ISSN 10227954, Russian Journal of Genetics, 2010, Vol. 46, No. 9, pp. 1062–1066. © Pleiades Publishing, Inc., 2010.

Original Russian Text © B.F. Chadov, N.B. Fedorova, E.V. Chadova, E.A. Khotskina, M.P. Moshkin, D.V. Petrovski, 2010, published in Genetika, 2010, Vol. 46, No. 9, pp. 1196–1201.

Genetic Mutation Affects the Energy Status of Drosophila

B. F. Chadova, N. B. Fedorovaa, E. V. Chadovaa, E. A. Khotskinaa,
M. P. Moshkina,b, and D. V. Petrovskib
a
Research Institute of Cytology and Genetics, Russian Academy of Sciences, Novosibirsk, 630090Russia
email: chadov@bionet.nsc.ru
b
Research Institute of Systematics and Animal Ecology, Russian Academy of Sciences, Novosibirsk, 630005 Russia
Received January 28, 2010

Abstract—Conditional dominant lethals (CDL) represent a special class of genetic mutations observed in
Drosophila. Mutation manifests as a dominant lethal in one genotype, but lethality is not expressed in another
genotype. CDL mutants exhibit a set of traits discriminating them from classic mutations. We observed
unusually high mobility of flies and high sexual activity of males carrying these mutations. We used special
tests for evaluation of energy metabolism of CDL mutants. Indirect calorimetry (CO2 excretion measure
ment) has been used for estimation of energy exchange in four mutant and two control fly lines. A special
device has been used for evaluation of locomotor activity of these fly lines. Energy exchange and locomotor
activity in CDL mutants were significantly higher than in control lines. We conclude that some genetic muta
tions are capable of increasing energy dissipation in their carriers.
DOI: 10.1134/S1022795410090127

INTRODUCTION protocols permitted to produce large numbers of

The genetic material is organized in chromosomes.
Chromosomes’ functions are conservation, transmis
sion, and manifestation of the genetic information.
The definition of the chromosome function is
acknowledged but incomplete. A special process of
energy circulation underlying the basis of life is hidden
by manifestation of genetic information. “Energy cap
ture and retention in the infinite sequence of cyclic
and quasicyclic chemical reactions” were designated
as the essence of life [1]. Energy aspect in genetic sys
tem function is revealed in examination of a special
mutation class, conditional dominant lethals.
CONDITIONAL DOMINANT LETHALS:
RECOGNITION AND UNUSUAL PROPERTIES
The existence of a special mutation class (condi
tional dominant lethals, CDL) was suggested in 2000,
when the first CDL in the X chromosome were identi
fied in Drosophila melanogaster [2]. It was thought that
selection of this class of mutations would enable to
reveal genes responsible for traits of intraspecies simi
larity [2]. Mutations were induced by γirradiation. A
new approach to mutant selection has been employed:
the mutation should be manifested differently in the
individuals of the same species, it should be lethal in
the carriers of one genotype and nonlethal in the car
riers of another genotype [2]. Drosophila was used in
the development of several protocols for mutation
generation in X chromosomes and the chromosomes
of the second and the third pairs [3, 4]. In contrast to
accidental CDL findings [5], the involvement of new
CDLs including those whose manifestation were not
associated with sex [3]. Gradually, the general view of
these mutations was developed and CDL were as
attributed to a special mutation class [6].
Originally, CDL were distinguished by two types of
manifestation. These were both recessive and domi
nant (in case of some genotypes) mutations. CDL
could lose dominant lethal manifestation in case of
chromosomal rearrangements [7]. Mutation manifes
tation was accompanied by a parental effect [3, 7]. The
mutant offspring often showed nonsymmetrical distur
bances in development (morphoses) [3, 8] (Fig. 1).
Depending on the line and type of cross, the propor
tion of the offspring with morphoses varied from sev
eral percent to tens of percents [9]. The capacity of the
mutants to form morphoses and conditional manifes
tation of mutations suggested that the genes revealed
are regulatory and control ontogeny [4, 8]. In addition
the studies of CDL cultures have shown that CDL
produced genomic instability [9, 10].
MUTATION LOCALIZATION
In the three out of four proposed protocols for
CDL identification, the mutation could be exactly
located on the chromosome already in the course of its
selection. Later the mutation is maintained as a reces
sive lethal in the heterozygote with the corresponding
inverted chromosome. The fourth protocol involves
selection of the CDLcarrying proband by the pres
ence of a morphose. After proband formation the
mutation is located in one of the chromosome pairs

