
"Mate signalling is multimodal in Bicyclus anynana: females use volatile sex pheromones as well as visual signals in mate choice decisions (Costanzo & Monteiro 2007; Nieberding et al. 2008, 2012), as do other insects (Datta et al. 2008; Fujii et al. 2011). Here we tested whether pheromones interact with learning of visual signals in B. anynana and whether they influence a female's response to visual learning models. "
[Show abstract][Hide abstract] ABSTRACT: Mating displays are often composed of multiple signals in multiple sensory modalities, with each individual signal contributing to the attractiveness of the displaying individual. Adult mate preferences for some of these signals are learned during premating, or juvenile, social experience with a sexually mature individual. While learned mate preferences have been described in multiple taxa, it is still unclear how the different display signals perceived during the learning period influence the development of adult mate preferences. Of particular interest is whether a learned mate preference for a sexual signal in one modality is context dependent (i.e. dependent on a second signal in either the same or a different sensory modality). Here we test whether a signal in one modality (odour) influences the interpretation (aversion or preference learning) of signals in a different modality (wing colour patterns) using the butterfly Bicyclus anynana. Previously we showed that female B. anynana learn to prefer additional ornaments, UV-reflective white spots, on the wings of males if they are exposed to these ornaments on the first day after eclosion from pupae. We now show that females exposed to males with manipulated odour do not learn to prefer these additional ornaments, and learn to avoid the wild-type male ornamentation. This aversion learning, where animals learn to avoid visual signals previously coupled with unattractive odours and to prefer visual signals previously coupled with attractive odours, demonstrates that visual mate preference learning in a butterfly is context dependent, and that specific sexual signals may have epistatic effects on mate preference development.
[Show abstract][Hide abstract] ABSTRACT: Sex pheromone communication, acting as a prezygotic barrier to mating, is believed to have contributed to the speciation of moths and butterflies in the order Lepidoptera. Five decades after the discovery of the first moth sex pheromone, little is known about the molecular mechanisms that underlie the evolution of pheromone communication between closely related species. Although Asian and European corn borers (ACB and ECB) can be interbred in the laboratory, they are behaviorally isolated from mating naturally by their responses to subtly different sex pheromone isomers, (E)-12- and (Z)-12-tetradecenyl acetate and (E)-11- and (Z)-11-tetradecenyl acetate (ACB: E12, Z12; ECB; E11, Z11). Male moth olfactory systems respond specifically to the pheromone blend produced by their conspecific females. In vitro, ECB(Z) odorant receptor 3 (OR3), a sex pheromone receptor expressed in male antennae, responds strongly to E11 but also generally to the Z11, E12, and Z12 pheromones. In contrast, we show that ACB OR3, a gene that has been subjected to positive selection (ω = 2.9), responds preferentially to the ACB E12 and Z12 pheromones. In Ostrinia species the amino acid residue corresponding to position 148 in transmembrane domain 3 of OR3 is alanine (A), except for ACB OR3 that has a threonine (T) in this position. Mutation of this residue from A to T alters the pheromone recognition pattern by selectively reducing the E11 response ∼14-fold. These results suggest that discrete mutations that narrow the specificity of more broadly responsive sex pheromone receptors may provide a mechanism that contributes to speciation.
Proceedings of the National Academy of Sciences 08/2012; 109(35):14081-6. DOI:10.1073/pnas.1204661109 · 9.67 Impact Factor