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The inversion of the dorsoventral axis in the separation
of Bilataria
The basic classification of bilateral animals is based on the comparison of their embryonic
development and was confirmed in modern molecular phylogeny by the analysis of the
relationship of the genes involved. Conserved groups of genes are responsible for the
formation of the body axes. The separation of protostomes and deuterostomes is based on
the inversion of the dorsoventral axis.
The basic division of the majority of the animal kingdom into protostomes and deuterostomes
is one of the most important findings from comparative embryology of the late 19th century.
These bilaterian phyla differ mainly in embryonic development. During gastrulation, the cells
continue to be rearranged to form the archenteron (primitive gut), the open end of which is
called the blastopore. Gastrulation is a process in multicellular animals (with the exception of
sponges) in which mesenchyme cells enter the blastocoel. The cells at the vegetal pole buckle
inwards towards the blastocoel, a narrow pouch is formed by the gastrula's endoderm. The
endoderm of the archenteron fuses with the ectoderm of the blastocoel wall.
Schematic of gastrulation. The primary body opening (vertical arrow) is the blastopore. (Figure: University of
Heidelberg)
The open end of the archenteron is connected with the outside by way of the blastopore. In
protostomes, the blastopore becomes a mouth, and the anus develops at the other end of the
archenteron. [However, this is more complicated in many protosomes: the blastopore is
prolonged to form a shallow dip along the longitudinal axis of the embryo and closes up from
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the middle like a zipper; the mouth at one end and the anus at the other end remain open.]
In deuterostomes, which include humans and our relatives among the chordates, the
echinoderms and other less known phyla, the blastopore becomes the anus (or develops at
least in close vicinity to it) and the mouth develops at the other end of the archenteron.
“Protostome” means “mouth first” while deuterostome means “mouth comes second”.
Dichotomy of bilateria
Since the majority of phyla – with the exception of Porifera (sponges), Cnidaria and Ctenophora
(comb jellies) – can be grouped into protostomes or deuterostomes, it can be assumed that
this is a fundamental, very old distinctive feature. It must have formed before the Cambrian
Era (more than 545 million years ago) when the early representatives of phyla appeared and
which can now be clearly classified as either protostomes or deuterostomes. Unfortunately, no
fossils are available that could provide us with information as to how these two lineages
developed.
Protostomes: Longitudinal cut through the front end of an earthworm (Figure: fsbio-hannover.de)
It was possible to confirm this basic division of the animal kingdom into protostomes and
deuterostomes by modern analyses used in molecular phylogeny. Of course, there were also
some new views: A few invisible candidates – such as Brachiopoda and Bryozoa – which were
often regarded as deuterostomes, now count as protostomes. In terms of the division of major
phyla, the molecular data suggest some radical changes. Previously, scientists thought that
annelids (bristle worms) were related to arthropods due to their segmentation. Nowadays, they
are grouped as Lophotrochozoa, together with molluscs. This classification can be seen as a
late triumph for the classical developmental biologists or embryologists, who suggested a big
similarity between Trochophora larvae and marine annelids and snails. The arthropods (insects,
crayfish, spiders, centipedes, etc.) and other relatives are nowadays grouped as Ecdysozoa
together with the unsegmented nematodes (ring worms like for example the favourite
experimental animal of molecular biologists , Caenorhabditis elegans). They differ from other
phyla because they shed their skin (Greek: Ecdysis) during individual development.
Conserved genes during embryonic development
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Protostomes and deuterostomes together (plus a small group of primitive worms, known as
Acoela or acoelomorphic platyhelminthes, which are nowadays no longer in the group of
protosomic flatworms) are grouped as Bilateria (animals with two sides), which are more or
less symmetric along their longitudinal axis. Their ancestor is a small worm with an end-to-end
digestive tract, with a front and a back end. It is likely that our Precambrian ancestor was such
an inconspicuous worm.
