Table Of Content©Paleontological Research, vol.1, no.1, pp.1-14, 7Figs., April 30, 1997
by the Palaeontological Society of Japan
Origin of high-rank groups of organisms
1.
JAN BERGSTRÖM
Swedish Museum of Natural History, Box 50007, S-104 05 Stockholm, Sweden
Received 16 December 1996 Revised manuscript accepted 23 February 1997
;
Abstract It is outlined howseeminglyfundamental differences between high-level groups such as phyla
and classes may have been introduced in fairly simple and rapid ways. Examples of such ways are
development of endosymbiosis, heterochrony involving change of adult mode of feeding with associated
changes of basic life habits and body plan, development of asymmetry, and turning upside-down. The
lattermodification hasresulted infundamental misinterpretationsofso-calleddeuterostomes(ornotoneur-
alians). The basal deuterostomes, the hemichordates, are much more similarto protostomesthan text-
bookauthorshavebeenwillingtoadmit Infact itisdifficultto understandwhytheyareatallconsidered
asdeuterostomes. Forinstance, protostomecharacteristicsfound inhemichordatesincludeamainnerve
cord on the ventral side, a circum oesophageal nerve ring, a larva surprisingly similar to a protostome
trochophora, blood circulation in the same direction as in protostomes, and (in all pterobranchians and
many enteropneusts) schizocoelic formation of the coelom. New consideration of morphologies and life
postures indicates that deuterostomes (notoneuralians) are not upside-down compared with protostomes
(gastroneuralians). Instead, it is vertebrates that are upside-down compared with all other animals,
including otherdeuterostomes. Fossilsvery poorly revealthechanges in body plans, butatleastindicate
that in general these changes are of (at least) Cambrian age. The oldest known group with vertebrate-
type orientation is the conodonts.
Key words: Body plan, deuterostomes, evolution, heterochrony, macroevolution
Introduction any prolonged formative period. There is rather reason to
believe that transitions were very swift, as in the Cambrian
Attempts to trace in the fossil record evolutionary steps radiation event.
leading to newmajorgroupsoforganisms usually have been Itcan be mentioned that molecular differences have been
in vain. New classes, phyla and divisions tend to occur used to indicate an original radiation of coelomate animals
abruptly, with an appreciable internal diversity virtually from 1,200 million years ago (Wray et al. 1996). This estimation
the beginning. This is the characteristic result of the was based on extrapolation backwards of Phanerozoic
Cambrian fossil explosion (or biotic radiation), in which many evolutionary rates. However, when time for earlier splits,
of our extant animal phyla and classes made their first including that between eubacteria and archaebacteria, is
appearance (even though their lineages may have been allowed for, the age ofthe same radiation is estimated to be
present earlier, represented by animals with an older body 'only' 670 million years (Doolittle et al. 1966).
plan). It is also characteristic of many later radiations, for Progress in the fields of endosymbiosis, ontogeny with
instance of flowering plants in the Early Cretaceous and of heterochrony, and molecular genetics has revealed evolu-
placental mammals in the Late Cretaceous and Early Terti- tionary processeswhich may lead—and apparently have led
ary. The common occurrence of such geologically sudden —to the development of new body plans, i.e., new funda-
appearances and radiations has seldom been taken atface mental designs. The interesting thing is that very little of
value. Instead, there hasbeenatendencyto postulate long genetic modification is needed—no macromutation or hope-
preceding intervals with successive slow evolution of group ful monster—and that the processes may be completed
characters. Thus, the rise of a high-rank group has been virtually instantaneously on the geological time scale. It
seen as a long series ofadditions of lower-rank groups until should be noted that lineages leading to extant phyla may
the necessary anatomical and morphological changes have have been separated well in advance ofthe appearances of
been performed. When classes and phyla form in this way new body plans. Fossils and molecules therefore may
it will conceivably be a matter of hundreds of millions of indicate different dates for the origins of groups.
years. Thiscan beexemplified bythetransitionfromtypical This contribution will concentrate on deuterostomes after
reptiles to full-fledged mammals, which took some 200 a short look at other organisms. The suggested modes of
million years. In many cases, however, there is no sign of group origination are only examples.
