Sex Pheromone Communication Research Articles

Host plant influences on sex pheromone behavior of phytophagous insects.

The sexual behavior of phytophagous insects is often integrated in a variety of ways with their host plants. This integration may be manifested as effects or influences of host plants on insect physiology and behavior, including sex pheromone communication, that reflect strategies by insects to optimize mating and reproduction. Certain insects sequester or otherwise acquire host plant compounds and use them as sex pheromones or sex pheromone precursors. Other insects produce or release sex pheromones in response to particular host plant cues. Chemicals from host plants often synergize or otherwise enhance insect responses to sex pheromones. By these means, host plants may be used by insects to regulate or mediate sexual communication. For many species of insects, host plant influences on insect sex pheromone communication may be important aspects of the formation of feeding and mating aggregations, of insect strategies to locate both hosts and mates, of behavioral reproductive isolation among sibling species, and of the regulation of reproduction to coincide with the availability of food and oviposition sites. Knowledge of these relationships is critical to understanding many different areas of the behavioral ecology of plant-feeding insects.

Use of Puffers for Disruption of Sex Pheromone Communication of Codling Moths (Lepidoptera: Tortricidae) in Walnut Orchards

Codlemone, ( E,E )-8,10-dodecadienol, the female sex pheromone of the codling moth, Cydia pomonella (L.), was released at 30-min intervals into the air of square, 16-ha walnut, Juglans regia L., orchards from puffers, machines designed for the dispensing of aerosols from pressurized canisters. The puffers were arrayed at 44-m intervals along the borders of the orchards. A codlemone release rate of 254 mg/ha per day caused a 9.5–98% disruption in pheromone communication. as measured by a reduction in the numbers of males that oriented to codlemone lure–baited or female-baited traps in the centers of the orchards.

Biosynthetic enzymes regulating ratios of sex pheromone components in female redbanded leafroller moths

Changes in key enzymes in the biosynthetic pathways of sex pheromone components can produce differences in component ratios and structures. The sex pheromone communication system is critical to reproduction and the maintenance of a species and so changes in this system can play a major role in the speciation process. Artificial selection of female redbanded leafroller moths that produced either higher or lower ratios of 14- 12 - carbon pheromone components was used to study how the biosynthetic pathways were affected in the high and low populations. The results showed that the chain shortening enzymes were selective for the ( E) isomer and so left the 14-carbon acyl intermediates enriched in the ( Z) isomer. Thus, the high population, which has a higher amount of 12-carbon components, also has a lower ratio of E11- Z11–14 : OAc pheromone components. The data also suggested that chain shortening occurred prior to reduction and acetylation of the 14-carbon components. These changes are not sufficient to isolate the redbanded leafroller populations, but we discuss some cases where significant changes in pheromone component ratios are affected by the chain-shortening enzymes.

Functional organization of the macroglomerular complex related to behaviourally expressed olfactory redundancy in male cabbage looper moths

Abstract. The neurophysiological bases for behaviourally expressed olfactory redundancy in the sex pheromone communication system of the cabbage looper moth, Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae), were examined by coupling the cut‐sensillum extracellular recording technique with a highly specific neuronal marking method for moth peripheral receptors. In seventy‐two antennal sensilla, axonal pathways of cobalt‐stained neurones could be traced into the male‐specific macroglomerular complex in the antennal lobe. In T. ni males this comprises five glomeruli, two of which are subdivided into morphologically, and in some instances functionally identifiable, regions. Axonal arborizations of forty‐eight neurones (single stainings) showed high fidelity (98%) for containment within a specific glomerulus or glomerular subdivision, and the neuropil targeted seemed to be related to the specificity of a neurone to a particular female‐emitted sex pheromone component (27‐12:Ac, Z7‐14:Ac, Z9‐14:Ac, 12:Ac, 11–12:Ac, Z5‐12:Ac), or to a behavioural antagonist (Z7‐12:OH). Double (twenty‐one) and multiple stainings (three) showed axons projecting into two or more glomeruli, respectively, with 100% fidelity for the component‐specific glomerulus or glomerular subdivision to be targeted. We suggest that the potential for a single minor component to cross‐stimulate two or more neurones within a sensillum may enable partial blends to continue to provide sensory input into all of the pheromone‐processing glomeruli of the complex. Our interpretation is that redundancy occurs at the receptor level on neighbouring dendrites, and thus allows various four‐component partial blends to evoke full pheromone‐mediated behaviour.

