NON-MENDELIAN FEMALE STERILITY IN DROSOPHZLA MELANOIGASTER: INFLUENCE OF AGING AND THERMIC

TREATMENTS. 111. CUMULATIVE EFFECTS INDUCED BY THESE FACTORS

ALAIN BUCHETON

Laboratoire de Gknktique - Universitk de Clermont-Ferrand 11, B.P. 45, 63170 Aubihe, France

Manuscript received November 20, 1978 revised copy received June 29, 1979

ABSTRACT

Crosses between various strains of Drosophila melanogaster may give rise to a female sterility of non-Mendelian determination. Reduced fertility is observed in females, known as SF females, bred from crosses between females of “reactive” strains and males of “inducer” strains. The reduced fertility of the SF females is the result of an interaction between an extrachromosomal property, the reactivity, and a chromosomal factor, 1. The extrachromo- somal property varies considerably in its ability to reduce fertility. The fer- tility reduction of the SF females corresponds to what is known as the react- ivity level of their reactive mothers. Two nongenetic factors can modify the level of reactivity: aging and temperature. The action of aging is cumulative. When the flies of a reactive strain are submitted at each generation to the action of this factor, the level of reactivity of this strain is gradually modified. The modifications induced are reversible. Indeed, when such a modified strain is returned to standard breeding conditions, the reactivity returns progressively to its initial level. The effect of thermic treatments also seems to be cumulative and reversible.

CROSSES between various strains of Drosophila melanogaster give, in some cases, daughters showing a specific kind of reduced fertility. On the basis of

the fertility of the daughters, all strains can be assigned to one of three cate- gories: reactive, inducer and neutral. The reduced fertility is observed in fe- males, denoted SF females, resulting from crosses between females of reactive strains and males of inducer strains. The reciprocal crosses (inducer females X

reactive males) produce females, called RSF females, that are normally fertile. Crosses involving neutral strains, or within a single category of strains, also give normally fertile progeny (PICARD et al. 1972a).

The reduced fertility of SF females results from the fact that a certain pro- portion of the eggs they lay fail to hatch, embryonic development being blocked before the blastoderm stage. Egg death is a maternal characteristic. Its frequen- cy does not depend on the males with which the SF females are crossed (PICARD et al. 1977). Genetics 93: 131-142 September, 1979.

132 -4. BUCHETON

The sterility of SF females is the result of an interaction between a cytoplas- mic property of reactive strains, called reactivity, and a chromosomal factor, I , which is contributed by inducer strains (PICARD et al. 1972b).

Reactivity and I factor show great variability, the level of SF female sterility depending, to a large extent, on the choice of the inducer and reactive parents. The reactivity level of a reactive strain is determined by the fertility reduction of the SF daughters obtained by crossing females of this strain with standard inducer males. A strain is considered strongly reactive when the hatching per- centage of eggs laid by such SF daughters is low. It is considered weakly reac- tive when this hatching percentage is high. In a similar way, it is possible to distinguish strong and weak inducer strains (BUCHETON et al. 1976).

Crosses between reactive strains displaying different levels of reactivity have shown that the level of reactivity of a female is mainly determined by maternal inheritance, but depends to a small extent on her father (BUCHETON 1973). It has been demonstrated that this paternal influence is associated with each of the three major chromosomes. This influence of chromosomes is still more evident when, by backcrosses and use of markers, reactive flies are bred that descend from maternal ancestors of one strain, but have acquired the whole genotype of another strain through their paternal ancestors. The level of reactivity of these flies, which at first is near the value characteristic of the maternal ances- tral strain, evolves over several generations towards the level of the paternal ancestral strain (BUCHETON and PICARD 1978). Therefore, in the long run, it is a polygenic system included in the chromosomal genotype that fixes the level of reactivity. But a strong tendency for this character to be transmitted un- changed from mother to daughter introduces a delay of several generations in the phenotypic expression of the genotype (BUCHETON and PICARD 1978; PICARD 1978a,b).