Jan Bergström
Endosymbiosis time, perhaps even 1000 years or less.
Twogroupsare particularly instructive in thisregard. The
It now appears to be generally accepted textbook knowl- first of them is the Endoprocta (Figure 1). An endoproct is
edgethat mosteukaryotic cellscontain modified bacteriaas virtuallyatrochophora larvaonastalk. Theonlycharacters
endosymbiotic organelles (cf. for instance Margulis 1970 in an endoproctthat do notfit into such a larvaarethestalk
;
Taylor 1980,1994). One interesting category of endosym- attachment and the reproduction ability(for instance Hyman
bionts is the coloured plastids, including the chloroplasts, 1951). Thus, we can easily believe that paedomorphic
which obviously stem from coloured bacteria. It is quite heterochrony made its adult characters unlike that of any
clear that such coloured bacteria have come to form en- other group, and particularly unlike that of the immediate
dosymbionts not only once, but several times. The host ancestor, thus creating endoprocts as a discrete phylum.
organisms were protozoans. Thus there has been a Since the endoproct characters are those of coelomate
repeated transition between two of the kingdoms that have larvae, endoprocts are coelomates by affinity (although not
been recognized of old : the Animalia and the Plantae, or in by construction), not pseudocoelomates. This isalso borne
somewhat newerterms, the Protozoaand theAlgae. It has out by the pattern of egg cleavage, which is most similar to
been suggested thatthe chloroplastsofred algaestemfrom that of annelids and similar animals.
cyanophytes, those of green algae and land plants from The second instructive group is the Phoronida (for
prochlorophytes. There even seem to be cases where a instance Hyman 1959). Phoronid larvae are typical
protozoan hasturned into an alga not byengulfing acolour- coelomate planktic larvae with three transverse bands of
ed bacterium, but a eukaryotic alga. The result is some- cilia. One of the bands develops tentacles in the larva
thing like a biological Russian doll, with the largest cell already before it settles on the sea bottom, and the adult
engulfingsmallercellswhich inturn hadengulfedstillsmaller tentacles developfrom the same ciliary band. This demon-
cells. One such group of complex organisms are the stratesthe continuity in equipmentand feeding methodfrom
cryptomonads (Ludwig and Gibbs1985; Douglasetal. 1991). larva to adult.
The endosymbiotic phenomenon could not have been Endoprocts and phoronids differ fundamentally in detail.
detected on fossil material by palaeontologists. The strati- For instance, the tentacles develop from a preoral ciliary
graphic control on its origination is vague at most, but most band,the prototroch, in endoprocts,butfromapostoral band,
endosymbiosisevents presumablytookplace inthe Precam- the metatroch, in phoronids. The message is the same,
brian. however afundamentally newanimal, anewphylum, could
:
be shaped by simple heterochrony.
Heterochronic origins of animal phyla
Twisting
In many marine coelomates the larva and adult lead two
entirelydifferentmodesof life. Whereastheadultisbenthic Another class of processes leading to new groups is
and mayhaveoneortheothermodeoffeedingand locomo- twisting, that is, deformation of the body symmetry. The
tion, the larva is pelagic and swimsandfeedswith theaid of gastropods provide an interesting example of this simple
cilia. Also many adult coelomates use cilia for feeding. change behind high-level taxonomic separation (Peel 1987,
Some of these collect their food directly from the water. pp.305-306). The diagnostic difference between gas-
Brachiopods, bryozoans, phoronids, endoprocts and ptero- tropods and their ancestors, the monoplacophorans, is that
branchians (graptolites) are typical examples, with cilia situ- the latter are bilaterally symmetrical, whereas in the former
ated on tentacles. Others collect at least part oftheirfood the shell with its enclosed soft-parts is rotated 180° on the
from the sediment surface, although again with their cilia. foot. The evolutionary process isechoed in theembryology
In this category we find sipunculids, among others. of the individual gastropod : the small larva is symmetrical,
The question now is how these animals have developed but at one stage the rotational torsion starts. It can start
their adult mode of feeding. We can first note that the suddenly and be completed within minutes. Maybe it is a
tentaculated ciliaryfeeders belong tothe mostderived (most mechanical instability that causes the torsion, and did so
highly developed) of the three groups or levels of bilaterian when it was evolutionary invented. The torsion gives
animals, the three being acoelomates, pseudocoelomates gastropods a great advantage compared with monoplaco-
and coelomates. Thereforethere is everyreasonto believe phorans: the mantlecavityisshifted anteriorlyandgivesthe
thattentaculate ciliary feeding is a derived mode offeeding animal the possibility to hide inside its shell.
