Male Pheromone Response Research Articles

Genetic mapping of male pheromone response in the European corn borer identifies candidate genes regulating neurogenesis

The sexual pheromone communication system of moths is a model system for studies of the evolution of reproductive isolation. Females emit a blend of volatile components that males detect at a distance. Species differences in female pheromone composition and male response directly reinforce reproductive isolation in nature, because even slight variations in the species-specific pheromone blend are usually rejected by the male. The mechanisms by which a new pheromone signal-response system could evolve are enigmatic, because any deviation from the optimally attractive blend should be selected against. Here we investigate the genetic mechanisms enabling a switch in male response. We used a quantitative trait locus-mapping approach to identify the genetic basis of male response in the two pheromone races of the European corn borer, Ostrinia nubilalis Male response to a 99:1 vs. a 3:97 ratio of the E and Z isomers of the female pheromone is governed by a single, sex-linked locus. We found that the chromosomal region most tightly linked to this locus contains genes involved in neurogenesis but, in accordance with an earlier study, does not contain the odorant receptors expressed in the male antenna that detect the pheromone. This finding implies that differences in the development of neuronal pathways conveying information from the antenna, not differences in pheromone detection by the odorant receptors, are primarily responsible for the behavioral response differences among the males in this system. Comparison with other moth species reveals a previously unexplored mechanism by which male pheromone response can change in evolution.

The roles of juvenile hormone and biogenic amines on pheromone response plasticity and diapause termination in male Caloptilia fraxinella

AbstractIn insects that exhibit a period of delayed reproduction, the timing of mating and reproduction is controlled by environmental conditions that regulate endogenous factors such as hormones and biogenic amines (BAs). Caloptilia fraxinella (Ely) (Lepidoptera: Gracillariidae) undergoes a 9‐month reproductive diapause from adult eclosion in the summer until diapause termination the following spring when adults mate. Male response to female sex pheromone is plastic, and is most acute when moths are reproductively active. The aim of this study is to further elucidate the mechanisms involved in the regulation of male response to pheromone in C. fraxinella, and to test whether the application of BAs with and without a juvenile hormone analogue (JHA) to males in different physiological states impacts pheromone responsiveness, as measured by electroantennogram and wind tunnel bioassays. Treatment of male C. fraxinella in reproductive diapause with one application of a JHA induces the highest subsequent pheromone response in the fall, but does not alter pheromone response earlier in reproductive diapause in the summer. The JHAs methoprene and pyriproxyfen similarly enhance pheromone response in the fall. Treatment with methoprene alone or in combination with one of the BAs octopamine, dopamine or serotonin increases male pheromone responsiveness in the fall. The increase in pheromone response can be attributed to methoprene only, as treatment with any of the BAs alone does not enhance male response to pheromone. Biogenic amine treatment lowers male responsiveness to pheromone in some experiments, indicating that there may be a role for BAs in maintaining low pheromone response during reproductive diapause in this species.

Environmental conditions terminate reproductive diapause and influence pheromone perception in the long‐lived moth Caloptilia fraxinella

AbstractReproductive diapause enables long‐lived insects to time mating with environmental conditions suitable for offspring development. Plasticity in the perception of pheromones used in sexual communication may enable mate‐finding at the appropriate time of year. The moth Caloptilia fraxinella (Ely) (Lepidoptera: Gracillariidae) undergoes a 9‐month reproductive diapause, during which the male response to pheromone is plastic and is highest during the period of reproductive activity. The mechanisms controlling this pheromone response plasticity are not well‐understood, and the aim of the present study is to determine the main factors involved. In the present study, the impact of temperature, photoperiod, juvenile hormone analogue (JHA) and adult nutrition on diapause termination are tested using electroantennogram (EAG) and behavioural response to pheromone in male C. fraxinella. Eclosion in a state of reproductive diapause occurs in most males; diapause is maintained under short‐day or cool conditions indoors, or under natural conditions outdoors. Exposure to long‐day, warm conditions over a period of 4 weeks causes a small number of males to become behaviourally responsive to pheromone; a larger number of males become behaviourally responsive over a period of 3 months of post‐eclosion. Treatment with a JHA impacts male EAG and the behavioural response to pheromone during the period of reproductive diapause. A carbohydrate food source is not required by reproductively active adult male C. fraxinella to respond to pheromone and express mate location behaviours. The main factors involved in controlling male pheromone response plasticity and the implications of these factors for the C. fraxinella population in its expanded range are discussed.