The degree of sterility of SF females depends also, in large part, on non- genetic factors. The first is age. The hatching percentage of eggs laid by SF females increases regularly as they get older (PICARD et al. 1977). A striking point is that aging has an effect not only when it directly concerns SF females, but also when it concerns their reactive ancestors. Indeed, SF females are less sterile when they are descended from older reactive mothers. This effect of aging is also observed with the reactive grandparents of SF females (BUCHETON and PICARD 1975; BUCHETON 1978). Thus, aging reduces the reactivity level of re- active females.

Temperature is another nongenetic agent that can influence SF sterility. If the temperature at which SF females are kept is raised from 20" to about 29", their fertility is either decreased or increased according to the stage during which the heat treatment is applied. In fact, a decrease is observed during all the preimaginal stages and during the first period of oogenesis in adult flies, late oogenesis being the only stage during which a heat treatment has an opposite effect (BUCHETON 1979a).

In the same way as in the case of aging, heat treatments are also effective when applied to the reactive ancestors of SF females. Warming reactive females

SF STERILITY I N DROSOPHILA 133

during their larval or pupal stages gives rise to more sterile SF daughters (BUCHETON 1979a). In contrast, less sterile SF daughters can be reversibly ob- tained by subjecting their adult reactive mothers to a short thermic treatment. The same effect can be observed by treating the reactive grandparents of SF females (BUCHETON 1978).

Thus, aging and heat treatment act in the same way on both the SF females and their reactive ancestors. However, the effects of these factors are much the greatest when their action is applied directly to the SF females. They are re- duced when their action is applied to the reactive mothers of SF females, and still further reduced when the reactive grandparents are involved. Therefore, the modifications in the levels of reactivity induced by aging or heat treatments are heritable, although passage from one generation to the next has a buffering effect (BUCHETON 1978).

In the experiments described in the present paper, the possibility that the action of these two factors may accumulate in the course of generations and the reversible character of the induced modifications were investigated.

MATERIALS A N D METHODS

The flies were raised at 20” on the axenic food described by DAVID (1959). Strains: eStz8 is a strongly reactive stock (see BUCHETON et a1 1976), obtained by selection

following the method described by PICARD et a1 (1972a) within a strain homozygous for the mutation ebony.

B2’ and Lu are two wild-type inducer strains obtained from flies caught in 1972 in west- ern France and in 1969 in southern France, respectively.

Measurements of hatching percentages: For each test, about 50 females whose fertility was to be measured were crossed with their brothers and placed in a tube containing axenic food and carbon black. The parents were removed after 24 hr, and numbers of hatched and un- hatched eggs were scored after another 443 hr. An average of 300 eggs was scored for each measurement. The temperature was kept at 20” throughout.

Measurements of the reactivity levels of the stocks: Five females from the stock to be tested were grown at 20” and mated soon after they eclosed to either B2’ or Lu males. About 50 SF daughters from this cross were tested for fertility as described above. This procedure was repeated 15 times for each measurement.

RESULTS

The est28 reactive strain was divided into various replicate stocks with which experiments were carried out to study the effects of aging and of heat treat- ments when applied during several generations.

Action of aging: In the first experiment, three replicate stocks were made. Two of them (Y and U’) were maintained constantly at 20’. The flies of each generation were collected from eggs laid by females two to four days old. For the sake of clarity, these stocks are called “young stocks” since the flies were continuously obtained from young parents. A third stock (0) also was main- tained constantly at 20°, but the flies of each generation were collected from eggs laid by females aged between 45 and 55 days. The flies of this stock were consistently obtained from old parents; it is called the “old stock.”

134 A. BUCHETON

FIGURE 1.-Cumulative and reversible effects induced by aging. The graphs represent the change of reactivity level of various replicate stocks. Each point corresponds to the average of 15 measurements. 0, A, (solid lines), (dotted line) correspond to the 0, OY1, OY2, Y stocks, respectively (see text).

For each stock, the change of level of reactivity was monitored in successive generations as indicated in the MATERIALS AND METHODS, using young reactive females raised at 20". The B2' inducer strain was used to measure the reactivity levels.

