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Patterson Zanardini CHROMOSOMAL POLYMORPHISM IN DROSOPHILA RUBIDA MATHER WHARTON B. MATHER' Zoology Department, University of Queensland, Brisbane, Australia Received January 30, 1961 HE population geneticist is essentially interested in the variation of gene fre- Tquencies in natural populations. Within chromosomal inversions blocks of genes are contained and in many species of Drosophila due to the presence of easily analysable giant chromosomes, the behavior of these blocks of genes can be easily studied in natural populations. Thus, of recent years chromosomal inver- sion polymorphism in the genus Drosophila has been extensively studied (see review by DA CUNHA1955 and discussion by GOLDSCHMIDT1958), the most extensive work having been done on the temperate species D.pseudoobscura Fro- lowa from northwestern America, D.robusta Sturtevant from eastern America and D. subobsczua Collin from Europe and the tropical species D. willistoni Sturtevant from South America. From this work it has been suggested that the genetical significance of inversions is to maintain coadapted gene sequences by the elimination of chromatids produced by crossing over within the limits of heterozygous inversions. PATTERSONand STONE(1952) list 17 species in the immigrans species group, the majority being from the Australian and Oriental geographical regions. In spite of the giant chromosomes of those members of the group which have been studied being very suitable for detailed analysis, anly D. immigrans has been examined for polymorphism. A number of inversions have been detected by FREIRE-MAIA,ZANARDINI and FREIRE-MAIA(1953) and BRNCIC(1955) in South America, GRUBER(1958) in Israel and TOYOFUKU(l957,1958a,b) in Japan. In 1958 Drosophila collections were made at Cairns in northeastern Australia and a new species of the immigrans species group discovered. This was subse- quently described as D.rubida (MATHER1960) and shown, like D.immigrans, to have excellent salivary chromosomes although the Cairns population appears to be free of inversions. In 1959 Drosophila collections were made in Papua-New Guinea at Port Moresby, Goroka and Lae (New Guinea), Kavieng (New Ireland) and Rabaul (New Britain), and the species was shown to be widespread (MATHER1959). It was also established by qualitatively analysing a number of mass cultures that it is rich in chromosomal inversion polymorphism. For these reasons it was de- cided to study D.rubida more fully with a view to obtaining data on the poly- morphism pattern of a polymorphic species from tropical Australasia. 1 Aided by a grant from the University of Queensland Research Fund. Genetics 46: 799-4710July 1961. 800 W. B. MATHER MATERIALS AND METHODS The flies used in this study were collected from fermenting banana baits ex- posed in rain forests at Cairns, Port Moresby, Goroka, Lae and Bulolo (New Guinea) and Rabaul (New Britain) (Figure 1). Thus the sampling stations are spread over a considerable geographical area as Rabaul is nearly 1000 miles from Cairns and whereas Cairns, Port Moresby, Lae and Rabaul are at sea level, Goroka and Bulolo are at heights of 5000 and 2500 ft., respectively. In order to extract the maximum amount of information from the samples collected, three complementary methods of analysis were made ( DOBZHANSKY and EPLING1944; STALKER1960). (1) Wild-caught males were analysed by mating them singly to virgin females from a standard strain (Cairns, May 1958) which has been shown to be inversion free. Seven larvae of which at least one was a female were scored. (2) Wild-caught females probably inseminated but kept until no fertile eggs were laid (i.e. despermed) were analysed by mating them singly to males from the standard strain and scoring seven female larvae. (3) The male progeny of females caught in the wild were tested as wild males (see ( 1 ) above). Experimental justification for this procedure is given by STALKER ll0" I too '0"n 0"- $Cairns I ,. : Miles 500I 2 0" 20". a 140 160" I I FIGURE1.-Sampling stations in Northern Australia and the Territory of Papua and New Guinea. D. RUBIDA INVERSIONS 801 (1960) who found that a comparison of wild-caught males, and the F1sons of wild-caught females captured at the same time in a large population of D.para- melunica in Iowa showed no difference in inversion frequencies between the two classes. Presumably F1females could be used in the same way but the validity of this has not been tested. It can be shown that by using seven larvae from each mating that there is over a 98 percent probability of testing both haploid chromosome sets from each in- dividual (DOBZHANSKYand EPLING1944). Further, because in each method a wild individual is mated to a standard gene order individual, the gene order of the chromosome under test can always easily