1062
 GENETIC MUTATION AFFECTS THE ENERGY STATUS
using the lines In(l)Muller5/+, In(2LR)Cy/+, and
In(3LR)D/+.
Mutation localization at the exact region of a poly
tene chromosome is problematic as it is conditionally
lethal. A lack of lethality manifestation (is the event
taken into accounted during localization) could result
either from the absence of the lethal in the region or
from genotype substitution in the examined descen
dant. The localization is possible if the lethal mutation
has in addition to lethal effect, a visible mutant pheno
type. For example, mapped to region 89 on chromo
some 3 the dimorphic “short legged” mutation, which
exhibited a visible mutant manifestation several gener
ations after its appearance.
Localization of four mutations with visible mani
festation to autosome 2 is currently in progress. Dele
tion mapping of one of the mutations ( “Small barrel”
phenotype) produced an unexpected result. In a series
of crosse with 105 deletions on chromosome 2, we
found three regions where the mutation was lethal.
One region is located on the left arm of autosome 2
while the other two are sited on the right arm of the
same chromosome. The length of the left arm interact
ing region was from 35B46 to 35B10C1. At the right
arm (54–55) seven deletions interact with the muta
tion inducing death of the descendents. These dele
tions form two distinct interacting loci, 54B1017 and
55A155B57. This demonstrates an additional prop
erty of CDL: being recessive in the heterozygote CDL
are capable of cisinteracting (lethal effect) with other
recessives in the same heterozygote (deletions).
ENERGY CHANGE
Extremely high mutant activity has been noted as
an unusual property of CDL. It was expressed as a high
speed of fly movement in the vial and high male mat
ing activity [2, 11]. It appeared that CDL changes the
energy of fly.
Our aim was studying changes in energy metabo
lism and locomotor activity of Drosophila in response
to CDL formation. The tested lines (7, 46, 101, and
103) were produced by γ irradiation of laboratory wild
lines Berlin wild (line 61) and CantonS (line 62). The
latter served as control. Males from the mutant and
control lines possessed similar phenotype and
appeared normal. Both control and mutant Drosophila
lines were maintained on standard medium at 24°С.
The same temperature was used during measurements
of movement activity and energy metabolism.
Locomotor activity. Locomotor activity of the adult
Drosophila was measured using Drosophila movement
activity device (Drosophila Monitor Activity, Model
DAM 2, TriKinetics, United States), which permits to
register simultaneously the activity of 32 individuals.
Each fly was placed into a glass tube 65 mm long and
4 mm in diameter with nutrient medium at one end.
The other end of the tube was sealed with cotton stop
per, which did not prevent air exchange. Tubes with
RUSSIAN JOURNAL OF GENETICS Vol. 46 No. 9
1063
flies were placed into the cells of the monitor so that an
infra red ray generated by the device passed the tube in
the center. The time the fly crossed the ray was auto
matically registered as an elementary activity act. The
data on the activity of each the examined fly was sum
marized by the software installed in the device during
the designated time period. In our experiment, the
time interval was 1 min.
We assessed the activity of 16 males of line 61, 12 of
line 62, 30 of line 7, 17 of line 46, 25 of line 101, and
29 of line 103. All the males were 3 days old. The activ
ity was registered during 10 days. For statistical analy
sis the data obtained after threeday adaptation of
males in the tubes were used.
The activity data averaged for each line were pre
sented as hour plot obtained after processing the pri
mary measurements using the method of sliding mean
with a step length of 60 (Fig. 2). The flies of the control
and the mutant lines have shown typical day activity
rhythms for Drosophila with activity maximum at day
hours. The peak activity of mutant lines (Fig. 2) signif
icantly exceeded that in control lines (F5,123 = 6.9986,
р < 0.001). The average day activity in mutant line was
also higher compared to controls (Fig. 3, left panel).
Energy turnover. The method of indirect calorime
try has been employed in the study, which is based on
detection of СО2 release intensity during respiration.
For this purpose the Drosophila males (10 individuals
from each line) were placed into a medical syringe
with a ground–in piston with a stopper, where they
were maintained for 1 h. The syringes were prelimi
nary tested for the capacity to keep the carbon dioxide
and later only the syringe models were used with СО2
loss lower than the measurement error. The volume of
the closed space was 6 ml. After 1 h 5 ml of the air mix
ture was sent the to an infrared gas analyzer PGA12
(KOSTIP, Russia), which measured СО2 concentra
tion with precision up to 0.01%. After that the males
were etherized (aether pronarcosi stabilisatum
P74/231/1) and weighted with precision of 1 mg. The
initial level of СО2 in the syringe was measured prior
the fly exposure. The amount of the released СО2
(VCO2), ml/g h was calculated as the difference in СО2
concentration before and after the experiment.
The experiment was conducted using the lines
developed under the same conditions. The total num
bers of measurements were 27 in line 61, 21 in line 62,
28 in line 7, 26 in line 46, 23 in line 101, and 29 in line
103. We used oneway analysis of variance and multi
ple comparisons of means based on LSDtest.
The lowest СО2 release was observed in flies of con
trol line 61 and the maximum one, in mutant lines 46
and 101 (Fig. 3, right panel). CO2 release in four
mutant lines significantly exceeded that of control line
61 while the release in three mutant lines also
exceeded that in both control lines 61 and 62. Thus,
mutant males overperformed control males in loco
motor activity and energy turnover. Our initial obser
2010
1064 CHADOV et al.

