Fly
ISSN: 1933-6934 (Print) 1933-6942 (Online) Journal homepage: https://www.tandfonline.com/loi/kfly20
Abdominal segment reduction
Development and evolution of a deeply fixed trait
John H. Yoder
To cite this article: John H. Yoder (2012) Abdominal segment reduction, Fly, 6:4, 240-245, DOI:
10.4161/fly.22109
To link to this article: https://doi.org/10.4161/fly.22109
Published online: 01 Oct 2012.
Submit your article to this journal
Article views: 308
View related articles
Citing articles: 2 View citing articles
Full Terms & Conditions of access and use can be found at
https://www.tandfonline.com/action/journalInformation?journalCode=kfly20
EXTRA VIEW
Fly 6:4, 240-245; October/November/December 2012; © 2012 Landes Bioscience
Abdominal segment reduction
John H. Yoder
Department of Biological Sciences; The University of Alabama; Tuscaloosa, AL USA
W
Keywords: Abdominal-B, wingless,
doublesex, DER, abdomen, segmentation,
apoptosis, Hox, tergite
Submitted: 08/03/12
Revised: 09/06/12
Accepted: 09/07/12
http://dx.doi.org/10.4161/fly.22109
Correspondence to: John H. Yoder;
Email: jhyoder@as.ua.edu
Extra View to: Wang W, Kidd BJ, Carroll SB,
Yoder JH. Sexually dimorphic regulation of the
Wingless morphogen controls sex-specific segment number in Drosophila. Proc Natl Acad Sci U
S A 2011; 108:11139-44; PMID:21690416;
http://dx.doi.org/10.1073/pnas.1108431108.
240
hen a new student first begins to
push flies, an immediate skill that
must be learned is sorting the sexes. In
Drosophila melanogaster several sexually dimorphic characters can be used to
readily distinguish males from females
including abdominal pigmentation,
male sex combs and genital morphology. Another, often-overlooked, sexual
dimorphism is adult abdominal segment
number. Externally, adult Drosophila
males possess one fewer abdominal segment than females; the terminal pregenital segment apparently either absent
or fused with the next-most anterior
segment. Beyond known roles for the
homeotic protein Abdominal-B (Abd-B)
and the sex-determining transcription
factor Doublesex (Dsx) as key regulators
of this trait, surprisingly little is known
about either the morphogenetic processes
or the downstream genetics responsible
for patterning these events. We have
explored both and found that rapid epithelial reorganization during pupation
eliminates a nascent terminal male segment. We found this Abd-B-dependent
process results from sex- and segmentspecific regulation of diverse developmental targets including the wingless
gene and surprisingly, dsx itself.1,2 Here, I
review our observations and discuss this
trait as a model to explore both dynamics
of epithelial morphogenesis as well as the
evolution of developmental mechanisms.
Development of the Abdominal
Epithelium
Development of the adult Drosophila
abdominal epithelium involves a number
Fly
of genetically tractable processes that make
this tissue an amenable model system for
investigating wide-ranging questions
addressing cell cycle regulation, pattern
formation and the evolution of novel
character traits. The epithelium is derived
from populations of imaginal histoblast
cells that are born during embryogenesis
and remain quiescent until the onset of
pupariation.3 Upon activation, discrete
nests of histoblasts proliferate and fuse
to form a continuous epithelium, replacing larval epidermal cells that are removed
by apoptosis and extrusion.4-6 Individual
abdominal segments are patterned by
many of the same genes responsible for
embryonic segmentation. Histoblast cells
within each developing segment retain
compartmental identities established during embryogenesis. Dorsally, an anterior
and posterior nest express cubitus interruptus (ci) and engrailed (en) respectively,
while a single ventral nest is composed of
cells separated into distinct anterior and
posterior populations.7-9 During larval
development a fourth nest, originating
from anteriorly fated tracheoblasts, joins
the larval epithelium and will generate
cells surrounding the spiracle.10 By 24 h
APF (after puparium formation) the four
nests have fused into a hemisegmental epithelium separated from adjacent segments
and contralateral hemisegments by narrow bands of remaining LECs. By 28–30
h APF fusion along the AP and DV axes
generates a continuous abdominal epithelium and proliferation continues until the
onset of differentiation at approximately
36–40 h APF.1,11 Cell identities along the
AP axis of each segment are patterned
principally by the transcription factor En
Volume 6 Issue 4
©2012 Landes Bioscience. Do not distribute.
