A M . ZOOLOCIST, 7:451-456 (1967).
Distribution of the Two Kinds of Myofilaments in Insect Muscles
JACQUES AUBER
Laboratoire de Cytologie, Faculte des Sciences, Paris, et Laboratoire de
Microscopie Electronique Appliquee a la Biologie, C.N.R.S., Paris 5, France
SYNOPSIS. Different insect muscles have been studied with the electron microscope
and the distribution of the two kinds of myofilaments compared. In muscles other
than those of flight, each thick filament is surrounded by 9-12 thin filaments, whereas,
in the flight muscles, the contraction frequency of which is much higher, there are
only 6 thin filaments surrounding each thick one; nevertheless, in the flight muscles
of some butterflies, the wing stroke frequency of which is particularly low, there are
7-9 thin filaments. It seems then that there may be a relation between the ratio of the
two kinds of myofilaments and the frequency of muscular contraction.
In the muscles which have more than 6 thin filaments surrounding each thick
one, the structure of the 7. line appears to be different from that which was
described in dipteran flight muscles. A peculiar aspect of the M line is observed
in lepidopteran flight muscles.
In insects, the arrangement of myofilaments was first described in the flight muscles of the blow-fly, Calliphora erythrocephala Meig (Huxley and Hanson, 1957) .
At the level of the A band of these muscles, each thin filament lies mid-way between two thick filaments, and as these
thick filaments lie in hexagonal array, each
of them is surrounded by 6 thin filaments.
This arrangement (Fig. 1), found again
in the flight muscles of many insects and
in some muscles of copepods (Bouligand,
1962; Fahrenbach, 1963), is nevertheless
not common for all arthropodan muscles.
Research on scorpion muscles (AuberThomay, 1963), crustacean muscles (Bouligand, 1964; Swan, 1963) and insect muscles other than those of flight (Toselli,
1965; Hagopian, 1966; Smith, 1966; Smith,
Gupta, and Smith, 1966; Auber, 1966), has
revealed that the hexagonal array remains
constant for the thick filaments, but the
number of thin filaments surrounding each
of them may vary from 9 to 12.
Observation of many Calliphora muscles,
in adults and larvae, shows that, except
in the flight muscles and in the haltere
[i.e., the mainflight muscles (indirect flying
muscles) but not the wing adjustor muscles]
muscles, there are always more than 6 thin
filaments surrounding each thick one; this
number is variable according to the muscle
under consideration; for example, it is
from 10 to 12 in the abdominal segmental
muscle and from 9 to 11 in the tergotrochanteral muscle (Figs. 2 and 3). In all
the muscles studied, the same ratio of thick
and thin filaments was found at every level
of the A band, except in the H band
where there were thick filaments only; the
greater number of thin filaments may,
therefore, not result from any possible
phenomena of supercontraction with
double overlap of the two sets of thin filaments of each sarcomere.
In insects, the distribution of myofilaments described in the flight muscles seems,
therefore, to be peculiar to this kind of
muscle. The flight muscles happen to have
a faster work rhythm than that of all the
other muscles, and in these other muscles,
the ratio of thin filaments is always higher.
In the flight muscles of some moths (Phytometra, Agrotis, Minucia, Abraxas), as in
those of Diptera, each thick filament is
surrounded by 6 thin filaments. But, when
the frequency of muscular contraction is
low enough, as in some butterflies (Pieris,
Vanessa) which have a wing-beat of not
more than 10/sec (Sotavalta, 1947), that is
to say 5 to 6 times less than the moths,
each thick filament is no longer surrounded
by 6, but by 7-9 thin filaments (Figs. 4 and
5) (Auber, 1967).
It should be noted that in the flight
muscles of all these Lepidoptera, the M
(451)
452
JACQUES AUBER
Explanation of Figures
Electron micrographs of insect muscle (cross
sections taken through the A band). Glutaraldehyde
fixation with osmium tetroxide postfixation. Sections stained by uranyl acetate followed by lead
citrate.
1'late )
HC. 1. Cross section of a fibril in a flight muscle
of Diptera (Bombylius). Each thick filament is surrounded by 6 thin filaments. X 65,000.
DISTRIBUTION O F M Y O F I L A M E N T S IN INSECTS
Plate II
FIG. 2. Cross section through the tergo-trochanteral
muscle of a fly (Calliphora). Each thick filament is
surrounded by 9 to 11 thin filaments. Note the
453
edge of the H band on the left part of the micrograph, which excludes the hypothesis of a supercontraction phenomena. X 95,000.