The results show that both "young stocks" Y (Figure 1) and Y' (Figure 2) had similar levels of reactivity and behaved as strongly reactive. Indeed, the hatching percentages of the eggs laid by the SF females were almost always in the range of 10 to 20%. This strong reactivity level of both stocks remained unchanged for more than 70 generations.

IUV I I

g e n e r a t i o n s

FIGURE 2.-Effects induced by heat treatments of adult flies (see legend of Figure 1). 0, A, A, (solid lines), (dotted line) correspond to the H, H Y I , HY2, H Y 4 and Y' stocks, respectively (see text).

SF STERILITY IN DROSOPHILA 135

In contrast, Figure 1 shows that the level of reactivity of the 0 (old) stock decreased quickly in the course of a few generations. After three generations of aging, the females of the 0 stock, which were initially strongly reactive, be- haved as weakly reactive females. From the third generation on, the hatching percentages of the eggs laid by the SF females reached about 90%. This is a value comparable with that obtained from the normally fertile RSF females bred from crosses between B2' inducer females and eStzs reactive males (the value obtained with such RSF females was 92.8 -I 0.7). Therefore, aging, which reduces the reactivity level, has a cumulative effect when applied during several successive generations.

In the 0 stock; after a few generations, the level of reactivity reached a state of equilibrium. It was of interest to determine whether the modifications in- duced by the particular breeding conditions to which the stock was submitted could be reversed by a return to the normal initial conditions. For this purpose, two stocks, OY1 and OY2, were isolated respectively at generations Gti and Gg from the 0 stock. They were submitted, from the time of their isolation on- wards, to the same breeding conditions as the Y and Y' stocks, i.e., they were constantly maintained at 20" and the flies of each generation were collected from eggs laid by females, two to four days old. The change of level of reactiv- ity of each stock was monitored in successive generations as indicated earlier, using the B2' inducer strain.

Figure 1 shows that the reactivity level of the OY1 stock increased progres- sively. The females of this stock, initially showing weak reactivity, behaved finally as strongly reactive. At the end of this evolution, the hatching percent- ages of the eggs laid by the SF females ranged between 10 and 20%. More than five generations were necessary to reach this level of reactivity, which was simi- lar to that of the Y and Y' stocks.

The same evolution is observed with OY2 (Figure l), but the study of this stock has not been continued for a number of generations sufficient to determine whether the transformation towards strong reactivity may be completed in this case.

Therefore, the cumulative modifications induced by aging in a reactive strain are reversible. When the strain is no longer subjected to the action of aging, the reactivity returns to its initial level.

Action of heat treatments: It was shown above that the cumulative effects of aging do not irreversibly remove reactivity. It was therefore of interest to try to obtain amplified effects by using the action of heat treatments, which have earlier been shown to affect reactivity (BUCHETON 1978).

Another replicate stock (H) was made from the estzs reactive strain. The flies were subjected to a heat treatment of 29" at each generation. After imaginal emergence, the flies were kept at 20" until the fifth day of life. They were put at 29" between the fifth and ninth day and afterwards put back to 20". The eggs laid by the 11- or 12-day-old-females were maintained at 20' to obtain the next generation. (BUCHETON (1978) showed that a thermic treatment applied for four days to eStzs females induces the largest reduction of reactivity level

136 -4. BUCHETON

about six or seven days after the beginning of the treatment.) This stock is called the “heated stock” since the flies were continuously obtained from heat- treated parents,

The change of level of reactivity was monitored in successive generations, as previously indicated, from young reactive females raised at 20°, using the B2’ inducer strain. Figure 2 shows that the level of reactivity of H diminished pro- gressively. After four generations of heat treatments, the females of this stock behaved as weakly reactive. At the fourth generation, the SF females had nor- mal fertility, and the weak reactivity of the females of the “heated stock” was maintained afterwards until the 46th generation.

It may be noted that in the H stock, the parental age was 11 to 12 days. Therefore, the flies of this stock were not only subjected to a thermic treatment, but also to a moderate action of aging. In order to try to distinguish between the effects induced by heat treatments and those due to aging, other replicate stocks were made from the est28 strain.

