DOSAGE OF THE MATERNAL, EFFECT GENE ASSOCIATED

WITH THE TUMOROUS-HEAD ABNORMALITY IN

DROSOPHILA MELANOGASTER

R. M. SIERVOGEL*
Department of Zoology, Arizona State University, Tempe, Arizona 85281
Manuscript received June 19, 1972

ABSTRACT

The penetrance of tuh-3 observed in the progeny of triploids with two doses
of tuh-I was not statistically different from that occurring in the progeny of
their diploid sisters with two doses. A higher penetrance was observed in
the progeny of triploids with three doses of tuh-l than in the progeny of their
diploid sisters with two doses. These observations suggest that the maternal
effect responsible for increasing the penetrance of tuh-3, the gene causing the
tumorous-head abnormality, is caused by a specific gene product of tuh-I, the
maternal-effect allele. In addition there is probably a maternal-effect threshold,
lying between amounts produced by one and two doses of tuh-I, below which
no increased penetrance of tuh-3 is observed.

HE genetic mechanism responsible for the tumorous-head abnormality was

Tworked out by GARDNER and WOOLF (1949). A semi-dominant gene (tuh-3)
is necessary for the expression of the trait. This gene has been localized to posi-
tion 58 in the right arm of the third chromosome (GARDNER 1959). The pene-
trance (frequency of flies with the trait) of this gene is about one to five percent
(WOOLF and LOTT 1965). The penetrance is increased by a sex-linked recessive
gene (tuh-I) which produces a maternal effect (GARDNER and WOOLF 1949).
The tuh-I gene is located at position 64.5 (GARDNER 1959). Penetrance is also
increased by high temperature during an early developmental period (GARDNER
and WOOLF 1950) and by a system of polygenic modifiers (GARDNER, SCOTTand
DEARDEN 1952; WOOLF, KNOWLESand JARVIS1964; WOOLF 1966). The present
study was undertaken to determine if the maternal effect gene, tuh-I, shows a
dosage effect.
MATERULS A N D METHODS

Dosage effects of tuh-1 were studied by using triploid females. These females were synthesized
using c3G, the recessive gene which causes nondisjunction in females. The females used possessed
an attached-X chromosome, C(I)RM, bearing the mutant genes broad (br), echinus (a), and
the maternal effect gene, tuh-l (WOOLF 1966). Triploid females were then backcrossed to males
from the tumorous-head strain for over five generations to insure that the triploids were, for the
most part, homozygous for tuh-3 and possessed many of the tumorous-head polygenic modifiers.
Two types of triploid females were synthesized, differing only by the free-X chromosome they

Present address: Department of Biostatistics, School of Public Health, University of North Carolina, Chapel Hill,
North Carolina 27514.

Genetics 72: 377-380 October 1972.

378 R. M. SIERVOGEL

TABLE 1
Frequency of tumorous-headabnormality among progeny of triploids ( C ( 1)RM, br ec tuh-I/Basc,
tuh-I +) with two doses of tuh-I and the progeny of their diploid sisters ( C ( 1 ) RM,
br ec tuh-ID)with two doses of tuh-I when these females m r e mated to
Basc, tuh-1+/Y males

Tumorous-head
Abnormal i ty Total

420
(57.1%) 736

I(2N) tuh-l.tuh-l/Y
I 1280
(58.5%)
2188

x21 = .466 .5 > P > . 3

possessed. One type had a free X with tuh-I (v B tuh-I) and the other type possessed the isoallele
of tuh-I, tuh-I+ (Bmc*,tuh-I+).In both cases C ( I ) R M , br ec tuh-I/Y female sibs of the triploids
were used as controls. All test matings consisted of a single female placed in a vial with five
males. The large number of males was necessary because of the high frequency of sterility
among tumorous-head males (WOOLF and CHURCH1963). A constant temperature of 25 k .5"C
was used. A fly was considered to possess the tumorous-head trait when any abnormality existed
on its head.

RESULTS

In Table 1, it is shown that 57.1% of the progeny of the C ( l ) R M , br ec tuh-I/

Basc, tuh-l+ triploids had the tumorous-head abnormality. This value is not
significantly different from the frequency of the tumorous-head abnormality
occurring in the progeny of their C(I)RM, br ec tuh-I/Y diploid sisters.
As shown in Table 2, a highly significant difference exists between the fre-
quency of the tumorous-head abnormality in the progeny of C ( I ) R M , br ec
tuh-I/v B tuh-1 triploids (76.0%) and that of their C ( I ) R M , br ec tuh-I/Y
diploid sisters (63.0%).
From the results of this study, two important factors can be perceived that give
some indication of the mode of action of the tumorous-head maternal effect. The
first is that the tuh-I maternal effect allele causes the increased penetrance of
tuh-3 by producing some product. The second is that there is a threshold mecha-
nism operating in the tumorous-head system.

