Sex pheromones specificity

After considering the evolutionary origins of the olfactory system and some basic principles of olfaction, this brief review examines one of the most extensively studied examples of neural processing of semiochemical information the sex pheromone-specific olfactory subsystem in male moths. This male-specific subsystem can be viewed as representing an exaggeration of organizational principles and functional mechanisms that are characteristic of olfactory systems in general. 

Hansson B. S., Hallberg E., Lofstedt C. and Steinbrecht R. A. (1994) Correlation between dendrite diameter and action potential amplitude in sex pheromone specific receptor neurons in male Ostrinia nubilalis (Lepidoptera pyralidae). Tissue Cell 26, 503-512. 

Ochieng S. A., Park K. C. and Baker T. C. (2002) Host plant volatiles synergize responses of sex pheromone-specific olfactory receptor neurons in male Helicoverpa zea. J. Comp. Physiol. A 188(4), 325-333. 

Carde, R. T., Carde, A. M., Hill, A. S. and Roelofs, W. L. (1977) Sex pheromone specificity as a reproductive isolating mechanism among the sibling species Archips argyro-spilus and A. mortuanus and other sympatric tortricine moths (Lepidoptera Tortri-cidae). J. Chem. Ecol., 3, 71-84. 

Jewett, D. M., Matsumura, F. and Coppel, H. C. (1976) Sex pheromone specificity in the pine sawflies interchange of acid moieties in an ester. Science, 192, 51-3. 

Roelofs, W. L. and Comeau, A. (1969) Sex pheromone specificity Taxanomic and evolutionary aspects in Lepidoptera. Science, 165, 398-400. 

Iwata T., Umezawa K., Toyoda F., Takahashi N., et al. (1999). Molecular cloning of newt sex pheromone precursor cDNAs evidence for the existence of species-specific forms of pheromones. FEBS Lett 457, 400-404. 

Lepidoptera is the second largest insect group and includes nearly 150,000 described species, which have evolved over 100 million years since the Mesozoic era. For the birth of a new species, it must be isolated from other species by some factor to prevent inter-species crossing. The sex pheromone, which is secreted by the adult (usually by a female moth and sometimes by a male moth or butterfly) for the benefit of a specific partner, plays an important role in reproductive isolation. Therefore, it is no wonder that the chemical structures of the species-specific pheromones exhibit considerable differences. 

Specific chain length fatty acids could be produced in two ways. One is through the action of a thioester hydrolase that interacts with fatty acid synthetase to produce fatty acids shorter in length. Aphids produce myristic acid (14 carbons) and a specific thioester hydrolase releases the fatty acid from fatty acid synthetase after 6 additions of malonyl-CoA. If the hydrolase is not present then the fatty acid synthetase produces stearic acid [27]. A specific thioester hydrolase was ruled out in the biosynthesis of moth sex pheromones because labeling studies showed that longer chain length fatty acids were incorporated into shorter chain length pheromone components [22,28]. 

Several families of moths utilize hydrocarbons or epoxides of hydrocarbons as their sex pheromone. Oenocyte cells produce hydrocarbons that are transported through the hemolymph by lipophorin [71]. In a study using arctiid moths it was shown that sex pheromone hydrocarbons are transported on the same lipophorin particle as the hydrocarbons destined for the cuticular surface [ 17]. Therefore, specific uptake of the sex pheromone hydrocarbon occurred in pheromone glands [17]. Similar findings have been found with other moths [72-74]. The mechanism behind this specific uptake of one hydrocarbon from a potential pool of other hydrocarbons is unknown. 

One of the sex pheromone components of the housefly, Musca domestica, is Z9-21 H that is found on the cuticular surface of the fly. This compound is formed by the elongation of Z9-18 CoA using malonyl-CoA and NADPH to Z15-24 CoA which is decarboxylated to form Z9-21 Hc (Fig. 3) [78-80]. Other pheromone components include an epoxide and ketone that are produced from Z9-21 Hc by a cytochrome P450 [81,82] and methyl-branched alkanes that are produced by the substitution of methylmalonyl-CoA in place of malonyl-CoA at specific points during chain elongation [83,84]. A novel microsomal fatty acid synthase is involved in production of methyl-branched alkanes in most insects [85-87]. This fatty acid synthase is different from the ubiquitous soluble fatty acid synthase that produces saturated straight chain fatty acids in that it is found in the microsomes and prefers methylmalonyl-CoA. The amino acids valine and isoleucine can provide the carbon skeletons for methylmalonyl-CoA as well as propionate [83]. 