Trade-Off Between Sensitivity and Specificity in the Cabbage Looper Moth Response to Sex Pheromone

The evolution of male moth responses to pheromone blends may be constrained by a trade-off between two response traits: sensitivity and breadth of response. Population genetic simulations predict that if sensitivity and breadth of response are negatively correlated (i.e., a trade-off exists), then selection will favor males with narrow response phenotypes and high sensitivity. Although sensitivity-breadth of response trade-offs are generally assumed to exist and are implicit to the shape of male preference function, this study is the first to provide empirical support measuring behavior at the level of the individual. Previous studies with the cabbage looper, Trichoplusia ni, have documented the existence of a mutant pheromone strain. While mutant females produce a pheromone blend significantly different from wild-type females, mutant males respond equally to the wild-type and mutant pheromone blends. This study used wind tunnel bioassays to document that relative to wild-type males, mutant males had broader response profiles but lower pheromone sensitivity. While wild-type male responses were highest to the wild-type pheromone blend, mutant males did not discriminate among pheromone blends. These results are consistent with a trade-off between breadth of response and sensitivity. Pure wild-type and mutant lines were crossed and hybrid males assayed. Both hybrid types (maternal wild-type and maternal mutant hybrids) responded similarly. Hybrid males had response profiles similar to wild-type males and the reduced sensitivity observed in mutant males. These results suggest a possible hybrid disadvantage and a putative mechanism for reinforcement of male pheromone response traits.

Circadian mating activity and effect of pheromone pre-exposure on pheromone response rhythms in the moth Spodoptera littoralis

Mating in moths is generally mediated by female-produced sex pheromones. Mating activity, female pheromone production/release and male pheromone responsiveness all show diurnal variations in many species. We found that the response of the male Egyptian cotton leafworm, Spodoptera littoralis, to sex pheromone gland extracts showed a diel rhythm in olfactometer tests, and the variation was persistent for at least 1 day in constant darkness. High male response to sex pheromone was correlated in time with high mating and locomotor activity. Male S. littoralis, maintained in constant darkness and exposed to pheromone gland extracts on a daily basis, showed an induced temporal variation in response after several days, in contrast to unexposed males. This suggests that in the absence of other external zeitgebers, exposure to sex pheromone may function to synchronise circadian behavioural rhythms in male moths. The daily rhythm in mating activity in S. littoralis is also shown to be persistent for at least 2 days in constant darkness. Pairs mated significantly less when either the male or female had been raised in a light:dark cycle 10 h out of phase, indicating that the proposed circadian rhythm in mating activity is composed of rhythmic mating preference/ability in both sexes.

Mating Response Behavior of Sterile Pink Bollworms (Lepidoptera: Gelechiidae) Compared with Natives

A timing pheromone trap was invented to capture male pink bollworm adults Pectinophora gossypiella (Saunders) for specific time intervals as they entered a commercial pheromone trap. The device was used to compare the window of male pheromone response of two different strains of released sterile pink bollworm populations with responses of native adult males. In all trials in cotton fields in Phoenix, AZ, and in Palo Verde, CA, the released sterile male adults entered commercial pheromone traps during the same time interval as native adult males. Native and sterile females were comparable in attracting and successfully mating with natives when confined in field stations. Thus, the quality of behavioral responses (male-pheromone response window) of laboratory-reared male pink bollworms was comparable to native adults infesting cotton fields in Arizona and California.

