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Cytogenetic Mapping of Enzyme Loci on Chromosomes J and U of Drosophila Subobscura

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Cytogenetic Mapping of Enzyme Loci on Chromosomes J and U of Drosophila Subobscura Copyright 0 1984 by the Genetics Society of America CYTOGENETIC MAPPING OF ENZYME LOCI ON CHROMOSOMES J AND U OF DROSOPHILA SUBOBSCURA W. PINSKER AND D. SPERLICH Lehrstuhl fur Populationsgenetik, Institut fur Biologie 11, Universitat Tubingen, Auf der Morgenstelle 28, 0-7400Tubingen, Federal Republic of Germany Manuscript received April 24, 1984 Revised copy accepted July 20, 1984 ABSTRACT Enzyme loci located on chromosome J and U were mapped cytologically by means of a Y translocation technique. A linkage map of the two chromosomes was established in a parallel experiment and the recombination frequency in different regions of the chromosomes determined. A comparison of the cyto- genetic localization of the enzyme genes in D. subobscura and D. melanogaster indicates that many paracentric inversions must have taken place in the course of divergent evolution. However, no displacements of genes from one element to another due to pericentric inversions, reciprocal translocations or transpos- ing elements can be observed. In spite of the large number of structural rear- rangements that have occurred in the phylogeny of the genus Drosophila, gross similarities of banding pattern in homologous regions of the chromosomes of the two species become apparent. ITH the introduction of gel electrophoresis, enzyme loci have become W very important marker genes for population genetic studies. Allozyme variation has proved especially useful for the estimation of the amount of genetic variation and for the calculation of genetic relationship between pop- ulations, species and other taxa. In addition, a number of studies have been devoted to the search for nonrandom associations between alleles of different loci or linkage disequilibrium, maintained by selective forces favoring certain allele associations by epistatic interaction. In spite of the large effort invested, unambiguous evidence for stable linkage disequilibria due to gene interaction is still scarce. In Drosophila subobscura the only good example has been re- ported by ZOUROS and KRIMBAS(1973) for the loci Ao and Xdh. On the other hand, nonrandom associations between genes and chromosomal inversions appear rather common. In the inversion polymorphic species D. subobscura, gene inversion associations have been described for the chromo- somes A (CABRERAet al. 1983), E (LOUKASand KRIMBAS 1975), J (PREVOSTI et al. 1982), 0 (CHARLESWORTHet al. 1979) and U (PINSKERand SPERLICH 1982). It can be assumed that practically all of the genes involved in these associations are located either inside the respective inversions or at least close to one or other of their breakpoints. Thus, inversions represent not only mere structural changes in the sequence of the genes but genetically differentiated Genetics 108: 913-926 December, 1984. 914 W. PINSKER AND D. SPERLICH regions of the chromosomes. Since gene flow between the inverted regions of different gene arrangements is assumed to be minimal because of the virtual absence of recombination in heterokaryotypes, gene arrangements can be con- sidered to have their own isolated gene pools. As a consequence, differences with respect to allelic frequencies for the loci within the inversions can be found (PINSKERand SPERLICH1981). Two mechanisms have been proposed to explain the cause of this genetic differentiation occurring between chromo- somal structures: The historical explanation advanced by ISHII and CHARLES- WORTH (1977) is the simplest and assumes only a chromosomal founder effect brought about by the formation of a new inversion. The second hypothesis, which is mainly due to Lewontin and his group (PRAKASHand LEWONTIN 1968), assumes coadaptation producing heterotic effects in heterokaryotypes due to the effects of the relationally balanced chromosome segments. Evidence in favor of both theories exists, and in nature probably both mechanisms contribute to the diversification of gene arrangements. However, for a careful and reliable investigation of the problem it is necessary to know the exact cytological positions of the gene loci under study, not only relatively with respect to other genes on the same chromosome but also cytologically with respect to the centromeres and the inversion breakpoints. In this study we have cytologically localized 11 genes of D. subobscura. Al- though D. subobscura is widely used for population genetic sudies, the existing linkage maps are still rudimentary or even partly incorrect. Cytogenetic infor- mation on the location of the enzyme loci is only available in form of linkage data with inversions. Using a recently developed Y autosome translocation technique (SPERLICHand PINSKER1984), we have