be determined for males, but due to crossing over in females, the linkage relationships are sometimes difficult to determine. Wild-caught females may be used, but here, to give a comparable probability of testing both haploid chromosome sets from each individual, eight instead of seven larvae must be used (DOBZHANSKYand EPLING1944). Also the possibility of multiple insemination introduces uncertainty. For estimating the frequency of inversions in populations, single larvae from each female inseminated in the wild have been used by a number of workers. In testing female flies, female larvae must be used to ensure testing both X chromosomes. In testing male flies at least one female larva must be used to be certain of testing the X. When analysing a complex inversion, a sketch was made, double and single thickness regions being particularly noted, both the standard and nonstandard halves traced out and each paired or homologous section lettered at both ends. Finally the sequence of letters in each half giant chromosome was noted and the minimum number of simple inversions deduced (DOBZHANSKYand EPLING 1944). The flies were grown on standard corn meal medium at 25" 2 l.O°C, salivary gland squashes made in 46 percent acetic acid after pretreatment with N HC1 and staining in aceto-orcein. The squashes were scored as paraffin sealed temporary mounts. All photographs were made on 35 mm Panatomic X film. Chromosomes: D. rubidu has a metaphase plate of two pairs of V's and two pairs of rods and a giant chromosome complement of four long arms and one dot. Thus, in evolving from the supposed primitive condition of five pairs of rods and a pair of dots the most likely explanation in the light of the cytology of the closely related D. purarubida (MATHER1961) seems to be that two pairs of rods fused but in one pair a subsequent pericentric inversion has produced a pair of long rods. Further, heterochromatin has been added to the original dots to pro- duce a pair of rods and to the remaining original rods to produce another pair of V'S. The giant salivary chromosomes show four long arms and one short and the arms can be readily identified by the banding of the free ends. The same desig- nation has been used as that given for D. immigrans (FREIRE-MAIAet al. 1953), viz. I for the X chromosome, IIL and IIR for the arbitrary left and right arms 802 W. B. MATHER of one pair of metaphase VIS, I11 for the long metaphase rod and IV for the small ann representing the euchromatic part of the largely heterochromatic metaphase rods. The X chromosome is further specified by being more lightly stained than the autosomes in preparations from male larvae. The third chromosome is nearly twice as long as IIL or IIR. There is no distinct chromocentre and IIL often appears to be continuous with IIR whereas I and I11 tend to separate at their centromere ends and from IIL and IIR. Chromosome IV is usually attached to the centromere end of one of the other chromosomes. RESULTS A giant chromosome photographic map (Figure 2) has been prepared from the standard inversion-free Cairns strain by systematically photographing clear preparatians under oil immersion and reconstructing the chromosomes from the prints produced. Each chromosome arm has been broken up into regions working from the free end towards the centromere. The regions begin with easily identi- fiable bands spaced at such distances that within each region approximately ten bands were distinguishable and indicated by dots. Thus a breakage point desig- nated IIR 2.3 means that the break occurs immediately to the right of band 3 in region 2 of the right arm of chromosome 11. The use of a photographic giant chromosome map instead of the more conventional camera lucida drawn map was first suggested by CARSON(1958) and has been adopted here in the belief that this type of map is of greater use to subsequent workers in that a particular break point can be more definitely designated. Photographs of the simple in- versions detected are given in Figure 3 and the complex inversions IIR D and E, together with interpretations, are given in Figure 4 with the aim of giving con- crete evidence of the position of the postulated break points. Chromosome I, the X chromosome, is free of inversions. IIL has one simple inversion A( 7.1-10.5) towards the proximal end involving 29 percent of the giant chromosome. The distal end of IIR has a subterminal simple inversion A ( 1.2-3.3) involv- ing 11 percent of the giant chromosome. This is followed by a further simple inversion B(3.3-5.5) apparently with the same distal break point and involving 17 percent of the chromosome. Finally, simple C (7.1-9.4) and complexes D (7.1- 14.1) and E(7.1-16.1) each have the same distal break point but different prox- imal break points.
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