Development and evolution of a deeply fixed trait
and the morphogen Hedgehog (Hh) produced by En expressing cells. In the posterior compartment En and Hh direct cells
toward unsclerotized cuticle fate (pleura)
while in the anterior compartment opposing Hh gradients direct planar cell polarity and establish discrete cell identities
distinguished by unique combinations of
pigment, trichomes (fine hairs) and bristle
types.7,8,12 In contrast to imaginal discs
and embryonic segmentation, Wg does
not have a predominant role in abdominal AP patterning.7-9,13 Rather, Wg and
Drosophila Epidermal Growth Factor
(DER) signaling were found to function
in complementary patterns along the DV
axis to direct cells away from pleural fate
and establish boundaries of the sclerotized anterior cuticle plates; the dorsal tergites and the ventral sternites. However,
activated Wg signaling in anterior compartment mitotic clones transforms subpopulation identities suggesting Wg does
have a role in AP patterning.14
As during embryogenesis, superimposed on these patterning events are
regional activities of the Hox proteins
Ultrabithorax (Ubx), Abdominal-A (AbdA) and Abdominal-B (Abd-B) which
promote unique morphology among the
seven abdominal segments A1-A7.15,16 For
example, in A1 Ubx promotes the absence
of a sternite, reduced tergite size and
unique bristle morphology and pigmentation.17 In the posterior abdomen (A5-A7)
Abd-B functions in collaboration with
sex-specific Dsx isoforms to generate male
specific pigmentation and modified cuticle
morphology.15 The terminal segment A7
presents the most striking of these modifications as female hemitergites do not
fuse dorsally and retain a characteristic
triangular shape while male A7 is superficially absent generating neither tergite
nor sternite (Fig. 1A and C). Male specific pigmentation and the roles of Abd-B
and Dsx in promoting this trait have been
extensively studied as a model for mechanisms of morphological evolution.18-22
Sex-specific pigmentation is under strong
sexual selection and as such has diverged
rapidly within the family Drosophilidae.
In contrast, reduction of male posterior segments is deeply fixed within the
monophyletic clade Cyclorrhapha which
diverged an estimated 145mya 23 and
www.landesbioscience.com
reflects a trend among the aerially acrobatic higher Diptera (Brachycera) toward
reduced body size. Although Abd-B and
Dsx have long been known to control this
trait in Drosophila17,24 no studies have
investigated either the morphogenesis of
male reduction or the genetic events regulated by these transcription factors. Here
I summarize our observations that show
reduction of Drosophila male A7 occurs
through rapid epithelial reorganization
driven largely by male-specific Abd-B
and Dsx dependent Wg repression as well
as segment-specific, but not sex-specific,
modulation of apoptosis.1 Additionally,
I review our more recent data that show
not only is Dsx a requisite Abd-B co-regulator of this trait, but it is also positively
regulated downstream of Abd-B. Finally, I
discuss this trait as a model to investigate
the evolution of a complex morphological
process.
Reduction of the Terminal
Male Segment
Prior to our investigation, the only genetic
alterations known to affect male A7 development modify the function of either
Abd-B or Dsx. Abd-B loss of function
alleles cause homeotic transformations
including A7 toward A6 identity producing a robust male A7 segment.17 Similar
transformations are observed when the
Hox co-factor Extradenticle is absent and
upon overexpression of the Hox antagonist Bric-á-brac (Bab).18,25 dsx loss of function flies have an intersex phenotype with
XX and XY individuals exhibiting similar
sexually intermediate characters.24 In both
sexes, A7 retains the characteristic triangular morphology of females but is reduced
in size compared with wild type A7. The
differences in A7 morphology between
Abd-B and dsx mutants suggest that while
dsx functions cooperatively with Abd-B to
promote male A7 reduction Abd-B also
regulates dsx-independent processes that
contribute to this trait. As the dsx null A7
is smaller than wild type female A7 this
suggests Abd-B and Dsx co-govern proliferation, and Abd-B governs processes that
eliminate A7 for which Dsx-F (the female
specific isoform) is an antagonist.