Pheromone behavioral responses in unusual male European corn borer hybrid progeny not correlated to electrophysiological phenotypes of their pheromone-specific antennal neurons

In genetic studies on the sex pheromone communication system of two races of European corn borer, which use opposite pheromone blends of the E and Z compounds, it was found that antennal olfactory cell response amplitudes to the two compounds were controlled by an autosomal factor, whereas behavioral responses to the blends were controlled by a sex-linked locus. Because of the difference in genetic controls, it was postulated that some unusual males would be produced in F2 crosses between these two races. These unusual males would have antennal olfactory cells that respond as the Z-race males, but would respond behaviorally to the E blend. The present studies combined behavioral studies in a flight tunnel and single cell electrophysiological studies to show that these unusual males do indeed exist. These findings show that the spike amplitude of peripheral olfactory cells is not important in regulating species- or race-specific pheromone responses, as compared to some central nervous system factor assesses the spike frequencies from different pheromone-component-specific cells on the antenna. This factor seems to be essential in governing the pheromone-blend specific behavioral responses of male moths.

Electrophysiological and behavioural evidence for a fourth sex pheromone component in the turnip moth, Agrotis segetum

Abstract. In addition to the pheromone components (Z)‐5‐decenyl, (Z)‐7‐dodecenyl and (Z)‐9‐tetradecenyl acetate (Z5‐10:OAc, Z7‐12:OAc and Z9‐14:OAc), it has previously been shown that the sex pheromone gland of the turnip moth, Agrotis segetum (Lepidoptera: Noctuidae Schiff) contains 10:OAc, 12:OAc, Z5‐12:OAc, Z9‐12:OAc, 11–12:OAc, Z5‐14:OAc, Z7‐14:OAc and Z11‐16:OAc. To find out whether any of these additional compounds is involved in the sex pheromone communication in A. segetum, a comprehensive electro‐physiological and behavioural investigation was conducted. Single‐sensillum recordings on male antennae revealed three subtypes of sensilla among the previously so‐called Z5‐10:OAc sensilla. One subtype was identified having one receptor neurone (A) that responded to Z5‐10:OAc with a large spike amplitude and another neurone (B) that responded to (Z)‐5‐decenol (Z5‐10:OH) with a small spike amplitude. In another subtype the B neurone responded to Z5‐12:OAc and sometimes also to 27‐12:OAc and 10:OAc, in addition to responding to Z5‐10:OH. In a third subtype the A neurone responded to all acetates identified from the female pheromone gland, whereas the small spike amplitude neurone was tuned to Z5‐10:OH. A flight tunnel assay showed that blends composed of nine, eight or seven compounds were equivalent to the previously identified three‐component pheromone blend in eliciting male behavioural responses. In field trapping tests, blends of eleven, nine or seven compounds did, however, catch significantly more moths than the three‐component blend. Further assays showed that only 25‐ 12:OAc could significantly increase the catch numbers when added to the three‐component blend, and thus qualified as a fourth pheromone component in A. segerum. The behavioural significance of additional female‐produced acetates — for which males possess antennal receptors — is suggested, but may be impossible to confirm because of ‘diminishing returns’ when trying to refine a multicomponent pheromone further.

