J[ Zool[ Syst[ Evol[ Research 27 "1999# 038Ð045
Þ 1999\ Blackwell Wissenschafts!Verlag\ Berlin
ISSN 9836!4634
Received on 5 March 1999
Institute of Developmental Biolo`y\ Russian Academy of Sciences\ Moscow\ Russia
Tornaria of hemichordates and other dipleurula!type larvae] a comparison
L[ P[ NEZLIN
Abstract
The evolutionary origin of phylum Chordata is the subject of intensive discussion\ with the most con~icting views prevalent[ One popular theory
advocates the separation of chordates from a dipleurula!like ancestor[ Thus the dipleurula!type larvae "tornaria of enteropneusts\ auricularia and
bipinnaria of echinoderms# are considered to recapitulate the ancestral features and the direct evolutionary path from Echinodermata and
Hemichordata to Chordata "i[e[ Garstang 0783 Zool[ Anzeiger 16\ 011Ð014^ Grobben 0897 Verh[ Zool[!Bot[ Ges[ Wien 47\ 380Ð400^ Dillon 0854
Evolution 08\ 325Ð335^ Jollie 0862 Acta Zool[ "Stockholm# 43\ 70Ð099^ Ivanova!Kazas and Ivanov 0876 Sov[ J[ Mar[ Biol[ 02\ 56Ð79^ Crowther
and Whittaker 0881 J[ Neurophysiol[ 12\ 179Ð181^ Lacalli 0883 Am[ Zool[ 23\ 422Ð430^ Lacalli et al[ 0888 Proc[ R[ Soc[ Biol[ Series B 155\ 0350Ð
0369^ Nielsen 0888 Dev[ Genes Evol[ 198\ 087Ð194#[ Comparison of the nervous system in enteropneust tornariae and echinoderm larvae has
revealed however\ striking di}erences in distribution of biogenic amines and cholinesterase activity[ In tornariae\ monoamine!containing cells
concentrate in the aboral and oesophageal ganglia[ In echinoderms\ they are located along the ciliary bands throughout their length[ The di}erence
in distribution of cholinesterase activity in each group reasonably suggests that acetylcholine!dependent control of locomotion also di}ers[ Our
data do not support the homology of the dipleurula!type larvae[ Therefore we believe in the course of adaptive evolution\ larvae of certain marine
invertebrates acquired a set of common morphological and behavioural characteristics\ yet retained di}erent physiological mechanisms of
behavioural regulation[ Thus\ similarities in the dipleurula!type larvae "tornaria\ auricularia or bipinnaria\ and actinotrocha# may have originated
from convergence rather then from a common dipleurula!type predecessor[ In consequence we must call into question any attempt to trace the
ancestors of Chordata to the dipleurula!type animal[
Key words] actinotrocha Ð dipleurula Ð Enteropneusta Ð larva Ð nervous system Ð pilidium Ð tornaria
Introduction
The evolutionary origin of the phylum Chordata is permanently
the subject of intensive discussion\ and many con~icting views
are held[ The reason for this is the fact that chordates di}er
much from all invertebrate phyla in several principal points\
and no intermediate groups can be found[ One of the main
di}erences is that the ventral nerve cord is characteristic for all
invertebrates\ although the chordates have a dorsal nerve tube
instead[ So all hypotheses have somehow to derive a dorsal
nervous system from the ventral one[ Over the last hundred
years\ hardly one major systematic group could be found that
has not been suggested to be a direct ancestor of chordates[
Thus\ di}erent authors descended chordates from nemertines
"Hubrecht 0772^ Jensen 0852^ Willmer 0863#\ annelids "Dohrn
0764\ see Engelbrecht 0858#\ molluscs "Lo
vtrup 0866#\ arthro!
pods "Patten 0789^ Raw 0859#\ and hemichordates "Bateson
0775^ Grobben 0897^ Livanov 0844^ Je}eries 0875#[ Most of
these theories remain now a matter of historical signi_cance[
However\ the theory separating chordates from a dipleurula!
like ancestor declared by Garstang "0783# has been the most
popular until now[ It was supported and developed by many
authors\ and quite recently\ a large number of papers on this
subject appeared[ The interpretations of Garstang|s theory vary
in detail but are basically similar[ They are all based on the
similarity between the tornaria and echinoderm dipleurula\ and
state that the dipleurula!type larvae "that is tornaria of hemi!
chordates\ or auricularia and bipinnaria of echinoderms# recap!
itulate the ancestral features[ A direct evolutionary path from
echinoderms and hemichordates to chordates is suggested "see]
Dillon 0854^ Jagersten 0861^ Jollie 0862\ 0871^ Ivanova!Kazas
and Ivanov 0876^ Ivanova!Kazas 0878\ 0884\ 0886^ Crowther
and Whittaker 0881^ Lacalli 0883^ Lacalli et al[ 0888^ Nielsen
0888#[
Presented at the Phylogenetic Symposium in Vienna:Austria from
08th to 10st November 0888[
U[S[ Copyright Clearance Center Code Statement]
Thus\ the term {dipleurula| _rst invented by Semon "0777#
for a hypothetical ancestor of echinoderms\ has two di}erent
meanings now[ On the one hand\ dipleurula is the early stage
of star_sh and sea cucumber larval development\ which turns
into bipinnaria in the former\ and auricularia in the latter[ On
the other hand\ based on Garstang|s theory\ larval echinoderms
and tornariae of hemichordates are de_ned as a dipleurula!