The flies of one of them (I) were submitted at each generation to a heat treatment. at 29” between the first and fifth day of life, and afterwards put back at 20”. The eggs laid by the six- or seven-day-old females were collected and maintained at 20” to obtain the next generation.

Another stock (N) was constantly maintained at 20’. The parental age in this stock was the same as in I (six or seven days).

A third stock (U”) was maintained in the same way as the Y and Y’ “young stocks” previously described.

The fourth stock (V) was also maintained permanently at 20°, but the flies of each generation were collected from eggs laid by ten- to Il-day-old females. It may be argued that the parental physiological age was not identical in the I and N stocks, since the flies of I were maintained at 29” for four days. If the rate of aging is doubled at this temperature, as may be presumed from the developmental rate, the flies from which the successive generations are consti- tuted in this control stock for parental physiological age, must be four days older than in I. Thus, this condition was obtained with the V stock, since the parental age was from ten to 11 days.

The changes of reactivity levels of these stocks were monitored as previously indicated, using the B2’ inducer strain. The results are given in Table 1.

The level of reactivity of the Y” stock remained strong, as did that of the Y and Y’ stocks.

In the I stock, which was subjected to heat treatments, the reactivity level diminished progressively as in the H stock (see Figure 2). This change may be attributed essentially to the action of the heat treatments, because in the N stock, in which the parental age was identical to I, the reactivity level changed very little. In the V stock, which was submitted to an action of aging greater than in I, the reactivity level reached after aging applied during four successive generations was stronger than that observed in I.

These results indicate that the change in the level of reactivity of the H stock is due, at least in part, to the action of thermic treatments.

SF STERILITY IN DROSOPHILA 137

TABLE 1 Hatching percentages of the eggs laid by SF females produced by four stocks derived

from the estzs reactive strain

Generation No Y’I N V I

GI 20.3k2.3 27.423.0 35.6552.2 63.5rt4.5 75.823.6

87.7+-0.8

Each value is the average of 15 measurements of fertility. The standard errors are given.

G2 25.222.4 42.323.7 G3 16.421.6 31.823.5 G4 17.922.1 34.123.7 58.623.9

To study the reversibility of the effects induced by repeated heat treaments, three stocks, HYI, HY2 and HY4, were established from H (generations G4, G13, and G z ~ , respectively). These stocks were submitted, from the time of their isolation onwards, to the same breeding conditions as the Y and Y’ stocks.

The change of level of reactivity of each stock was monitored in the succes- sive generations as indicated above, using the B2’ inducer strain.

Figure 2 shows that the level of reactivity in the three stocks became progres- sively stronger. HYI, HY2 and HY4 females, which were weakly reactive at the beginning, finally behaved as strongly reactive females, like those of the Y and Y’ stocks. This transformation was slow and required eight or ten genera- tions for completion.

Therefore, as in the case of aging, the modifications in the reactivity level induced by heat treatments can be completely reversed, if the “heated stock” is no longer subjected to the action of the thermic treatments.

Evidence for the persistence of a weak level of reactivity in the stocks sub- jected to aging and heat treatments: It may be noted that in the 0 and H stocks (Figures 1 and 2), once they have reached their equilibrium levels, no sterility can be detected in the progeny obtained after crossing females of these stocks with B2’ inducer males. This leaves open the question of whether the strains modified by repetitive actions of aging or heat treatments are still reactive, or whether they have evolved towards a true neutral state.

To answer this question, measurements of the levels of reactivity of the dif- ferent stocks were carried out at various generations as indicated in MATERIALS

AND METHODS using a stronger inducer strain than B2’: the strain Lu. The SF females obtained in this way from the Y and Y’ “young stocks” had

hatchabilities ranging between 0.2 and 4.3%. In the case of the Y stock, the hatching percentages of the eggs laid by the SF females bred from the Lu strain for the various generations were significantly lower than those obtained with the SF females bred from the B2’ inducer strain ( t = 8.3, df = 26, p < 0.001). The same was true for the Y’ stock ( t = 7.2, df = 31, p < 0.001).