Codling moth (Cydia pomonella): Disruptants of sex pheromonal communication

In a small section of an apple orchard, six traps were placed each in control and test areas and baited with live virgin female codling moths. Gray elastomer septa were used to dispense communication disruptants around the traps. Dyed male codling moths were released in control and test areas, and the numbers of males captured in control and test traps were compared. In 1991, linear regression curves of percent communication disruption versus logarithm of dose were obtained for three compositions: (E,E)-8,10-dodecadien-1-ol, codlemone (1); codlemone + dodecan-1-ol + tetradecan-1-ol (2); and an equilibrium mixture of the four isomers of 8,10-dodecadien-1-ol (30, (61%EE, 14%ZE, 20%EZ, and 5%ZZ). All three regressions gaver (2) values greater than 0.90. At the 95% confidence limits, slopes and intercepts of compositions 1 and 2 were equivalent, and different from that of composition 3, which produced the greatest percentages of disruption at all doses. In 1992, five treatments were compared at a single dose: 1, 3, none (4), (Z,E)-8,10-dodecadien-1-ol (5), (E,Z)-8,10-dodecadien-1-ol (6). Compositions 5 and 6 gave the greatest and similar percentages of disruption and were different from codlemone (1) and 4 (95% confidence), but not from composition 3. Communication disruption produced by composition 3 was greater than (codlemone), which was greater than 4.

Moth pheromone genetics and evolution

Sex pheromone communication in moths is a well investigated case of mate-finding by chemical signals, but the evolutionary causes of the great complexity and diversity of these signals are still not generally agreed on. In the present paper, I argue that there is no reason to dismiss species recognition as a possible cause of evolutionary change in moth sex pheromones. Admittedly, selection for species recognition cannot explain all of the diversity in sex pheromones and the data supporting this contention are weak, but the alternative causes suggested, invoking mate choice between conspecifics as the mechanism of sexual selection, has so far no empirical support. Finding and analysing genes responsible for m ate choice is important to corroborate any theory of sexual selection and speciation. In this respect genetic dissection of moth pheromone communication has provided important progress. Mendelian genes controlling differences in m ate choice and in the production of mate recognition signals have been found. Polymorphic pheromone systems give the population biologists unique possibilities to study mate choice and selection at the genotype level in nature.

Attraction of male beetles to grubs: Evidence for evolution of a sex pheromone from larval odor

Females of the scarabaeid beetleCyclocephala lurida produce a volatile sex pheromone which attracts conspecific males. Field experiments demonstrated that larvae of both sexes also emit volatile chemicals that stimulate similar responses in adult males, including attempts by the attracted males to mate with the nonreproductive immature stage. Significantly more adult males were caught in traps baited with conspecific male or female larvae or adult females than in blank control traps. Hexane extracts of both male and female grubs were at least as effective as live larvae in trapping male adults, demonstrating that the behavioral responses are mediated by volatile chemicals. Sensory and behavioral responses of males to sex pheromones emitted by adult females are part of the functional communication system. However, their response to grubs is not functional, because grubs are normally temporally and spatially inaccessible to mate-seeking males. In theory, the evolution of a communication system is problematic because it requires the development of a signal in one sex and the sensory and behavioral attributes to respond to that signal in the other sex. The ontogeny of sex pheromone communication inC. lurida suggests a partial solution to this evolutionary problem. We propose that this sex pheromone communication system is probably derived from noncommunicative volatile chemicals that are lost in adult males and retained by adult females.

Sex pheromones and their potential role in the evolution of reproductive isolation in small ermine moths (Yponomeutidae)

Sex pheromone communication in the nine European species of small ermine moths (Yponomeuta) is reviewed in regard to the potential role of pheromones in the speciation process. Six of the nine species studied (viz.,Y. evonymellus, Y. cagnagellus, Y. padellus, Y. irrorellus, Y. plumbellus, andY. vigintipunctatus) use a mixture of (E)-11-and (Z)-11-tetradecenyl acetate in different ratios as primary pheromone components, with combinations of tetradecyl acetate, (Z)-9-tetradecenyl acetate, (Z)-11-hexadecenyl acetate and the corresponding alcohols of the acetates as additional pheromone components. Analysis of (Z)- to (E)-11-tetradecenyl acetate ratios produced by individual females of these species demonstrated significant variation among females of all species. However, the ranges of ratios produced byY. cagnagellus, Y. irrorellus, andY. plumbellus, sharing the same host-plant species, spindle tree, did not overlap. Niche separation of all six species mentioned required consideration of at least one additional pheromone component or of temporal aspects. The remaining three species,i.e. Y. malinellus, Y. mahalebellus andY. rorellus, have pheromones that differ qualitatively. Biosynthetic routes to the pheromone components identified are proposed on the basis of fatty acid pheromone precursors found in the pheromone glands. A phylogenetic tree for the genus is constructed based on allozyme frequency data and changes in pheromone composition are superimposed on this tree. We suggest that the ancestral ermine moth pheromone is a mixture of (Z)-11- and (E)-11-tetradecenyl acetate and the corresponding alcohols, and a scenario of how present-day patterns evolved is outlined. The pheromone differences among the three species using spindle tree as their host-plant might have evolved throughreproductive character displacement upon secondary contact between populations that had already diverged genetically in allopatry. Pheromone differences within the so-calledpadellus-complex (includingY. cagnagellus, Y. mahalebellus, Y. malinellus, Y. padellus, andY. rorellus) in which species might have originated sympatrically, may have evolved byreinforcing selection as these species still hybridise and produce viable offspring when confined in cages. The role of pheromones in reproductive isolation amongYponomeuta species is emphasised by (1) the function of pheromone components of some of the species as behavioural antagonists to other species, (2) the cross-attraction under experimental conditions between allochronic species with similar pheromones, and (3) the formation of hybrids in the laboratory between species that are isolated in nature by pheromone differences.

