J. Embryo!, exp. Morph. Vol. 53, pp. 291-303, 1979
Printed in Great Britain © Company of Biologists Limited 1979
291
Replacement of posterior by anterior
structures in the Drosophila wing caused by the
mutation apterous-blot
By J. ROBERT S. WHITTLE 1
From the School of Biological Sciences, The University of Sussex
SUMMARY
The recessive mutation apterous-blot in Drosophila melanogaster causes replacement of
posterior wing structures by anterior ones, with variable penetrance and expressivity. Extreme
transformations resemble mirror-image duplicate anterior wings as in the mutant engrailed.
Anterior structures in the posterior wing only appear on the dorsal surface. Duplications
solely of posterior structures are also seen.
Clonal analysis shows that extra cell proliferation occurs in the posterior area but is
complete by 108 h after egg deposition. Lineage analysis is consistent with a clonal perpetuation of the transformation. Genetic mosaics to test the cell-autonomy of apterous-blot
show that it is not autonomously expressed in clones.
The results of lineage analysis, the phenotypes of combinations of apterous-blot with other
apterous alleles including a deletion for the locus and with various other homoeotic mutations,
are together used to distinguish three alternative modes of action of this mutation. It is
concluded that apterous-blot is unlikely to be a selector gene mutation but instead may cause
the transformation by an event like transdetermination following a local failure in cell
function in the wing disc.
INTRODUCTION
Analysis of genetic mosaics in Drosophila melanogaster reveals that determination events, in the form of cell lineage restrictions, occur during disc
development, separating groups of cells (polyclones) with different assigned
fates (Garcia-Bellido, Ripoll & Morata, 1973; Crick & Lawrence, 1975). One
early restriction divides cells of the wing disc into two compartments, anterior
and posterior (Garcia-Bellido et al., 1976). Garcia-Bellido (1975) has suggested
that the distinctions between different polyclones are maintained throughout
disc growth by the activity of particular genes (selector genes). Wings of the
mutant engrailed show mirror-image symmetry about the anterior-posterior
compartment border. This mutant has been ascribed a role in the maintenance
of the difference between the posterior and anterior compartments in the wing
and certain other discs (Lawrence & Morata, 1976) based upon its pattern of
clonal growth, its cell autonomy in genetic mosaics with wild-type tissue, and
1
Author's address: School of Biological Sciences, The University of Sussex, Falmer,
Brighton BNl 9QG, Sussex, U.K.
292
J. ROBERT S. WHITTLE
its behaviour in combination with homoeotic mutations of the bithorax complex
locus (Garcia-Bellido & Santamaria, 1972). This paper describes the analysis of
another mutation, apterous-blot, which leads to the formation of wings
phenotypically similar to those of engrailed. The conclusion is drawn that although
apterous-blot causes transformation of posterior cells to anterior cells in the wing,
yet it does so in a way unlike that expected from a failure in a selector gene.
MATERIALS AND METHODS
Flies were grown on normal yeast-agar-maize meal medium at 25 °C. The
recessive mutation apterous-blot (apm) was obtained from the stocks SM5/BI
stwi8 ap™ tuf sp and from stw apwt tuf. The linked mutations Bristle, straw,
tufted and cinnabar were used for recombination analysis and to follow segregation of apterous-blot. Comparisons between genotypes were made, wherever
possible, using segregants from the same mating. Wings were mounted in
Berlese fluid for examination. Mitotic recombination was induced by irradiation
with 1000 R from a 60Co source delivering 2-5 KR/minute. Age at irradiation is
expressed in hours after egg-laying (AEL). The cell markers straw (stw), pawn
(pwn) and multiple wing hairs (mwh) were used to identify induced mosaics. All
mutants are described in Lindsley & Grell (1968) except for pawn (GarciaBellido & Dapena, 1974). Minute-plus clones were induced using the Minute
mutations M(2)c^&, M(3)hS37 or M(3)i55. Comparisons of mean clone size were
made by t tests after normalizing the data by log transformation.