type larva to emphasize their close phylogenetic relationships
"Fig[ 0#[
Tornaria is one of two morphologically altered larva of enter!
opneusts\ or acorn worms "Phylum Hemichordata\ Class Enter!
opneusta#[ The word {Tornaria| means {turner| and refers to
the rotating metachronal wave of locomotory cilia in the telo!
troch\ a circumanal band of cilia propelling the animal[ Another
convoluted band collects food particles by a complicated system
of ciliated grooves and carries them to the mouth "for a detailed
description of the tornaria see Barrington 0854^ Had_eld 0864^
Tagawa et al[ 0887a#[
Generally\ tornaria is known to be less primitive then echino!
derm larvae\ otherwise they both have the usual primitive fea!
tures] the development starts from external fertilization\ and
includes holoblastic cleavage\ coeloblastula and gastrulation by
invagination[
The tornaria very closely resembles an early dipleurula:
auricularia larva of echinoderms as summarized by Hyman
"0848^ p[ 086#[
{The ciliated band takes a similar course in the tornaria
and the bipinnaria or auricularia\ although the telotroch is
lacking from all echinoderm larvae[ The digestive tract has
the same shape and the same subdivisions into foregut\ sto!
mach\ and intestine in echinoderm and hemichordate larvae\
and in both the blastopore becomes the larval anus[ The
greatest and most convincing resemblances\ however\ con!
cern the coelomic sacs\ which in both are\ in general\ of
enterocoelous origin|[
More recent studies have also found similarities in the struc!
9836Ð4634:1999:2792Ð9038,04[99:9
049
NEZLIN
Fig[ 0[ The dipleurula theory
derives hemichordates "b#\ hol!
othuroids "c#\ asteroids "d#\ and
echinoids "e# from a common diple!
urula!like ancestor "a#[ Lec!
ithotrophic larvae "f# are considered
to be secondary "from Ivanova!
Kazas 0884#
Fig[ 1[ Diagram illustrating the the!
ory of Garstang "after Garstang
0817#[ In a dipleurula!like larva\
two halves of a ciliated circumoral
band move dorsal "a# to create a
groove between them "b# which
later becomes a neural tube "c#
ture of the ciliary bands "Nielsen 0876#\ nerve cell types "Lacalli
and West 0882#\ nephridia "Ruppert and Balser 0875#\ primary
body cavity "Strathmann 0878#\ mesodermal pattern "Lacalli
0885#\ and food collection mechanisms "Garstang 0828^ Stra!
thmann and Bonar 0865^ Gilmour 0871^ Hart et al[ 0883^ Niel!
sen and Riisgard 0887#[
According to the dipleurula theory by Garstang "0817#\ the
two halves of the ciliary band of the dipleurula!type ancestral
animal moved together into closer parallelism on either side of
the mid!dorsal line to create a groove between them[ The whole
epithelium of the body thus became the former oral _eld[ Then\
the band halves were converted into an enclosed tube of the
kind that forms the chordate nervous system[ Apical sense
organs of the ciliated larva would also be incorporated into the
anterior or brain region or the neural tube "Fig[ 1^ cited after
Crowther and Whittaker 0881^ and Lacalli 0883#[ Recently\ it
has been proposed by Nielsen "0888# that the chordate neural
tube evolved through lateral fusion of a ventral\ post!oral loop
of a ciliary band in a dipleurula larva[
Thus\ the dipleurula!type larvae are considered to be primary
in the life cycles of hemichordates and echinoderms\ and recap!
itulate ancient adults[ If the tornaria is homologous to the
dipleurula\ they have to have common features in the structure
of various systems\ especially those considered to be evolu!
tionarily conservative[ Among them\ the structure of the ner!
vous system and distribution of neurons which express a par!
ticular transmitter phenotype\ is of interest\ since neuro!
transmitter speci_city is known to be highly conservative in
closely related groups "Sakharov 0863#[
On the other hand\ for marine larvae\ there is a profound
morphological convergence in virtually all phyla in the early
stages of larval life\ since they are of similar size and perform
similar functions[ Since the larvae have very precise tasks to
accomplish\ the selective pressure on them may be intense
Tornaria of hemichordates and other dipleurula!type larvae
040
Fig[ 2[ Overview of tornaria of the anchor worm B[ protero`onius "A#^ early bipinnaria of the star_sh Patiria pectinifera "B#^ actinotrocha of the
phoronid Phoronopsis harmeri "C#^ and pilidium of the type Pilidium ma`num "D#[ A\D lateral view^ B\C ventral view^ ab\ aboral organ^ an\ anus^
mo\ mouth opening^ ph\ pre!oral hood^ st\ stomach^ Tel[]\ telotroch^ 09\ tentacles[ Scale bars 099 mm
"Willmer 0889#[ Besides tornaria of enteropneusts and dipleu!