Analyses of wild type adult cuticles
reveal that male A7 is not completely
Fly
absent. In the lateral pleura, adjacent to
the dorsal tergite of each female abdominal segment and male A1-A5, lies a bilateral pair of trachea spiracle pits. However,
two spiracle pairs are associated with male
A6 suggesting A7 either only partially
develops or fuses with A6 during pupation
(Fig. 1B and D). We developed a dissection and imaging protocol that preserves
abdominal epithelial morphology26 and
imaged fixed pupae with nuclei fluorescently labeled to monitor the fate of male
A7 histoblasts.1 We confirmed that histoblast nests in male A7 third instar larvae
have similar cell numbers compared with
more anterior segments,3 therefore the
absence of adult cuticle does not result
from a failure to establish or maintain
histoblast populations. Additionally,
by 24 h APF histoblasts nests in all segments, including male A7, have undergone
extensive proliferation and are fused into
individual segment epithelia (Fig. 1E–F).
While the absence of adult male A7 cannot be attributed to a failure of histoblast
proliferation we found A7 mitotic counts
in both sexes are significantly lower compared with more anterior segments and
male A7 counts are more than 2-fold
lower than female A7. In support of a role
for Abd-B in suppressing cell division we
recently found that A7 Abd-B null clones
in either sex exhibit increased proliferation
compared with surrounding wild type tissue (unpublished data).
To track the fate of male A7 we
monitored expression of GFP driven by
En-GAL4 to mark posterior compartments. Rapidly, between 28 and 40 h
APF, anterior A7 (aA7) cell number
decreases such that by 42hr APF few, if
any, aA7 cells remain and the posterior
compartments of A6 and A7 are tightly
juxtaposed. Strikingly, we observed during this process that pA6 gradually buckles around the anterior-fated A7 spiracle
and passes this structure before merging
with pA7. As a result the A7 spiracle pit
is repositioned and becomes associated
with aA6. Therefore, although a nascent
male A7 segment develops during early
pupation it is rapidly eliminated prior
to the onset of differentiation. We initially hypothesized that male-specific
programmed cell death in combination
with decreased A7 proliferation may be
241
©2012 Landes Bioscience. Do not distribute.
EXTRA VIEW
EXTRA VIEW
sufficient to drive this elimination. We
found no clear male-specific pattern of
apoptosis, however cell death is enhanced
surrounding all spiracle pits and is significantly enriched around A7 spiracles of
both sexes. We used a Dsx -GAL4 driver,
which is strongly expressed in all abdominal histoblasts, to block apoptosis during
pupation through ectopic expression of
the baculovirus anti-apoptotic gene p35.27
Importantly, this GAL4 transgene is inactive in the LECs where apoptosis has
been shown necessary to promote proper
histoblast proliferation and expansion.4
Reducing histoblast apoptosis in the pupal
abdomen does not promote widespread
defects in cuticle formation suggesting
histoblast apoptosis does not play a major
role in development of adult abdominal
segments. Interestingly, in adult males of
this genotype there is excess pleural tissue posterior to the A6 tergite suggesting
male aA7 is not completely eliminated.
However this A7 tissue does not develop
tergite or sternite cuticle plates.
Therefore, mechanisms in addition
to regulating proliferation and apoptosis
must be involved in male A7 reduction.
Insight into this came from our observations of dynamic En-driven GFP expression. During the 12-h period when male
aA7 is eliminated we found that pA6
expands and is several cell diameters wider
242
©2012 Landes Bioscience. Do not distribute.
Figure 1. Morphogenesis of the terminal
abdominal segment. Adult Drosophila males
externally lack the terminal abdominal
segment A7. (A and C) Whole abdominal
cuticle preparation of adult male and female
dissected longitudinally along the dorsal axis.
Segment tergites are numbered. Note a robust, but characteristically modified, female
A7 is present (C), but males lack both tergite
and sternite (A). (B and D) Higher magnification of same cuticles framing the posteriormost tergites. Arrows indicate spiracle pits.
A single spiracle pit is associated with each
female tergite (D) however in males the A7
spiracle has moved anteriorly and is associated with the A6 tergite (E and F) Despite
its absence in adults, male A7 undergoes
substantial proliferation during the first 28 h
of pupation. By 24 h APF, male A7 histoblasts
(small nuclei) have proliferated and formed
a continuous segmental epithelium (E). (G
and H) Abd-B and Dsx mediated repression
of Wg is a major contributor of the ultimate
reduction of male A7. The same pupae shown
in (E and F) stained with an anti-Wg antibody
show absence of Wg from male A7 (G).
