Development 113, 419-430 (1991)
Printed in Great Britain © The Company of Biologists Limited 1991
419
Segmentation gene expression in the housefly Musca domestica
RALF SOMMER* and DIETHARD TAUTZ*
Institut fiir Genctik and Mikrobiologie, Umvcrsittit MUnchen, Mana-Wardstrasse la, 8000 MUnchen 19, FRG
•Present address: Institut fllr Zoologie, UniversitSt MUnchen, Luisenstr. 14, 8000 MUnchen 2, FRG
Summary
Drosophila and Musca both belong to the group of higher
dipteran flies and show morphologically a very similar
early development. However, these two species are
evolutionary separated by at least 100 million years.
This presents the opportunity for a comparative analysis
of segmentation gene expression across a large evolution-
ary distance in a very similar embryonic background.
We have analysed in detail the early expression of the
maternal gene bicoid, the gap genes hunchback, Kriippel,
knirps and tailless, the pair-rule gene hairy, the segment-
polarity gene engrailed and the homoeotic gene Ultra-
bithorax. We show that the primary expression domains
of these genes are conserved, while some secondary
expression aspects have diverged. Most notable is the
finding of hunchback expression in 11-13 stripes shortly
before gastrulation, as well as a delayed expression of
terminal domains of various genes. We conclude that the
early developmental gene hierarchy, as it has been
defined in Drosophila, is evolutionary conserved in
Musca domestica.
Key words: Musca domestica, development, segmentation
gene evolution.
Introduction
Extensive genetic and molecular studies have led to a
detailed insight into the processes underlying pattern
formation in Drosophila (reviewed by Ingham, 1988).
Segmentation of the Drosophila embryo depends on
the successive activities of several classes of genes. On
top of the hierarchy are the maternal genes, which
provide the positional information for the expression of
the zygotic gap genes. The gap genes in turn regulate
the expression of the pair-rule and segment-polarity
genes, which eventually subdivide the embryo into its
segmental units. The segmental units are then specified
by the homoeotic genes.
The genes involved in the segmentation process in
Drosophila have been identified on a functional basis in
appropriate mutagenesis screens. Cloning and ex-
pression analysis of these genes has yielded a very
detailed understanding of the molecular interactions
involved in the early pattern formation process in
Drosophila. It is, therefore, now of great interest to
ask, whether these molecular interactions have been
conserved in evolution. However, it seems unreason-
able to perform a similar extensive genetic screen, as in
Drosophila, for any other insect system. Instead, it
should be possible to make these inferences on the basis
of the expression analysis of the homologous genes in
other species. This requires, first, to find the homolo-
gous genes and, second, to assume that they have
homologous functions. Such an assumption can be
tested, if the first step in the analysis is the comparison
of the expression of homologous genes in a species that
shows a homologous embryonic development.
We have therefore compared the expression domains
of several key genes of the segmentation gene hierarchy
of the two higher dipteran fly species Drosophila and
Musca. Though the two species are evolutionary
separated by probably at least 100 million years
(Hennig, 1981), the morphology and the early embry-
ology of the higher dipterans are very similar (Weis-
mann, 1866). The only difference so far detected is the
mitosis behavior of the blastoderm nuclei (Lundquist,
1981; Sommer and Tautz, 1991), which is most likely not
related to the segmentation process (van der Meer et al.
1982). One could expect that the molecular mechanisms
that lead to the segmentation of the embryo should be
conserved. On the other hand, a divergence of the
primary segmentation gene expression pattern seems
also a theoretical possibility. We know that redundant
segmentation pathways exist in Drosophila (Hiilskamp
and Tautz, 1991) and one could, therefore, imagine that
these are subject to modification during evolution. One
particular function of a gene could for example be lost
in favor of the redundant function of another gene and
one would then expect a diverged expression pattern of
the respective genes. We believe that it is important to
test the assumption of homologous segmentation gene
expression in a homologous embryonic background.
A recurrent feature of most of the segmentation
genes in Drosophila is that they are not only involved in