Sex pheromone communication in the screwworm,Cochliomyia hominivorax: Ontogenetic and strain effects

A laboratory behavioral assay was used to examine ontogenetic and strain effects on sex pheromone production and reception in the screwworm, which employs a female-produced contact pheromone to stimulate male copulatory attempts. Pheromone levels peaked between three and six days after adult emergence in females of two strains that had been colonized fewer than 50 generations. Pheromone was detectable at low levels in newly emerged flies of both sexes but disappeared from males by two days of age, when males first became responsive to females. A similar decline in pheromone with ontogenetic age was previously described for females of a strain colonized over 100 generations. Interstrain tests between the two newer strains, which differed by 35 generations in duration of colonization, demonstrated lower female pheromone activity but higher male responsiveness to pheromone in the older strain, despite the similar shape within these strains of curves relating female age and pheromone activity. The data suggest that conditions of screwworm colonization result in gradual loss of the pheromone peak that develops three to six days after emergence in newly colonized females. Higher male responsiveness associated with longer colonization involved change in both thresholds and dose dependency and may be relevant to control of the screwworm via the sterile insect technique.

Gene Flow Among Three Races of European Corn Borers (Lepidoptera: Pyralidae) in New York State

In New York state, there are three races of European corn borer moths, which are characterized principally by differences in voltinism and the sex pheromone communication system. One race is bivoltine, with females producing and males responding to a 99:1 E / Z isomeric ratio of ∆11-14:0Ac's as the sex pheromone. Two races, one univoltine and one bivoltine, produce and respond to a 3:97 E / Z blend of ∆11-14:OAc's. The races are referred to as BE, UZ, and BZ to denote these differences. Analyses by gas chromatography of field-collected females indicate that there is significant hybridization between the Z and E races when in sympatry, with hybrid females producing a 68:32 ratio of E / Z 11-14:OAc. Gene flow among the races was investigated using differences in triose phosphate isomerase (TPI) allozyme frequencies of moths from sites sampled across the state. The fixed nature of the Tpi-1 allele in the BE race and increases in the Tpi-1 allele frequencies in UZ populations in sympatry with the BE race support the hypothesis that gene flow following hybridization is unidirectional from BE populations into the Z populations. In addition, the TPI genotypes of the 10 hybrid females analyzed were consistent with hybridization occurring by E males mating with Z females.

Disruption of Sex Pheromone Communication in Cylas formicarius (Coleoptera: Apionidae) as a Potential Means of Control

