Contributions
The
of dorso-ventral
improbability
axis
29-36
(2002)
The
Hague
evolution,
E.
Biggelaar¹
Edsinger-Gonzales
den
van
& F.R. Schram³
¹,²,
1 Faculty of Biology, Dept, of Experimental Zoology,
Netherlands,
tion,
sity
701
and
e-mail:
e-mail:
[email protected];
34949■
FL
Seaway Drive, Fort Pierce,
Ecosystem Dynamics, University of
schram@science.
Keywords: amphistomy,
uva.
axis
e-mail:
the
in
as
vertebrates,
lution from
that
dorsal,
inversion, deuterostomes,
noted in
in
such
as
same
in
and
ventral.
a
the
result
in
deuterostomes.
in
the
axis
to cells
cells
moving into
what had
of
of
the
In
of the
is
while
the
real
attractive
events
of
In
been
the
the
Amsterdam,
Netherlands,
spiral cleavage, protostomes, gastrulation
Introduction
Basic
position.
developmental
gene
30
Dorso-ventral organization of
A
the
blastopore
32
32
Amphistomy
.,
broader perspective
34
Acknowledgements
35
References
35
as
blasto-
annelids
or
and almost exclusively
In
1822,
with
What
dorsal
of the
and in
migration,
This is
side.
hypothesis
This
a
unified
postulated
formulated the
body plan throughout the
kingdom. Being
animal
a
vertebrate
himself,
he
that all animals would have vertebrae.
In vertebrates, the
vertebrae
internal, whereas
are
the
part
into
and
in invertebrates the “vertebrae”
ternal,
in
embryo
dorsal
more
embryonic ventral
initial
blastopore moving
were
originally dorsal
into
an
cells
to
a
as
as
for instance in
pothesized vertebrae
rings. Thus,
annelids,
antero-
were
said to be
to
are
arthropods
visible
as
where the
ex-
resulting from
hy-
circular cuticular
Geoffroy Saint-Hilaire arthropods,
and vertebrates could be reduced
body plan. However, in
contrast
to
to
the
the verte-
ani-
brates, the dorso-ventral axis of annelids and
cells
crus-
move
fully explains the conservation of
expression patterns
initially dorsally specified
of
coupled
part moving
not extended and the
the
Saint-Hilaire
Geoffroy
uneven
embryo,
uneven
initial anterior-
such
Introduction
same
is bent,
29
embryology
devel-
original antero-posterior
embryonic lateral
larva is
of this
while the
protostomes,
of the
of the
ofthis
developing
ventral
for Biodiver-
move-
body plans of protostomes
less evenly
or
the embryonic
mal-vegetal position.
toa
course of evo-
morphogenetic
the original ventral side
spatially
posterior axis
or
deuterostomes,
extremely
inside
position. Because
ide
deuterostomes,
spatial inversion
a
adult
is extended
more
animal-vegetal
s
the
in deuterostomes
However,
patterns
remains located
posteriorly.
the
Institute
blastopore is formed with exactly
gastropods, the growth
with
of
inverted during the
suggestion ignores
differences in
in gastrulation
limited
1092 AD,
1
the onset ofgastrulation in deuterostomes
protostomes
posterior axis
poie
axis
have
in
proposed
protostomes, i.e., what
a
opmental architecture
versus
first
idea,
embryonic, antero-posterior/dorso-ventral polarity.
Subsequent
ment
old
dorso-ventral
is in protostomes
its simplicity,
the
the
of
has been
embryogenesis. During
as well
[email protected];
Utrecht,
Smithsonian Institu-
nl
the field of developmental genetics
resurrection
early 19th century, that the
such
Smithsonian Marine Station,
Contents
Recent discoveries
to
2
Amsterdam, Mauritskade 57,
Abstract
lead
CH
University of Utrecht, Padualaan 8, 3584
'
J.A.M.
is
animal
during
(1/3)
Publishing bv,
presumed by Geoffroy Saint Hilaire
as
of
inversion
71
Zoology,
to
SPB Academic
a
shift
secondarily ventral
po-
taceans
would have had
to be
what is the dorsal surface
inverted
such that
in deuterostomes is
the
ventral in protostomes.
sition.