rula of echinoderms\ ciliated bands of similar structure can be
found in other ciliated larvae of marine invertebrates including
actinotrocha of phoronids and pilidium of nemertines^ both of
these being systematically far from the dipleurula type[
Distribution of various neurotransmitters has been described
in detail for echinoderm larvae "Burke 0867\ 0872a\ b^ Nakajima
0876^ Dautov and Nezlin 0889^ Nezlin and Yushin 0883#\ acti!
notrocha "Nezlin 0877^ Hay!Schmidt 0889a\ b#\ and pilidium
"Hay!Schmidt 0889c#[ Unfortunately\ the data for tornaria are
scanty[ Earlier\ catecholamine!containing "CA# neurons and
cholinesterase "ChE# activity was mapped in the tornaria of
Balano`lossus protero`onius "Dautov and Nezlin 0881#[ Below\
we compare the distribution of CA cells and ChE activity in
tornaria\ echinoderm dipleurula\ actinotrocha\ and pilidium
"Fig[ 2#[
Observations and discussion
Tornaria has a barrel!shaped body and two ciliated bands
"Fig[ 2a#[ As described by Lacalli "0883#\ tornaria is similar to
the echinoderm larvae in that {they both lack any sign of an
internal centralized system of ganglia[ They instead have only
ciliary nerves\ and no indication that those have any primitive
association with or derivation from any more centralized
system[ Clearly\ the two groups may have similar types of nerve
cells and subcellular mechanisms\ derived from common ances!
tral cell types|[
However\ according to our data\ as revealed by visualization
of biogenic amines "de la Torre and Surgeon 0865#\ tornaria
has a well!centralized nervous system\ which consists of aboral
and post!oral ganglia[ "Fig[ 3\ see also Dautov and Nezlin 0881#[
Both are aggregations of neurons at the base of the epithelium[
The mid!ventral nerve arises from the post!oral ganglion and
goes posteriorly[ In addition\ there is a ring with several cell
bodies around the border between the stomach and the intes!
tine\ and several cells scattered in the telotroch and the post!
oral part of the ciliated band[ Each cell is linked by a _bre into
the nerve underlying the band[
On the contrary\ in echinoderm dipleurula:bipinnaria:
auricularia "Fig[ 2B#\ catecholaminergic neurons are evenly dis!
tributed along the ciliary bands\ being only slightly denser
around the mouth opening "Fig[ 4\ see also Dautov and Nezlin
0889#[ The di}erences between the tornaria and dipleurula are
profound[ In our view\ the most important among them is
the lack in the latter of] "i# any ganglion!like aggregations of
neurons^ "ii# structures similar to the aboral organ "no con!
centration of neurons\ no apical plate\ no tuft of cilia\ etc[#^ and
"iii# a mid!ventral nerve[ Only at the later stage\ the brachiolaria\
shortly before settlement and metamorphosis\ do aggregations
of neurons appear in several sensory organs at the frontal
extreme of the body[ The mid!ventral nerve in tornaria is in
the agreement with the well!known fact that tornariae have a
ventrally situated\ median\ longitudinal band of cilia which
extends from the mouth in a posterior direction "Jagersten 0861#
and has never been found in any echinoderm larvae[
Histochemical visulization of ChE activity "Koelle and Frie!
denwald 0838# in the two larvae has demonstrated that it is
localized along the ciliated bands in both "Fig[ 5A\B\C#[ Non!
etheless\ in tornaria\ the locomotory telotroch demonstrated no
activity at all\ thus suggesting that locomotion may be not
acetylcholine dependent[ In bipinnaria\ the bands are used for
both locomotion and feeding[ Earlier\ the experiments by Dau!
tov and Semenova "0877# have proved that locomotion is ace!
tylcholine!dependent in echinoderm larvae[ Thus\ the tornaria
di}ers from echinoderm dipleurula in both the topography of
CA cells and cholinergic elements\ and probably in underlying
physiological mechanisms[
Comparison with two other ecologically similar although
phylogenetically distant larval types\ the actinotrocha of pho!
ronids and pilidium of nemertines\ leads to interesting
conclusions[
Phoronids belong to Tentaculata Ð a protostome group that
exhibits characters of both proto! and deuterostomes "Salvini!
Plawen 0871#[ Their larva\ actinotrocha\ has a similar barrel!
shaped body\ pre!oral hood with a well!developed aboral plate\
tentacles to catch food particles\ and telotroch to propel the
animal "Fig[ 2C#[
Distribution of CA cells in the pre!oral hood and tentacles
resembles that in bipinnaria "Fig[ 6\ see also Nezlin 0877^ Hay!