than in more anterior segments or female
A6. By co-labeling these GFP expressing
pupae with an anti-En antibody we found
that during reduction the posterior-most
pA6 En positive nuclei do not co-express
Fly
GFP. Our interpretation of these data are
that during pupation the fate of the anterior-most a7A cells is transformed toward
posterior identity; they begin to express
engrailed de novo and become a part of
Volume 6 Issue 4
www.landesbioscience.com
ectopic wg restores male A7 tergite and
sternite, though weakly as compared with
either Abd-B or dsx mutants. It is possible
that simultaneously blocking apoptosis
may enhance A7 rescue, however this
experiment leads to early pupal lethality
and could not be assayed. We also considered it likely that Abd-B and Dsx also differentially regulate other developmental
pathways. For example, DER signaling is
required for dorsolateral and ventral cuticle
fate.11 Consistent with this, we found activation of DER signaling, through overexpression of the ligand Vein, also partially
restores male A7. A role for modification of
DER signaling was recently confirmed and
found to be associated with Abd-B/Dsx
dependent repression of the ligand Spitz
(Spi).31 Because both Wg and DER signaling have mitogenic functions, the dramatic decrease in male A7 proliferation is
likely due to the combined repression of
these two pathways. Furthermore, it was
shown that male A7-specific cell extrusion
plays a significant role in the elimination
of histoblast cells from the developing epithelium. This process is regulated downstream of Abd-B and Dsx-M through
positive regulation of extramacrocheate
(emc) which encodes an HLH transcription factor.31 These analyses suggest that
emc, in turn, promotes elevated expression of the myosin light chain regulatory
subunit spaghetti-squash (sqh) promoting
basal extrusion of male A7 histoblasts.
This process is similar to extrusion of
LECs from the larval abdominal epithelium which has been shown to require
myosin-dependent apical constriction.4
Our observations, combined with other
studies, suggest a model in which Abd-B
and Dsx-M cooperatively repress wg and
spi in male A7, promoting decreased proliferation and preventing cuticle differentiation. Additionally, Abd-B and Dsx-M
promote elevated A7 levels of emc leading
to segment-specific activation of epithelial
cell extrusion. Independent of Dsx, we
propose Abd-B enhances a segmentally
reiterated pattern of spiracle-associated
apoptosis. The mechanism of cell death
regulation is less clear and would require
collaboration with some unidentified factor restricted to the spiracle perimeter.
Together, the combination of reduced
proliferation,
aA7
transformation,
Fly
enriched A7 apoptosis and cell extrusion
are sufficient to completely eliminate the
nascent male A7 segment. In females,
subtle modification to the regulation of
these processes by Dsx-F, acting either in
combination with or antagonistically to
Abd-B activity, likely sculpts the unique
morphology of the female terminal segment. We have recently revised our model
to include an additional level of regulatory
complexity. We found that not only does
Dsx function cooperatively with Abd-B
to control these morphogenetic events,
but dsx is itself regulated downstream of
Abd-B.2 Similar observations were subsequently reported independently.31 During
early pupation, when proliferation and
apoptosis promote sex-specific A7 epithelial morphogenesis, Dsx expression is
restricted to A7 of both sexes under positive regulation by Abd-B. Although Dsx
is expressed within similar domains in
male and female pupae, Dsx-M protein
levels are approximately 2.5 fold higher
than Dsx-F. Appropriate levels of Dsx-F
are clearly necessary for proper morphogenesis as we find that overexpression of
Dsx-F during pupation leads to A7 tergite
enlargement (unpublished data).
A Model for Development
and Evolution
Morphogenesis of the Drosophila abdominal epithelium requires organized control
of diverse cellular events. This tissue has
been developed as a model to explore the
coordination of cell cycle regulation, apoptosis and differentiation in an expanding
epithelial population.4-6 Additionally, this
system has provided valuable insight into
epithelial axial patterning and planar cell
polarity.7-9,14,16,32 Our focus on the terminal abdominal segment is complimentary
to these two lines of investigation and
highlights the synergy of these varied
processes and their coordinated regulation by homeotic and sex-determination
pathways.
Our investigations also shed light on
the evolution of this novel morphology.