The
surprising
between
genes
conservation of
pattern
forming
vertebrates and invertebrates has
recently revived the discussions of the unity of body
plan, including the centuries old idea of dorso-ventral
axis
inversion
Arendt et ah,
(Arendt
2001;
and
Niibler-Jung,
Gerhart, 2001).
1997;
JAM.
30
Basic
embryology
In the
great majority
trical
animals,
van
den
Biggelaar
etal
-
Improbable dorso-ventral
hemisphere contribute
the central
etal
the
of the
blastulae
polarity. Generally,
to the
where the
pole
cells of the animal
thelial
living, bilaterally
have
the animal
polar
an
are
hemisphere form
animal-veg-
covering of the future adult (cf.
whereas the cells of the
ah, 2001),
pole
way
formed. The
the
Henry
opposite
be
et
inside the
move
in which
self is
epi-
outer
and the
inversion
development of
mesoderm.
During gastrulation the cells around the vegetal
symme-
pole corresponds
bodies
gut tube
to the
axis
gastrulation
common
assumed
embryo.
that evolution
in the
that
gastrulation
1
A) into
a
changed
a
ing, the blastopore,
at
the
can
embryos of the
bipolar
bipolar gastrula (Fig.
it-
gastrulation
occurs,
to almost all animals. Thus, it
ancestors of the bilaterians resulted in
veg-
of the
Irrespective
a
process
blastula
1B) with
one
of
(Fig.
open-
vegetal pole. This blas-
topore opening persists and
can
the formation of the mouth,
function either in
the anus,
or
both,
or
neither.
In the
at
the
the
Deuterostomata,
1A) and is transformed into
Tagawa
I. Median
Fig.
oriented
with
sections
with
of
gastmlae
anterior-posterior
doro-ventral axis
initiation
of
from
top
axis
in
amphioxus;
from left to
to bottom.
A,
that
will
right
become
B. advanced
the anus.
at the
dorsal blastopore lip
presumptive chorda-mesoderm. (Modified
from
as
2.
be
to
other
hand,
the
In
3C)
anus
(Fig. IB) (cf.
a
In
protostomes
Blastula
in
of 32-cell
A.
stage
(Modified
in
Patella
from van den
the
the
anterior mouth open-
due to rotation
from
the posterior
near
end of the
Nelsen,
vulgata prior
on
initially posterior blastopore (Fig.
embryo
to
an
anterior-ventral
position.
One way to achieve this rotation involves
indicated
mouth
secondarily towards the
embryo.
2B) eventually becomes
the
the
deuterostomes,
formed
anterior end of the
the
1953).
Fig.
ah, 2001).
opening has
are
gastrula
Note
et
ing (Fig.
position ofneurogenic ectoderm
the
anad
Young gastrula with
blastopore formation beginning.
posterior blastopore
sections
blastopore is formed
vegetal (posterior) pole of the embryo (Fig.
to the
Biggelaar, 1977;
initiation
van
den
of
gastrulation.
Biggelaar
and
A.
vegetal
view.
Guerrier, 1979).
B. median-section
a com-
of same
Contributions
Fig-
3.
ventral
of cell
view.
2d, which
B.
plex series of
1997).
ages
The
over
dorsal
cell
and
the
course
the
migration
Iyy
ar|d
dorsal
2002
of
24-28 hour
trochophore
32-cell
deduced
stage
from A
(Damen and Dictus,
of
cell lin-
blastopore
gastrulation
such that
are
internalization of
an
lineages and
of the
31
in the
position
median-section
there is
spatially replace
a
corresponding
D-quadrant
them. The
midline line-
more
lateral A-
lineages of the blastopore lip pull
migrate dorsally
to
occupy
what had been
D-quadrant midline.
Fhe specifics
eral
-
post gastrulation,
a
spatial dynamics
C-quadrant
away,
(1/3)
movements
midline
ages to
of
has
view. C.
least in
spiralians
external
71
Zoology,
Schematic drawings
progeny
at
to
steps and
can
of these
be
v
entrally
from
of the
migrations
clearly
dciivatives
of cells
their
seen
2d grow
(Fig.