Analysis of Some Biological Factors Affecting Differential Pheromone Trap Efficiency between Generations in the Rice Stem Borer Moth, Chilo suppressalis(WALKER)(Lepidoptera:Pyralidae)

Pheromone trap efficiencies in C. suppressalis tend to be relatively low in the first generation as compared to those of the overwintered generation. In order to clarify the factors affecting this phenomenon, three possible biological aspects, such as the male pheromone responsiveness, the flight ability of male moths, and the effect of female population densities were compared between the two generations. The responses of male moths to varying doses of the synthetic sex pheromone were not significantly different between the two generations for each concentration. No significant differences in the flight ability (duration, distance, sped) between the two generations were found. Significant declines in pheromone trap catches with increasing female population densities, evaluated by the light trap catches, were detected in both generations. However, the effects of the female population density were apparently greater in the first generation than in the overwintered one. Consequently, the female population density in the paddy fields was thought to be one of the critical factors affecting the difference in pheromone trap performance between the two generations.

No Evidence for Selection in a Pheromonally Polymorphic Moth Population

Previous articleNext article No AccessNotes and CommentsNo Evidence for Selection in a Pheromonally Polymorphic Moth PopulationBengt O. Bengtsson and Christer LofstedtBengt O. Bengtsson Search for more articles by this author and Christer Lofstedt Search for more articles by this author PDFPDF PLUS Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by The American Naturalist Volume 136, Number 5Nov., 1990 Published for The American Society of Naturalists Article DOIhttps://doi.org/10.1086/285127 Views: 2Total views on this site Citations: 8Citations are reported from Crossref Copyright 1990 The University of ChicagoPDF download Crossref reports the following articles citing this article:Fotini A. Koutroumpa, Astrid T. Groot, Teun Dekker, David G. Heckel Genetic mapping of male pheromone response in the European corn borer identifies candidate genes regulating neurogenesis, Proceedings of the National Academy of Sciences 113, no.4242 (Oct 2016).https://doi.org/10.1073/pnas.1610515113J. Tabata, Y. Ishikawa Genetic Basis Regulating the Sex Pheromone Blend in Ostrinia zealis (Lepidoptera: Crambidae) and Its Allies Inferred From Crossing Experiments, Annals of the Entomological Society of America 104, no.22 (Mar 2011): 326–336.https://doi.org/10.1603/AN10124B. O. BENGTSSON, C. LÖFSTEDT Direct and indirect selection in moth pheromone evolution: population genetical simulations of asymmetric sexual interactions, Biological Journal of the Linnean Society 90, no.11 (Jan 2007): 117–123.https://doi.org/10.1111/j.1095-8312.2007.00715.xTAKUMA TAKANASHI, YONGPING HUANG, K. RYO TAKAHASI, SUGIHIKO HOSHIZAKI, SADAHIRO TATSUKI, YUKIO ISHIKAWA Genetic analysis and population survey of sex pheromone variation in the adzuki bean borer moth, Ostrinia scapulalis, Biological Journal of the Linnean Society 84, no.11 (Dec 2004): 143–160.https://doi.org/10.1111/j.1095-8312.2005.00421.xRing T. Cardé, Kenneth F. Haynes Structure of the pheromone communication channel in moths, (Jun 2004): 283–332.https://doi.org/10.1017/CBO9780511542664.009CHARLES E. LINN JR, MARIA S. YOUNG, MATTHEW GENDLE, THOMAS J. GLOVER, WENDELL L. ROELOFS Sex pheromone blend discrimination in two races and hybrids of the European corn borer moth, Ostrinia nubilalis, Physiological Entomology 22, no.33 (Sep 1997): 212–223.https://doi.org/10.1111/j.1365-3032.1997.tb01161.xWilliam J. Bell, Larry R. Kipp, Robert D. Collins The Role of Chemo-orientation in Search Behavior, (Jan 1995): 105–152.https://doi.org/10.1007/978-1-4615-1765-8_4Michael J. Stanhope, Maureen M. Connelly, Brian Hartwick Evolution of a crustacean chemical communication channel: Behavioral and ecological genetic evidence for a habitat-modified, race-specific pheromone, Journal of Chemical Ecology 18, no.1010 (Oct 1992): 1871–1887.https://doi.org/10.1007/BF02751110