Male posterior segment reduction and
modifications to corresponding female
segments (usually as a retractable ovipositor) is a characteristic trait, if not a synapomorphy, of Cyclorrhapha. Though many
243
©2012 Landes Bioscience. Do not distribute.
pA6. A similar fate transformation has
been observed during embryonic posterior
spiracle morphogenesis.28 Another possible interpretation of these results is that
the non-GFP, En-positive cells at the male
A6/A7 border are not transformed aA7
cells, but instead are true pA6 cells which
in more anterior segments and female A6
express En at undetectable levels. Such a
scenario would require an Abd-B/Dsx-M
mediated mechanisms of enriching en
expression in pA6. It is also possible that
these cells reflect the early embryonic lineage of the anterior-most anterior compartment cells. In early embryos these
cells initially express en but this expression
decays as Wg expression, necessary for en
maintenance, is refined within the anterior
compartment.29 As such, the dynamics of
en expression we have observed may occur
at all segment borders but are enhanced
at A6/A7 in an Abd-B/Dsx-M dependent
manner. Accordingly, we do observe similar non co-labeled cells, though far fewer
and only sporadically, in more anterior
segments of both sexes. Addressing these
possibilities through lineage analyses is
challenged by the fact that no reliable
characters distinguish the anterior-most
A compartment cells from the posteriormost P compartment cells in the adult
abdominal cuticle.7
The sex-specific modulation of en compelled us to investigate expression of other
segmentation genes, or their protein products, with previously characterized roles
in adult abdominal segmentation.7,8,11,12,16
Strikingly, only Wg shows sexually dimorphic expression; it is strongly repressed in
developing male A7 and this repression is
dependent on both Abd-B and Dsx (Fig.
1G-H). We propose that, regardless of
the mode of En expression dynamics, the
absence of Wg in male A7 promotes these
modifications and contributes to the loss
of cells from aA7. More rigorous analyses,
perhaps employing ectopic Wg expressing
clones in male A7, will be necessary for
further clarification.
Beyond a potential role in modulating
en expression, Wg is a potent mitogen and
is necessary for abdominal cuticle differentiation;13,30 therefore its absence in male
A7 leads to logical conclusions concerning
reduced proliferation in this segment and
the absence of adult cuticle. Importantly,
244
the Cyclorrhapha. Therefore, segment
reduction may be viewed as an extreme
example of this trait. However, it is also
possible that male segment reduction
evolved as a necessary adaptation for
another Cyclorrhaphan synapomorphy,
genital circumversion.
Peculiar among Diptera, the male genitalia of Cyclorrhapha undergo a 360° rotation during pupation or immediately after
eclosion. This process, while retaining
the dorsoventral orientation of the genitalia, produces abdominal ventroflexion
allowing mating to occur with males positioned dorsally, rather than tail-to-tail as
in most Diptera. Reduction of male posterior segmentation probably allows necessary abdominal flexion during mating
and is therefore under strong stabilizing
selection.
7.
8.
9.
10.
11.
12.
13.
Acknowledgments
I thank all members of my lab, past and
present, for their contributions to this
work. I am especially indebted to W. Wang
for his hard work and determination. I
thank G. Struhl for insightful discussions
and interpretations on segment compartment fate transformation. This work was
supported by a grant from the National
Science Foundation (IOS-0919891).
References
1. Wang W, Kidd BJ, Carroll SB, Yoder JH. Sexually
dimorphic regulation of the Wingless morphogen
controls sex-specific segment number in Drosophila.
Proc Natl Acad Sci U S A 2011; 108:11139-44;
PMID :21690416 ;
http://dx.doi.org/10.1073/
pnas.1108431108.
2. Wang W, Yoder JH. Hox-mediated regulation of
doublesex sculpts sex-specific abdomen morphology in Drosophila. Dev Dyn 2012; 241:1076-90;
PMID:22488883;
http://dx.doi.org/10.1002/
dvdy.23791.
3. Madhavan MM, Madhavan K. Morphogenesis of the
epidermis of adult abdomen of Drosophila. J Embryol
Exp Morphol 1980; 60:1-31; PMID:6796636.
4. Ninov N, Chiarelli DA, Martín-Blanco E. Extrinsic
and intrinsic mechanisms directing epithelial cell
sheet replacement during Drosophila metamorphosis.
Development 2007; 134:367-79; PMID:17166923;
http://dx.doi.org/10.1242/dev.02728.
5. Ninov N, Manjón C, Martín-Blanco E. Dynamic
control of cell cycle and growth coupling by ecdysone,
EGFR, and PI3K signaling in Drosophila histoblasts.
PLoS Biol 2009; 7:e1000079; PMID:19355788;
http://dx.doi.org/10.1371/journal.pbio.1000079.
