doi:10.1016/S0960-9822(00)00151-2 
Copyright © 1994 Elsevier Science Ltd. All rights reserved.
Research Paper
The role of the Distal-less gene in the development and evolution of insect limbs
Grace Panganiban1, Lisa Nagy1 and Sean B Carroll
, 1
1 Howard Hughes Medical Institute, Laboratory of Molecular Biology, University of Wisconsin-;Madison, 1525 Linden Drive, Madison, Wisconsin 53706, USA
Received 18 May 1994;
accepted 23 June 1994.
Available online 7 October 2004.
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Abstract
Background Arthropod diversity is apparent in the variations in limb number, type, and position along the body axis. Among the insects, for example, butterflies and moths (Lepidoptera) develop larval abdominal and caudal appendages (‘prolegs’), whereas flies (Diptera) do not. Comparative studies of the expression and regulation during development of limb-patterning genes, such as Distal-less (Dll), may provide insights into arthropod evolution.
Results We report the cloning of a Dll homolog from the butterfly Precis coenia, and present data showing that it is expressed in all developing limbs (except the mandible), including the prolegs; the relationship between Dll and wingless expression observed in Drosophila is conserved in Precis among all limbs. However, Dll is deployed in distinct spatial and temporal patterns within each limp type.
Conclusion These data suggest that Dll function, suppressed in the abdomen early in insect evolution, has been derepressed in Lepidoptera, and also suggest that there is a common mechanism underlying the formation of all insect appendages. The limb-type-specific patterns of Dll expression (and its exclusion from the mandible) indicate that regulation of Dll expression may be critical to limb morphology, and are inconsistent with Dll functioning in a simple distal-to-proximal concentration gradient.
Figure 1. Sequence alignment of proteins predicted from Drosophila and Precis Dll sequences. The Precis coenia Dll gene encodes a protein (top) that is identical to the Drosophila melanogaster Dll protein (bottom) throughout the homeodomain (boxed), with 57% amino-acid sequence similarity amino-terminal to the homeodomain. The alignment was generated with the UWGCG's GAP program, using the amino-acid sequences of Precis cDNA 5-1, and the Drosophila cDNA sequence of Vachon et al. [7]. Solid lines indicate identical amino acids, and double dots indicate conservative substitutions.
Figure 2. Drosophila and Precis Dll genes are expressed in cephalic and thoracic limbs during early embryogenesis. (a) In Drosophila, Dll transcripts are first detected in the head as the blastoderm is cellularizing [6 and 11] and in the primordia of the labral (lr), antennal (an), maxillary (mx) and labial (la) head segments by early gastrulation [6]. (b) Once the germ band is extended, Drosophila Dll is expressed in thoracic leg primordia (t1, t2, t3) [6 and 7], which encompass the vestigial larval legs (Keilin's organs [9]) and leg imaginal discs (primordia of the adult legs) [6 and 7]. (c) In Precis, Dll expression is initiated in the antennal primordium at 
10% of embryogenesis (defined in [12]). (d) By 12% of embryogenesis in Precis, Dll transcripts also appear in the maxillary, labial, and three thoracic segments. Neither Dll gene is expressed in the intercalary (ic) or mandibular (md) segments (see also Figure 3). Scale BARS = 0.1 mm.
Figure 3. The Precis Dll gene is expressed in developing abdominal limbs. (a) As embryogenesis proceeds, Precis Dll is activated in the labrum, as well as in the antennae, maxillae, labia and thoracic legs. At 20% of embryonic development, Dll transcripts can be readily detected in the first (a1) and last abdominal segments, in the primordia of the tympanum and anal prolegs (ap), respectively. (b) By 30% of embryogenesis, Precis Dll transcripts are restricted in the cephalic limbs to a distal ‘sock’, and, in each elongating thoracic leg, to a distal ‘sock’ plus a proximal ring (see also Figure 4). (c) By 40% of embryonic development, Dll transcripts are also readily detected in the developing prolegs of abdominal segments 3–6 (a3, a4, a5, a6). Scale BAR = 0.1 mm.
Figure 4. Expression of the Precis Dll gene in the abdominal prolegs suggests homology between thoracic and abdominal larval legs. (a) The Precis wingless (wg) gene is initially expressed in a stripe in the posterior of each segment as it forms. (b) This wg stripe becomes restricted to the presumptive antero–ventral portion of each limb, including the abdominal proleg, as the limb develops. (c) Dll expression resolves to a distal ‘sock’ and proximal ring in Precis larval thoracic legs. (d) Precis abdominal prolegs also express Dll. (e) Although less pronounced, expression of Dll in an everting Drosophila thoracic leg (5 hours after pupariation) also resembles a ‘sock’ and a ring. (f,g) Optical sections of Precis abdominal prolegs, which by 50% development have only the proximal ring of Dll expression. Scale BARS = 0.1 mm.
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