In Drosophila expression of position-effect variegation is enhanced by culturing flies  at low temperatures. It is demonstrated that this effect may not be solely temperature  dependent. Maternal age influences offspring development times. Futhermore, at a given  temperature, the longer a fly takes to develop, the more likely is it to exhibit position-effect  variegation.Chez la Drosophile, l’expression de la diversité de « l’effet position est favorisée lorsque les mouches se développent sous des températures basses. Il a été démontré que   cet effet n’est pas uniquement dépendant de la température. L’âge maternel influence la  durée de développement des descendants. De plus, pour une température donnée, il semble   que plus la durée de développement est longue, plus l’expression de « l’effet position » est  diversifiée

Hartmann-Goldstein, I

Mills, A

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Maternal age, development time, position effect variegation in <it>Drosophila melanogaster</it>

A Mills

I Hartmann-Goldstein

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Maternal age, development time, position effect variegation
in Drosophila melanogaster
A. MILLS I. HARTMANN-GOLDSTEIN
LN.R.A., Station de Recherches avicoles
Centre de Recherches de Tours, Nouzilly, F 37380 Monnaie
"’ Department of Genetics. University of Sheffield
Western Bank, Sheffield SIO 2TN, Great Britain
Summary
In Drosophila expression of position-effect variegation is enhanced by culturing flies
at low temperatures. It is demonstrated that this effect may not be solely temperature
dependent. Maternal age influences offspring development times. Futhermore, at a given
temperature, the longer a fly takes to develop, the more likely is it to exhibit position-effect
variegation.
Key words : Maternal age, development time, Drosophila, position-effect.
Résumé
Age maternel, durée de développement et effet de position (type « variegation »)
chez Drosophila melanogaster
Chez la Drosophile, l’expression de la diversité de « l’effet position est favorisée
lorsque les mouches se développent sous des températures basses. Il a été démontré que
cet effet n’est pas uniquement dépendant de la température. L’âge maternel influence la
durée de développement des descendants. De plus, pour une température donnée, il semble
que plus la durée de développement est longue, plus l’expression de « l’effet position est
diversifiée.
Mots clés : Age maternel, durée de développement, Drosophile, effet position.
I. Introduction
In Drosophila sp. the transposition of genes, which accompanies chromosome
translocations, sometimes results in changes in gene action which are expressed as
mutant phenotypes (SPOFFORD, 1976). Such phenomena are known as position-effects
(STURTEVANT, 1925). Position-effects are of two types (SPOFFORD, 1976). In one type
the change in gene action is somatically stable and is expressed in all cells. In the
other type the change in gene action is subject to wide and frequent statistical fluctua-
tion in homogenous cells. In certain tissues, for example the ommatidia of the
compound eye (HARTMANN-GOLDSTEI,1967), this results in somatic mosaicisms which
are generally known as « eversporting displacements » (MuELLER, 1930), or « variega-
tions (SCHULTZ, 1936).
Position-effect variegation may thus be defined as the mosaic expression of a gene
(or genes) lying near the « break-point » in a chromosome re-arrangement (SPOFFORD,
1976). However, not all translocations induce variegation ; and the phenomenon is
generally restricted to those transpositions which bring genes normally lying in eu-
chromatic chromosomal segments into the vicinity of heterochromatin (LEms, 1950 ;
SPOFFORD, 1976).
Variegated phenotypes are a reflection of localised gene deactivation, i.e. of a
gene being active in some cells but not in others. In the majority of cases the effect
appears to be attributable to the heterochromatization of transposed euchromatin
within affected cells (HARTMANN-GOLDSTEI,1967 ; SPOFFORD, 1976). However the
exact cytochemical and molecular mechanisms of variegation are not well understood.
One of the characteristics of position-effect variegation is the sensitivity of the
variegated phenotype to factors extrinsic to the actual chromosome translocation. Tem-
perature at critical stages during development, the amount of heterochromatin in the
genome, the parental source of the translocated chromosome segment, and other gene
loci may all act as modifiers of the expression of variegation associated with a given
translocation (SPOFFORD, 1976).
In strain T(1 : 4) w m 258-1 / In (1) L 49 w lz of Drosophila melanogaster
(LINDSLEY & GRELL, 1968), hereafter refered to as w m 2GS - 21, position-effect on band
3C7 of a translocated X chromosome results in variegation in expression of the Notclz
locus (HARTMANN-GOLDSTEI 1967) ; a wing abnormality which involves variable
nicking or scalloping of the wing margins, thickening of the wing veins, and bristle
abnormalities (WELSHONS, 1965, see also figure 4).