Initiation mechanism of mating behaviour in the rice stem borer, Chilo suppressalis Walker

The effects of endogenous and exogenous factors on mating behaviour were investigated to clarify the mechanisms of mating initiation, as one of the fundamental studies on the rice stem borer, Chilo suppressalis. The periodicity of mating behaviour is controlled basically by an endogenous circadian rhythm, and it is further affected by exogenous factors, such as temperature, day length, light intensity, light wave length and so on. Seasonal variations of mating behaviour can be observed under field conditions. The time of the onset of mating behaviour in August was delayed about 2 hours compared with that of June. Such variation of mating periodicity can be ascribed to the change in the hours of female calling and male pheromone response under different conditions among the seasons. Some of the important behavioural and physiological phenomena concerning mating initiation of Chilo suppressalis are discussed.

Population variation and genetic control of pheromone communication systems in moths

AbstractThe nature of variation in moth pheromone communication systems and its genetic control is critical for the evolution of these systems and for their role in mate‐finding and reproductive isolation. Significant additive genetic variance has been demonstrated in female pheromone production in monomorphic populations. However, corresponding variance in male pheromone response with respect to the blend which is most active, appears to be low, as can be expected from the general asymmetry of sexual selection. Pheromone polymorphism and differences in communication systems between closely related species seem to be controlled by a small number of Mendelian genes. The critical biosynthetic steps, which are influenced by the genes controlling pheromone production, can be inferred from our present knowledge of pheromone biosynthesis. A mechanistic understanding of how male response to pheromones is controlled is further away. Failure to demonstrate genes with pleiotropic effects on critical sender and receiver traits, suggests that reciprocal selection on genetically independent sender and receiver loci is the more likely explanation for the generally observed coordination between pheromone production and response in moth populations. Further research on the evolutionary significance of Z‐linked pheromone response genes, documented in several species, should be encouraged. Investigations, in the field, of populations that vary in pheromone production and response, and theoretical and empirical studies of the survival of sender and receiver mutants in otherwise monomorphic populations are also important to advance our understanding of how pheromone communication systems evolve.

Heritable variation in pheromone response of the pink bollworm,Pectinophora gossypiella (Lepidoptera: Gelechiidae)

Heritability of variation in male pheromone response by pink bollworm moths,Pectinophora gossypiella (Saunders), was examined using a still-air, wing-fanning bioassay. Heritability (±SE) of overall responsiveness, as measured by the mean duration of wing fanning to the blend of pheromone components produced by females [44∶56 ratio of (Z, E)- to (Z, Z)-7,11-hexadecadienyl acetate], was 0.385 ± 0.095. Heritabilities of wingfanning duration to blends with 25 and 65%Z, E isomer were 0.377 ± 0.113 and -0.145 ± 0.103, respectively. These findings indicate an asymmetry in the genetic component of variation in response to pheromone blends with high and low proportions of theZ, E isomer. An index of response specificity for individual males was developed based on the response to an off-blend (either 25 or 65%Z, E isomer) relative to the response to the 44%Z, E blend. Heritabilities of response specificity were 0.117 ± 0.059 and -0.043 ± 0.067 for the 25 and 65%Z, E blends, respectively.

Wing fanning as a measure of pheromone response in the male pink bollworm,Pectinophora gossypiella (Lepidoptera: Gelechiidae)

A still-air, wing fanning bioassay measured male pheromone response in the pink bollworm moth,Pectinophora gossypiella (Saunders). As pheromone concentration was increased, the duration of wing fanning increased while its latency decreased. Response duration was longest for the natural pheromone blend [44∶:56 (Z,E)- and (Z,Z)-7,11-hexadecadienyl acetates], although responses to 38% and 50%Z,E blends were not significantly briefer. Preexposure to pheromone had no effect on wing fanning in males retested after 24 hr. Wing fanning was highly correlated with upwind flight and other responses observed in a wind tunnel. Wing fanning duration provides a continuous measure of pheromone response and allows a large number of males to be tested in a short time; these two characteristics of the wingfanning assay are helpful for genetic analyses of male response.