in adult bilaterian animals. Modern echinoderms, and even most fossil ones, have a
One way to develop ciliary feeding in adults with ciliary- nice pentameric symmetry. Their larvae are bilaterallysym-
feeding larvae certainlywould be by heterochronic retention metrical. Certainlytheirancestorsweresymmetrical alsoas
of such feeding into the adult (Figure1). Since hetero- adults. There is general agreement that pentameric sym-
chronic changes by themselves need to involve only minor metrywas reached viaastagewith asymmetrydistorting the
genetic changes, they can reasonably occur in very short ancestral bilateral asymmetry. This is so during ontogeny,
time. Logically, therefore, a shift to tentacle-feeding from and we know of many asymmetric forms from the Palae-
grazing, mud-eating or hunting could lead to a tentaculate ozoic. Some ofthem reclined on theirsides on the bottom.
phylum from something fundamentally different within a This isthecasewiththe carpoids'. Itispossible,even most
million years, and presumably within a very much shorter probable, that the forms leading to pentameric echinoderms
Origin of high-rank groups of organisms
original adult
^%^^^m^Mm^^
. creeping larva
egg
original life
cycle
swimming
larva
larva
attaches
to substrate
Figure1. Endoprocta as an example of possible origination of new phyla by heterochrony. The original life cycle is
supposed to have had an adultwith features offlatworms, molluscsand several typesofmarine larvae. By prolonging the
larval typeoffeeding intotheadulttherewould have beenaneedtoextendtheciliarybandalongtentaclestoenhancethe
efficiency. Asessilemodeoflifewouldbeoptimal. Itiseasytounderstandthattheshiftfromtheprimarytothesecondary
lifecyclewouldbefairlyabrupt, andthatthefunctionaland morphological changesinvolvedwouldremodeltheadultsothat
relationships would be obscured-and so a new phylum would be born.
Jan Bergström
were attached. 'Carpoids', including 'calcichordates', being thatzoologists havebeen completelymisled in producingour
asymmetric recliners, may therefore represent blind ends in current view of the differences between protostomes and
evolution. In any case, echinoderms provide still another deuterostomes.
exampleofnewbodyplanscreated bysmallmeans, presum- The new understanding of how a vertebrate must be
ably with little genetic change and in short time. oriented in orderto becorrectlycompared with aprotostome
has prompted an attempt to see what this implies for other
Deuterostomes (notoneuralians) deuterostomes (Bergström, Viehweg and Naumann in prep.)
Are all so-called deuterostomes 'upside-down' in compari-
The constructional gap between vertebrates and their son with protostomes,oronlyvertebrates, orsome intermedi-
relatives on one side, and 'protostomes' (orgastroneuralians) ate-sized assemblage? Between which groups did the
ontheother, has long disturbed attemptstocomparethetwo inversion occur? How could this influence our ideas of
groups. As a result, the phylogenetic and evolutionary protostome-deuterostome relationships?
relationships have been poorly understood and hotly debat- We can first state that enteropneusts, cephalochordates
ed. and vertebrates are the only deuterostome groups with a
As the names indicate, students have thought that in dorsoventral life orientation that can be compared with that
protostomes/gastroneuralians the mouth has a primary of protostome worms, molluscs and arthropods. It simply
position and the central nervous system is ventral. In has no sense to compare pentaradiate echinoderms or
deuterostomes/notoneuralians the mouth would have a sessile groups with a U-shaped gut with ordinary worms,
secondary position andthe central nervoussystem would be since dorsal and ventral cannot be defined in a comparable
dorsal (for instance Nielsen 1995). In the following I occa- way. In search for the solution ofthe orientation problem, I
sionally use the terms neural side and cardialside when the was struck by the fact that cephalochordates (amphioxus)
terms dorsal and ventral may be confusing or irrelevant. tend to rest on their neural side, that is, upside down as the
One attempt to understand the origination of the verte- text-books see it. This raised two immediate questions:
brates has been to start from a protostome that was turned arethey upside down in their life posture, orarethey in text-
upside down, so that the originally ventral nerve cord book drawings? And if the textbook drawings are upside-
became dorsal in vertebrates. An early proponent of this down, whatare the implicationsfor ouranatomical compari-
idea was Etienne Geoffroy St. Hilaire (1822), who suggested sons with other animals, such as the hemichordates?