6. Bischoff M, Cseresnyés Z. Cell rearrangements, cell
divisions and cell death in a migrating epithelial
sheet in the abdomen of Drosophila. Development
2009; 136:2403-11; PMID:19542353; http://dx.doi.
org/10.1242/dev.035410.
Fly
14.
15.
16.
17.
18.
19.
20.
21.
22.
Struhl G, Barbash DA, Lawrence PA. Hedgehog
acts by distinct gradient and signal relay mechanisms to organise cell type and cell polarity in the
Drosophila abdomen. Development 1997; 124:215565; PMID:9187142.
Struhl G, Barbash DA, Lawrence PA. Hedgehog
organises the pattern and polarity of epidermal cells
in the Drosophila abdomen. Development 1997;
124:2143-54; PMID:9187141.
Kopp A, Duncan I. Control of cell fate and polarity
in the adult abdominal segments of Drosophila by
optomotor-blind. Development 1997; 124:3715-26;
PMID:9367427.
Pitsouli C, Perrimon N. Embryonic multipotent
progenitors remodel the Drosophila airways during metamorphosis. Development 2010; 137:361524; PMID:20940225; http://dx.doi.org/10.1242/
dev.056408.
Kopp A, Blackman RK, Duncan I. Wingless, decapentaplegic and EGF receptor signaling pathways
interact to specify dorso-ventral pattern in the
adult abdomen of Drosophila. Development 1999;
126:3495-507; PMID:10409497.
Kopp A, Muskavitch MA, Duncan I. The roles of
hedgehog and engrailed in patterning adult abdominal segments of Drosophila. Development 1997;
124:3703-14; PMID:9367426.
Shirras AD, Couso JP. Cell fates in the adult abdomen of Drosophila are determined by wingless during pupal development. Dev Biol 1996; 175:2436; PMID:8608866; http://dx.doi.org/10.1006/
dbio.1996.0092.
Lawrence PA, Casal J, Struhl G. Towards a model of
the organisation of planar polarity and pattern in the
Drosophila abdomen. Development 2002; 129:274960; PMID:12015301.
Lewis EB. A gene complex controlling segmentation in Drosophila. Nature 1978;
276 :565-70 ;
PMID:103000 ;
http://dx.doi.
org/10.1038/276565a0.
Kopp A, Duncan I. Anteroposterior patterning in
adult abdominal segments of Drosophila. Dev Biol
2002; 242:15-30; PMID:11795937; http://dx.doi.
org/10.1006/dbio.2001.0529.
Bender W, Akam M, Karch F, Beachy PA, Peifer M,
Spierer P, et al. Molecular Genetics of the Bithorax
Complex in Drosophila melanogaster. Science
1983; 221:23-9; PMID:17737996; http://dx.doi.
org/10.1126/science.221.4605.23.
Kopp A, Duncan I, Godt D, Carroll SB.
Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 2000;
408:553-9;
PMID:11117736 ;
http://dx.doi.
org/10.1038/35046017.
Williams TM, Selegue JE, Werner T, Gompel N,
Kopp A, Carroll SB. The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 2008; 134:610-23;
PMID:18724934;
http://dx.doi.org/10.1016/j.
cell.2008.06.052.
Jeong S, Rokas A, Carroll SB. Regulation of body
pigmentation by the Abdominal-B Hox protein and
its gain and loss in Drosophila evolution. Cell
2006; 125:1387-99; PMID:16814723; http://dx.doi.
org/10.1016/j.cell.2006.04.043.
Jeong S, Rebeiz M, Andolfatto P, Werner T, True
J, Carroll SB. The evolution of gene regulation
underlies a morphological difference between two
Drosophila sister species. Cell 2008; 132:783-93;
PMID:18329365;
http://dx.doi.org/10.1016/j.
cell.2008.01.014.
Wittkopp PJ, True JR, Carroll SB. Reciprocal functions of the Drosophila yellow and ebony proteins in
the development and evolution of pigment patterns.
Development 2002; 129:1849-58; PMID:11934851.