Expression of variegation of the Notch phenotype in strain w 11 25s- 21 can be
enhanced by culturing the strain at low temperatures. This effect is apparently exerted
during the embryonic and larval stages of development (HARTMANN-GOLDSTEI,1967).
In view of this, since it is common knowledge that in Drosophila sp. low ambient
temperatures prolong generation times, and thus the duration of developmental sta-
ges, the question arises as to whether or not the variegation seen in flies raised at low
temperatures is a direct effect of temperature, or is a consequence of extended deve-
lopment time which for some reason ’ permits’ more variegation. In order to try and
answer this question we studied the incidence of Notch variegation in flies whose
development times differed because of a factor other than temperature.
Since parental age is known to influence larval development time in D. melano-
gaster (SANG, 1956 ; DELCOUR, 1969), we took eggs from flies of different ages and
investigated the influences of parental age and development time on the incidence
of Notch variegation.
II. Material and methods
Pure line flies from the strain IV I 258 -- 21 of D. melanogaster were used throug-
hout the study. Variegation of the Notch phenotype in this strain occurs as a conse-
quence of position-effect on salivary band 3C7 of the X-chromosome, arising through
the translocation of the distal portion of one X-chromosome to a position proximal
to the chromocentre. The translocation is both hemi and homozygous lethal. The non-
translocated X-homologue carries the white (w) allele, and an inversion that is ho-
mozygous sterilising. Each generation of the strain thus contains white eyed males
hemizygous for the inversion, white eyed females homozygous for the inversion, here-
after refered to as X’X’ females, and red-eyed females heterozygous for the inversion
and the translocation, hereafter refered to as X’Xi females (MILLS, 1979). The deve-
lopment times of males, Xi females, and Xti females were considered separately ;
and as only X’Xi females exhibit the Notch phenotype study of the incidence of varie-
gation was by necessity restricted to flies of this type.
The development rate of D. melanogaster is influenced by various factors such
as ambient temperature, larval diet, and larval population density (SANG, 1956 ; DEL-
couR, 1969). In designing this experiment every care was taken to ensure that culture
conditions were constant for all larval populations.
A total of 30 replicate populations of flies (25 JJ and 25 ! ! in each) were
used. Each group of flies was maintained at 19 °C. Eggs were taken from flies whose
mean ages (± 0.5 d.) were 3.5, 4.5, 6.5, 9.5, 12.5 and 15.5 d. respectively. Since the
developmental stage of freshly deposited D. melanogaster eggs may be anywhere bet-
ween the moment after fertilization to just before emergence of the larvae (HUETTNER,
1923) which in strain w m 258 - 21, at 19 °C, represents a period of 55 hr (HARTMANN-
GOLDSTEIN, 1967), eggs were collected only from females which were likely to have
already laid during the two hours prior to collection of eggs. This was achieved in
the following manner. Each of the 30 replicate populations of flies (d6 and 9 9)
was transfered to an empty wide necked bottle. Each of these bottles was then
capped with an agar filled watch glass. The bottles were then inverted and left for
1 hr. At the end of this period each bottle was re-capped with a fresh agar filled
watch glass and left for a further 2 hr. Eggs laid on the first agar cap were discarded.
Eggs laid on the second agar cap were retained for experimental purposes, but only
if a large number (> 20) of eggs had been laid in the first hour. This technique for
the collection of fresh D. melanogaster eggs is essentially similar to that described by
SorrNErraLicx (1950). The uterus of the fruit-fly contains only one egg at a time
(NONIDEZ, 1920), thus when a female lays more than one egg in a relatively short
period of time, the second and subsequent eggs will be at similar stages of develop-
ment i.e. shortly after fertilization. Thus by taking eggs only from females which were
likely to have laid shortly beforehand we were able to ensure that most, if not all,
6f the eggs taken were at a similar stage of development. After collection batches
of 55 eggs were ’ seeded’ in 2.5 cm diameter vials containing 5 ml of glucose-yeast
culture medium. The vials were then placed in a culture room maintained at 19 °C,
and the larvae left to develop. Once imagines commenced to eclose vials were cleared
daily, the development times of the flies noted, and Xti females scored for the pre-
sence or absence of the Notch phenotype. A fuller description of the experimental
procedures used is given by MILLS (1979).
III. Results
Figure 1 shows the influence of maternal age on development times. Although
there were significant differences between the development times of males, Xi, and
Xti females - in general males exhibited the longest development times, and Xti
females the shortest - the influence of maternal age was the same in all 3 groups.