thatthe vertebrate origin was among the arthropods. Other
mostly 19th Century authors (F. Leydig, C.Semper, A. Dohrn Anatomy, function and relationships
and A. Naef, see Nübler-Jung and Arendt1994) havetriedto
find an origin among annelid-type worms also by means of In this approach I am not suggesting any bold new ideas
dorsoventral inversion. In the 20th Century, W. Patten (1912) on the relationship between phyla. The deuterostomes, as
has been intrigued bythe idea of inversion. He believed in delimited here, are what they are in most textbooks: hemi-
a derivation from chelicerate arthropods. However, on the chordates, echinoderms and chordates. There are strong
wholethe idea of inversion has had onlya limited numberof reasons to believe that these groups are closely related.
proponents. In reality, mostzoologists have considered the These reasons are well known and need not be repeated
idea to be of entirely historical interest. here.
Recently, however, there has been brought impressive am not suggesting that any one group evolved from any
I
molecular evidence that indicates, or rather proves, that othergroup such astheyare delimited today. Forexample,
vertebrates in fact are upside-down in comparison with I do not believe that vertebrates evolved from modem
'protostomes'. It started with a contribution by Arendt and cephalochordates, but from a common ancestor which had
Nübler-Jung (1994 see also 1996), where they demonstrat- already achieved important derived characters, such as
;
ed that genes controlling dorsoventral patterning ofembryos segmentation of musculature and nerve system. This
show close correspondences between vertebrates and means that the ancestor was able to swim, as are also
insects. The striking difference isthata gene complex(the modern cephalochordates, if only in short darts.
achaete-scute complex) influencing neuronal precursorcells It isworth noting thatall preceding stepson theevolution-
ventrally in insects {Drosophila) influences the same type of ary ladderwithinthedeuterostomes—pterobranchs,enterop-
cells dorsally in vertebrates (Xenopus). In the other direc- neusts, urochordates, cephalochordates—include ciliary
tion, decapentaplegic-related genes affect mesoderm and feeding but not active search for food, and no eyes are
ectoderm dorsally in insects and ventrally in vertebrates. involved in feeding. Vertebrates, on the other hand, have
Hoiley er al. (1995) found that the sog (short gastrulation) well-developed sensory organs including eyes for orienta-
gene, expressed in the region of the ventral nerve cord in tion, and they search theirfood actively, not by ciliary feed-
insects, corresponds to the chordin gene, that is expressed ing. Therefore it is a logical conclusion that vertebrates
inthemid-dorsalareainvertebrates,aroundthedorsal nerve have come into being by a radical shift of habits. As in
cord. De RobertisandSasai(1996)addedfurthersubstance cases referred to above, we see this shift also in the
tothe ideaofinversion. Arendtand Nübler-Jung(1996)also ontogeny, since larval lampreys live and feed just as the
demonstrated a close longitudinal correspondence between amphioxus.
the brains of insects and vertebrates, both in gene control This is not unique to vertebrates. Function is intimately
and in functional respects. These hard facts demonstrate tied to body plans. We must therefore expect evolution to
Origin of high-rank groups of organisms
have produced similar solutions over and over again. anterior end of which commissures rise to embrace the
Repeated heterochronic retention of ciliaryfeeding resulting oesophagus and join the (occasionally hollow) 'brain' tube in
in a number of tentaculate phyla was mentioned above as the mesosoma(Figure2). There is alsoadorsal nerve cord,
one example. Unfortunately many scientists are so impres- but it is the ventral cord that is the thickest and that is in
sed byoneortheother individual similaritythattheyoverlook close association with the longitudinal musculature. It is
the overwhelming amount of parallel and convergent evolu- notable that there is one or more dorsal (and lateral) cords
tion that is clearly evident from the mosaic distribution of also in certain protostome groups, such as the flatworms,
characters among animals. nematodes and nemertines.