(in part),
eternally (Figs. 2B, 3C),
involve
in Patella
original
embryo
2b
and
larva of Patella
shown
B.
(A
in
Fig. 2,
vulgata.
has
Cell
attained
and B modified
a
lineages marked.
ventral
from Damen
sev-
(Damen,
posteriorly
position
3A, C).
on
the
Second,
3a, and 3b
move
and another part of the
position in
and
2b
lineage
3).
Third, the derivatives of the
moves
Dictus,
Note
the
that the
A.
larva.
1997).
laterally and dorsally (Figs. 2B,
macromeres
move
internally (Figs. 2, 3C). Thus, the ventral midline
itself of
and
spiralians, which separates the stomodeum
is
anus,
age, located
quadrant,
derived
specifically from the 2d lineat the
initially
midline of the
of these movements,
tain
an
anterior
the
ventral
Wilson,
1892;
reveals that
general
cases,
blastopore
pore
the
by
across
1967;
morphogenetic
feature of
some
spiralian
migrates
to
90
an
a
As
a
comes
D-
result
to
at-
position. Examination of
Akesson,
this results in
tal axis
embryonic dorsal,
blastopore lip.
published cell lineage work
4). First, derivations of cell
dorsal side
as
the
Spiralia (cf.
Anderson,
transformations
development.
In
1966)
are
a
most
bending of the animal-vege-
degrees,
as
the
antero-ventral
B-quadrant midline.
In
vegetal blastoposition
along
embryos of the oligocha-
JAM.
32
Tubifex (Penners
cte
and of the
1999) the cells of the ventral
(Stent,
also derived from the
Dorso-ventral
the
organization of
a
bilateral symmetry with
mental
architecture,
antero-posterior,
by extension
termed
1982)
nerve
cord
are
a
blastopore
gastrulae already
tri-axial
develop-
embryonic
dorso-ventral
axes,
could infer that in the metazoan
ground pattern the gastrula also might have had
three
embryonic
This
axes.
of such
opore
a
onic dorsal,
ventral, and
a
dorsal
it has
means
that
lateral
two
the
an
as
is
same
It is
nelids, the cells of
also have
Second,
stome
the
MAPK
in
blastopore
the
the
Third,
cells
a
Brachyury
around the
annelid
blastopore, i.e., in
blastopore
stomes
in both
indicates
protostomes and
the
in
is
animals
the dorsal
(2001)
gene is first
have
expressed
blastopore
expression
protostomian
rostomian
vulgata,
the
macromere
strong and homologous
the
all
Platynereis dumerilii.
on
the
a
spatial
polarity of
similarity
of
deuterostomes. The inversion of
of dorso-ventral
embryos
embryos is
in
a
patterning
genes in
comparison with deuteresult
this
of differences
in
an
alterna-
openings
particular mode of gastrulation,
cells
on
sition. The lateral
two
openings:
the
mouth,
come
an
and
the “dorsal”
the
gastrula relocates
blastopore
lips
side of the
to
aperture
a
leaving
that will become
the
blastopore de-
velops into both anal and mouth openings.
is
amphistomy
an
often
Nielsen &
opore, and the
(Arendt and Niibler-Jung,
1997).
lips of the blast-
formation of the ventral midline
the fused lateral
lips,
as
described by Nielsen
originated from descriptions
an
Norrevang, 1985),
invoked in molecular considerations
The idea of fusion of the lateral
ment of an
of the
onychophoran,
early develop-
Peripatopsis (Manton,
Pontonema
(Malakhov,
arthropod, Lucilia (Davis,
(2002) also
assume
an
1967).
by
(2001)
annelid, Polygordius (Woltereck,
nematode,
Such
feature of the Trochea
integral
Theory (Nielsen, 2001;
early
“ventral” po-
opening that will be-
posterior
Under this scenario,
anus.
exten-
then said to fuse
are
anterior
a
of axis inversion
deuterostomes and proto-
initial
In
In
Brachyury
development
as
of two
during gastrulation has not yet been considered (Fig.
and is
Fig. 2B). Such
dorso-ventral
discussion, amphistomy
of
dorsal side of the
3D (cf.
early
the adult.
tive method for the
sion of the
proto-
Lartillot et al. (2002) have demonstrated
first expressed
note
Nelsen, 1953).