Sweetpotato weevil, Cylas formicarius (Fabricius), is the most limiting factor of sweet potato, Ipomoea batatas (L.) Lam., production worldwide (Jansson & Raman 1991). Feeding and oviposition damage in roots and vines can cause severe cosmetic and economic damage. In response to tissue damage, sweet potato roots produce foul tasting terpenoids (Uritani et al. 1975) rendering them unpalatable for human consumption. Thus, commercial growers can tolerate very little sweetpotato weevil damage. Historically, weevil management has relied heavily on cultural and chemical control (Sutherland 1986, Chalfant et al. 1990). However, chemical control provides little protection once an egg is laid because immatures develop within roots and vines (Chalfant et al. 1990). Cultural controls, such as sanitation, crop rotation, planting away from weevilinfested fields, removal of alternate hosts, hilling plants, etc., can help to reduce damage (Talekar 1991); however, they require considerable labor and have not been universally adopted. Recent studies indicate that entomopathogenic nematodes and sex pheromones may provide new means to control the sweetpotato weevil (Jansson 1991, Jansson et al. 1991). Pheromones have typically been used three ways: (1) monitoring insect populations using pheromone-baited traps; (2) mass-trapping, where large numbers of traps are used to reduce the insect population; and (3) mating disruption, in which the pheromone is used at high dosages to permeate the atmosphere so as to disrupt communication between the sexes, thus reducing mating (Kydonieus & Beroza 1982, Campion 1984). Mating disruption has been examined in many insect systems (McLaughlin et al. 1972, Shorey et al. 1972, Landolt et al. 1982, Sower 1982, Schwalbe & Mastro 1988, for reviews see Kydonieus & Beroza 1982, Campion 1984), and in general, some success has been achieved. The objective of our study was to examine the potential of sweetpotato weevil synthetic sex pheromone as a mating disruptant by examining male confusion (i.e. communication disruption) in a large commercial field plot.

Electrophysiological and chemical analysis of sex pheromone communication system of the mottled umber,Erannis defoliaria (Lepidoptera: Geometridae)

(Z,Z,Z)-3,6,9-nonadecatriene (Z3,Z6,Z9-19Hy) and (Z,Z)-3,9-cis-6,7-epoxy-nonadecadiene (Z3,Z9-cis-6,7-epo-19Hy) were identified in pheromone gland extracts from femaleErannis defoliaria. The two components were found in a 1∶3 ratio, with the main component,Z3,Z9-cis-6,7-epo-19Hy present at an amount of about 1.5 ng per female. The components were identified by means of gas chromatography-mass spectrometry, gas chromatography-electroantennography and gas chromatography-single sensillum recordings. Single sensillum measurements on the male antenna showed two physiological types of sensilla. One type was characterized by a large spike amplitude cell responding toZ3,Z9-cis-6,7-epoxy-19Hy and a small spike amplitude cell responding toZ3,Z6,Z9-19Hy. A second type responded only with a large spike amplitude cell to the epoxide, and this cell was inhibited by the triene. Of the two pheromone components, the epoxide gave the higher response in the EAG tests. Preliminary field tests support the identification of the pheromone components. The epoxide was also found to be present in the extract of the pheromone gland ofColotois pennaria, and males ofC. pennaria andAgriopis marginaria were trapped by the mixture of the identified compounds.

Sex pheromone communication in brachionus plicatilis (rotifera)

1. 1. Sex pheromone communication plays an important role in regulating mating behavior of aquatic invertebrates but is poorly understood. A mate recognition bioassay using the rotifer Brachionus plicatilis is described that permits investigation of the molecular nature of chemical communication between females and males. 2. 2. The female signal molecule is a glycoprotein that can be removed by washing females with 10 mM CHAPS or 100 mM EDTA. Washing females with 100 mM sodium phosphate pH 8.0, 2 M NaCl or 100 mM Tris-HCl pH 9.5 had no effect on their ability to elicit male mating responses. 3. 3. Females treated with the glycosidase N-glycanase for 5 min elicited significantly fewer male copulations than untreated females. Males treated with N-glycanase for 10 min attempted significantly fewer copulations with females. 4. 4. Lectins were used to probe the biochemical features of the oligosaccharide portion of the MRG. Females were exposed to nine lectins and evaluated for their ability to elicit male mating responses. Five lectins did not block mate recognition, but females treated with Concanavalin A, Lens culinaris, Pisum sativum and Vicia faba lectins elicited male mating with a lower probability than control females. Males treated with these same five lectins had lower rates of copulation with untreated females. 5. 5. Dose-response experiments revealed that females treated with 112 μg/ml of Con A and 15 μg/ml of Lens elicited only 50% as many male mating attempts as control females.