The SF females obtained by crossing females of the 0 stock from the G4 gen- eration onwards, with Lu inducer males, had hatchabilities ranging between 51.7 and 78.4%. Thus, in the (4 “old stock,” the reactivity had not disappeared.

’I38 A. BUCHETON

Indeed, a quite significant reduction of fertility was observed when Lu inducer males were used, compared to the results obtained with RSF females coming from crosses between Lu inducer females and eStz8 reactive males (the hatching percentages of eggs laid by these RSF females was 90.5

For generations Gq to G I ~ , the hatching percentages of the eggs laid by the SF females bred from Lu fathers were significantly lower than those obtained with the SF females bred from B2’ fathers ( t = 11 .O, df = 20, p < 0.001). This clearly shows that the 0 stock cannot be considered as neutral. After the initial decrease, it stabilized at a weak level of reactivity, and this kind of equilibrium was maintained in spite of the continuation of the aging action at each genera- tion.

Similarly, the results obtained with the Lu inducer strain show that the H “heated stock” did not evolve towards a neutral state. The hatching percentages of the eggs laid by the SF females coming from the Gq to G a generations were significantly lower when the SF females were bred from Lu fathers (their values were in the range of 56.3 to 76.6%) than when they were bred from B2’ fathers ( t = 15.6, df = 36, p < 0.001). Therefore, it may be concluded that the reactivity of a strongly reactive strain may be reduced, but not suppressed, by subjecting the strain to heat treatment and aging at each generation. After several generations, the strain stabilizes at a weak level of reactivity, which re- mains stable in spite of the continuation of the treatments.

Action of a continuous thermic treatment: When heat treatments are applied to a single generation of reactive females, they modify the level of reactivity in either of the two following opposite ways: applied to late oogenesis, they reduce reactivity, and applied to earlier stages of oogenesis or during any preimaginal stage of development, they reinforce reactivity (BUCHETON 1979a). The action of continuous thermic treatments applied during several successive generations was studied.

Three stocks were constituted from the H and Y’ stocks. Two of them (HYH and HY3) were made starting from the 15th generation of the H stock. HYH was constantly maintained at 29”. The flies of each generation were collected from eggs laid by two- or three-day-old females. Thus, the flies were continu- ously obtained from young parents permanently raised at 29”. HY3 was con- stantly maintained at 20°, like the Y and Y’ stocks. The flies of this stock were continuously obtained from young parents raised at 20”. The third stock (Y’YH) was derived from the 26th generation of the Y’ “young stock” and maintained in the same breeding conditions as the HYH stock: flies obtained from young parents constantly maintained at 29”.

The change of reactivity level of each stock was monitored in successive generations as previously indicated, using the B2’ inducer strain. The results are given in Figure 3. As expected from the behavior of the HYI, HY2 and HY4 stocks, it may be seen that the reactivity of the HY3 stocks increased pro- gressively and finally reached a level similar to that of the Y or Y’ “young stocks.” However, the reactivity level of the HYH stock, which was constantly maintained at 29”, followed a change similar to that of HY3. It may be noted

1.4).

SF STERILITY I N DROSOPHILA 139

FIGURE 3.-Effects on the level of reactivity of various heat treatments. 0, A, 0 (solid lines), 0, 0 (dotted lines) correspond to the H, HY3, Y'YH, HYH, Y' stocks, respectively (see text).

that in the Y'YH stock, which was also constantly maintained at 29", the level of reactivity remained strong.

Therefore, continuously raising the flies at 29' either increases the reactivity when the stock is derived from a strain subjected to short heat treatments dur- ing the imaginal life, or maintains it at a strong level when the stock is derived from a strain whuse flies were previously kept at 20' and bred from young par- ents. In the case of the HYH and Y'YH stocks, the periods of opposite sensitiv- ity are likewise subjected to the action of warming, and the treatment of late oogenesis seems to be compensated by the earlier treatments. This compensation has the result that the level of reactivity of a stock bred from young parents, does not appear to depend on the temperature at which it is constantly kept.

