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Turnip Moth, Agrotis Segetum WENQI WU, SYLVIA ANTON, CHRISTER LOFSTEDT, and BILL S

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Turnip Moth, Agrotis Segetum WENQI WU, SYLVIA ANTON, CHRISTER LOFSTEDT, and BILL S Proc. Natl. Acad. Sci. USA Vol. 93, pp. 8022-8027, July 1996 Neurobiology Discrimination among pheromone component blends by interneurons in male antennal lobes of two populations of the turnip moth, Agrotis segetum WENQI WU, SYLVIA ANTON, CHRISTER LOFSTEDT, AND BILL S. HANSSON* Department of Ecology, Lund University, S-223 62 Lund, Sweden Communicated by Wendell Roelofs, Cornell University, Geneva, NY, March 22, 1996 (received for review November 21, 1995) ABSTRACT A difference in female pheromone produc- for gaining further insight into how information concerning tion and male behavioral response has previously been found different inter- and intra-populational blends is processed and in two populations of the turnip moth, Agrotis segetum, orig- integrated in the AL. In the present comparative study, we inating from Sweden and Zimbabwe, respectively. In this examined deutocerebral neurons of the two turnip moth study, we investigated the pheromone response of antennal populations, stimulating them with four single pheromone lobe interneurons of males of the two populations by intra- components, one behavioral antagonist [(Z)-5-decenol (Z5- cellular recordings, stimulating with single pheromone com- 10:0H)], and mixtures with various combinations of the four ponents and various inter- and intra-populational pheromone components. blends. Three major physiological types of antennal lobe neurons were established in the two populations according to their responses to different stimuli. One type responded MATERIALS AND METHODS broadly to almost all the stimuli tested. The second type Preparation. The Zimbabwean turnip moth culture was responded selectively to some of the single components and established in our laboratory from pupae shipped from Zim- blends. The third type did not respond to any single compo- babwe. The so-called Swedish turnip moths were collected nents but did respond to certain blends. Furthermore, some from southern Sweden and Denmark and maintained in the neurons of the second and third type recognized strain specific laboratory for more than 10 years. The culture has been differences in ratios between pheromone components. Both rejuvenated on several occasions by addition of field collected projection neurons and local interneurons were found among insects. A male moth was mounted head up in a plastic pipette these three types. Two pheromone responding bilateral pro- (Finnpipette) tip. The cuticle, tracheal sacs, and muscles were jection neurons are reported for the first time in this paper. carefully removed to expose the brain. The AL was manually desheathed to facilitate microelectrode penetration. A flow The species-specificity of sex pheromones has been well doc- system perfused the head cavity with saline (6). umented in several moth species (1-3). Males of one species Intracellular Recording and Stimulation. Intracellular re- are, in most cases, selectively attracted to the complete pher- cordings were performed according to standard methods (12). omone blend produced by conspecific females, although sym- A glass microelectrode filled with either 4% Lucifer yellow CH patric species often share some of the same pheromone solution or 2 M KCl was used as the recording electrode. components (4, 5). This invites the question of how male moths Olfactory stimuli used in the experiments were five single discriminate among different pheromone blends. In the central compounds at 1 ng, two Swedish blends, and two Zimbabwean nervous system, pheromone sensitive interneurons have been blends (Tables 1 and 2). For the Swedish males, blends with studied in several insect species (ref. 6 and references therein) different combinations of two or three pheromone compo- and the question concerning the blend discrimination by nents in the ratio found in the Swedish female extracts were antennal lobe (AL) interneurons has also been investigated in also included as stimuli (Table 2). The amount of each the moths Antheraea spp. (7) and Heliothis spp. (8, 9). How- component in the blend was assigned according to their ever, the limited number of stimuli used in the previous studies amount relative to 1 ng of Z5-10:OAc in the two populational prevents a thorough understanding of pheromone discrimina- blends, respectively, resembling the natural emission of a tion at the central nervous system level in insects. female (W.W., C. B. Cottrell, B.S.H., and C.L., unpublished The sex pheromone of the turnip moth, Agrotis segetum, work). All the stimuli were checked by gas chromatography to consists of a mixture of at least four olefinic