Schmidt 0889a\ b#[ The cells are evenly distributed in the epi!
thelium of the ciliated bands throughout their length[ However\
actinotrocha has a group of CA!ergic cells at the base of the
apical organ\ and a ganglion!like aggregation below the mouth\
that is similar to the tornaria[
041
NEZLIN
Fig[ 3[ Glyoxilic acid!induced ~uorescence of catecholamines in tornaria\ ventral view[ "A#\ aboral gandlion at the base of the apical plate[ "B#\
post!oral ganglion located caudal to the mouth opening "mo# and ventral to the esophagus "es#[ Mid!ventral nerve "arrows# arises from the post!
oral ganglion and goes backward ventral to the stomach "st#[ "C#\ circumintestinal nerve ring "arrowheads# and cells in the telotroch "arrows#^ an\
anus[ "D#\ at higher magni_cation\ these cells are seen to lie in the epithelium of the telotroch "arrows# and send _bres anteriorly[ Scale bars 19 mm
ChE activity "Fig[ 5C# in the actinotrocha was detected along
the ciliated bands\ although the locomotory one\ telotroch gave
a negative reaction that was similar to that in the tornaria[
Pilidium of nemertines "Fig[ 2D#\ the protostomian group\
has CA cells scattered along the ciliated band and around the
mouth\ and a well!developed apical plate although without CA
cell bodies "Fig[ 7\ see also Nezlin 0877^ Hay!Schmidt 0889c#[
Figure 8 summarizes the data for CA cells and ChE activity[
In our opinion\ these results clearly show that tornaria and
dipleurula are not homologous and most probably do not
recapitulate any ancestral features[ The similarities between the
larvae may be a result of morphological convergence[
We do not know if these larvae are primary or secondary[
They probably appeared independently in di}erent groups and
the similarities and di}erences between them could depend on
the peculiarities in their life[
Thus\ tornaria\ bipinnaria\ and actinotrocha settle down
prior to metamorphosis\ and they all have CA cells in the
sensory organs at the anterior end\ which are used to examine
the substrate before settlement[ On the contrary\ pilidium
undergoes metamorphosis in plankton\ which means that it has
no need for speci_c sensory structures[ Accordingly\ its apical
organ is much simpler with no CA cells found[
Tornaria\ actinotrocha and pilidium are propelled by pos!
teriorly positioned ciliated bands\ so they need a rudder and all
of them have an aboral organ with a tuft of cilia at the frontal
extreme[ Echinoderm dipleurula:bipinnaria:auricularia is pro!
pelled by ciliated bands on its arms\ and is known to taxi by
Tornaria of hemichordates and other dipleurula!type larvae
042
Fig[ 4[ Glyoxilic acid induced ~uorescence of catecholamines in bipinnaria of Patiria pectinifera[ "A#\ overview of the dipleurula stage with the
nerve underlying the ciliary bands and neurons scattered along the nerve^ an\ anus^ es\ oesophagus^ mo\ mouth opening^ st\ stomach[ "B#\ apical
region of the bipinnaria with a plexus between the pre!oral "pr# and the post!oral "po# ciliary bands[ No structures similar to the aboral organ
can be found[ "C#\ the same stage\ neuron bodies "arrows# scattered along the double nerve in the post!oral ciliary band[ "D#\ three sites of
concentration of the neurons around the mouth opening "mo# at the brachiolaria stage[ "E#\ Concentration of neurons "arrows# in several apical
sensory structures at the brachiolaria stage[ A\B\E lateral view^ C\D ventral view[ Scale bars] A\E 099 mm^ B 49 mm^ CD 19 mm
Fig[ 5[ Visualization of chol!
inesterase activity in tornaria "A#\
bipinnaria "B# and actinotrocha
"C#^ m\ mouth^ pos\ post!oral ciliary
band^ pre\ pre!oral ciliary band^ tel[
telotroch^ 09\ tentacles[ Scale bars
099 mm
043
Fig[ 6[ Glyoxilic acid!induced ~uorescence of catecholamines in the
anterior part of actinotrocha\ ventral view[ Neurons are located in the
aboral organ "arrow#\ behind the mouth opening "mo#\ and along the
double nerve surrounding the margin of the pre!oral hood "ph#[ Scale
bar 49 mm
NEZLIN
moving the arms[ So\ it has no need in the apical organ until
the settlement approaches[
Bipinnaria and pilidium undergo catastrophic meta!
morphosis\ so the whole larval body degenerates[ The body of
actinotrocha\ at least its central part evolves into the adult
animal[ There is not much knowledge about the metamorphosis
in tornaria\ but it is considered to be noncatastrophic[ All this
corresponds well to the degree of neuron concentration in larval
bodies[
Actually\ there are more data which cast doubt on the hom!
ology between tornaria and dipleurula[ Both Enteropneusta
and Echinodermata possess less specialized larvae of another
type] they are lecithotrophic and ciliated over almost all of the
body[ The lecithotrophic larva of enteropneusts agrees with a
typical tornaria only by a strong ring of cilia at the posterior
end[ No matter what larval type\ planctotrophic or leci!