DISCUSSION

The results reported in this paper confirm that two nongenetic factors, aging and temperature, can change the level of reactivity. It was previously demon- strated that the modifications induced by these two factors are partially trans- mitted from mother to daughter (BUCHETON 1978). The present results clearly show that aging has cumulative effects when applied systematically to several successive generations. Indeed, when a strongly reactive strain previously main- tained in standard breeding conditions is subjected at each generation to the action of aging, the reactivity observed in this strain is progressively reduced and evolves towards a weak level. It takes several generations to reach this level, but afterwards it is maintained unchanged indefinitely, in spite of the continu- ing action of aging. It appears, therefore, to correspond to a new equilibrium that is characteristic of the changed breeding conditions of the stock.

The modifications induced in a strain by such a change in the breeding con- ditions are always reversible. When a modified stock is no longer subjected to

140 4 . BUCHETON

the action of aging and is returned to standard breeding conditions (flies of each new generation collected from young parents raised at 20'), its reactivity re- verts slowly back towards the initial strong level.

In the 0 stock, the parental age is in the range 45 to 55 days, and not all of the females survive. It might be argued that high levels of reactivity are associated with decreased longevity. If this were the case, the change of reactivity level in 0 might be due to such selection for longevity. It may be seen that in the N and V stocks, subjected to a moderate action of aging without selection for longevity, a similar change in reactivity, although lower than in 0, is observed. The same conclusion has been drawn from the study of another stock submitted to a mod- erate action of aging (BUCHETON 1979b). Moreover, it has also been verified that the chromosomes from strains modified by repetitive action of aging show the same properties as those of the chromosomes from the original strong reac- tive strain (BUCHETON 1976b). Therefore, the modifications of reactivity levels induced by this factor actually correspond to an effect on the reactive extra- chromosomal state.

The study of strains subjected to repetitive action of thermic treatments ap- plied during late oogenesis seems to indicate that such treatments also induce modifications of the reactivity level maintained in the strains. As in the case of aging, these effects are always reversible.

The response of reactivity to changes in nongenetic factors must be compared to the observations previously reported (BUCHETON and PICARD 1978) concern- ing the action of the genotype. It is known that, in uniform breeding conditions, strains may be found that differ largely by the level of reactivity that they maintain. From crosses between these strains, it was concluded that, in the short term, the level of reactivity tends to be maternally inherited, but is de- pendent, in the long run, on a polygenic system included in the chromosomal genotype. Changing, by appropriate crosses, the genotype within a maternal line may therefore trigger a slow evolution towards a new level of reactivity, which is quite similar to what is observed in the case of nongenetic factors.

On the whole, the phenomenon called reactivity appears as the expression of a cytoplasmic state, subject to a large range of quantitative variation. Like a classical quantitative character, it depends on the interaction between genotype and certain breeding conditions. However, due to its strong tendency to be transmitted unchanged from mother to daughter, what is determined by this interaction is only the equilibrium level that will eventually be reached and preserved, if both genetic and nongenetic factors are kept uniform for a suffi- cient number of generations. Thus, a very important feature of reactivity is the striking inertia with which the cytoplasmic state responds to either the action of nongenetic factors or changes in the genotype.

It should be noted that other observations bearing some similarity to those concerning reactivity have been reported in the Drosophila literature. The most similar situation to the SF sterility phenomenon is found in the transmission of the extrachromosomal element delta in Drosophila melanogaster. Indeed, rais- ing flies at a low temperature (18') reduces the level of delta. But when the

SF STERILITY IN DROSOPHILA I41

flies are again reared at the usual temperature, this level increases and returns progressively to its initial value. However, this evolution is slow and requires about nine generations for completion (MINAMORI 1969). It also may be noted that modifications in the genotype change the amount of the element carried by the flies, and that this amount is gradually restored over several generations to the original level with the restoration of the original genotype (MINAMORI 1972). Thus, the accumulation of delta in successive generations shows some analogies with the cumulative and reversible effects induced by nongenetic fac- tors reported in this paper and with the inertia with which the cytoplasmic reactive state reacts to changes in the genotype.