Amphistomy
in
Brachyury
gene
closing
that in the mollusc, Patella
gene is
into
5).
involved in
Arendt et al.
Recently,
embryo of the
addition,
embryo
al, 1978).
lip and in the elongation of the poste-
axis.
vegetal
as
is
mesoderm formation in
demonstrated that
in
well
2001), especially evident
(Technau,
body
as
expression
et
pathway of the organizer (Lambert
2001).
Nagy,
an-
lip of the blastopore
in both deuterostome
embryos,
involved
rior
the dorsal
organizer function (Guerrier
an
signaling
and
molluscs and
as
from
movements that transform the
morphogenetic
In the above
such
(Modified
are
relevant.
First, in protostomes,
of gastrulation in the amphibian embryo,
of Spemann’s organizer.
However
that in proto-
Several observations
true.
position
organizer, the
an
sufficiently recognized
been
the
4. Initiation
Fig.
embry-
“lips.”
Spemann’s organizer (Fig. 4).
not
blast-
least in chordates the
at
blastopore lip functions
stomes
that
creature must have had
generally recognized
so-called
axis inversion
Biggelaar- Improbable dorso-ventral
Theremyzon
here the
left-right,
one
den
dorsal cell 2d.
originally
in most recent animals the
Since
have
1924; Shimizu,
1922,
leeches Helobdella and
van
1994),
1904),
1949),
and
Lartillot
et
a
an
al.
amphistomous gastrulation
in the mollusc Patella. We
suggest that the amphis-
derives
tomy hypothesis mistakenly
the
protostome
Contributions
F
'g.
5.
to
Amphistomy.
anterior part
v
1
cage
to
mouth.
separate
up
occurs
(1/3)
of
2002
-
stages
to
gastrulation
33
of the
(Modified
stomoproctodeal
midline from cell
blastopore
What
lng
a
71
sequence
into
migration leading
cntial
e
A.
develops
“‘astopore closes,
U1
Zoology,
in
annelid, Polygordius
from
slit
Nielsen, 2001),
opens
of
in annelids? In
gastrulation.
position
at the
4a and 4c
grow
a
ustopore. The lateral micromeres
of
from
posterior aspect
Manton, 1949).
blastopore closes, only
C.
have
come
to
will persist
opening
as
note
that
as
in
cell
means
the
stages
an
hourglass. Af-
touch each other, the
blastopore is effectively divided into
The anterior
of
(Fig. 5A), by which
achieves the form of
both cells
moseleyi,
sequence
Schierenberg, 1997).
towards each other
ter
of
stages of Peripatopsis
from
blastopore
Polygordius, accord-
micromeres 4a-4d have
that
note
Caenorhabditis elegans (Modified
Woltereck (1904), the four cells of the fourth
quartet of
sp.,
sequence
anteriorly (Modified
lineages forming lips of
at the onset
B.
two
openings.
becomes the prostoma, which
the mouth
opening
to the
separately
34
J.A.M.
Wol-
developing midgut. Then, curiously enough,
tereck
states that the
explicitly
posterior
within
later
5A). Only
amongst
appear
completely
ess
does the actual
on
derivatives
with
corresponds
above for Patella. Instead of
and anus, the
the
velops
of
blastopore
anal
2d.
of cell
giving
ogy
the
only de-
an
on
an
in Peripatopsis.
The
of
study
blastopore
and out
germinal disc
from this
in the diversification of life.
original
Manton
embryol-
develops
level of
highly disparate
genes
sog/chordin
dcnn
5B). This
the neural midline
is closed, and
or
opening
appears
opening
separate, slightly
a
later
during development,
mo-proctodeal slit. This in
anterior
verge
turn
and
fuse
leaving
dence that these
anterior and
the
an
There is
no
a
hard evi-
as
an
that
appears
example (Schierenberg,
prior
postero-dorsal
to
gastrulation the
and the
D
cell
a
1973).
