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Sonoran Desert Drosophila (Polysubstrate Monooxygenase/Allelochemical Detoxicatlon/Alkalold Resistance/Alkaloid Metabolism/Larval Viability) MICHAEL R

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Sonoran Desert Drosophila (Polysubstrate Monooxygenase/Allelochemical Detoxicatlon/Alkalold Resistance/Alkaloid Metabolism/Larval Viability) MICHAEL R Proc. Natl. Acad. Sci. USA Vol. 89, pp. 11998-12002, December 1992 Ecology Involvement of cytochrome P450 in host-plant utilization by Sonoran Desert Drosophila (polysubstrate monooxygenase/allelochemical detoxicatlon/alkalold resistance/alkaloid metabolism/larval viability) MICHAEL R. FRANK AND JAMES C. FOGLEMAN* Department of Biological Sciences, University of Denver, Denver, CO 80208 Communicated by Bruce Wallace, September 17, 1992 ABSTRACT The four Drosophila species endemic to the relationship, as demonstrated by extensive rearing records Sonoran Desert (Drosophila mettleri, Drosophila mojavensis, and collection of adults from naturally occurring rots (1). In Drosophila nigrospiracula, and Drosophila pachea) utilize te- any particular location, each Drosophila species generally crotic cactus tissue or soil soaked by rot exudate as breeding utilizes the necrotic tissue ofonly one cactus species. Due to substrates. Each Drosophila species uses a different cactus differences in the geographic distribution ofthe cacti and one species as its primary host. D. pachea is limited to senita cactus case of behavioral preference, three of the four fly species by a biochemical dependency on unusual sterols available only exhibit a shift in host plants between the Baja Peninsula and in that cactus. For the other Drosophila species, no such the mainland Sonoran Desert. D. nigrospiracula uses saguaro chemical dependencies exist to explain the relationships with (Carnegiea gigantea) on the mainland and card6n (Pachy- their primary host plants. Each cactus species has a different cereus pringlei) on the peninsula. Saguaro cactus is only array of allelochemicals that have detrimental effects on non- found on the mainland, and card6n is primarily restricted to resident fly species. We have hypothesized that the desert the Baja peninsula. The two cacti are morphologically and fly-cactus associations are due, in part, to differences between chemically very similar and have low concentrations (1% the fly species in their allelochemical detoxication enzymes, the dry weight) of simple isoquinoline alkaloids (e.g., carnegine cytochrome P450 system. To test whether P450s are involved in and gigantine in saguaro) as their primary allelochemicals. the detoxication of cactus allelochemicals, several experiments The host plants for D. mojavensis are agria (Stenocereus were done. (i) The effect of a specific P450 inhibitor, piperonyl gummosus) and organ pipe (Stenocereus thurberi), which are butoxide, on larval survival through eclosion on each cactus sympatric on the peninsula. D. mojavensis shows a clear substrate was investigated. (it) In vitro metabolism of cactus preference for agria and utilizes organ pipe on the mainland, alkaoids was determined for each Drosophila species. The where agria is all but absent. Agria and organ pipe do not effects ofspecific inducers and inhibitors were included in these contain alkaloids, but both have sterol diols, medium-chain experiments. (fii) The basal and induced content ofcytochrome (CS-C12) fatty acids, and triterpene glycosides. These com- P450 in each species was determined. The results support the pounds have been shown to reduce fitness as measured by hypothesis that P450 enzymes are involved in host-plant utili- larval viability, development time, adult longevity, and/or zation by these Sonoran Desert Drosophila species. thorax size (3-5). D. pachea has a nutritional dependency on unusual sterols found only in senita cactus (Lophocereus For >20 yr, the interrelationships of columnar cacti and schottii) and so undergoes no host shift (3). Senita contains Drosophila ofthe Sonoran Desert ofthe southwestern United fairly high concentrations (3-15% dry weight) of more com- States and northwestern Mexico have provided an excellent plex isoquinoline alkaloids (lophocereine and its trimers, model system with which to study relevant questions in pilocereine and piloceredine) that are toxic to both adults and evolution, ecological genetics, and chemical ecology. These larvae of D. nigrospiracula, D. mojavensis, and to species cactophilic Drosophila use the necrotic pockets that form in found on the margin of the desert, including Drosophila the stems of the columnar cacti or in soil soaked by rot melanogaster (6). exudate for all stages of their life cycle. To do this, the flies D. mettleri exhibits a trait that is very unusual in the genus must be able to locate suitable rot pockets, assimilate re- Drosophila: oviposition in soaked soil. Only two other