Cell lineage and differentiation on the male foreleg of Drosophila melanogaster

doi:10.1016/0012-1606(62)90054-4

Developmental Biology

Volume 4, Issue 3, June 1962, Pages 489-516

https://doi.org/10.1016/0012-1606(62)90054-4 Get rights and content

Abstract

Cell lineage was studied in the epidermis of the basitarsus of the foreleg of male Drosophila melanogaster. This was accomplished by “marking” single cells, and their descendants, with genotypes different from the rest of the tissues. The mosaic basitarsi thus produced had areas with yellow chaetae on a background of black chaetae.

On the basis of cell lineage data, the male basitarsus can be divided in two main parts. Region A occupies most of the segment including the primary sex comb and the central bristle. It does not include the area of the longitudinal rows 1, 2, and 3 and that of the secondary sex comb which shows a close developmental relation to rows 1 and 2. These areas constitute region B. Within region A cell lineage data yield a subdivision into A-1 which includes longitudinal row 1′, the transverse rows, longitudinal rows 7 and 6 and 5.5, the primary sex comb and the central bristle; and A-2 the remaining area which includes longitudinal rows 4 and 5.

In region A-1 the following developmental relations were found. (a) The descendants of a yellow cell tend to form longitudinal strips of tissue both along the longitudinal rows and in the area of the transverse rows. (b) The proximal teeth of the sex comb and the central bristle are closely related to the posterior part of the transverse rows. (c) The middle teeth are closely related to the middle and the anterior parts of the transverse rows and to row 7. (d) The bractless bristles 5.5 are closely related to the distal teeth within the middle part of the sex comb. (e) The distal teeth of the sex comb are closely related to longitudinal row 6, and less closely, to row 7.

The data suggest that the prospective area of the primary sex comb initially occupies the same distal part of the basitarsus as the most distal transverse rows of the female basitarsus. They suggest further that in the male the tissue of this area shifts anteriorly, whereby it changes its direction by approximately 90 degrees. This not only is deduced from the results of the cell lineage studies, but explains the position of the bracts at the base of the sex comb teeth and the direction assumed by the teeth, both of which deviate by about 90 degrees from that of the other chaetae of the segment.

The above results on pure male basitarsi were confirmed by cell lineage studies of gynandric basitarsi. Systematic deviations from the norm in the location and direction of the male sex comb teeth and of female chaetae at the distal part of the segment are the result of the differential morphogenesis of the male and female tissues in this area.

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There are more references available in the full text version of this article.

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The “teeth” (bristle shafts) that make up the sex comb show a number of structural modifications compared to the ancestral bristle morphology (Fig. 1). In D. melanogaster and some other species, sex combs also rotate by up to 90° during pupal development, from a transverse to an oblique or longitudinal orientation (Atallah et al., 2012, 2009a, 2009b; Tanaka et al., 2009; Tokunaga, 1962) (Fig. 1E). Sex comb evolution involved the deployment of doublesex (dsx), a transcription factor that mediates sex-specific differentiation in Drosophila and other insects, in a novel spatial pattern in the prothoracic leg (Tanaka et al., 2011).
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The four cells of the mature mechanosensory organ (bristle, socket, sheath, and neuron) arise from asymmetric divisions of the sensory organ precursor (SOP) cell (Jan and Jan, 2001). The bract cell is not lineally related but is induced from the surrounding epithelium by cells within the SOP lineage (García-Bellido, 1966; Tobler, 1966; Tokunaga, 1962). The specific cell within the sensory organ that produces the inductive signal was not easily discerned, as disrupting development of either the socket cell or shaft cell produced bractless organs (Tobler, 1969; Tobler et al., 1973).
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Males have 5–6 TRs of bracted bristles, whereas females have two additional TRs (Hannah-Alava, 1958; Bryant, 1978; Held, 2002). In males, these two rows are replaced by the sex comb and by one central bristle (Hannah-Alava, 1958; Bryant, 1978; Tokunaga, 1962; Held, 2002). T2 leg has no TRs but has two longitudinal (proximal–distal) rows of thick and shorter bristles on the ventral side (rows 1 and 8; Hannah-Alava, 1958; Held, 2002).
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Chapter 3 Genotype-Phenotype Mapping. Developmental Biology Confronts the Toolkit Paradox
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The formation of the sex comb—from a cellular perspective—is a complex and dynamic process. In D. melanogaster, the comb rotates almost 90° during development (Held et al., 2004; Tokunaga, 1962). An understanding of the mechanics of this process had to wait for live imaging of sex comb development using a fluorescent marker, which has shown that the rotation involves male-specific convergent extension in the cells surrounding the comb (Atallah et al., 2009a; Tanaka et al., 2009).
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Animal diversity is shaped by the origin and diversification of new morphological structures. Many examples of evolutionary innovations are provided by male-specific traits involved in mating and sexual selection. The origin of new sex-specific characters requires the evolution of new regulatory interactions between sex-determining genes and genes that control spatial patterning and cell differentiation. Here, we show that sex-specific regulation of the HOX gene Sex combs reduced (Scr) is associated with the origin and evolution of the Drosophila sex comb — a novel and rapidly diversifying male-specific organ. In species that primitively lack sex combs, Scr expression shows little spatial modulation, whereas in species that have sex combs, Scr is upregulated in the presumptive sex comb region and is frequently sexually dimorphic. Phylogenetic analysis shows that sex-specific regulation of Scr has been gained and lost multiple times in Drosophila evolution and correlates with convergent origin of similar sex comb morphologies in several independent lineages. Some of these transitions occurred on microevolutionary timescales, indicating that HOX gene expression can evolve with surprising ease. This is the first example of a sex-specific regulation of a HOX gene contributing to the development and evolution of a secondary sexual trait.
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Many studies have shown that morphological diversity among homologous animal structures is generated by the homeotic (Hox) genes. However, the mechanisms through which Hox genes specify particular morphological features are not fully understood. We have addressed this issue by investigating how diverse sensory organ patterns are formed among the legs of the Drosophila melanogaster adult. The Drosophila adult has one pair of legs on each of its three thoracic segments (the T1–T3 segments). Although homologous, legs from different segments have distinct morphological features. Our focus is on the formation of diverse patterns of small mechanosensory bristles or microchaetae (mCs) among the legs. On T2 legs, the mCs are organized into a series of longitudinal rows (L-rows) precisely positioned along the leg circumference. The L-rows are observed on all three pairs of legs, but additional and novel pattern elements are found on T1 and T3 legs. For example, at specific positions on T1 and T3 legs, some mCs are organized into transverse rows (T-rows). Our studies indicate that the T-rows on T1 and T3 legs are established as a result of Hox gene modulation of the pathway for patterning the L-row mC bristles. Our findings suggest that the Hox genes, Sex combs reduced (Scr) and Ultrabithorax (Ubx), establish differential expression of the proneural gene achaete (ac) by modifying expression of the ac prepattern regulator, Delta (Dl), in T1 and T3 legs, respectively. This study identifies Dl as a potential link between Hox genes and the sensory organ patterning hierarchy, providing insight into the connection between Hox gene function and the formation of specific morphological features.