RESULTS
Phenotypic description of apterous-blot wings
The penetrance of this mutant is incomplete (for example, in a sample of 582
wings 38 % showed alterations in wing shape or bristle disposition visible at
x 12 magnification), and expressivity is very variable. The most mild effect is
blistering in the wing blade centred on the posterior crossvein. Some wings show
clear mirror-image partial duplications only involving posterior structures
(Fig. 1 A). Other wings have disruptions in the venation pattern involving veins
2-5 and the crossveins (Fig. 1B). These include extra veins and distal branching
of veins 3 and 4, often concomitantly with the loss of parts of vein 5. Table 1
contains details of the extent of phenotypic variability in a sample of 50 wings
showing alterations from the normal phenotype. The frequency of disruption of
venation is highest for vein 5 and falls off for the veins in more anterior positions,
but even so vein 3 in the anterior compartment is disrupted in 60 % of the sample.
By comparison with wings of the mutant engrailed (Table 1) the disruptions in
apterous-blot wings are less extreme for vein 4 but clearly involve veins 2 and 3,
anterior compartment structures, which are unaffected by engrailed. Camera
lucida drawings of the venation of 30 such wings were compared one to another
to see whether each wing represented a combination of parts of two alternative
Wing transformation in Drosophila
293
B
Fig. 1. Apterous-blot wings. (A) Duplication of posterior wing structures. (B) Mirrorimage duplicate veins, sensilla and bristles in the posterior margin. (C) Posterior
compartment including dorsal vein network with many sensilla campaniformia.
(D) Wing shape resembling the engrailed phenotype. The posterior margin includes
dorsal triple row bristles. (E) Posterior margin of wing showing dorsal elements of
triple row bristles opposite ventral cell hairs.
apterous-blot
engrailed
apterous-blot
engrailed
Genotype
50
60
50
Number
of wings
V2
60
0
19
V3
76
981
97t
V4
88
90J
100t
PXV*
45-6±5-8
590±71
51-8±5-l
Bristle number
14-9±15-3
5OO±19-5
25-9 + 17-2
MTR
840 ±8-9
900 ± 8 0
90-5 ±100
* PXV = posterior cross vein,
t Replaced by duplicate vein 3.
% Absent.
96 J
100}
92
V5
Veins severely reduced or disrupted
(% of sample)
apterous-blot engrailed
DR
151 + 10 2
30-2±17-3
81-5±27-2
96-5±251
39-5 ±14-6
23-8±13-7
Marginal
hair number
between most
distal DR
bristles
Table 1. Phenotypic variability of various parameters in wings of the genotypes apterous-blot, engrailed and the double mutant
r
w
H
H
o
w
w
Wing transformation in Drosophila
295
vein patterns, but this could not be concluded from the drawings. All extra
venation is dorsal, and extra sensilla campaniformia are formed, as many as
22 per wing (Fig. 1C). Very occasionally small outgrowths of wing-blade
material project from the wing blade adjacent to the posterior crossvein, The
shape of the wing is frequently altered towards a symmetrical structure about
the long axis (Fig. 1D). The dorsal row of hairs on the posterior edge may be
replaced by the two types of bristles normally found as the dorsal two rows of
the anterior triple row (Fig. 1D) or by the dorsal element of the anterior
double row bristles. When both double (DR) and triple (TR) row bristles appear
in the posterior margin the double row bristles are always distal to the triple row
elements. This aspect of the transformation is patchy and incomplete, the
posterior edge often being composed of a mixture of bristles and double row
hairs (Figs. IB, ID) more particularly amongst the DR bristles. The ventral
double row hairs opposite these bristles are normal in their spacing; mean interhair distance was not significantly different between wild-type and in transformed apterous-blot wings (n = 100, t = 0-20). No single instance has been
observed of a ventral bristle along the posterior margin.