thotrophic is considered primary and so the telotroch should
be a conservative ancestral feature if the larvae are homologous[
However\ telotroch is nevertheless totally absent in all echino!
derm larvae[
Thus\ the only basic resemblance between the tornaria and
dipleurula\ which can not result from convergence is the coel!
omic sacs[ But this only means that both groups are deut!
erostome since three body regions with characteristic coelomic
compartments are present in all nonchordate deuterostome
phylla] phoronids\ brachiopods\ pterobranchs\ echinoderms\
and enteropneusts[
Recent molecular genetic data on the relationships between
the two groups are very contradictory[ According to the DNA
sequence\ the groups seem to be close "Wada and Satoh 0883^
Halanych!Kenneth 0884#[ On the contrary\ the expression of
some conservative genes shows major di}erences "Arendt and
Nubler!Jung 0883^ Tagawa et al[ 0887b^ Peterson et al[ 0888#[
Unfortunately\ our data only call into question the dipleu!
rula!like chordate predecessor\ and give no evidence on what
the stem ancestor could be[ Was it a bentic animal that under!
went a dorso!ventral inversion "Arendt and Nubler!Jung 0883^
Ruppert et al[ 0888#\ or a type of nonspecialized lecithotrophic
larva as suggested by Salvini!Plawen "0887#< To date\ there is
no data on the structure of the nervous system in hemichordate
lecithotrophic larvae[
To sum up\ the results on the distribution of CA neurons
and ChE activity in the nervous systems of the dipleurula!
type larvae do not support the idea of the homology between
tornaria and echinoderm dipleurula[ The similarities are most
probably the result of convergence\ thus supporting the idea of
Salvini!Plawen "0887# that highly specialized planktotrophic
larvae can not be accepted as a starting evolutionary point[
Thus\ in our opinion\ the popular dipleurula theory does not
re~ect the real phylogenetic relationships between invertebrate
and vertebrate animals[
Zusammenfassung
Tornaria!Larven der Hemichordata und andere Larven des Typs
Dipleurula] ein Vergleich
Fig[ 7[ Glyoxilic acid!induced ~uorescence of catecholamines in the
pilidium\ lateral view[ "A#\ Neuron bodies "arrows# scattered along the
nerve underlying the ciliary band[ "B#\ aboral organ with positive _bres[
Arrow points at the tuft of cilia[ "C#\ cell bodies concentrated around
the mouth opening[ Scale bars 19 mm
Der evolutionare Ursprung des Stammes Chordata wird intensiv diskuti!
ert\ wobei sehr gegensatzliche Au}assungen vorherrschen[ Eine ver!
breitete Theorie vertritt die Meinung\ dass die Abspaltung der Chordata
von einem Dipleurula!artigen Vorfahren erfolgte[ Daher wird ange!
nommen\ dass Larven des Typs Dipleurula "Tornaria der Enterop!
neusta\ Auricularia und Bipinnaria der Echinodermata# die
ursprunglichen Eigenschaften und den direkten evolutionaren Weg von
Echinodermata und Hemichordata zu den Chordata rekapitulieren
Tornaria of hemichordates and other dipleurula!type larvae
044
Fig[ 8[ Schematic diagrams summarizing the distribution of catecholamines "left# and cholinesterase activity "right\ thick gray line# in tornaria "a#\
bipinnaria "b#\ actinotrocha "c#\ and pilidium d#[ Ventral view\ except "d# where both schemes overlap in the lateral projection
"z[B[ Garstang 0783 Zool[ Anzeiger 16\ 011Ð014^ Grobben 0897 Verh[
Zool[!Bot[ Ges[ Wien 47\ 380Ð400^ Dillon 0854 Evolution 08\ 325Ð335^
Jollie 0862 Acta Zool[ "Stockholm# 43\ 70Ð099^ Ivanova!Kazas and
Ivanov 0876 Sov[ J[ Mar[ Biol[ 02\ 56Ð79^ Crowther and Whittaker
0881 J[ Neurophysiol[ 12\ 179Ð181^ Lacalli 0883 Am[ Zool[ 23\ 422Ð
430^ Lacalli et al[ 0888 Proc[ R[ Soc[ Biol[ Series B 155\ 0350Ð0369^
Nielsen 0888 Dev[ Genes Evol[ 198\ 087Ð194#[ Beim Vergleich der
Nervensysteme von Tornaria!Larven der Entereopneusta und Larven
von Echinodermata zeigten sich allerdings erstaunliche Unterschiede in
der Verteilung biogener Amine und der Acetylcholinesterase!Aktivitat[
Bei Tornaria!Larven sind monoaminhaltige Zellen im aboralen und
osophagialen Ganglion konzentriert\ wohingegen diese bei Echinoder!
mata!Larven entlang der gesamten Lange der Cilienbander vorkom!
men[ Die Verteilung der Acetylcholinesterase!Aktivitat in beiden Grup!