Sex pheromone communication in the lepidoptera: New research progress

Significant progress has been made recently in research on lepidopterous sex pheromones. Advances in understanding the biochemical, neurobiological, and behavioral events that results in both successful and unsuccessful pheromone communication have allowed researchers to gain new insights into the genetic control and evolution of phermone systems.

Genetic regulation of sex pheromone production and response

The sex pheromone communication system of the European corn borer moth varies intraspecifically. Analyses of pheromonal extracts of wild females, collected in a region where the types (each producing a different isomeric proportion ofZ- andE-11-tetradecenyl acetate) are sympatric, showed that theZ pheromone-production allele frequency was ca. 4 times greater than theE allele. The paucity ofE production and response alleles in the population indicates that moths inheriting those alleles concomitantly inherit some undefined disadvantage. The types interbreed, but the frequency of heterozygous pheromone-production types among wild females was less than predicted by Hardy-Weinberg equilibrium and was evidence of positive assortative mating. Rates of male captures in field traps baited with females of the three pheromonal types also evidenced assortative mating in the population. Progeny tests with males captured in the traps provided circumstantial evidence that pheromone response and production functions in the species are regulated by separate genetic loci and that the loci are not always complementary; i.e., a male can carry an allele coding for production of one pheromonal isomer ratio but can be genetically predisposed to respond to another.

Control of Rhyacionia zozana (Lepidoptera: Tortricidae) by Mating Disruption with Synthetic Sex Pheromone1

Hercon laminated-tape dispensers containing synthetic sex pheromone (a 95:5 mixture of E-9-dodecenyl acetate and E-9-dodecenol) of the ponderosa pine tip moth, Rhyacionia zozana (Kearfott), were manually applied on 57 ha of ponderosa pine plantations in southern Oregon. The nominal dosage was 13.5g of pheromone (AI)/ha from 100 releasers per hectare spaced at 10 m. Male moth response to pheromone-baited traps and to virgin females in mating tables showed nearly total disruption of female sex pheromone communication with males. After the mating-disruption application, larval populations were reduced 83.2%in treated areas. The frequency of damaged terminal shoots was lower in pheromone-treated plantations than in check plots.

Cross-attraction of Five Species of Stored-product Phycitinae (Lepidoptera: Pyralidae) in a Wind Tunnel

Sharing of the sex-pheromone communication channel by five species of phycitine moths was measured in a wind tunnel. Overall, male pheromonal response was characterized both by high levels of interspecific attraction and broad overlap in the circadian periods of male response, with attraction to nonconspecific females 75% of that to conspecifics, on average. Cadra cautella (Walker), Plodia interpunctella (Hubner), and Anagasta kuehniella (Zeller) males demonstrated high levels of upwind-flight response throughout an 8-h scotophase. P. interpunctella and A. kuehniella males responded to nonconspecific females at levels that were as high as to conspecifics. Ephestia elutella (H¨bner) males showed the greatest level of response discrimination with the probability of flight to nonconspecific females only 41% of that to conspecific females, although relative importance of pheromonal differences and temporal effects could not be determined. Poor reproductive isolation by long-distance parameters points to a greater reliance on less efficient short-range mechanisms, such as courtship and male pheromones. Significance of these findings to current thought concerning evolution of reproductive isolating mechanisms is considered.

Characterization of a sex pheromone in the blue crab,Callinectes sapidus: Crustecdysone studies

The molting hormone/sex pheromone hypothesis of Kittredge and Takahashi (1972) and Kittredge et al. (1971) was explored inC. sapidus. Two concentrations of crustecdysone (5 × 10(-5) M and 5 × 10(-6) M) were presented to male crabs in a bioassay system in which courtship behavior was monitored. The results demonstrate that crustecdysone does not stimulate courtship in this species. The physical properties of crustecdysone were also compared to those of the partially purified sex pheromone derived from pubescent females. Using HPLC and mass spectral analysis, no correspondence of crustecdysone with the bioactive material could be shown. These results, in conjunction with the findings of others, do not support an evolutionary relationship between the molting hormone and sex pheromone communication in the Crustacea.