Volume 6 Issue 4
©2012 Landes Bioscience. Do not distribute.
non-Cyclorrhaphan flies have evolved
variations in segment number and morphology, most retain the ancestral phenotype of sexually monomorphic abdominal
segment number. Therefore, our observations present testable hypotheses about the
evolution of posterior segment morphology within the Cyclorrhapha. Considering
male segment reduction specifically, we
predict that the patterning function and
requirement for cuticle differentiation
of Wg and EGF signaling are conserved
through the insects. In support of this, a
requirement for Wg in tergite differentiation has been shown in the milkweed bug
O. fasciatus, a hemimetabolous insect.33
Therefore, within the Cyclorrhaphan
diptera we hypothesize that this trait
evolved through regulatory changes that
brought wg, spi and emc under transcriptional regulation downstream of Abd-B
and Dsx. Comparative expression studies will be needed to confirm this prediction. Whether Abd-B and Dsx expression
are conserved throughout the Diptera
is an important question that must also
be addressed. Abd-B expression in the
posterior abdomen is likely conserved as
I have previously shown that its embryonic expression domains are conserved
between Drosophila and basal dipterans.34 Whether dsx, for which the production and function of sex-specific isoforms
is deeply conserved, was ancestrally an
Abd-B target in the abdomen will provide
important clues about the stepwise evolution of this trait. The two transcription
factors are co-expressed in Drosophila
genitalia and likely have conserved co-regulatory functions. Through the evolution
of Abd-B regulated dsx abdominal expression, these developmental modules may
have been co-opted into morphogenesis of
the posterior abdomen. Alternatively, dsx
may have ancestrally been expressed in the
abdomen and been required for more subtle morphogenetic processes. Selection for
male segment reduction would then have
brought wg, spi, emc and apoptosis under
dual regulation of these proteins.
This raises the question of what selection pressure promoted male segment
reduction and how it has remained a rigidly fixed trait within the Cyclorrhapha?
Reduction in body size is a trend within
the suborder Brachycera, which includes
www.landesbioscience.com
29. Bejsovec A, Martinez Arias A. Roles of wingless
in patterning the larval epidermis of Drosophila.
Development 1991; 113:471-85; PMID:1782860.
30. Neumann CJ, Cohen SM. Distinct mitogenic and
cell fate specification functions of wingless in different regions of the wing. Development 1996;
122:1781-9; PMID:8674417.
31. Foronda D, Martín P, Sánchez-Herrero E. Drosophila
Hox and Sex-Determination Genes Control
Segment Elimination through EGFR and extramacrochetae Activity. PLoS Genet 2012; 8:e1002874;
PMID:22912593; http://dx.doi.org/10.1371/journal.
pgen.1002874.
32. Lawrence PA, Casal J, Struhl G. Cell interactions
and planar polarity in the abdominal epidermis
of Drosophila. Development 2004; 131:4651-64;
PMID :15329345;
http://dx.doi.org/10.1242/
dev.01351.
Fly
33. Angelini DR, Kaufman TC. Functional analyses in
the milkweed bug Oncopeltus fasciatus (Hemiptera)
support a role for Wnt signaling in body segmentation but not appendage development. Dev Biol
2005; 283:409-23; PMID:15939417; http://dx.doi.
org/10.1016/j.ydbio.2005.04.034.
34. Yoder JH, Carroll SB. The evolution of abdominal reduction and the recent origin of distinct
Abdominal-B transcript classes in Diptera. Evol Dev
2006; 8:241-51; PMID:16686635; http://dx.doi.
org/10.1111/j.1525-142X.2006.00095.x.
©2012 Landes Bioscience. Do not distribute.
23. Wiegmann BM, Yeates DK, Thorne JL, Kishino H.
Time flies, a new molecular time-scale for brachyceran fly evolution without a clock. Syst Biol 2003;
52:745-56; PMID:14668115.
24. Hildreth PE. Doublesex, A recessive gene that transforms both males and females of Drosophila into intersexes. Genetics 1965; 51:659-78; PMID:14330702.
25. González-Crespo S, Morata G. Control of Drosophila
adult pattern by extradenticle. Development 1995;
121:2117-25; PMID:7635057.
26. Wang W, Yoder JH. Drosophila pupal abdomen
immunohistochemistry. J Vis Exp 2011; •••:e3139;
PMID:21988937.
27. Hay BA, Wolff T, Rubin GM. Expression of baculovirus P35 prevents cell death in Drosophila.
Development 1994; 120:2121-9; PMID:7925015.
28. Merabet S, Hombria JC-G, Hu N, Pradel J, Graba
Y. Hox-controlled reorganisation of intrasegmental
patterning cues underlies Drosophila posterior spiracle organogenesis. Development 2005; 132:3093102; PMID:15930099; http://dx.doi.org/10.1242/
dev.01889.
245