acetates, (Z)-5- ensure purity, which was >99% with respect to geometrical decenyl acetate (Z5-10:OAc), (Z)-7-dodecenyl acetate (Z7- isomers, and ratio of components. Each odorant was applied 12:OAc), (Z)-9-tetradecenyl acetate (Z9-14:OAc) and (Z)-5- to a piece of filter paper that was then inserted into a Pasteur dodecenyl acetate (Z5-12:OAc) (10). A distinctive difference pipette. A 0.5-sec air pulse was sent through the cartridge in the ratio of the pheromone components has been shown containing either clean air or an odorant by means of a between a Zimbabwean and a Swedish population of A. stimulation device (Syntech, Hilversum, The Netherlands) segetum. Females of the Swedish population produce Z5- (13). The odor stimuli were chosen randomly, interspersed by 10:OAc, Z7-12:OAc, Z9-14:OAc, and Z5-12:OAc in a 10-30 sec. In a first set of experiments, the Zimbabwean 1:5:2.5:0.1 ratio, whereas the ratio of the four components in four-component blend was not included. The physiological the Zimbabwean pheromone blend was 1:0.25:0.03:0.1. Males data were stored on a Vetter video recorder and visualized on from each population respond preferentially to their own a Tektronix digital oscilloscope and on a Gould (Cleveland) population's blend in field and flight tunnel tests (ref. 11 and W.W., C. B. Cottrell, B.S.H., and C.L., unpublished work). Abbreviations: AL, antennal lobe; MGC, macroglomerular complex; These two populations therefore provide us with a good model ILPR, inferior lateral protocerebrum; LAL, lateral accessory lobe; PN, projection neuron; LN, local interneuron; Z5-10:OAc, (Z)-5- decenyl acetate; Z5-12:OAc, (Z)-5-dodecenyl acetate; Z7-12:OAc, The publication costs of this article were defrayed in part by page charge (Z)-7-dodecenyl acetate; Z9-14:OAc, (Z)-9-tetradecenyl acetate; Z5- payment. This article must therefore be hereby marked "advertisement" in 10:OH, (Z)-5-decenol. accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. 8022 Downloaded by guest on September 28, 2021 Neurobiology: Wu et al. Proc. Natl. Acad. Sci. USA 93 (1996) 8023 Table 1. Physiological responses of AL interneurons in B Zimbabwean male moths 1+3 1+2+ 1+2+ 1+2+ wo>H491lb No. 1 2 3 4 5 +4(Z) 3+4(Z) 4(S) 3+4(S) Cell type* Generalist neurons 1 1 + + + + + + nt + + 2 +++ + ++ + ++ ++ + na 3 ++ ++ ++ + + + + + 4 ++ + ++ + + + + + 2 5 ++ + ++ + + + ++ ++ na 6 + + ++++ + ++ ++ ++ 7 ++ + + + + +H ++ ++ ++ na 8 ++ + + + + + + + + 9 ++ + + + ++ +HH - -+ + + na 3 1;, 10 ++ + + + + + -+ + + PN(a) 11 ++ + + + + + + + + na 12 + + + + 0 + + + + 4 Component-specific neurons , 13 0 + + + + + nt + + LN 14 ++ 0 + + + ++ nt ++ + na 15 + 0 + + + + ++ ++ + na 5 16 ++ 0 + + + + ++ + 17 + + 0 + 0 + + + + PN(a) 18 + + + + + nt + ++ na 19 + + 0 + 0 ++ nt ++ PN(a) + 20 + + 0 + 0 + nt + 1+3+4 (Z) 21 ++ + 0 + + + nt ++ .2LS 22 + + + 0 + + nt + + na 23 ++ + + 0 + + ++ PN(a+b) 24 ++ + + 0 + ++ ++ na 1+2+3+4 (Z) 25 0 0 + + + + nt + + na _v1< 26 0 0 + + 0 0 + 0 0 na 27 0 + 0 +++ 0 nt + 28 + 0 0 + ++ ++ nt ++ ++ PN(b+c) 29 + 0 0 + 0 0 nt + + PN(a) 1+3+4 (S) 30 + 0 0 0 0 + + + + na 31 ++ 0 0 0 + + + ++ + PN(b) 32 + 0 0 0 + 0 0 0 L...ill;. 33 + 0 0 0 + + nt + + LN 1+2+3+4 (S) I. .01 34 0 + 0 0 + 0 nt 0 + -\I-IM 35 0 ++ 0 0 + 0 nt 0 + PN(d) 36 0 0 + 0 0 + nt + + na FIG. 1. Physiological responses of a generalist neuron (no. 8) of a 37 0 0 + 0 + + nt + nt Zimbabwean male moth. Note the strong hyperpolarization after the 38 0 0 + 0 + 0 ++ end of stimulation for all stimuli containing Z5-10:OAc (compound 1). The bar beneath the registration indicates onset and duration of the 39 0 0 0 + + 0 + ++0 stimulation. B, blank. (Horizontal bar = 1 sec; vertical bar = 10 mV) 40 0 0 0 + + + + + + 41 0 0 0 + + + nt + obscured excitatory responses over the entire stimulation 0 + + 0 42 0 0 0 + + period. After recording, the responses, Lucifer yellow was 0 0 0 0 + 0 nt 0 0 na 43 injected iontophoretically into the neuron. The brain was then dissected out and fixed. After dehydration, the brain was embed- Blend-specialist neurons ded in Spurr's resin and sectioned at 10 Am. Each section was 44 0 0 0 0 0 0 nt 0 + na photographed for final reconstruction of the neuron. 45 0 0 0 0 0 + + + + LN 46 0 0 0 0 + + nt 0 0 LN 47 0 0 0 0 0 + ++ + + PN(a+b+c+d) RESULTS The physiological responses are quantified as + (c 9 net spikes), The morphology of the AL in Zimbabwean male turnip moths ++(= 10-19 net spikes), and +++ (2 20 net spikes). Net spikes = was found to be the same as the AL in Swedish males. The (spikes during 300 msec after stimulation) - (spikes occuring 300 msec macroglomerular complex (MGC) can be divided into four before stimulation) - blank. 1, Z5-10:OAc; 2, Z5-12:OAc; 3, Z7- glomeruli (14). The largest glomerulus a is situated just at the 12:OAc; 4, Z9-14:OAc; 5, Z5-10:OH. 1+3+4(Z) is a blend of com- nerve.
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