1997),
C
cell
has
D
to
the
posterior pole
ventral
lineage
sal
direction. So, also in
position prior
an
a
nematode
one
can
original exclusively dor-
gastrulation
to
move
and then continue in antero-
observe that cells with
at the
a
moves
antero-ventral ly whereas part of the C progeny
later
can
be found
and
despite potential
the ultimate fate of the
tostome
lineages,
a
blastopore
differences in
in different pro-
closer examination
of
mor-
phogenesis in protostomes reveals that the ventral
midline of the adult is derived from cells with
initially
dorsal
or
inversion of the
terians
can
dorso-lateral
been used
to resur-
position.
dorsal-ventral axis
in
adult bila-
be attributed to differences in
genetic transformation
of
embryo
morpho-
to adult.
dorso-
nerve
cords
has lead
to
inversion of axial-de-
of
as
the ventral
versus
protostomes
circular
arguments
and ancestry
homology
comparative
a
con-
between dis-
parate body plans.
caution is
we
called
hypotheses.
The
expressions
on
vorced issues of
for
firmly believe that
in
considering
is
a
developmental
ting edge,” where
to
radical
genes have
di-
developmental genetics from critical
manifestation of the
development
extreme
such
proponents of axis inversion based
of
embryological cell lineage
“new
work.
Perhaps in part
phenomenon
and modern” research
gets carried
away
in
it
of the “cut-
its
in
enthusiasm
supplant “old and staid” studies of embryology.
have
inversion
Saint-Hilaire:
of
the mistake
repeated
much
too
phases of development
attention is
Geoffrey
paid
at the expense
of axis
of
to
later
ignoring
information from the earliest stages of ontogeny.
Though
an
Thus the
proto-
(Wilkins, 2002), and
Whatever the reason, modern proponents
ventral side.
Collectively,
axial
patterning
protostome-deuterostome
a
Nevertheless,
it
posterior position
(Fig. 5C). During gastrulation the
cerning
well-recog-
network in
gene
structures between taxa, such
dorsal
al., 2000).
et
now
dorsal-ventral axis of
genetic network has
deuterostomes,
take Caenor-
we
or
perspective, the topological
versus
instance,
For
(Gauchat,
deuterostomes
idea of
previously
presumed inversion of the
dpp/bmp-4
versus
this neural
rect the
fining
mirrored
situation that is
stomes
in
genes
patterning the primary adult
ventral axis inversion. However, from
con-
openings correspond with the
two
happens in nematodes? If
What
an
anterior stomodeal and
great number of arthropods (cf. Anderson,
habditis
sto-
elongates along
posterior openings of the former blas-
topore. This indeed is
a
anterior
posterior axis while the lateral lips
posterior proctodeal opening.
in
more
in
nized conservation but
-
a
body plans.
Within the Bilateria there is the
proliferate
(Fig.
suggested
eumetazoans
across
developmental
homologous
evidence for the conserved uti-
beneath the ectoderm to form the endothen begins to shrink,
has
to
axes
homology between otherwise
and
axes
increasing
lization of Hox
body axis
on
cells
opening,
related taxa
distantly
The
body plans.
and function of
expression
Fundamental
and evolution of the adult
homology
between animal
unrecognized
stage.
extensive
tery
highly divergent adult body plans
the Eumetazoa is the great, unsolved mys-
across
there is
happens in the onychophorans?
carried
(1949)
described
Polygordius
at the blastula
inversion
perspective
The evolution of
this is the
and the ventral midline is devel-
mouth,
position
What
opening
rise to mouth
oped from derivatives of cell 2d that had
dorsal
(Fig.
This proc-
that
axis
opening
short time
a
Improbable dorso-ventral
A broader
does not become the anus! Rather, that part of the
blastopore opening closes
-
den Biggelaar
van
is
indeed
the conservation of
particularly
and dissimilarities
pretation of
these
developmental
striking, given
of bilaterian
the
genes
diversity
body plans,
inter-
expression patterns requires that
they be tempered within
an
operant framework of
Contributions to
71
Zoology,
(1/3)
multiple alternative hypotheses.
in
attractive
to its
gards
its
and
simplicity
2002
-
35
while
Inversion,
compelling
in
the
mosquito
possibility.
one
sericata.
Cell
lineage studies
that
suggests
of earliest
of micromere derivatives
alternative
as
an
for dichotomous
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