The length of the developmental period decreased with maternal age up to 6.5 days,
increased sharply between 6.5 and 9.5 days, and thereafter showed a general though
fluctuating tendency to increase.
The incidence of the Notch phenotype (i.e. the proportion of flies exhibiting the
phenotype) decreased with parental age up to 4.5 days. Thereafter the incidence of
Notch was positively correlated with parental age (r = 0.9126, n = 616, 0.05 > P >
0.02, fig. 2). The incidence of Notch was also positively correlated with the deve-
lopment time of the flies (r = 0.7666, n = 659, P < 0.001, fig. 3).
IV. Discussion and conclusions
These present results do not explain why maternal age influences progeny de-
velopment times. Nor do they shed much light on the cytochemical and molecular
mechanisms of position-effect variegation. However, what these results do indicate
is that, at least in ra w m 258- 21, low ambient temperature enhancement of posi-
tion-effect variegation is not necessarily a direct effect of temperature, but is in part
a function of extended development time. This finding is consistent with HARTMANN-
GOLDSTEIN’S(1967) suggestion that there are sensitive’ periods during development,
which if extended, and/or if during which animals are subjected to environmental
shocks (e.g. temperature), expression of position-effect variegation may be influenced.
Quite how this effect operates is unclear, but it has been demonstrated that ageing
brings about physiological changes in the Drosophila female (ROBERTSON & SANG,
1944) ; and it is tempting to speculate that the influence of maternal age on develop-
ment time and the relationship between development time and expression of position
effect variegation are in some way related.
Received January 9, 1984.
Accepted July 16, 1984.
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Maternal age, development time, position effect variegation in Drosophila melanogaster

Mills, Maryse

Hartmann-Goldstein, I.

ProdInra

Maternal age, development time, position effect variegation  in Drosophila melanogaster

A. MILLS

I. HARTMANN-GOLDSTEIN

EDP Sciences OAI-PMH repository (1.2.0)

Springer

Crossref

Analysis of a gene in Drosophila.

Effect of nutrition on fecundity and egg hatching :

Influence de l’âge parental sur la dimension des ceufs, la durée de développement, et la taille thoracique des descendants, chez Drosophila rnelanogaster.

On the relationship between heterochromatization and variegation in Drosophila with special reference to temperature sensitive-periods.

Parental age, development time, and position effect variegation

Position-effect variegation in Drosophila.

The early embryology of Drosophila melanogasrer.

The effects of unequal crossing over at the Bar locus in Drosophila.

The internal phenomena of reproduction in

The origin of germ cells in Drosophila melanogaster.

The phenomenon of position effect.

The quantitative nutritional requirements of Drosophila melanogaster.

Types of visible variations induced by x-rays in Drosophila.

Variegation in Drosophila and inert chromosome regions.

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Maternal age, development time, position effect variegation in Drosophila melanogaster

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