Pheromone-blend discrimination by European corn borer moths with inter-race and inter-sex antennal transplants

Linn, Charles E.; Poole, Kathy; Zhang, A.; Roelofs, Wendell L.

doi:10.1007/s003590050325

Cited by 14 publications

(10 citation statements)

References 19 publications

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“…A third possibility is a change in the antennal lobe itself, governing which OSNs will connect to which glomeruli. Such a change is suggested by the results of transplanting antennae of E-strain males onto Z-strain males: The chimeric males responded only to the Z blend (64). In this example, the Z genotype of the recipient bearing the antennal lobe had a greater influence than the E genotype of the OSNs in the transplanted antennae.…”

Section: Discussionmentioning

confidence: 89%

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

Koutroumpa

Groot

Dekker

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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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.Ostrinia nubilalis | Z chromosome | pheromone response | sexual communication | QTL analysis

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Section: Discussionmentioning

confidence: 89%

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

Koutroumpa

Groot

Dekker

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…The transplant procedure was initially developed by Schneiderman et al (1982) for the large sphingid moth, M. sexta, and modified by Linn et al (1999) for the much smaller pyralid moth, O. nubilalis. The sex of individual larvae was ascertained (Lavenseau, 1982), and imaginal discs were transplanted in the middle of the final larval instar.…”

Section: Transplantation Proceduresmentioning

confidence: 99%

“…Conditions within the wind tunnel were as follows: 22°C, 60% RH, a wind speed of 0.5 m/second, and illumination of 11 lux of red light at the tunnel floor (Linn et al, 1999). Moths were scored for activation, with no locking on to the pheromone plume, and upwind flight in the pheromone plume over a 1.5 m distance to the pheromone source.…”

Section: Flight Tunnelmentioning

confidence: 99%

“…Recently, studies involving transplants have been performed to better understand the interactions between ORNs and central tissues during development of the adult olfactory system (Rössler et al, 1999b). In addition, Linn et al (1999) transplanted antennal imaginal discs across two different races of European corn borer (Ostrinia nubilalis). Because the constituents of the pheromonal odors that attract males are so well understood in this species and many other Lepidoptera, Linn et al (1999) were also able to assay the effects of the transplant procedure upon the ability of recipient males to discriminate between different odor blends and determined that males and females with the antennae of a different race continued to prefer their normal pheromone blend.…”

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confidence: 99%

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Consequences of interspecies antennal imaginal disc transplantation on organization of olfactory glomeruli and pheromone blend discrimination

Vickers

Poole

Linn

2003

J of Comparative Neurology

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The antennal imaginal disc was transplanted between male larvae of two different heliothine moth species, Heliothis virescens (HV) and Helicoverpa zea (HZ). Males of these species respond to distinct pheromone blends, have different peripheral and central olfactory neuron specificities, as well as distinct arrangements of antennal lobe olfactory glomeruli, in the specialized male macroglomerular complex (MGC). After pupal development and adult eclosion, unilateral (with one antennal disc left intact) and bilateral antennal transplant males were assayed in a wind tunnel to both species' pheromone blends to determine their ability to discriminate between the two signals. The postmetamorphic developmental effects of interspecific transplantation upon the primary olfactory centers in the moth brain were then examined in these same individuals. Behavioral tests showed that both types of unilateral transplant continued to exhibit upwind anemotactic flight to the normal recipient blend with occasional flights to the donor blend. In contrast, bilateral transplants preferred the HV pheromone blend regardless of the direction of transplant, with some males of each type also responding to the HZ blend. Neuroanatomic evaluation of the MGC revealed that the donor arrangement of MGC glomeruli was induced in 73% HZ donor to HV recipient transplants and 56% of the reciprocal transplant. Surprisingly, several V-Z bilateral transplant males responded to both HV and HZ pheromone blends and had two HV MGC structures. This behavioral outcome was unexpected, because responses to the HV blend are mediated by inputs that are normally antagonistic to HZ males and the normal HV antenna lacks olfactory receptor neurons capable of responding to the essential minor pheromone component of the HZ blend. These data indicate a plasticity in developmental pathways regulating the expression of peripheral olfactory receptor neurons and in the glomerular processing of species-specific olfactory information.

