A prominent sex-specific abdominal muscle in male Drosophila is the Muscle of Lawrence (MOL), which is induced by male-specific innervation. We have examined MOL development in wild-type males, in males fed hydroxyurea to ablate the muscle precursors and in fruitless mutants, in which the MOL muscle develops aberrantly. One striking feature of MOLs in wild-type males was the presence of additional muscle nuclei compared with neighboring muscles or MOL-homologues in females. We tested whether muscle length and the sex-specific expression of a reporter gene depended critically on the number of nuclei present within a MOL fiber. MOL fibers developing from a reduced myoblast pool in hydroxyurea-affected hemisegments were recognizable by their attachment points and still contained more nuclei than did neighboring medial fibers, suggesting that these MOL fibers were able to actively recruit myoblasts nearly as well as wild-type MOLs. However, many of the hydroxyurea-affected MOL fibers were incapable of the normal male-specific expression of a muscle-specific reporter gene. We suggest that early events in MOL development, such as finding the correct muscle attachment points, are relatively insensitive to the number of MOL nuclei compared with later events, such as the sex-specific expression of a reporter gene. In fruitless mutant males, MOL-position fibers are smaller and had substantially fewer nuclei compared to wild-type MOLs. Since the number and distribution of muscle precursors was the same in fruitless mutant and wild-type animals, we propose that one fru+ function is to direct the male-specific recruitment of myoblasts into MOL-myotubes. However, fruitless+ must have more than one role in MOL fiber development, since simple reduction in the number of muscle nuclei, as demonstrated by the hydroxyurea ablations, is insufficient to account for all of the MOL muscle phenotypes in fruitless mutant males.

Reference

Bainbridge
P. S.
,
Bownes
M.
(
1981
)
Staging the metamorphosis of Drosophila melanogaster.
J. Embryol. exp. Morph
66
,
57
80
Baker
B. S.
(
1989
)
Sex in flies: the splice of life.
Nature
340
,
521
524
Bate
M.
(
1990
)
The embryonic development of larval muscles in Drosophila.
Development
110
,
791
804
Bate
M.
,
Rushton
E.
,
Currie
D. A.
(
1991
)
Cells with persistent twist expression are the embryonic precursors of adult muscles in Drosophila.
Development
113
,
79
89
Broadie
K. S.
,
Bate
M.
(
1991
)
The development of adult muscles in Drosophila: ablation of identified muscle precursor cells.
Development
113
,
103
118
Burtis
K. C.
(
1993
)
The regulation of sex determination and sexually dimorphic differentiation in Drosophila.
Curr. Opin. Cell. Biol
5
,
1006
1014
Castrillon
D. H.
,
Gönczy
P.
,
Alexander
S.
,
Rawson.
R.
,
Eberhart
C. G.
,
Viswanathan
S.
,
DiNardo
S.
,
Wasserman
S. A.
(
1993
)
Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: Characterization of male-sterile mutants generated by single P element mutagenesis.
Genetics
135
,
489
505
Courchesne-Smith
C. L.
,
Tobin
S. L.
(
1989
)
Tissue-specific expression of the 79B actin gene during Drosophila development.
Dev. Biol
133
,
313
321
Currie
D. A.
,
Bate
M.
(
1991
)
The development of adult abdominalmuscles in Drosophila: myoblasts express twist and are associated with nerves.
Development
113
,
91
102
Currie
D. A.
,
Bate
M.
(
1995
)
Innervation is essential for the development and differentiation of a sex specific adult muscle in Drosophila melanogaster.
Development
121
,
2549
2557
Furst
A.
,
Mahowald
A.
(
1985
)
Cell division cycle of cultured neural precursor cells from Drosophila.
Dev. Biol
112
,
467
476
Gailey
D. A.
,
Hall
J. C.
(
1989
)
Behavior and cytogenetics of fruitless in Drosophila melanogaster: Different courtship defects caused by separate, closely linked lesions.
Genetics
121
,
773
785
Gailey
D. A.
,
Taylor
B. J.
,
Hall
J. C.
(
1991
)
Elements of the fruitless locus regulate development of the muscle of Lawrence, a male-specific structure in the abdomen of Drosophilamelanogaster adults.
Development
113
,
879
890
Giebultowicz
J. M.
,
Truman
J. W.
(
1984
)
Sexual differentiation in the terminal ganglion of the moth Manduca sexta: Role of sex-specific neuronal death.
J. Comp. Neurol
226
,
87
95
Gill
K. S.
(
1963
)
A mutation causing abnormal courtship and mating behavior in males of Drosophila melanogaster. (Abstract).
Am Zool
3
,
507
–.
Hall
J. C.
(
1978
)
Courtship among males due to a male-sterile mutation in Drosophila melanogaster.
Behavior Genet
8
,
125
141
Hall
J. C.
(
1994
)
The mating of a fly.
Science
264
,
1702
1714
Lawrence
P. A.
,
Johnston
P.
(
1984
)
The genetic specification of pattern in a Drosophila muscle.
Cell
36
,
775
782
Lawrence
P. A.
,
Johnston
P.
(
1986
)
The muscle pattern of a segment of Drosophila may be determined by neurons and not by contributing myoblasts.
Cell
45
,
505
513
McKeown
M.
,
Madigan
S. J.
(
1992
)
Sex determination and differentiation in invertebrates: Drosophila and Caenorhabditis elegans.
Curr. Opin. Cell. Biol
4
,
948
954
Metcalf
W. K.
(
1985
)
Sensory neuron growth cones comigrate with posterior lateral line primordial cells in Zebrafish.
J. Comp. Neurol
238
,
218
224
Taylor
B. J.
(
1992
)
Differentiation of a male-specific muscle in Drosophila melanogaster does not require the sex-determining genes doublesex and intersex.
Genetics
132
,
179
191
Taylor
B. J.
,
Villella
A.
,
Ryner
L. C.
,
Baker
B. S.
,
Hall
J. C.
(
1994
)
Behavioral and neurobiological implications of sex-determining factors in Drosophila.
Dev. Genet
15
,
275
296
Taylor
H. M.
,
Truman
J. W.
(
1974
)
Metamorphosis of the abdominal ganglion of the tobacco hornworm, Manduca sexta: Changes in populations of identified motor neurons.
J. Comp. Physiol
90
,
367
386
Thorn
R. S.
,
Truman
J. W.
(
1989
)
Sex-specific neuronal respecification during the metamorphosis of the genital segments of the tobacco hornworm moth Manduca sexta.
J. Comp. Neurol
284
,
489
503
Truman
J. W.
,
Booker
R.
(
1986
)
Adult-specific neurons in the nervous system of the moth, Manduca sexta: selective chemical ablation using hydroxyurea.
J. Neurobiol
17
,
613
625
Wheeler
D. A.
,
Kulkarni
S. J.
,
Gailey
D. A.
,
Hall
J. C.
(
1989
)
Spectral analysis of courtship songs in behavioral mutants of Drosophila melanogaster.
Behavior Genet
19
,
503
528
This content is only available via PDF.