Counts were made of the number of median triple row bristles (MTR) and
double row bristles (DR) separately in anterior and posterior locations in wings
of genotype apterous-blot and of engrailed (Table 1). There are significantly
fewer posteriorly located MTR bristles in apterous-blot wings than in engrailed
wings (t108 = 6-9, P < 1 %), and also significantly fewer posterior DR bristles
in apterous-blot wings than in engrailed wings. However, since all those DR
bristles in apterous-blot wings on the posterior margin are dorsal, the mean of
15-1 DR bristles is not different from half the DR mean bristle number in
engrailed wings. The number of posterior marginal hairs between the most
distal anterior DR bristle and the most distal posterior DR bristle was significantly larger in apterous-blot wings than in engrailed wings, reflecting the less
complete nature of transformation of wing margin structures in the former
(Table 1).
Genetic analysis
Analysis of the recombinants provided by females of the constitution Bl
stw48 apm tuf sp/dp en bw showed that the wing phenotype described earlier
behaved as a single mutation to the right of straw at 55-1 cMs and to the left of
tufted at 55-5 cMs. Of 18 recombinants between Bristle (54-0 cMs) and cinnabar
(57-5 cMs) nine showed recombination between Bristle and the factor; apterousblot is located at 55-2 cMs.
A number of combinations of apterous-blot with other mutations in chromosome two were constructed. The double heterozygote between apterous-blot
and engrailed was wild-type whether the mutations were in cis or trans arrangement, as was the Fl between apterous-blot and tufted1, or tufted2, an extreme
allele which is homozygous lethal (Whittle, unpublished). The heterozygotes
296
hlt
J. ROBERT S. WHITTLE
56t
blt
and ap /Df(2R)MS4 (a deficiency including the apterous locus)
ap /ap
showed blistering but no transformation; the latter genotype has a Minute
phenotype since the deficiency includes a Minute locus. The genotype apm/
M(2)c33a has wings with slight upsets in venation near the posterior crossvein.
The double homozygote apterous-blot engrailed was viable and the phenotype of wings from this genotype is described in Table 1, and may be contrasted
with the phenotypes of each separate homozygote. By comparison with apterousblot, vein 3 in the double homozygote is significantly less often affected (X2 =
12-8, P < 1 %) though this anterior structure is still disrupted in 19 % of wings.
Vein 4 is always replaced by a mirror-image duplicate of vein 3, and the dorsal
vestige of the vein in the normal location of vein 5 carries a sensillum. The mean
number of posterior MTR bristles in the double homozygote is intermediate, but
significantly different from either homozygote. The alula is no longer a separate
discernible structure in the double homozygote though the large hairs characteristic of the alula are present on the margin intermingled with bristles typical
of the distal costa region. About 1 % of the double homozygotes have antennae
with mirror-image duplication from segment II.
The more extreme allele apterous561, which has no wings, drastically reduces
haltere size, but there was no evidence of any transformation effect of apterousblot in the haltere, though the lack of distinctive morphological markers of the
anterior compartments in the capitellum leaves some uncertainty on this point.
The halteres of various genetic combinations with apterous-blot were examined
for signs of transformations in the hope of identifying the compartment origin
of the 'anterior' elements seen in the posterior wing margin. No differences in
the dorsal metathoracic disc structures formed could be detected after the
addition of apterous-blot either to the genotype bx3/UbxlsQ (37 halteres) or to
the genotype pbx/Ubx130 (50 halteres). Neither did homozygosity for apterousblot change expressivity in the partially haltere-like dorsal mesothoracic disc
derivatives formed by Contrabithorax heterozygotes.
The penetrance and expressivity of apterous-blot in wings is severely reduced
in combinations with the Minute mutations M(3)i55 and M(3)h*31, the abnormalities being reduced to local alterations in venation.
Clonal analysis
Table 2 shows the mean cell number in multiple wing hairs clones induced in
homozygous apterous-blot genotypes at various ages. It is apparent that growth
rates at these ages are not significantly different either between anterior and
posterior compartments or between normal wings and wings which show the
transformations of posterior structures. Regression analysis of posterior clone
size on anterior clone size using pairs of such clones found in the same wing in
this sample showed no significant differences in this relationship when normal
and transformed wings were compared. This was true both for clones induced
at 108 h AEL and 120 h AEL (19 pairs of clones in normal wings and 17 pairs
Wing transformation in Drosophila
297
Table 2. Clone size in phenotypically normal and transformed
wings of apterous-blot
Mean cell number in clone
Anterior
Age at induction
of clone
108±8h AEL
120±4h AEL
Normal
14-5
84
(1-21 ±119)*
1-8
48
(0-51 ±0-44)*
Transformed
9-7
102
(1-30 ±1-12)*
2-5
38
(0-72 ±0-63)*
Posterior
Normal
00
18-4 55
(1-90 ±1-38)*
2-6
19
(0-82 ±0-53)*
Transformed
160
74
(205 ±1-23)*
3-4 44
(0-97 ±0-75)*
* Mean log clone size ± standard error.