No linkage between genes controlling female pheromone production and male pheromone response in the European corn borer, Ostrinia nubilalis Hübner (Lepidoptera; Pyralidae).

The E and Z pheromonal strains of the European corn borer, Ostrinia nubilalis, are characterized by female production of and male preference for opposite blends of (E)-11-and (Z)-11-tetradecenyl acetate. It is known that the pheromone production is controlled by an autosomal gene and that the males' behavior is determined by a sex-linked gene. A third gene, autosomally inherited, has been shown to determine the organization of the male pheromone receptors. In the present study the linkage relationship between the autosomal genes controlling sex pheromone production and male olfactory sensilla was investigated. A recombination experiment showed unequivocally that the genes determining the variation in pheromone production and male pheromone receptors are not closely linked and are most likely inherited independently.

Sex Pheromone Mediated Behavior of the Navel Orangeworm, Amyelois transitella12

The female navel orangeworm, Amyelois transitella (Walker), produces a sex pheromone that elicits both sexual excitation and upwind flight of males in laboratory bioassays. Quantitative bioassays were developed that employed either orientation (upwind movement) or activation (locomotion, wing-fluttering, clasper extension) as response criteria. Pheromone was released by females only during the last ⅓ of a 10-h scotophase, a time that coincided with maximal male pheromone responsiveness and mating. There were no significant differences between 1-, 2-, 3-, or 4-day-old unmated females in either the percentage of females calling or in the quantity of pheromone present in the superficial rinses of of excised abdominal tips during the 8th–10th h of the scotophase. Similarly, no significant differences were observed in pheromone responsiveness in 2- to 3-, or 4-day-old unmated males. Mating resulted in >90% reduction in female calling and at least a 10-fold decrease in the quantity of extractable pheromone. The activation and orientation responses of laboratory males did not differ significantly when pheromone extracts were prepared from either laboratory-reared or feral (collected as last-instar larvae) females.

Environmental regulation of female calling and male pheromone response periodicities in the codling moth ( Laspeyresia pomonella)

Codling moth female calling and male pheromone responsiveness under the defined conditions of 23°C and light:dark (LD) 16:8 occurred primarily during scotophase. Under either continuous photophase or scotophase females called with periodicities very similar to their periodicity under the LD cycle, indicating that the rhythmicity is circadian. Male response rhythmicity was maintained under continuous photophase. A decrease in the temperature from 23° to 16°C resulted in a reduction in the proportion calling when the decrease in temperature occurred during scotophase and a shift of maximal calling into photophase when the decrease in temperature occurred 3 hr prior to the initiation of scotophase. Decreases of temperature from 23° to 16°C and of light intensity did not produce similar shifts in the periodicity of male upwind orientation. Of 6 pheromone dosages from 10 −5 to 10 2 μg, 10 −1 and 10 0 μg elicited the most male upwind orientation.

Perception of Z -7-dodecen-1-ol and Modification of the Sex Pheromone Response of Male Loopers 1

Z -7-dodecen-1-ol prevents males of Trichoplusia ni (Hubner) and Pseudoplusia includens (Walker) from orienting to a locus of the evaporating sex pheromone, Z -7-dodecen-1-ol acetate. Pheromone perception is not blocked by the inhibitor in that males exhibit excited upwind flight and clasper extension when exposed to pheromone plus inhibitor and preexposure to the inhibitor does not cause fatigue (habituation) of the male pheromone response. We conclude that the inhibitor is most probably perceived via a sensory neuron separate from that for the pheromone and modification of the pheromone response occurs via a more central integrative process.