FIG. 3. Higher magnification. X 135,000.
454
JACQUES AUBER
Plate III
FIG. 4. Flight muscle of a butterfly (Vanessa).
Slightly oblique cross section of a myofibril showing
the edge of the A band, and below, the beginning
ot the I band. Each thick filament is surrounded
by 7 to 10 thin filaments. X 85,000.
FIG. 5. Higher magnification. X 150,000.
DISTRIBUTION OF MYOFILAMENTS IN INSECTS
455
With regard to the arrangement of myofilaments, it is possible to observe in the
flight muscles of the blow-fly, during the
first stages of myofibrillogenesis, isolated
thick filaments surrounded by 6 thin filaments. This suggests, as in the hypothesis
previously put forward by Swan (1963)
concerning crayfish muscles which have a
high ratio of thin filaments, that each
thick filament may interact with its own
set of 6 thin filaments. As a result of this,
in a myofibril, each thick filament would
be surrounded by 12 thin ones. When each
thick filament is surrounded by 7-11 thin
filaments, some of these would be shared
between two thick filaments next to each
other. In the flight muscles, where each
thick filament is only surrounded by 6
thin ones, each of these filaments is shared
between two thick ones. The number of
cross-bridges issuing from each thick filament seems to be constant whatever may
be the number of thin filaments and, when
there are more than 6 thin filaments surrounding each thick one, the bridges seem
to link at random. It is in the muscles
which vary most from the hexagonal patAn examination of the frequency of con- tern, with 6 thin filaments, that the contraction of flight muscle and of the num- traction-rhythm would seem to be the
ber of thin filaments in various insects, lowest.
shows that in the Calliphora with a rate
of wing-beat of 200 per second, as in the
REFERENCES
Phytometra, with a rate of wing-beat of
50/sec, there are 6 thin filaments sur- Auber, J. 1966. Distribution des deux types de
rounding each thick one. The arrangement
myofilaments dans divers muscles de Dipteres. J.
of myofilaments seems, therefore, to be
Microscopie 5:28a.
independent of the manner of working of Auber, J. 1967. Particularites ultrastructurales des
myofibrilles des muscles du vol des Lepidopteres.
the flight muscles, "asynchronous" (see
Comp. Rend. Acad. Sci., Paris 264:621-624.
Pringle, 1957) in the case of Diptera, or Auber,
J., and R. Couteaux. 1963. infrastructure
"synchronous" in the case of Lepidoptera.
de la strie Z dans des muscles de Dipteres. J.
However, in Aesclma mixta (Odonata),
Microscopie 2:309-324.
whose wing-beats average 30/sec, there are Auber-Thomay, M. 1963. Remarques sur l'ultrastructure des myofibrilles chez des scorpions. J.
6 to 8 thin filaments; in butterflies with a
Microscopie 2:233-236.
rate of wing-beat of only 10/sec, this num- Bouligand,
Y. 1962. Les ultrastructures du muscle
ber rises to 9 and for muscles other than
stri<5 et de ses attaches au squelette chez les
Cyclops (Crustaces Copepodes). J. Microscopie
the flight muscles, the rhythm of which
1:377-394.
is even slower, it may reach 12.
line presents a particular aspect: at this
level, the thick filaments become flattened
and appear generally to be composed of
two subunits placed side by side. A similar
structure of the M line was also observed
in the flight muscles of an hemipteroid
insect (Reedy, 1966). In addition, in the
flight muscles of moths, the sarcoplasmic
reticulum penetrates into the myofibrils
themselves (Auber, 1967). With regard to
the Z line, its structure appears to be related to the number of thin filaments:
in the flight muscles of moths, as in those
of Diptera (Auber and Couteaux, 1963),
the thin filaments are grouped in threes
and participate in tubular formations,
which -give the Z line the aspect of a perforated plate. On the other hand, in the
flight muscles of butterflies, as in other
muscles with more than 6 thin filaments
around each thick one, the Z line exhibits
only, in an electron dense substance, filaments of about 50 A in diameter, distributed without apparent order, which seem
to be prolongations of the actin-containing filaments.
It seems then, that there may be a relation between the ratio of the two kinds
of myofilaments and the frequency of muscular contraction when this frequency falls
below a certain level.
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Fahrenbach, W. H. 1963. The sarcoplasmic reticulum of striated muscle of a cyclopoid copepod. J.
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JACQUES AUBER
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muscle fibers in an insect, Periplaneta americana
L. J. Cell Biol. 29:449-459.
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