of clones in wings with transformations at 108 h, t36 = 0-10; at 120 h 11 and
12 clone pairs respectively and t23 = 0-3). Thus the relative growth rates in the
anterior and posterior compartments in phenotypically normal and in transformed apterous-blot wings were not different at this age. At 96 hours AEL,
clone size in the anterior compartment was the same in normal and transformed
wings (X = 30-6, In clone size = 2-93 ±1-11). Mean clone size in the posterior
compartment of transformed wings (X = 136-8, In clone size = 4-62 ± 0-90) was
not significantly larger than in the anterior compartment (t25 = 1-0) but showed
considerably greater variability.
Partition of the posterior clones in wings showing transformation by their
location with respect to the transformed structures yielded clearer information.
Clones found within the areas with disrupted venation or close to bristles on the
posterior margin were far larger (X = 191-3) than those elsewhere in. the transformed wings (X = 90-0, t12 = 1-2).
An examination was made of the structures included in clones induced at
various ages during larval development in wings exhibiting transformations.
No clone, of 137 found in the posterior region, embraced both transformed
'anterior' structures and also normal posterior structures. The criterion set was
that the multiple wing hairs clone should clearly occupy an area including anterior
margin bristles and posterior margin hairs. In the same sample of mosaics, no
evidence was found for any clonal relationship between the cells contributing
to the normal anterior structures of the wing and the transformed 'anterior'
structures in the posterior wing.
The suppression effect of Minute mutations upon the apterous-blot phenotype
precluded the use of Minute-plus clones in the analysis of lineage relationships
in transformed wings. Instead it was possible to test the cell-autonomy of the
phenotypic suppression of the apterous-blot wing transformation using the same
mosaics, since in the genotype stw apm; M(3)hS37 large multiple wing hairs clones
298
J. ROBERT S. WHITTLE
produced by mitotic recombination lacked the Minute mutation. In particular,
posterior compartment clones both dorsal and ventral which touched the
posterior border were inspected to see whether they formed 'anterior' bristles
on the posterior margin or distorted wing shape towards that characteristic for
apterous-blot homozygotes. None of the 119 clones found (Table 3, column 5)
showed any alteration in posterior wing structures even though many clones
were in excess of several thousand cells; the average size of these clones is given
in Table 3. Column 7 of Table 3 shows the number of clones touching the
anterior-posterior border over a distance of more than 20 cells. Every clone
respected this border.
The crucial question in investigating the basis of the apterous-blot mutation
was whether it showed cell-autonomous behaviour, whether the phenotype of
marked clones homozygous for apterous-blot growing in wing discs otherwise
heterozygous for the mutation would resemble that of the homozygous mutation.
The genotypes stw aphlt pwn/M(2)c33ai and pwn/M(2)c33& were irradiated as
larvae and a search was made for pawn clones. Clones were only recovered in
the controls (for example, at 72 h AEL five clones in the 30 wings in the controls
and none in 79 wings of the experimental group). This apparent cell-lethality of
the clones of genotype stw aput pwn was confirmed by their absence from the
tergites of the same sample.
The failure to recover straw pawn clones in stw apm pwn/'M(2)c33a flies may be
attributable to the combination of the two cell-marker mutations, and so an
alternative approach was adopted. The genotypes stw ap^/pwn and It stw/pwn
were irradiated during larval life to induce clones. Pawn is clearly detectable
both in bristles and trichomes (Garcia-Bellido & Dapena, 1974), and the
expectation was that many of the mitotic recombination events producing pawn
clones would also give a straw twin-spot. Examination of the abdomens of the
two genotypes above after irradiation between 72 and 96 h AEL showed that
approximately half of the pawn clones were accompanied by a straw twin-spot
clone (Table 4). Straw has the drawback that it can only be unambiguously
classified in bristles in the wing, but each pawn clone was examined to see firstly
whether it was associated with any local disruptions in wing organization.