DISCUSSION

The progeny of diploid females with tuh-3 homozygous, polygenic modifiers

present and with zero or one dose of tuh-1 show less than 5 % penetrance of tuh-3
(WOOLF and LOTT1965). A similar observation has been made for the pene-
trance of tuh-3 in the progeny of triploids with zero or one dose of tuh-I (SIER-
VOGEL, unpublished). As shown in Table 1, tuh-1 need not be homozygous in
mothers for the increased penetrance of tuh-3 to occur among their progeny.
* Basc = Muller-5 = In(l)sc4*LscsR+S, scB's@w'B.
 TUMOROUS-HEAD MATERNAL EFFECT 3 79
TABLE 2
Frequency of tumorous-head abnormality among progeny of triploids (C(I)RM, br ec tuh-l/v B
tuh-1) with three doses of tuh-1 and the progeny of their diploid sisters ( C (1 ) RM,
br ec tuh-1/Y) with tw doses of tuh-1when mated to v B tuh-l/Y males

Tumorous-head
Abnormality Total

I(3N) tuh-1. tuh-l/tuh-1

I 5 80
(76.0%) 763 I
(2N) tuh-l*tuh-l/Y 1570 249 1
(63.0%)
x; = 44.0 P < .01

Thus, the implication is that it is the presence of the tuh-I gene product and not
the absence of the tuh-I+ gene product that results in the maternal effect.
These observations also provide evidence for a threshold mechanism. One dose
of tuh-I does not produce enough of its gene product to reach this threshold,
whereas two doses produce enough to pass the threshold and cause an increased
penetrance of tuh-3. Two doses produce the same effect whether in a diploid or a
triploid (Table 1). Three doses of tuh-I appear to produce an even greater effect
(Table 2).
One model that is compatible with these observations follows: As the result of
the gene action of tuh-I, a maternal-effect substance is produced and deposited in
the egg. I n the presence of tuh-3, the effect of tuh-1 is independent of tuh-Z+,
since no dominance interactions seem to be present. There is a threshold which
involves the amount of the maternal-effect substance present. Most modifiers
seem to regulate the expression of the trait by regulating the maternal-effect
substance, possibly by influencing the amount produced, the amount deposited
in the egg, or its physiological activity. Much later in development the gene
product of tuh-3 in some way interacts with the maternal-effect substance or
products of it. The interaction of these substances affects certain imaginal discs
in such a way as to make them develop improperly (homestically) resulting in
the tumorous-head phenotype.
An additional maternal effect was discovered by WOOLF(1966) that when
present with tuh-3 and polygenic modifiers causes abnormal development of the
male genital disc. This maternal effect is the result of the isoallele of tuh-I,
tuh-I+. It is postulated that the mechanism of its action may be similar to that
just described for tuh-I.
I am grateful to Professor CHARLFSM. WOOLF,whose ideas provided the basis for this
research, for his suggestions throughout t h e course of this study and for carefully reading the
manuscript and offering valuable comments.

LITERATURE CITED
GARDNER,
E. J., 1959 Genetic mechanism of maternal effect for tumorous-head in Drosophila
mlanogaster. Genetics 44: 471-481.
380 R. M. SIERVOGEL

GARDNER,E. J., G. H. SCOTTand D. M. DEARDEN, 1952 Modifiers of tumorous-head genes in

natural populations and laboratory stocks of Drosophila melanogaster. Genetics 37: 573-585.
GARDNER,E. J. and C. M.WOOLF, 194.9 Maternal effect involved in the inheritance of abnormal
growths in the head region of Drmophila mehogaster. Genetics a:573-585. -,
1950 The influence of high and low temperatures on the expression of tumorous-head in
Drosophila melanogaster. Genetics 35: 44-55.
C. M.,1966 Maternal effect influencing male genital disc development in Drosophila
WOOLF,
melanogaster. Genetics 53: 295-302.
WOOLF,C. M. and K. CHURCH,1963 Studies on the advantage of heterokaryotypes in tumorous-
head strain of Drosophila melanogaster. Evolution 17: 486-492.
WOOLP,C. M., B. G. KNOW- and M. A. JARVIS, 1964 Genetic analysis of fitness traits in
tumorous-head strains of Drosophila melanogaster. Genetics 50 :597-610.
WOOLF,C. M. and M. Lon, 1965 Relationship between penetrance and karyotype in the
tumorous-head strain of Drosophila melanogaster. Am. Naturalist 99: 511-513.