Chlorpyrifos inhibits substrate-borne reception and emission of sex pheromone in Tri-chogramma brassicae, an entomophagus insect massively used as a biological control agent of com borers, among survivors of an LC20 dose. Inhibition was probably due to nervous system effects and was not specific to pheromone communication (Delpuech et al. 1998). 

The sex pheromone communication system basically involves the release of specific chemicals from a pheromone producer (emitter), the transmission of these chemicals in the environment to a receiver, and the processing of these signals to mediate appropriate behavioral responses in the receiver. The chemicals transmitted downwind have been the most obvious targets for characterization. The code was first broken with the publication in 1959 (3) of the sex pheromone for the domesticated silkworm Bombyx mori after extraction of a half million female silkworm pheromone glands and 30 years of classical chemical analyses. The pheromone was found to be (E10, Z12)-hexadecadien-l-ol, which was called bombykol. This work showed that there was nothing magical about the communication system, and chemists around the world were "attracted" to this area of research on insect pheromones. 

FIGURE 3 Pheromone biosynthetic pathways commonly used in moth sex pheromone glands to produce precursors for specific blends of acetates, alcohols, or aldehydes. Cascades of precursors are produced by combinations of unique A- -desaturases and limited chain-shortening steps. The six precursors for the cabbage looper blend (Figure 2) are in boldface type. 

The sex pheromones of moths generally are mixtures of two or more chemical components, typically aldehydes, acetates, alcohols, or hydrocarbons, produced in specialized glands by biosynthesis and modification of fatty acids (34). Often, a species-specific blend of components is the message, and males of many moth species, including M. sexta, give their characteristic, qualitatively and quantitatively optimal behavioral responses only when stimulated by the correct blend of sex-pheromone components and not by individual components or partial blends lacking key components (43, 44). 

Axons of antennal ORCs project through the antennal nerve to enter the brain at the level of the ipsilateral antennal lobe (AL) of the deutocerebrum (52). ORC axons project from the flagellum to targets in the AL, but axons from antennal mechanosensory neurons bypass the AL and project instead to an "antennal mechanosensory and motor center" in the deutocerebrum posteroventral (with respect to the body axis of the animal) to the AL (52, 58, 64). In moths and certain other insect groups, sex-pheromonal information is processed in a prominent male-specific neuropil structure in each AL called the macroglomerular complex (MGC) (16, 52, 64, 65). 

Axons of male-specific antennal ORCs specialized to detect components of the sex pheromone project exclusively to the MGC (64, 89), and all AL neurons that respond to antennal stimulation with sex pheromone components have arborizations in the MGC (65, 72, 73). The MGC in M. sexta has two major, easily distinguishable divisions a donut-shaped neuropil structure (the "toroid") and a globular structure (the "cumulus") adjacent to the toroid and closer to the entrance of the antennal nerve into the AL (74). AL PNs that respond to antennal stimulation with sex pheromone component A have arborizations in the toroid and PNs responsive to component B, in the cumulus (74). Thus first-order synaptic processing of sensory information about these key components of the sex pheromone apparently is confined to different, distinctive neuropil regions of the MGC. 

By means of intracellular recording and staining methods, we have examined the responses of AL neurons to stimulation of the ipsilateral antenna with each of the sex pheromone components as well as partial and complete blends (75). In accordance with results of behavioral and sensory-receptor studies, components A and B are the most effective and potent sex pheromone components for eliciting physiological responses in the male-specific AL neurons. On the basis of these responses, we classified the neurons into two broad categories pheromone generalists and pheromone specialists (76). Pheromone generalists are neurons that respond similarly to stimulation of either the component A input channel or the component B input channel and do not respond differently when the complete, natural pheromone blend is presented to the antenna. In contrast, pheromone specialists are neurons that can discriminate between antennal stimulation with component A and stimulation with component B. There are several types of pheromone specialists. Some... 

The male moth s pheromone-analyzing olfactory subsystem is composed of pheromone-specific antennal ORCs projecting to the similarly specialized, anatomically defined MGC in the AL and MGC output neurons that project to olfactory foci in the protocerebrum. This subsystem is an example of a labeled-line pathway (18). Its specialization to detect, amplify, and analyze features of sex-pheromonal signals and its consequent exaggeration of common olfactory organizational principles... 

This way of viewing the olfactory system spotlights the kinds of information about odor stimuli to which the brain attends. For example, although the blend of components is essential to evoke and sustain the normal male responses to the sex pheromone, information about specific components is preserved through many levels of the pathway. Thus it appears that information about single components as well as their blend may be important for chemical communication in these insects. 

---