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Evolution of the Alpha-Esterase Duplication Within the Montana Subphylad of the Virilis Species Group of Drosophila

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Evolution of the Alpha-Esterase Duplication Within the Montana Subphylad of the Virilis Species Group of Drosophila EVOLUTION OF THE ALPHA-ESTERASE DUPLICATION WITHIN THE MONTANA SUBPHYLAD OF THE VIRILIS SPECIES GROUP OF DROSOPHILA WILLIAM K. BAKER Department of Biology, University of Utah, Salt Luke City, Utah 84112 Manuscript received May 1, 1979 Revised copy received August 27, 1979 ABSTRACT Previous studies on linkage disequilibrium involving four tightly linked genes that code for the alpha-esterases of Drosophila montana suggest that these loci arose from a primitive esterase gene by gene duplication, Iollowed by tandem duplication (ROBERTSand BAKER 1973). We have examined the esterase variants in the closely related species, Zacicola, fluvomontana and borealis. These studies reveal that borealis has only a single esterase locus, and flmomontana may have only two loci. Cytological studies, using aceto-orcein staining and Hoechst fluorescence of squashes of ganglion chromosomes, reveal acrocentric Y chromosomes for all six species of the montana phylad, with the exception of borealis, which has the primitive rod-shaped Y chromosome. These studies provide evidence ayainst the hypothesis (STONE,GUEST and WILSON1960) that borealis and flavomontana are derived from montana, but support THROCKMORTON’S(1978) conclusion of the early divergence of the former two species. This phylogenetic relationship supports our contention that the difference in the number of esterase genes with active alleles between borealis and montana is based on an increase in the number of genes coding for the alpha-esterases, rather than the retention in borealis of three genes with null alleles. HERE are four tightly linked genes on chromosome 2 of D. montana that code for esterases and that can utilize alpha-naphthyl acetate as a substrate. They have the following characteristics (ROBERTSand BAKER1973; BAKER1975): (1) Each gene has one active allele (whose protein has a characteristic electro- phoretic migration) and a null allele, both of which are present in the population at high frequencies. Other active alleles are known at each locus, but are only rarely found in natural populations. (2) The gene order on the chromosome is GI,Gs, G,, G,. (3) There is strong linkage disequilibrium in natural populations favoring chromosomes with two active and two null alleles. Chromosomes with 0, 1, 3 and 4 active alleles are found in the populations much less frequently than expected. (4) However, only particular chromosomes with two active alleles are “favored,” namely those with one active allele at gene 1 or 2 and the other active allele at gene 3 or 4. Genetics 94: 733-748 March, 1980. 734 W. K. B.SKER Data (BAKER1975) support the hypothesis that this specific and unusual link- age disequilibrium is maintained by selection, instead of being caused by histori- cal accident, since it is stable over time and space. On a selective basis, one can propose that G, and G, code for a group of related esterases, Cs, and G, and G, for E,’s; a chromosome with two active loci that code for both types of esterases is favored. Such a system of related and tightly linked genes could have arisen during evolution by either of the processes of gene duplication shown in Figure 1. It should be realized that the proposed scheme of gene order and function in present-day montana is based on a selectionist interpretation of the linkage disequilibrium data from natural populations and that the postulated duplicative events leading to this arrangement are hypothetical. We have studied the alpha-esterase variants in a series of species closely related to montarm and have found substantial support for the duplicative origin of these loci, as proposed in Figure 1. Cytological studies confirm that borealis, with but a single esterase locus, is phylogenetically more primitive than montana: with four loci. Scheme 1 Scheme 2 .Primitive gene U Differentiation of function duplication U 1 Gene Any duplication -0- joining the two alleles to the same Differentiation of chromosome is function favored because it preserves polymorphism Tandem Tandem duplication I -1 duplication Present-day montana FIGURE1.