pen lasst darauf schlie)en\ dass die Kontrolle der Lokomotion mittels
Acetylcholin ebenfalls unterschiedlich ist[ Unsere Daten sprechen daher
gegen eine Homologie verschiedener Larven vom Dipleurula!Typ[ Sie
fuhren vielmehr zu dem Schluss\ dass bei Larven bestimmter mariner
Invertebraten adaptive Evolution zwar zu einer Reihe gemeinsamer
morphologischer Eigenschaften und Verhaltensformen fuhrte\ jedoch
unterschiedliche physiologische Mechanismen zur Verhaltensregulation
Ý hnlichkeit der Larven vom Dipleurula!Typ
entwickelt wurden[ Die A
konnte vielmehr auf Konvergenz statt auf Abstammung von einem
gemeinsamen Vorfahren des Typs Dipleurula beruhen[ Aus diesem
Grund mussen wir Ansatze in Frage stellen\ die den Vorfahren der
Chordata bei einem Tier vom Dipleurula!Typ suchen[
References
Arendt\ D[^ Nubler!Jung\ K[\ 0883] Inversion of dorsoventral axis<
Nature[ 260\ 15[
Barrington\ E[ J[ W[\ 0854] The Biology of Hemichordata and Pro!
tochordata[ Edinburgh\ London] Oliver + Boyd[
Bateson\ W[\ 0775] The ancestry of the Chordata[ J[ Microsc[ Sci[ 15\
424Ð460[
Burke\ R[ D[\ 0867] The structure of the nervous system of the pluteus
larva of Stron`ylocentrotus droebachiensis[ Cell[ Tissue Res[ 080\ 122Ð
136[
Burke\ R[ D[\ 0872a] Development of the larval nervous system of the
sand dollar Dendraster excentricus[ Cell[ Tissue Res[ 188\ 034Ð043[
Burke\ R[ D[\ 0872b] The structure of the larval nervous system of
Pisaster ochraceus "Echinodermata] asteroidea#[ J[ Morphol[ 067\ 12Ð
14[
Crowther\ R[ J[^ Whittaker\ J[ R[\ 0881] Structure of the caudal neural
tube in an Ascidian larva] vestiges of its possible evolutionary origin
from a ciliated band[ J[ Neurophysiol[ 12\ 179Ð181[
Dautov\ S[ Sh[^ Nezlin\ L[ P[\ 0889] Nervous system and behaviour
during development of star_sh larvae[ Sov[ J[ Developm[ Biol[ 10\
056Ð065[
Dautov\ S[ Sh[^ Nezlin\ L[ P[\ 0881] Nervous system of the tornaria larva
"Hemichordata] Enteropneusta#[ Histochemical and ultrastructural
study[ Biol[ Bull[ 072\ 352Ð364[
Dautov\ S[ Sh[^ Semenova\ M[ M[\ 0877] ðParticipation of cholinergic
system in the regulation of locomotion of star_sh larvaeŁ[ In] D[
Sakharov^ V[ Golubev "eds#\ Prostye Nervnye Sistemy[ Leningrad]
Nauka[ pp[ 70Ð72 "in Russian#[
Dillon\ L[ S[\ 0854] The hydrocoel and the ancestry of the chordates[
Evolution 08\ 325Ð335[
Engelbrecht\ D[\ 0858] The annelid ancestry of the chordates and the
origin of the chordate central nervous system and the notochord[ Z[
Zool[ Syst[ Zvolutionsforsch[ 6\ 07Ð29[
Garstang\ W[\ 0783] Preliminary note on a new theory of the phylogeny
of the Chordata[ Zool[ Anzeiger 16\ 011Ð014[
Garstang\ W[\ 0817] The morphology of the Tunicata and its bearing
on the phylogeny of the Chordata[ J[ Micr[ Sci[ 61\ 40Ð076[
Garstang\ W[\ 0828] Spolia Bermudiana[ II[ The ciliary feeding mech!
anism of Tornaria[ Quart[ J[ Micr[ Sci[ 70\ 236Ð255[
Gilmour\ T[ H[ J[\ 0871] Feeding in tornaria larvae and the development
of gill slits in enteropneust hemichordates[ Can J[ Zool[ 59\ 2909Ð
2919[
Grobben\ K[\ 0897] Die systematische Einteilung des Tierreiches[ Verh[
Zool[!Bot[ Ges[ Wien 47\ 380Ð400[
Had_eld\ M[ G[\ 0864] Hemichordata[ In] Giese\ A[ C[^ Pearse\ J[
S[ "eds#\ Reproduction of Marine Invertebrates[ VII[ New York]
Academic Press[ pp[ 074Ð139[
Halanych!Kenneth\ M[\ 0884] The phylogenetic position of the ptero!
branch hemichordates based on 07S rDNA sequence data[ Mol[
Phylogenetics Evol[ 3\ 61Ð65[
Hart\ M[ W[^ Miller\ R[ L[^ Madin\ L[ P[\ 0883] Form and feeding
mechanism of a living Planctosphaera pela`ica "phylum Hemichor!
