THE EFFECTS OF THE ENVIRONMENTAL CONDITIONS ON CURLY EXPRESSIVITY IN DROSOPHILA MELANOGAST ER. Ken NOZAWA
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1 THE EFFECTS OF THE ENVIRONMENTAL CONDITIONS ON CURLY EXPRESSIVITY IN DROSOPHILA MELANOGAST ER Ken NOZAWA Department of Animal Breeding, Faculty of Agriculture, Nagoya University, Anjo, Japan Received August 31, 1955 UDC : : Curly wing in Drosophila melanogaster is a dominant mutant character accompanied with two large inversions in the second chromosome. So, it has long been used as one of the most suitable markers for genetic research since L. Ward first described it (Ward, 1923). However, the author, through his investigation of Cy/l balanced lehtal stock, observed that this character changed its expressivity according to some environmental factors, especially culture conditions and temperature. In many cases the Curly individuals had the typical expression of Curly wing, namely showing both cross and longitudinal wrinkles ; but sometimes genotypic Curly ones, which were identified by the progeny test, expressed normal appearance. Changes in the expressivity of mutant character depending on culture conditions can be noticed by the fact that the date of emergence can affect the degree of gene expression. Such cases were reported by T. H. Morgan (1915) in "Abnormal Abdomen" of Drosophila melanogaster, T. Komai (1926) in "crippled" of the same species, D. Moriwaki and K. Oyama (1947) in "gap" and "Shaven" of D. ananassae, and others. On the other hand, the influences of temperature on gene expression were also investigated by many authors and the temperature-effective periods were determined in some mutant genes, namely "Bar" (Driver, 1931), "vestigial" (Stanley, 1935), etc. On the base of these reports, the author analized the influencing patterns of the two main environmental factors, i, e, culture conditions and temperature, on Curly expressivity. Materials and Methods A balanced lethal stock, Cy/l, was used ; this lethal gene, l (2) 50 c, was separated from the laboratory stock of Tokyo wild type. Crossing over between Cy and l on the second chromosomes, by which the flies of true wild type could rarely appear, was considered to be negligible by the analogy of the fact that the frequency of appearance of Cy bw/bw type from Cy/bw stock was counted to be 1/2435. In order to describe the degree of Curly appearance, the adult flies were classified into three types "high " "intermediate" and "low" ;and the expressivity of a population was measured by the sum of percentage of "high" type and a half
2 164 THE JAPANESE JOURNAL OF GENETICS Vol. 31 No. 6 of percentage of "intermediate" type. The standards of the classification were as follows : "high" type : Individuals having the typical Curly wings showing both cross and longitudinal wrinkles. "intermediate" type : Individuals having the wings showing only longitudinal wrinkles. "low" type : Individuals showing a slight upward bend at the tip of the wings, including the flies of the apparent wild type. In all the experiments, the ordinary corn meal agar media were prepared in the culture bottles of 3 cm. diameter and drops of suspension or extracts of dry yeast were poured on each medium as food of the developing larvae. Experimental Results A. The effect of larval population density. 1. Changes in Curly expressivity depending on the date of emergence. Ten pairs of Cyfl flies were allowed to breed in each of 254 culture bottles for about one week. The experiments were conducted at 24±1 C. All the emerged flies Fig, relation 1. to Changes in the date of Curly expressivity with emergence. were counted ; Curly expressivity were enumerated by means of the above mentioned method ; and body weight of male flies were measured. These examinations were made every other day from the beginning to the end of emergence without considering alternation of generations. Changes in Curly expressivity of all the adult flies through the course of emergence were shown in Fig. 1. Total number of the flies counted was Curly expressivity is always higher in the females than in the males. In the first day, the expressivity is almost 100/, that is to say, all the emerged flies of both sexes have the typical Curly character ; then as emergence
3 June 1956 K. NOZAWA : THE ENVIRONMENTAL CONDITIONS IN DROSOPHILA 165 goes on, the flies become more and more normal in appearance ; but with approaching to the end of emergence, the expressivity returns gradually to higher level, until at last the flies show almost 100 o expressivity again. It is worth noting that these expressivity curves are antagonistic to the emergence curve while the change of the mean body weight of male flies is nearly parallel to the expressivity curves. From these results it was considered that Curly expressivity was influenced by the effect of larval population density. 2. Egg. sample test. To verify the effect of population density, the definite number of eggs from the Cy/l stock were allowed to develop in the ordinary culture media and three drops of 5% suspension of dry yeast were poured in each bottle. The number of egg samples were 50, 100, 150, 200, 250, 300, 350 and 400 per bottle. Curly expresssivity of the adult populations was summarized in Fig. 2. There was a negative correlation between number of egg samples and Curly expressivity of the adult flies. 3. The relation to the quantity of yeast. The data stated above drew the suggestion, that the nutritional condition in the larval stage controlled Curly exsressivity of the adult flies. In order to examine the nutritional factor the following experiments were carried out. Five pairs of Cy/l parents were allowed to breed on the culture media and the experiments were divided into following four series according to the quantity of added yeast. S : Dry yeast and water were supplied to the culture media every day so as the larvae to be sated with food (Satiation test). C: Two drops of 02 o suspens ion of dry yeast were poured immedia tely after preparation of the culture media. D: Two drops of 1 o suspens ion of dry preceding N: yeast were poured in the same Yeast were not poured, in the bottles. manner. Fig. 2. Results of egg sample test. Circles point the individual experimental results ; two curves show the changes in each mean value. expectation that these parents carried yeast from the