been able to map the enzyme loci on the giant chromosomes more accurately. In this paper we describe the mapping of the autosomes J and U for which the available information is especially poor. A linkage map for chromosome J has been published previ- ously (LOUKASet al. 1979), but the recombination data given there are incom- plete and the assumed sequence of genes is ambiguous. For chromosome U no linkage map has hitherto been available. Consequently, recombinational linkage maps for these two chromosomes were also constructed to supplement the results of the cytogenetic study. Furthermore, the accurate cytological localization of the enzyme loci allows us to investigate chromosomal homologies at the interspecific level. In species that cannot be intercrossed, chromosomal homologies can be only found by searching for similarities in the banding pattern of the giant chromosomes or, more precisely, with the aid of homologous marker genes. The first approach is somewhat subjective and useful only for groups of species that are closely related and differ in chromosome structure only by a few rearrangements. For the second approach, well-defined structural genes of orthologous relationship are a prerequisite. This requirement is perfectly fulfilled by the enzyme loci. Since most of the enzyme loci have been already localized cytologically in D. melanogaster by means of deletion mapping, a knowledge of their cytogenetic position in D. subobscura allows a direct coordination of chromosomal segments of the two species and, consequently, the chromosomal evolution in the two species can be inferred. CYTOGENETIC MAPPING IN DROSOPHILA 915 MATERIALS AND METHODS Strains: All allozyme strains used in the following experiments are derived from natural popu- lation samples collected between 1975 and 1983 at different localities from Europe and North Africa. Homozygous strains for rare allozyme variants were established for the following enzymes: alcohol dehydrogenase (Adh), alkaline phosphatase (APh), diaphorase (Diu), esterase-3 (Est-3), a- glycerophosphate dehydrogenase (aGpdh), isocitrate dehydrogenase (Idh), malate dehydrogenase (Mdh) and phosphoglucomutase (Pgm).In addition three morphological mutants were provided by A. PREVOSTI(Barcelona, Spain): the eye pigment mutants cinnabar (cn) and maroon (ma), both located on chromosomej, and the wing vein mutant net (net), which is on chromosome U. For the translocation experiments the following marker chromosomes were constructed: ChromosomeJ: (a) Aph"', IdhIo5, Pgm'', +" (b) Aph'", Idh"', Pgm105,cn Chromosome V (a) aGpdhlo4, Mdhn6, (b) aGpdh'", MdhQ6,net Translocation technique: This method, originally developed by TAN(1 937), has been recently adapted for the localization of enzyme loci by SPERLICHand PINSKER(1 984). Translocations between the Y chromosome and an autosome are induced by X-rays, and irradiated males of the wild-type strains (a) are crossed to females homozygous for a recessive mutant (b). F1 males are then individually backcrossed to mutant females (b). The occurrence of a translocation can be detected by phenotypic examination of the progeny since the autosomal genes transferred to the Y chromosome display patroclinous inheritance. The translocated enzyme genes can be determined by electrophoretic investigation of the F2 or of the offspring of further crosses. A cytological analysis of the polytene chromosomes reveals the size and breakpoints of the translocated segment. Electrophoretic techniques: Electrophoresis was carried out in horizontal starch gels according to the methods of AYALAet al. (1972) and LOUKASand KRIMBAS(1980). The designation of allozymes follows the system proposed by SAURAet al. (1973). In zymograms of the Aph allozymes the staining intensity of the bands was measured with a Quick Scan Densitometer (Desaga, Heidelberg, Federal Republic of Germany). For this purpose the starch gels were made transparent in 5% glycerol using the method of NUMACHI(1 98 1). Cytological analysis: For the determination of the translocation breakpoints the polytene salivary gland chromosomes of male larvae were stained with acetic orcein. The subsections of the D. subobscura chromosomes are designated according to the chromosome map of KUNZE-MUHL and MULLER(1 958). Mitotic metaphase chromosomes were prepared from larval neuroblast cells using the squash technique proposed by GUESTand Hsu (1973). RESULTS Photographic maps of the polytene chromosomes U and J of D. subobscura are presented in Figure 1, which shows the positions of the translocation break- points, the breakpoints of some common inversions and the location of the enzyme genes. Each gene locus is mapped between the adjacent translocation breakpoints. An example of the mode of cytological localization is given in Figure 2 which describes the situation found with translocation J7, where the distal end of chromosome
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