Secondly, where pawn clones were found dorsally in the posterior margin, a
search was made for adjacent twin straw clones showing transformations including triple row or double row bristles. Table 4 indicates the numbers of
pawn clones recovered and their mean size. No disturbances were associated with
any of the pawn clones found in the posterior compartment nor was any of the
pawn clones on the posterior margin associated with a clone including straw
marginal bristles. An anterior dorsal pawn clone in the genotype stw aph]t/pwn
included dorsal triple row bristles and an adjacent straw twin-spot, demonstrating that it was possible to recognize such twin-spots were they produced.
69
247
262
59
35
48
72*
96*
120
144
012
005
015
0-31
117
Clones
per wing
A
2
9
26
8
18
V
^
i
1
2
2
3
2
D
\
N
0
4
12
1
0
V
* Includes clones induced in aphlt; iM(3)i55/mwh.
6
14
13
10
23
D
Clones
Clones touching
posterior margin
5
7
7
3
4
Clones
touching
anteriorposterior
border
1740
4750
1260
1390
100
Clone size
6-2 ±2-2
8-4 ±0-6
5-1 ±2-6
60±21
20 ±1-9
loge clone size
±S.E.
pawn
clones
21
72-96
3
25
48-72
84-108
Tergites 2-6
Anterior
Age at induction
of clone
(hAEL)
4
24
pawn
clones
10
clones per abdomen
0-26
15
7
27
76-6
22-7
002
0-22
pawn/straw
twin-spots
Anterior
Clone size
3
17
Posterior
9
002
0-20
pawn/straw
twin-spots
1041
22-9
Clone size
0-27
clones per abdomen
Clone frequency
A
Clone frequency
A
Posterior
// stw/pwn
stw apwt/pwn
Table 4. Numbers and clone sizes o/pawn clones found in the wings of the genotypes stw apblfc/pwn and It stw/pwn after X-irradiation
at various stages
Total wings
examined
Age at
induction
of clone
(h AEL)
Table 3. Multiple wing hairs Minute-plus clones in wings of genotype stw ap b l t ; M(3)hS37/mwh
K)
ng transforma tion in Drcjsophite
300
J. ROBERT S. WHITTLE
DISCUSSION
The wings of penetrant homozygotes for apterous-blot show replacement of
some posterior structures by anterior structures; extra dorsal venation, sensilla
campaniformia and margin bristles are all characteristic of the anterior compartment. There is a symmetry about the long axis of the wing in shape, disposition of the extra dorsal veins and of margin bristles particularly at the
junction of veins with the margin. Although the ventral posterior region of
these wings is frequently larger in area, it otherwise retains the characteristics
of the posterior compartment, invariably forming hairs and not bristles at the
ventral posterior margin, and no duplicate to vein 2 is seen. Waddington (1939)
described this mutant as showing posterior duplications (cf. Fig. 1A) but the
extra anterior structures have not been reported before.
The more extreme alterations in apterous-blot wings are very similar to those
of the mutation engrailed (Garcia-Bellido & Santamaria, 1972) but are distinguished from the latter in that there are no ventral bristles on the posterior
margin, anterior compartment structures (for example vein 3) are also disrupted, and some wings display duplications within the posterior compartment
whilst having normal anterior structures. The fact that the double mutant
aphlt en has a wing phenotype very similar to engrailed argues that both mutations
interfere with a similar event or process in wing development. Apterous-blot
flies do not, however, have duplicated sex combs in males.
Three alternative explanations are considered here as possibilities for the
origin of this transformation phenotype, and they can be distinguished by the
experiments described.