4 166 THE JAPANESE JOURNAL OF GENETICS Vol. 31 No. 6 Table 1 The relation between the quantity of yeast and Curly expressivity Table 1 represents the comparisons of the total or mean measurements. In these experiments C, D and N shows the fact that the more abundant yeast are poured more flies emerge and then the expressivity and body weight are decreased. But the series S indicates a different fact that the sufficient supply of food makes Curly expressivity of the adult flies to maintain nearly level even under the condition of high larval population density. From above mentioned three experiments, the nutritional condition, which may be influenced by the larval population density, may be considered to be one of the important controlling factor of Curly expressivity of the adult flies. B. The effect of temperature. Curly expressivity was controlled mainly by the nutritional condition at normal temperature (24 ± 1 C.), but through the course of these experiments, the author noticed by a certain accident that the expressivity was also influenced by cultural temperature. Then he investigated the effect of temperature on Curly expressivity. 1. Preliminary tests. a) Five pairs of Cy/l flies were allowed to breed on the ordinary culture bottles. The experiments were divided into three series according to temperatures, 31 ± 1 C., 24 ± 1 C. and 19 ± 1 C., to which these cultures were exposed. Comparisons on Curly expressivity were made in the emerged adult flies, development of which was completed at these temperatures. Table 2 gives the results, showing a positive Table 2 The relation expressivity when living between the cultural yeast suspension is temperature used as food and Curly of the larvae correlation between cultural It was, however, considered temperature and that 31 ±1 C. Curly expressivity of the adult flies. was nearly lethal temperature, because
5 June 1956 K. NOZAWA : THE ENVIRONMENTAL CONDITIONS IN DROSOPHILA 167 the number of emerged flies was very few ; therefore in the following experiments, the high temperature tests were conducted at 29 ± 1 C. b) Concerning these experiments, the author considered that it was necessary to decide whether the effect of temperature was direct or not, because it was likely that the nutritional condition of the developing larvae could become better by acceleration of propagation of yeast at high temperature and act secondarily on Curly expressivity of the adult flies. To test such a possibility, one drop of sterilized yeast extract prepared from suspension of dry yeast was used as food of the larvae developed from one hundred eggs. Comparisons on Curly expressivity were made according to the cultural temperature, 29 ± 1 C and 24 ± 1 C. 'Table 3 shows clearly also a Table 3 The relation between the cultural temperature and Curly when yeast extract is used as food of the larvae expressivity positivetion corelabetween the cultural temperature and Curly expressivity when yeast extract is used. Therefore it seems to be decisive that the effect of temperature on Curly expressivity are direct one. 2. Determination of the temperature-effective period. a) In order to determine whether the temperature-effective period of Curly expressivity was in the larval stage or in the pupal one, the following experiments were carried out. One hundred egg samples were allowed to develop on each culture medium poured with one drop of 5% suspension of dry yeast ; and when the larvae pupated, they were transf erect to the other bottle supplied with sufficient humidity within 12 hours after pupation. Temperature was kept at 19 ± 1 C., 24 ± 11 C. and 29 ± 1 C. during the larval and pupal stages respectively, and the experiment was divided into nine classes, combining the temperature conditions of the two developmental stages. Table 4 represents five comparisons on the emerged adult flies. From this table it can be recognized that Curly expressivity of the adult flies are exclusively influenced by temperature of the pupal stage irrespective of the culture conditions which are expressed themselves in number of the emerged flies, mean body weight and so on. b) In order to decide the temperature-effective period after pupation more accurately, the three following series of experiments were carried out. One hundred egg samples were allowed to develop on each culture medium poured with one drop of 5% suspension of dry yeast at 24 ± 1 C., and transfered to
6 168 THE JAPANESE JOURNAL OF GENETICS Vol. 31 No. 6 Table 4 Results of the experiments carried out in order to determine the temperature-effective period of Curly expressivity was in larval or pupal stage. L : Larval stage, p: Pupal stage whether the other stages of bottle of 19 ± 1 C. or 29 ± 1 C., when the insects development : arrived at the following
7 June 1956 K. NOZAWA : THE ENVIRONMENTAL CONDITIONS IN DROSOPHILA 169 1) ii) iii) about 195 The stage of eye pigmentation : about 145 hours after egg-hatching. The stage of wing pigmentation : about 170 hours after egg-hatching. The adult flies immediately after emergence whose wing did not begin hours after egg-hatching. extension Fig. 3. Results os the experiments to determine the temperature-effective period. Positions of the groups of three histograms show times of temperature-change from 24 C. after egg-hatching. The detailed explanations are in text. Fig. 3 represents summarily Curly expressivity of the adult flies in each experimental series. From these results showing the difference of Curly expressivity between the two experimental series, the stages of temperature-change of which are the stages of wing pigmentation and the earliest adult flies respectively, the temperature-effective period is determined to be in about the last one day of the pupal stage. C. Combination of the effects of larval population density and temperature. Since two factors, i, e. larval population density and temperature, were found to control Curly expressivity, the problem of interaction between these two factors was given rise to discussion. In order to decide which factor was dominating to determine Curly expressivity, two combinations were made : low population densitylow temperature and high population density-high temperature. The experimental series of low larval population density were carried by the above mentioned satiation tests for one pair of the parents; in the experimental series of high larval population density 20 to 25 pairs of parents were allowed to breed on each culture medium on which one drop of 5% suspension of dry yeast was poured. Temperature conditions of five experimental series were shown in Table 5.