Deuterostomes: Longitudinal cut through amphioxus (Photo: Int. J. Biol. Sci. 2006; 2: 149-160)
One of the most important discoveries of modern evo-devo research (evolution plus
development) is that the embryonic longitudinal axis in animals develops according to the
same principle, i.e. controlled by the Hox genes. The Hox genes were initially discovered in
Drosophila and have a typical sequence of approximately 180 base pairs (homeobox), which
encode a particular DNA-binding region. The proteins encoded by the Hox genes either directly
or indirectly control the transcription of numerous genes, including those that are responsible
for the formation of typical features in the individual embryo segments. Drosophila has eight
Hox genes that are arranged in linear order on the chromosome. Each of the genes is
expressed in particular body segments. It is slightly confusing that these segments do not
correspond with the developing segments of the fly. Scientists found that the same
homologous gene cassette also occurs in other animals, although the number of Hox genes
varies. In the amphioxus lancelet (Branchiostoma lanceolatum), a primitive deuterostome
regarded as a model of the ancestors of vertebrates, there are 10 Hox genes, mice and
humans have 38 arranged in four clusters that developed through duplication.
Inversion of the body axis
The researchers found that a conserved gene cassette controls the development of the
dorsoventral axis in Drosophila. The key gene in this process, dpp, codes for the synthesis of a
protein that activates other genes during early embryogenesis. These genes are responsible for
the development of dorsal structures and which suppress the formation of ventral structures,
including neurogenesis.
Although a homologue of dpp, bmp-4, was found and cloned in frog embryos, scientists did
not find a parallel between insect morphogenesis and vertebrate embryos. Apparently, a clear
and undisguised view was required. In 1994, Detlev Arendt, then a PhD student at the Institute
of Zoology in Freiburg (now head of a group of researchers at EMBL in Heidelberg), and Dr.
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Dr. Detlev Arendt, European Molecular Biology Laboratory in Heidelberg. (Photo: EMBL)
Katharina Nübler-Jung (from Freiburg), published a short paper in which they showed that the
two genes had similar functions, albeit in opposing body regions. They concluded that the body
axis must have been inversed not long after the evolutionary lineages separated from a
common ancestor (“Nature“ 371: 26, 1994; “Development“ 126: 2309-2325, 1999).
In protostomes (for example in Drosophila or earthworms) the central nervous system is
located on the ventral side of the intestine. The blood is pumped from the heart, which is
located on the dorsal side of the intestine, through a main artery, which is also located on the
dorsal side. In deuterostomes (for example amphioxus or vertebrates) it is exactly the opposite:
the central nerve cord is located on the dorsal side of the intestine, while the heart and the
major blood vessels are located on the ventral side of the intestine. Many people regarded the
idea that deuterostomes developed from ancient Bilateria through the conversion of the axis as
extremely heretical. Nowadays, the idea is accepted by the majority of scientists as it has been
confirmed by molecular data.
Artemia salina, a prostome swimming on its back (Photo: Tierreich.de) © Tierreich.de
It is a lot easier to imagine such a conversion rather than imagining that the entire internal
design of the animals had to be changed. In addition, there are living animals that have
become specialised in swimming on their backs and that can be used as models, including the
Notonectidae (backswimmers), a family of water bugs, Artemia salina which is a popular
aquarium fish food, and some fish such as Synodontis nigriventris (upside down catfish).
Assuming that Artemia, which have most likely acquired this behaviour in the recent geological
past, would have millions of years to evolve and adapt to this new way of movement, then what
was formerly the belly would become the back and the ventral nervous system would become
a dorsal one.
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Nothing new under the sun
Back in 1822, decades before Darwin wrote his “Origin of Species”, the French zoologist
Geoffroy St.-Hilaire proposed the controversial hypothesis that vertebrate were upside down
arthropods. He was heavily attacked and mocked by the dominant scientist of the time, George
Cuvier. Now, Geoffroy St.-Hilaire has been rediscovered as the father of modern evolutionary
research (Panchen, A.L. 2001: Ètienne Geoffroy St.-Hilaire: Father of ’evo-devo’?, in: Evolution
and Development 3, 41-46).
'And there is nothing new under the sun. Is there anything of which one can say, “Look! This is
something new”? It was here already, long ago; it was here before our time.’
(Ecclesiastes 1, 9-10 NIV).
Article
21-Feb-2008
EJ
BioRN
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