data#[ Mar[ Biol[ 019\ 410Ð422[
Hay!Schmidt\ A[\ 0889a] Distribution of catecholamine!containing\
serotonin!like and neuropeptide FMRFamide!like immunoreactive
cells and processes of the nervous system of the actinotroch larva of
Phoronis muelleri "Phoronida#[ Cell Tissue Res[ 148\ 094Ð007[
Hay!Schmidt\ A[\ 0889b] Catecholamine!containing\ serotonin!like\
and FMRFamide!like immunoreactive cells and processes of the
nervous system of the early actinotroch larva of Phoronis van!
couverensis "Phoronida#] distribution and development[ Can[ J[ Zool[
57\ 0414Ð0425[
Hay!Schmidt\ A[\ 0889c] Catecholamine!containing\ serotonin!like and
neuropeptide FMRFamide!like immunoreactive cells and processes
of the nervous system of the pilidium larva "Nemertini#[ Zoo!
morphology 098\ 120Ð133[
Hubrecht\ A[ A[ W[\ 0772] On the ancestral form of the chordate[
Quart[ J[ Micr[ Sci[ 12\ 238Ð256[
Hyman\ L[ H[\ 0848] The Invertebrates\ Vol[ 4] Smaller Coelomate
Groups[ New York] McGraw!Hill[
Ivanova!Kazas\ O[ M[\ 0878] Current state of the problem of the origin
of chordates[ Sov[ J[ Mar[ Biol[ 04\ 112Ð123[
045
Ivanova!Kazas\ O[ M[\ 0884] ðEvolutional EmbryologyŁ[ St!Petersburg]
Nauka "in Russian#[
Ivanova!Kazas\ O[ M[\ 0886] On the ancestry of chordates and Deut!
erostomia as a whole[ Rus[ J[ Mar[ Biol[ 12\ 136Ð143[
Ivanova!Kazas\ O[ M[^ Ivanov\ A[ V[\ 0876] The trochaea theory and
phylogenetic signi_cance of ciliated larvae[ Sov[ J[ Mar[ Biol[ 02\ 56Ð
79[
Jagersten\ G[\ 0861] Evolution of the Metazoan Life Cycle[ London\
New York] Academic Press[
Je}eries\ R[ P[ S[\ 0875] The Ancestry of the Vertebrates[ London]
British Museum "Natural History#[
Jensen\ D[ D[\ 0852] Hoplonemertines\ myxinoids\ and vertebrate
origins[ In] E[ C[ Dougherty "ed#\ The Lower Metazoa[ Berkley\ Los
Angeles] California Press[ pp[ 002Ð015[
Jollie\ M[\ 0862] The origin of the chordates[ Acta Zool[ "Stockholm#
43\ 70Ð099[
Jollie\ M[\ 0871] What are the Calcichordata< Zool[ J[ Linn[ Soc[ 64\
056Ð077[
Koelle\ G[ B[^ Friedenwald\ J[ S[\ 0838] A histochemical method for
localizing cholinesterase activity[ Proc[ Soc[ Exp[ Biol[ Med[ 69\ 506Ð
511[
Lacalli\ T[ C[\ 0883] Apical organs\ epithelial domains\ and the origin
of the chordate central nervous system[ Am[ Zool[ 23\ 422Ð430[
Lacalli\ T[ C[\ 0885] Mesodermal pattern and pattern repeats in the
star_sh bipinnaria larva\ and related patterns in other deuterostome
larvae and chordates[ Phil[ Trans[ R[ Soc[ Lond[ B 240\ 0626Ð0647[
Lacalli\ T[ C[^ West\ J[ E[\ 0882] A distinctive nerve cell type common
to diverse deuterostome larvae] comparative data from echinoderms\
hemichordates and amphioxus[ Acta Zool[ "Stockholm# 63\ 0Ð7[
Lacalli\ T[ C[^ Gilmour\ T[ H[ J[^ Kelly\ S[ J[\ 0888] The oral plexus in
amphioxus larvae] function\ cell types and phylogenetic signi_cance[
Proc[ R[ Soc[ Biol[ Series B 155\ 0350Ð0369[
Livanov\ N[ A[\ 0844] ðEvolutionary Pathways of the Animal WorldŁ[
Moscow] Nauka "in Russian#[
Lo
vtrup\ S[\ 0866] The Phylogeny of Vertebrata[ London\ New York]
John Wiley + Sons[
Nakajima\ Y[\ 0876] Localization of catecholaminergic nerves in larval
echinoderms[ Zool[ Sci[ "Tokyo# 3\ 182Ð188[
Nezlin\ L[ P[\ 0877] ðDevelopment of monoaminergic elements in the
nervous system of actinotrocha\ free!sweeming larvae of Phoronopsis
harmeriŁ[ Zhurn[ Evol[ Biohim[ Fiziol[ 13\ 65Ð79[
Nezlin\ L[ P[^ Yushin\ V[ V[\ 0883] The digestive tract of the ech!
