Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species

Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, MT 59717, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 08/2012; 109(35):14081-6. DOI: 10.1073/pnas.1204661109
Source: PubMed


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.

Download full-text


Available from: Peggy L Bunger,
66 Reads
  • Source
    • "At an extreme, some receptors belonging to the PR sub-family do not bind sex pheromone components but rather plant volatiles (Jordan et al., 2009; Bengtsson et al., 2014). Whereas functional properties are generally more conserved between orthologous genes from closely related species, only a few amino acid changes can modify these properties, sometimes drastically (Leary et al., 2012; Jiang et al., 2014; Steinwender et al., 2015). Moths from the genus Spodoptera (Lepidoptera, Noctuidae) form a group of economically important crop pests. "
    [Show abstract] [Hide abstract]
    ABSTRACT: In moths, mate finding strongly rely on the detection of sex pheromones by pheromone receptors (PRs). Any modification in the functional properties of these receptors can have a drastic impact on reproduction. In the course of characterizing candidate PRs in the noctuid moth Spodoptera littoralis, we expressed them in Drosophila olfactory sensory neurons and stimulated them with a large panel of moth pheromone compounds. We found that two PRs detect (Z,E)-9,12-14:OAc, a minor component of the female pheromone blend. Whereas SlitOR6 is highly specific to this component, SlitOR13 is less sensitive and not strictly specific as it also detects (Z)9-14:OAc, another minor component of the sex pheromone. Interestingly, SlitOR13 expression is restricted to the distal part of male antennae, where we could identify a novel functional class of pheromone-sensitive neurons whose response spectrum matches that of SlitOR13. Based on a phylogenetic analysis of Lepidoptera PRs, we found that the ability to bind (Z,E)-9,12-14:OAc appeared independently within three paralogous lineages, and an analysis of selective pressures revealed sites under positive selection that could have played a role in the emergence of functional properties of OR6 and OR13 in Spodoptera species.
    08/2015; 3. DOI:10.3389/fevo.2015.00095
  • Source
    • "The converse mutation ( A148T ) to O . nubilais OR3 reduced the sensitivity to E11 to a similar extent ( Leary et al . , 2012 ) . Similarly , a single amino acid substitution ( V91A ) in TMD2 of DmelOR59b , reflecting a natural polymorphism , significantly affected the response to the insect repellent DEET ( Pellegrino et al . , 2011 ) . Also a few amino acids at the interface between extracellular loop 2 ( ECL2 ) and TMD3 were implicated as determinants of od"
    [Show abstract] [Hide abstract]
    ABSTRACT: Insects detect odorants primarily using odorant receptors (OR) housed in the dendritic membrane of olfactory sensory neurons (OSN). Pioneering studies indicated that insects, like mammals, detect odorants in a combinatorial fashion with a specific odor ligand activating several broadly tuned ORs, and each OR being activated by several ligands. Several recent studies, however, challenge this view by providing examples where ecologically relevant odorants are detected by high-specificity ORs activating dedicated neuronal circuits. Here we review these contrasting findings on the ligand selectivity of insect ORs and their neuronal wiring, and outline scenarios describing how adaptive and neutral evolution might shape both narrow and broad receptor tuning. The fact that not all ORs display narrow tuning might partly be due to key ligands having been missed from screens or too high stimuli concentrations being used. However, the birth-and-death model of OR evolution, involving both adaptive and neutral events, could also explain the evolution of broad tuning in certain receptors due to positive selection or relaxed constraint. If the insect olfactory system indeed contains both narrowly and broadly tuned ORs, this suggests that it is a hybrid between dedicated channels and combinatorial coding. The relative extent of the two coding modes is then likely to differ between species, depending on requirements of perceived chemical space and the size of the OR repertoire. We address this by outlining scenarios where certain insect groups may be more likely to have evolved combinatorial coding as their dominant coding strategy. Combinatorial coding may have evolved predominantly in insects that benefit from the ability to discriminate between a larger number of odorants and odor objects, such as polyphagous or social species. Alternatively, combinatorial coding may have evolved simply as a mechanism to increase perceived odor space in species with small OR repertoires.
    05/2015; 3:53. DOI:10.3389/fevo.2015.00053
  • Source
    • "Functional studies on Drosophila melanogaster (Hallem et al., 2004) and Anopheles gambiae (Carey et al., 2010; Wang et al., 2010) support the theory that nPRs exhibit broad molecular receptivity. However, moth pheromone receptors (PRs) function according to a more rigid lock-and-key mechanism as they are activated by single pheromone components (Große-Wilde et al., 2007; Miura et al., 2009; Wang et al., 2011; Leary et al., 2012; Sun et al., 2013). Together, nPRs and PRs allow the peripheral olfactory system to encode the identity and quantity of odorants over a wide range of molecules and concentrations. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The molecular basis of odorant detection and its corollary, the task of the odorant receptor, are fundamental to understanding olfactory coding and sensory ecology. Based on their molecular receptive range, olfactory receptors have been classified as pheromone and non-pheromone receptors, which are respectively activated by a single pheromone component (" specialist ") or by multiple odorant ligands (" generalist "). This functional distinction is unique among ligand-gated ion channels and has shaped how we model olfactory coding both at the peripheral and central levels. Here, we revisit the long-standing combinatorial theory of olfaction and argue, based on physiological, pharmacological, evolutionary, and experimental grounds that the task of the odorant receptor is not different from that of neurotransmitter receptors localized in neuronal synapses.
    05/2015; 3. DOI:10.3389/fevo.2015.00039
Show more