Alternative 1. The mutation is a partial failure in a gene specifically concerned
in the maintenance of posterior compartment determination during cell
proliferation and therefore having a role similar to that ascribed to engrailed
as a compartment-specific selector gene (Garcia-Bellido & Santamaria, 1972;
Lawrence & Morata, 1976). It would be distinguished from engrailed in that
its function is restricted to the dorsal posterior polyclone. This explanation,
although the most interesting, is unlikely in the light of the following
observations. Firstly the mutant does not act cell-autonomously in clones, an
essential criterion for a gene involved in the maintenance of a specific determined
state through cell proliferation. The formation of large Minute-plus clones of
apterous-blot in the posterior compartment as early as 48 h AEL does not relieve
the phenotypic suppression by the Minute. Although twin clones are expected to
be common following mitotic recombination in the genotype stw aphlt/pwn,
no single transformation, for example upsets in venation or size of the posterior
compartment, let alone any posterior edge transformed clone including straw
bristles was found accompanying any pawn clone. The most critical evidence is
the absence of transformed straw twin clones adjacent to pawn clones in the
dorsal posterior margin. However, apterous-blot wings show widespread
Wing transformation in Drosophila
301
disruptions of veins and increase in cell number and frequently show transformations to anterior structures in the posterior area yet have an uninterrupted
posterior margin of hairs, and so absence of any disruption or transformation
adjacent to 'interstitial' pawn clones in the wing blade is also evidence against
cell-autonomy of apterous-blot.
The allele aphlt is intermediate in the allelic series at this locus. The dominant
allele ap^& shows wing-scalloping and cell-death (Fristrom, 1969). The allele
tf/?56f behaves as recessive to aphlt and yet shows no homoeotic effects. The
mutant combined with a deficiency for the apterous locus (aphlt/Df(2R)MS4)
shows no transformation effects, thus not behaving as a hypomorphic selector
gene mutant (see Garcia-Bellido, 1977). It is also difficult on this hypothesis to
explain why a selector gene failure should occasionally lead to posterior
duplications (Fig. 1 A). Finally, the effect of the mutation is not restricted to the
posterior compartment but abnormalities frequently include anterior structures
(Fig. ID).
Alternative 2. The second possibility is that the mutation aphlt disrupts
integrity of cell-cell contacts near the anterior-posterior compartment border
so that some cells of the anterior polyclone become separated and enclosed by
cells of the posterior polyclone. These 'trapped' cells would be supposed to
maintain their state of determination, behaving as do mosaics of posterior
compartment clones homozygous for engrailed in wild-type wings. Locally and
clonally they would lead to a 'patchy' appearance of anterior structures in the
posterior compartment, possibly causing local increases in wing size near them
(Lawrence & Morata, 1976). This explanation clearly predicts that anterior
structures in the posterior wing will show close lineage relationships to
structures in the anterior compartment, whereas anterior and posterior areas
are normally established as separate lineages (polyclones) in early embryogenesis (Garcia-Bellido, et al. 1973). No clones were found which behaved
in this manner. If this mutant functioned in the same way in the haltere it
would have been expected that some aphlt; pbx/Ubx1ZQ halteres would show
unusual areas of haltere tissue in the homoeotic posterior wing tissue formed
by postbithorax. Furthermore, halteres of aphlt; bx/Ubx130might show 'invasion'
of posterior haltere tissue by anterior wing structures, yet neither were seen.
However, the results of Adler (1978) on the behaviour of cultured fragments of
bithorax haltere discs, the tendency of haltere and wing disc cells to separate,
and the low expressivity of apterous-blot in the mesothoracic wings of these
flies leave considerable doubt about how definitive these experiments are.
Byrant (1975) demonstrated that during intercalary regeneration cells could
change their compartment-determined state, and it has recently been shown
that when cells cross the anterior/posterior border in situ they clearly do
redetermine to the state of the cells around them on that side of the compartment border (Simpson, Szabad & Nothiger, 1979) making unlikely the hypothesis considered as alternative 2. It is interesting to note that these authors also
2O
EMB
53
302
J. ROBERT S. WHITTLE
report the appearance of bristles characteristic of the anterior compartment on
the posterior margin of wings that during larval life had been subjected either
to surgical operations in situ or to heat-shock when carrying temperaturesensitive cell-lethal mutations.