inopluteus of Echinocardium cordatum "Echinodermata\ Echinoida#]
its ultrastructure and innervation[ Can[ J[ Zool[ 61\ 1989Ð1988[
Nielsen\ C[\ 0876] Structure and function of metazoan ciliary bands
and their phylogenetic signi_cance[ Acta Zool[ "Stockholm# 57\ 194Ð
151[
Nielsen\ C[\ 0888] Origin of the chordate central nervous system Ð and
the origin of chordates[ Dev[ Genes Evol[ 198\ 087Ð194[
Nielsen\ C[^ Riisgard\ H[ U[\ 0887] Tentacle structure and _lter!feeding
in Crisia eburnea and other cyclostomatous bryozoans\ with a review
of upstream!collecting mechanisms[ Mar[ Ecol[ Prog[ Ser[ 057\ 052Ð
075[
NEZLIN
Patten\ W[\ 0789] On the origin of vertebrates from arachnids[ Q[ J[
Micr[ Sci[ 20\ 206Ð267[
Peterson\ K[ J[^ Cameron\ R[ A[^ Tagawa\ K[^ Satoh\ N[^ Davidson\ E[
H[\ 0888] A comparative molecular approach to mesodermal pattern
in basal deuterostomes] the expression pattern of Brachyury in the
enteropneust hemichordate Ptychodera ~ava[ Development 015\ 74Ð
84[
Raw\ F[\ 0859] Outline of a theory of origin of the Vertebrata[ J[
Paleontol[ 23\ 386Ð428[
Ruppert\ E[ E[^ Balser\ E[ J[\ 0875] Nephridia in the larvae of hem!
ichordates and echinoderms[ Biol[ Bull[ 060\ 077Ð085[
Ruppert\ E[ E[^ Cameron\ C[ B[^ Frick\ J[ E[\ 0888] Endostyle!like
features of the dorsal epibranchial ridge of an enteropneust and the
hypothesis of dorsal!ventral axis inversion in chordates[ Inv[ Biol[
007\ 191Ð101[
Sakharov\ D[ A[\ 0863] Genealogy of Neurons[ Moscow] Nauka "in
Russian#[
Salvini!Plawen\ L[ V[\ 0871] A paedomorphic origin of oligomaerous
animals< Zool[ Scripta 00\ 66Ð70[
Salvini!Plawen\ L[ V[\ 0887] The urochordate larva and archichordate
organization] chordate origin and anagenesis revisited[ J[ Zool[ Syst[
Evol[ Research 25\ 018Ð034[
Semon\ R[\ 0777] Die Entwicklung der Synapta digitata und Stammge!
schichte der Echinoderm[ Zen[ Ztschr\ Naturwiss[ 11\ 064Ð298[
Strathmann\ R[ R[\ 0878] Existence and functions of a gel _lled primary
body cavity in development of echinoderms and hemichordates[ Biol[
Bull[ 065\ 14Ð20[
Strathmann\ R[ R[^ Bonar\ D[\ 0865] Ciliary feeding of tornaria larvae
of Ptychdera ~ava "Hemichordata] Enteropneusta#[ Mar[ Biol[ 23\
206Ð213[
Tagawa\ K[^ Nishino\ A[^ Humphreys\ T[^ Satoh\ N[\ 0887a] The spawn!
ing and early development of the Hawaiian acorn worm "Hemi!
chordate#\ Ptychodera ~ava[ Zool[ Sci[ "Tokyo# 04\ 74Ð80[
Tagawa\ K[^ Humphreys\ T[^ Satoh\ N[\ 0887b] Novel pattern of Bra!
chyury gene expression in hemichordate embryos[ Mechanisms Dev
64\ 028Ð032[
de la Torre\ J[^ Surgeon\ J[\ 0865] A methodological approach to rapid
and sensitive monoamine ~uorescence using a modi_ed glyoxylic acid
technique] the SPG!method[ Histochemistry 38\ 70Ð82[
Wada\ H[^ Satoh\ N[\ 0883] Details of the evolutionary history from
invertebrates to vertebrates\ as deducted from the sequences of 07S
rDNA[ Proc[ Natl[ Acad[ Sci[ USA 80\ 0790Ð0793[
Willmer\ E[ N[\ 0863] The possible contribution of the nemertines to
the problem of the phylogeny of the protochordates[ In] E[ J[ W[
Barrington\ R[ P[ S[ Je}eries "eds#\ Protochordates[ L[ London\ New
York] Academic Press[ pp[ 208Ð235[
Willmer\ P[\ 0889] Invertebrate Relationships[ Patterns in Animal Evol!
ution[ Cambridge] Cambridge University Press[
Author|s address] Dr L[ P[ Nezlin\ Physiologisches Institut\ Universitat
Gottingen\ Humboldtallee 12\ D!26962 Gottingen\ Germany[ E!mail]
leonÝneuro!physiol[med[uni!goettingen[de