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“…The ratios of the acetate pheromone components (Z)-11-tetradecenyl acetate (Z11-14:OAc) and E11-14:OAc, produced by females of two races of O. nubilalis differ dramatically (97:3 vs. 3:97), and are mostly controlled by a single autosomal gene (Klun, 1975;Löfstedt et al, 1989) that is not linked to a second gene that controls male behavioral response to the pheromone (Löfstedt et al, 1989;Cossé et al, 1995;Linn et al, 1999). Studies of F 2 and backcross progeny from hybridization of other lepidopteran species have also uncovered evidence for single gene control of production of specific pheromone component ratios (Haynes and Hunt, 1990;Jurenka et al, 1994;Zhu et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

Introgressing Pheromone QTL Between Species: Towards an Evolutionary Understanding of Differentiation in Sexual Communication

et al. 2004

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Abstract-As a first step toward understanding how noctuid moths evolve species-specific pheromone communication systems, we hybridized and backcrossed two closely related moth species, Heliothis virescens (Hv) and H. subflexa (Hs), which differ qualitatively and quantitatively in their multicomponent sex pheromone blends. We used amplified fragment length polymorphism (AFLP) marker-based mapping of backcross families to determine which of the 30 autosomes in these moths contained quantitative trait loci (QTL) controlling the percentages of specific chemical components in the pheromone blends. In two previous backcrosses to Hs, we found a strong depressive effect of Hv-chromosome 22 on the percentage of three acetate components in the pheromone gland. These acetates are present in Hs and absent in Hv. Here, we describe how we introgressed Hv-chromosome 22 into the genomic background of Hs. Selection for Hv-chromosome 22 started from backcross 3 (BC 3 ) females. All females that had Hv-chromosome 22 and a low percentage of acetates (<3% of the total amount of pheromone components present) were backcrossed to Hs males. In BC 5 to BC 8 , we determined whether Hvchromosome 22 was present by a) running only the primer pairs that would yield the markers for that chromosome, and/or b) determining the relative percentages of acetates in the pheromone glands. Either or both genotype and phenotype were used as a criterion to continue to backcross these females to Hs males. In BC 9 , we confirmed the isolation of Hv-chromosome 22 in the Hs genomic background, and backcrossed the males to Hs females to eliminate the Hv-sex chromosome as well as mitochondrial DNA. The pheromone composition was determined in BC 3 , BC 5 , and BC 11 females with and without * To whom correspondence should be addressed. E-mail: astrid groot@ncsu.edu Hv-chromosome 22. All backcross females with Hv-chromosome 22 contained significantly less acetates than females without this chromosome. In addition, BC 3 females with Hv-chromosome 22 contained significantly more Z11-16:OH than BC 3 females without Hv-chromosome 22. However, in BC 5 and BC 11 females, the correlation between Z11-16:OH and Hv-chromosome 22 was lost, suggesting that there are separate QTL for the acetates and for Z11-16:OH, and that the relative amount of the alcohol component is only affected in epistasis with other (minor) QTL. Now that we have succeeded in isolating the chromosome that has a major effect on acetate production, we can test in behavioral experiments whether the presence of acetates may have been a driving force for a shift in pheromone composition. Such tests are necessary to move towards an evolutionary understanding of the differentiation in sexual communication in Heliothis spp. moths.

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Pheromone-blend discrimination by European corn borer moths with inter-race and inter-sex antennal transplants

Cited by 14 publications

References 19 publications

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

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

Consequences of interspecies antennal imaginal disc transplantation on organization of olfactory glomeruli and pheromone blend discrimination

Introgressing Pheromone QTL Between Species: Towards an Evolutionary Understanding of Differentiation in Sexual Communication

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