-Two schemes for origin of the apparently tandemly duplicated alpha-esterase loci of montana. Scheme 1 proposed by BRUCE WALLACE(personal communication); Scheme 2 proposed by ROBERTSand BAKFR(2973). EVOLUTION OI? A GENE DUPLICATION 735 MATERIALS AND METHODS The alpha-esterase enzymes were studied in the following species of the montana phylad of the virilis group: monrana (MO);ouiuororum (Ou), a strain of montana; Zacicola (Lc);fluvo- montana (Fl) ; and borealis (Bo). Listed in Table 1 are geographic locations of the strains of these species that were examined. Most of these strains were derived from single females inseminated in nature or from pair matings of virgin females to males from the same locale. Thus, barring multiple inseminations, four second chromosomes were originally segregating in each strain. Electrophoresis was performed in 7% acrylamide slab gels, using the Aardvark Instruments apparatus. Individual flies were homogenized in the electrophoresis buffer (0.1 M tris-borate with EDTA, pH 8.9) with 10% sucrose. Electrophoresis was for 2 hr at MO volts, after which the gels were placed in 0.5 M boric acid in the cold for 30 min, then stained for 60 min or more TABLE 1 Geographical location of strains used Number of strains examined of each species Location MO Ov Lc RI Bo Bethel, Alaska I Yukon, Alaska I Anchorage, Alaska 1 Mount Hood, Oregon 1 Pompeys Pillar, Montana 1 Shields River, Montana Woods Landing, Wyoming 2 Jackson, Wyoming 4 Chester, Idaho 1 Little Salmon River, Idaho 1 Verdi, Utah 1 Cottonwood Canyon, Utah American Fork Canyon, Utah 29 1 Wadsworth, Nevada 3 Craig, Colorado 19 13 Hamilton, Colorado 1 Walden, Colorado 1 Spencer Heights, Colorado 3 Gothic, Colorado 253 (1012 chromosomes) Horse Ranch Park, Colorado (190 chromosomes) Ohio Creek, Colorado 58 (2.30 chromosomes) Mount Lemon, Arizona 1 Whiteshell Provincial Park, Manitoba 8 31 Beaver Creek Campground, Manitoba 8 Jamestown, North Dakota 5 Lake Itasca, Minnesota 15 Fenske Lake, Minnesota Brule, Wisconsin Sioux Narrows, Ontario Saranac, New York Kent, Connecticut 1 Karesuando, Sweden 1 Inari, Finland 1 Total strains 382 2 20 65 74 Total locations 18 2 6 9 8 736 W. K. BAKER in 100 ml of 0.1 M phosphate buffer, pH 6.5, containing 20 mg each of alpha-naphthyl and beta- naphthyl acetate, plus 50 mg Fast Blue BB. Routinely, in pockets 1, 8, 16 and 24 of these 24-pocket gels, a mixture of montana esterase enzymes with mobilities of 93, 100, 106, 112, and 118 was placed to serve as markers. In order to accommodate the variants with new migration characteristics found in the other species, we have chnnged from an alphabetical system of nomenclature for the variants to a numerical one. Variant F of montana is given a migration value ol100, and the other variants are designated by their migration relative to 100. For the previously reportec! variants of montana, the conversion is as follows: A = 81, B = 87, B' = 90, C = 93, D = 96, E = 98, F = 100, G = 101, H = 103, I = 106, J = 107, K = 108, L = 109, M = 112, N = 114, P = 118 (see Table 2). Even with the use of these five marker enzymes of montuna in pockets distributed throughout the gel, it was occasionally not possible to determine with certainty whether an enzyme in one species co-migrated with one or the other of two close-migrating montana enzymes, or whether its migration was distinct. In these cases, gels were made with the two close-migrating montana enzymes in pockets oi the gel that alternated with the enzyme from the other species being characterized. This usually resolved the question. Of course, co-migration is not proof of protein identity. The cytological preparations in Figure 2 are aceto-orcein squashes of ganglion cells photo- graphed with phase microscopy. The specific strains of flies used in both Figures 2 and 3 are: Ou-Karesuando, Sweden; MeGothic, Colorado, GR7-10-76 Q b; Lc-WSPP, Manitoba, is0 Q g; Bo-WSPP, Manitoba is0 0 ee, and Craig, Colorado, C8-17-74k 0 x C8-17-74i 6' ; FZ- Wadsworth, Nevada, is0 8 a; ezouna Ez-Hokkaido, Japan, 30W.35; Zittorilas Lt-Finland, 480. Fluorescent Hoechst 33258 staining was accomplished according to the method of GATTI, PIMPINELLIand S~NTTNI(1976); however, the fixation was in one part 45% acetic acid to One part 95% ethanol, and no hypotonic treatment was given. The slides were examined in a Zeiss Ultraphot microscope under incident UV illumination from a HBO 200 mercury lamp. Since the UV illumination passes through the objective onto the preparation, only a small area is jlluminated, reducing fading. Scanning and examination were done with a loo><, 1.3 NA oil immersion Ph3 Neofluar Zeiss objective. Examination and photomicrography employed the Zeiss optically matched filters for examination of rhodomine or those matched for fluorescene. ESTERASE PATTERNS In order for the results to be reviewed with some perspective, the closeness of the relationship between the species being discussed should be pointed out. Hybrids can be produced between many species combinations, although some hybrids are sterile and a few survive only to the larval stage (STONE,GUEST and WILSON1960; PATTERSONand STONE 1952). The morphological similarity of the adults is so close that only fiauomontana (because of its lighter coloration) can be told with assurance. Identification is based on internal dissection but, occasionally, crosses must be made for confirmation. For example, two diagnos- tic characteristics are the number of coils in the testes in males and the shape of the spermatheca in females. Against this background of evolutionary close- ness, the diversity we are about to describe in the genetic systems for alpha- esterases appears particularly striking, The data on the alpha-esterase variants present in different strains of the species under discussion are presented in Table 2.
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