I express special thanks to J. C. BREGLIANO and Ph. L’H~ITIER for advice throughout this work and for helpful comments on the manuscript. This work was supported by grants from the Centre National de la Recherche Scientifique (ERA 692: phdnomknes d’hkrkditb non menddlienne chez la Drosophile), from the University of Clermont-Ferrand 11, and from the Fondation pour la Recherche Mkdicale Francaise.

LITERATURE CITED

BUCHETON, A., 1973 Contribution B l’ktude de la stkrilitk femelle non mendklienne chez Drosophila melanogaster. Transmission hdrkditaire des degrbs d’efticacith du facteur “rkacteur”. Comptes Rendus Ac. Sc. Paris (D) 276: 641-644. -, 1978 Non-Men- delian female sterility in Drosophila melanogaster: Influence of ageing and thermic treatments. I. Evidence for a partly inheritable effect of these two factors. Heredity 41: 357-369. -, 1979a Non-Mendelian female sterility in Drosophila melanogaster: In- fluence of ageing and thermic treatments. 11. Action of thermic treatments on the sterility of SF females and on the reactivity of reactive females. Biologie Cellulaire 34: 43-49. - , 19791, Contribution A l’htude d’un cas d‘interaction nuclko-cytoplasmique: le sys- tkme inducteur-rkacteur de Drosophila melanogaster. ContrBle gknetique de la rkacti- vitk. PhD. thesis, Universite de Clermont-Ferrand 11.

Mise en dvidence d’une influence partiellement hkri- table de 1’8ge sur un phdnomkne de stkrilitk femelle B dbterminisme non mendklien chez Drosophila melanogaster. Comptes Rendus Ac. Sc. Paris (D) 281: 1035-1038. -, 1978 Non-Mendelian female sterility in Drosophila melanogaster: hereditary trans- mission of reactivity levels. Heredity 40 : 207-223.

BUCHETON, A., J. M. LAVIGE, G. PICARD, and PH L’H~RITIER, 1976 Non-Mendelian female sterility in Drosophila melanogaster: quantitative variations in the efficiency of inducer and reactive strains. Heredity 36: 305-314.

DAVID, J., 1959 Etude quantitative du developpement de la Drosophile Bevke en milieu axknique. Bul. Soc. Biol. France et Belgique 93: 472.

MINAMORI, S., 1969 Extrachromosomal element delta in Drosophila melanogaster. I. Gene dependence of killing action and of multiplication. Genetics 62: 583-596. -, 1972 Extrachromosomal element delta in Drosophila melanogaster. VIII. Inseparable associa- tion with sensitive second chromosome. Genetics 70 : 557-566.

Non-Mendelian female sterility in Drosophila melanogaster: sterility in the daughter progeny of SF and RSF females. Biologie Cellulaire 31: 235-244. -, 1978b Non-Mendelian female sterility in Drosophila melanogaster: sterility in stocks derived from the genotypically inducer or reactive offspring of SF and RSF females. Biologie Cellulaire 31 : 245-254.

BUCHETON, A. and G. PICARD, 1975

PICARD, G., 1978a

142 A. BUCIIETON

PICARD, G., A. BUCHETON, J. M. LAVIGE, and A. FLEURIET, 1972a Contribution B l'6tude d'un phenomhne de sthrilitk B dhterminisme non mendelien chez Drosophilia melanogaster. Comptes Rendus Ac. Sc. Paris D, 275: 933-936.

PICARD, G., A. BUCHETON, J. M. LAVIGE, A. FLEURIET, J. C. BREGLIANO and PH. L'HBRITIER, 1972b Further data on non-Mendelian female sterility in Drosophila melanogaster.

PICARD, G., J. M. LAVIGE, A. BUCHETON, and J. C. BREGLIANO, 1977 Non-Mendelian female sterility in Drosophila melanogaster: physiological pattern of embryo lethality. Biologie Cellulaire 29: 89-98.

Corresponding editor: J. F. KIDWELL