Alternative 3. The mutant causes transdetermination of some cells of the posterior polyclone so that they become anterior. Such a type of mutation has in
fact been anticipated by Garcia-Bellido (1977) as likely to be found within
homoeotic mutations as a general class. Again one expects such transdetermined cells to behave as do mosaics of engrailed in the posterior compartment,
but there is no reason to suppose that the mutant itself need behave cellautonomously in the initial lesion it produces.
The duplication of posterior structures (Fig. 1A) might reflect either the
varying location or extent of the initial cell lesion in the disc. The position of
apmt in the allelic series as an allele of intermediate effect is now more understandable, the dominant allele #/?Xa causing some cell death and the recessive
extreme allele ap™1 not supporting the growth or differentiation of cells in the
wing blade at all. The atypically large size of clones induced at 96 h AEL in
transformed areas of these wings may reflect cell loss and subsequent proliferation during replacement, and this may provide the opportunity for this
'transdetermination' from posterior to anterior to occur.
This analysis makes clear again the value of investigating clonal parameters
of a mutant before assigning a role to a gene (Garcia-Bellido, 1975). The
intriguing aspect remaining to this mutant is the restriction of all the
transformations to cells of the dorsal surface of the wing, and this is being
further investigated.
I thank the Science Research Council for funding this research, the British Council for
travel support to a discussion meeting and Mrs Corryn Willsone for excellent technical
support.
REFERENCES
ADLER, P. N. (1978). Mutants of the bithorax complex and determinative states in the thorax
of Drosophila melanogaster. Devi Biol. 65, 477-461.
BRYANT, P. J. (1975). Pattern formation in the imaginal wing disc of Drosophila melanogaster:
fate map, regeneration and duplication. /. exp. Zool. 193, 49-77.
CRICK, F. H. C. & LAWRENCE, P. A. (1975). Compartments and polyclones in insect development. Science, N.Y. 189, 340-347.
FRISTROM, D. (1969). Cellular degeneration in the production of some mutant phenotypes in
Drosophila melanogaster. Molec. Gen. Genet. 103, 363-379.
GARCIA-BELLIDO, A. (1975). Genetic control of wing disc development in Drosophila. In 'Cell
Patterning', Ciba Foundation Symposium, vol. 29, pp. 161-182.
GARCIA-BELLIDO, A. (1977). Homoeotic and atavic mutations in insects. Amer. Zool. 17,
613-629.
GARCIA-BELLIDO, A. & DAPENA, J. (1974). Induction, detection and characterization of cell
differentiation mutants in Drosophila. Molec. gen. Genet. 128, 117-130.
GARCIA-BELLIDO, A. & SANTAMARIA, P. (1972). Developmental analysis of the wing disc in
the mutant engrailed of Drosophila. Genetics 72, 87-107.
Wing transformation in Drosophilia
303
GARCIA-BELLIDO, A., RIPOLL, P. & MORATA, G. (1973). Developmental compartmentalisation
in the wing disc of Drosophila. Nature New Biology 245, 251-253
GARCIA-BELLIDO, A., RIPOLL, P. & MORATA, G. (1976). Developmental segregations in the
dorsal mesothoracic disc of Drosophila. Devi Biol. 48, 132-147.
LAWRENCE, P. A. & MORATA, G. (1976). Compartments in the wing of Drosophila: A study
of the engrailed gene. Devi Biol. 50, 321-327.
LINDSLEY, D. L. & GRELL, E L . (1968). Genetic variations of Drosophila melanogaster.
Carnegie Just. Wash. Publ. no. 627.
SIMPSON, P., SZABAD, J. & NOTHIGER, R. (1979). Regeneration and compartments in Droso-
phila. J. Embryol. exp. Morph. 49, 229-241.
WADDINGTON, C. H. (1939). Preliminary notes on the development of the wings in normal
and mutant strains of Drosophila. Proc. natn. Acad. Sci., U.S.A. 25, 299-307.
(Received 22 February 1979, revised 9 May 1979)