(a) (b)

(c) (d)

(e) (f)

(g) (h)

RUSSIAN JOURNAL OF GENETICS Vol. 46 No. 9 2010

 GENETIC MUTATION AFFECTS THE ENERGY STATUS 1065

Fig. 1. Morphoses in lines carrying dominant lethals. (a,b) two variants of a smallersize head replacing an eye; (c) two heads on
one neck; (d) doubled exterior male genitals; (e) abdomen rotation at 180°; (f) eye bifurcation; (g) tergite fragment on the abdo
men; (h) the lack of two tergites on the right.

100

80

60
Activity, acts/h

40

20

0
11 17 23 5 11 17 23 5 11 17 23 5
Time day, hours

Fig. 2. Imago locomotor activity in six lines of Drosophila during three days. Mutant lines: 7 (solid diamond), 46 (solid square),
101 (solid circle), and 103 (solid triangle); control lines: 61 (open circle) and 62 (open triangle). Axe Y, the number of fly crossings
of the tube center.

50 A 7
A A
A
A
CO2 excretion, ml/g h

40 B 6
B, C B
Activity, acts/h

30 B, C 5 C
C
20 4 D

10 3

0 2
61 62 101 103 7 46 61 62 7 103 46 101
Lines

Fig. 3. Day average locomotor activity (left panel) and CO2 excretion (right panel) in control (61, 62) and mutant (7, 46, 101, and
103) fly lines. The letters over bars indicate significantly different average values of activity (F5, 123 = 7. 34, p < 0.001) and CO2
release (F5, 148 = 31.89, р < 0.001). Multiple averages comparison were done using LSDtest.

vation on unusually high activity of mutants was con the most important property. Indeed, the genome is an
firmed. instrument responsible for energy dissipation from the
external source in the systems operating with cyclic
The obtained results indicate an increase in energy and quasicyclic chemical reactions [1].
turnover in response to the appearance of definite class
of mutation. These results suggest that in a large pool
of genetic mutations, mutations that increase energy ACKNOWLEDGMENTS
dissipation could exist. These mutations might permit
other mutations to work in the opposite direction, to We thank Prof. John T. Berns from Bethany Col
make the individual more evolutionally complex by lege, United States for the data on chronobiology and
increasing its negenthropy [12]. The role of genetic for assistance in organizing experiments on movement
mutations could be more important than changes in activity of flies.
the mutant phenotype, which geneticists use for muta The study was supported by the Russian Founda
tion recognition and considered them their major and tion for Basic Research (project no. 080400094).

RUSSIAN JOURNAL OF GENETICS Vol. 46 No. 9 2010

1066 CHADOV et al.
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