spe- quired nutrients, and tolerate the array of toxic allelochem- cies display this behavior. Drosophila heedi is a known soil icals in the cactus tissue. Chemical interactions between the breeder and is found in a xeric area of the island of Hawaii. cacti and the flies, therefore, are of major importance in Drosophila micromettleri, which is the closest relative ofD. determining the pattern of host-plant-Drosophila relation- mettleri, is thought to utilize soaked soil produced by col- ships that exist in the Sonoran Desert (1). umnar cacti in the Caribbean (2, 7). Because D. mettleri The four Drosophila species that are endemic to the oviposits in soil soaked by rot exudate and this situation Sonoran desert are Drosophila nigrospiracula, Drosophila occurs more frequently with saguaro and card6n than with mettleri, Drosophila mojavensis, and Drosophila pachea. the other cacti due to differences in the size of the cactus The four species are not closely related phylogenetically, stems, D. mettleri exhibits the same host-plant association although all are members ofthe major virilis-repleta radiation and host shift as D. nigrospiracula. D. mettleri can tolerate of the genus Drosophila. These species appear to have the allelochemicals found in senita, agria, and organ pipe but adapted independently to the desert environment (2). The is limited to soil breeding by a strong behavioral preference major population center of the nearest relative of each (7). In the soil, this species may encounter all the secondary species is found outside the desert or overlaps only slightly plant compounds in concentrations significantly higher than with the desert. Each of the endemic species also uses a in the necrotic tissue due to water evaporation (8, 9). Al- different cactus species as a host, in a nearly one-to-one though D. nigrospiracula, D. mojavensis, and D. pachea can tolerate the secondary plant compounds in the concentration The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" Abbreviation: PBO, piperonyl butoxide. in accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. 11998 Downloaded by guest on October 4, 2021 Ecology: Frank and Fogleman Proc. Natl. Acad. Sci. USA 89 (1992) 11999 encountered in the tissue of their respective hosts, none can butoxide (PBO), a specific cytochrome P450 inhibitor. (ii) In tolerate the higher concentrations found in soaked soil. vitro metabolism of the relevant allelochemicals by cy- In contrast to the ability to tolerate these diverse alle- tochrome P450, both induced and uninduced, was evaluated. lochemicals that the Sonoran Drosophila exhibit, D. mela- (iii) Determination of basal cytochrome P450 content and nogaster is unable to survive in the necrotic tissue of agria, inducibility by phenobarbital and cactus allelochemicals organ pipe, senita, or saguaro cactus (6). Furthermore, D. were determined. melanogaster has never been reared out of naturally occur- ring rots of the first three cacti, and only a few adult D. melanogaster have been reared from saguaro (10). MATERIALS AND METHODS The response of insects to toxic allelochemicals may be Drosophila Strains and Larval Induction. Stocks of D. behavioral adaptations, modified physiological processes, or nigrospiracula, D. mettleri, D. mojavensis, and D. melano- biochemical resistance mechanisms. Although the first two gaster (strains Canton-S and Hikone-R) had been maintained are important, there is reasonable agreement that biochem- in the laboratory for >4 yr. D. nigrospiracula, D. mettleri, ical resistance mechanisms are of primary importance in the and D. mojavensis were multi-female lines collected from the development of patterns of host utilization by insects (11). mainland section ofthe Sonoran Desert. Due to the difficulty Within this category, there are several enzyme systems that of maintaining D. pachea in the laboratory, it was excluded have been implicated in the detoxication of allelochemicals. from the present study. All species were raised on yeasted Ofthese, the most intensively studied is the cytochrome P450 instant Drosophila medium at ambient temperature and hu- enzyme system, considered to be the major detoxication midity. Larval induction was accomplished by adding 1.0 g of system, due to the ability ofcytochrome P450s to metabolize powdered cactus tissue to the medium surface, rehydrated by an extremely broad range of substrates. The cytochrome adding deionized water. This amount of rehydrated tissue P450 enzyme system is also called the polysubstrate mono- produced a layer "6 mm thick on the medium surface. oxygenase system or the mixed-function oxidase system. Induction by phenobarbital was similarly accomplished by The cytochrome P450 enzymes, made up of the terminal adding 1 ml of 2% sodium phenobarbital (pH 9). Induction oxidase cytochrome P450 and NADPH-cytochrome P450 was carried out for a period of
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