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^☆: Supported by a grant from the National Science Foundation to Curt Stern.

²: Permanent address: Kobe College, Nishinomiya, Japan.

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Developmental Biology

Abstract

References (18)

Boundaries of differentiation of cephalic imaginal discs in Drosophila

J. Exptl. Zool

An induced maternal effect on the stability of the ring-X-chromosome of Drosophila melanogaster

The production of gynandromorphs through the use of unstable ring chromosomes in Drosophila melanogaster

Anat. Record

Non-autonomy of yellow in gynandromorphs of Drosophila melanogaster

J. Exptl. Zool

Environmental factors affecting elimination of the ring X chromosome in Drosophila melanogaster. Z. Induktive Abstammungs-u

Vererbungslehre

Developmental genetics of the posterior legs in Drosophila melanogaster

Genetics

Morphology and chaetotaxy of the legs of Drosophila melanogaster

J. Morphol

The topological distribution of sex chromatin positive nuclei in a 60 mm human foetus exhibiting XY/XXY mosaicism

Genetic analysis of certain problems of the physiology of development of Drosophila melanogaster

Biol. Zhur

Cited by (65)

Sex-specific repression of dachshund is required for Drosophila sex comb development

Planar Polarized Protrusions Break the Symmetry of EGFR Signaling during Drosophila Bract Cell Fate Induction

The three leg imaginal discs of Drosophila: "Vive la différence"

Chapter 3 Genotype-Phenotype Mapping. Developmental Biology Confronts the Toolkit Paradox

Sex-specific expression of a HOX gene associated with rapid morphological evolution

Differential Delta expression underlies the diversity of sensory organ patterns among the legs of the Drosophila adult

Cell lineage and differentiation on the male foreleg of Drosophila melanogaster☆

Abstract

Boundaries of differentiation of cephalic imaginal discs in Drosophila

J. Exptl. Zool

An induced maternal effect on the stability of the ring-X-chromosome of Drosophila melanogaster

The production of gynandromorphs through the use of unstable ring chromosomes in Drosophila melanogaster

Anat. Record

Non-autonomy of yellow in gynandromorphs of Drosophila melanogaster

J. Exptl. Zool

Environmental factors affecting elimination of the ring X chromosome in Drosophila melanogaster. Z. Induktive Abstammungs-u

Vererbungslehre

Developmental genetics of the posterior legs in Drosophila melanogaster

Genetics

Morphology and chaetotaxy of the legs of Drosophila melanogaster

J. Morphol

The topological distribution of sex chromatin positive nuclei in a 60 mm human foetus exhibiting XY/XXY mosaicism

Genetic analysis of certain problems of the physiology of development of Drosophila melanogaster

Biol. Zhur