8 170 THE JAPANESE JOURNAL OF GENETICS Vol. 31 No. 6 Table 5 Combination of the effects of larval population density and temperature From these results, which show that the expressivity are determined almost exclusively by temperature condition, we can consider that within the range of these experiments the effect of temperature in the pupal stage is more dominating than that of larval population density to determine Curly expressivity of the adult flies. Discussion Under the ordinary culture conditions, Curly expressivity correlated positively with body weight and negatively with number of the emerged flies. Satiation tests showed also a clear positive correlation between body weight and Curly expressivity. If body weight of the adult flies can be recognized as the indicator of their nutritional conditions in the larval stage, it may be considered from these experimental results, that Curly expressivity of the adult flies is controlled by the nutritional conditions in the larval stage ; the larvae which have taken food abundantly develop to the adults having typical Curly character, and the genotypic Curly flies which have been compelled to take insufficient food show a nearly wild type of expression. The quantity of food taken is changed according to competition. Its severity under the ordinary culture conditions we can suppose from the fact that many flies can emerge as long as the conditions are good as shown in the satiation tests. Moreover, it may be considered that under the ordinary culture conditions the larval population sizes are firstly regulated by the quantity of poured yeast and that the quantity of food taken by the individual insects are determined secondarily by interrelation between the quantity of propagating yeast and the population size of the growing larvae. By this consideration an explanation may be given for the above mentioned negative correlation between the quantity of poured yeast and Curly expressivity of the adult flies (A-2 Experiments C, D and N), which at first sight appeared to be contradictory. The temperature-effective period on Curly expressivity was determined to be in the last one day of the pupal stage. In this period the wings of the flies are still constricted, in the stage of extension of which Curly flies can be distinguished morphogenetically from wild type (Waddington, 1939). Therefore temperature may influence physically or chemically on the material basis managing contraction of the wing surface. If such a basis is constructed from the food materials anabolically. in
9 June 1956 K. NOZAWA : THE ENVIRONMENTAL CONDITIONS IN DROSOPHILA 171 the flies of Curly genotype, we may also be able to conjecture the relation between Curly expressivity and the larval nutritional condition. On the question which effect of the two environmental conditions is more important to determine Curly expressivity, we may think that the effect of temperature in the pupal stage is more dominating than that of larval population density judging from the experimental results. But we can not consider such an answer as gives a decisive conclusion. At any rate, because these two effects have nearly whole-range influences on Curly expressivity separately from each other, we may be able to control expression of the Curly character by regulating one of the two environmental conditions. Lastly, these experiments show that Curly expressivity of the females is nearly always higher than that of the males. About the cause of this sexual difference the author and studied can not discuss at present. Summary 1) Two environmental effects on the expressivity of Curly character were found with Cy/l (2) 50 c flies as material. 2) One of these effects was larval population density. It influenced Curly expr essivity through the nutritional conditions of the larvae ; the good nutritional conditions of the larval stage were observed to give typical Curly expression. 3) Another was cultural temperature ; higher temperature gave higher expressivity of Curly character. The temperature-effective period was determined to be in the last one day of the pupal stage. 4) Within the range of these experiments the effect of temperature in the pupal stage was appeared to be more dominating than that of larval population density to determine Curly expressivity. Acknowledgement The author wishes to acknowledge to Dr. D. Moriwaki, Tokyo Metropolitan University, for his kindness in the interpretation of the data and in the preparation of the manuscript. The author is also grateful to Prof. K. Masui and Assist. Prof. K. Kondo for their constructive criticisms during the work. Literature Cited Driver, E.C Temperature and gene expression in Drosophila. Jour. Exp. Zool. 59 : Komai, T Crippled, a new mutant character of Drosophila melanogaster, and its inheritance. Genetics 11: Morgan, T. H The role of the environment in the realization of a sex-linked Mendelian character in Drosophila. Amer. Nat. 49 : Moriwaki, D. and K. Oyama (U. Taku) Manifestation of character in Drosophila ananassae. I. Date of emergence and its effects. Jap. Jour. Genet., Supp. Vol. 1 : (In Japanese with English Resume). Stanley, W. L The effect of temperature upon wing size in Drosophila. Jour. Exp. Zool. 69: Waddington, C. H Organisers and Genes. London. Ward, L The genetics of curly wing in Drosophila. Another case of balanced lethal factors. Genetics 8 :
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