Nielsen (1995) has produced one ofthe latestphylogenetic The central nervous system of enteropneusts is therefore
trees. His tree is founded on a series of hypothetical typically protostomian in its character. It is commonly said
ancestral stages, partly larval,forwhichthere isnoevidence. that the hollowness of the 'brain' is found elsewhere only in
His guiding idea is that two types of larval ciliary feeding, chordates but no chordate has a hollow nerve tube on the
downstream and upstream food collecting, defines two cardial side of the body. Arendt and Nübler-Jung (1996, p.
phylogenetic groups. It is obvious that upstream ciliary 258) have rightly pointed out the true character of the
collecting is closely tied to mesotroch ciliary feeding. This enteropneust nervous system. It is obvious that enterop-
combination is found in brachiopods, phoronids, bryozoans, neustsare notupside-down in comparisonwith protostomes.
echinoderms, pterobranchs and enteropneusts, all ciliary Since they have a ventral mouth and a circum-oesophageal
feeders as adults. Endoprocts, which have prototroch nerve commissure, it would appear to be a mistake to call
ciliary feeding, have a downstream collecting system, like them deuterostomes. Their mouth is mostprobablywhere it
echiurids, annelids, nemerteans and molluscs, which are not has always been in their ancestors, technically they are
ciliary feeders as adults. A downstream collecting system protostomes, whether or not they are related to vertebrates.
appears to be primitive among coelomates. Whenever And they are gastroneuralians, since the central nervous
animals have shifted to mesotroch ciliary feeding there system is dominantly ventral.
appears also to have been a shiftto upstream collecting.
I
do not understand why this is so, nor does Nielsen indicate Enteropneusts and chordates
any understanding ofthe phenomenon. There is no reason
whatsoever that upstream collecting should not have The circum-oesophageal commissure is generally lost in
evolved several times, and there is no justification for using chordates, but there is still a nerve ring in appendicularians
downstream and upstream collecting systems to distinguish (Urochordata), even if there is no longer any brain on the
phylogenetic groups. Nielsen's results are not in line with cardial side (Olsson et al. 1990). The existence of a nerve
either modern molecular phylogeny or molecular genetics. ring ismostimportantforthecomparison between hemichor-
For instance, the very striking resemblance in genetic steer- dates and chordates. Ifthe central nervous system is used
ing of morphogenesis between insects and vertebrates to compare appendicularians with enteropneusts, it appears
(Arendt and Nübler-Jung 1994,1996; Holley et al. 1995) thatthe neural (dorsal)side oftheformermustcorrespondto
demonstrates that it is unreasonable to distinguish the the neural side of the latter, that is, the side that is consid-
Protostomia and Deuterostomia as two main groups, and ered as ventral in text-books. This is at oddswith conven-
unreasonabletoregardctenophoresasatwig onthedeuter- tional wisdom, according to which the neural (dorsal) side of
ostome branch. vertebrates, and therefore the neural side of appendicular-
There is also in Nielsen'sapproach thecommon tendency ians and other urochordates, corresponds to the cardial
togeneralize, andtogive protostomesand supposed deuter- (dorsal) side of enteropneusts.
ostomes characters which they do not have, or that only Onthewhole, however, urochordatesaretooderivedtobe
some of them have. For instance, Nielsen (1994, Table19) conveniently compared with enteropneusts. Cephalochor-
claimsthatphoronids, pterobranchs, enteropneusts, urochor- dates (amphioxus)can be more rewarding. When amphiox-
dates and cephalochordates have a dorsal central nervous us is placed with its neural (biologically ventral, but conven-
system, and that pterobranchs, which lack a pelagic larva, tionally dorsal) side down, a series of similarities with enter-
have dipleurula-like ciliary bands. As stated elsewere, in opneusts are apparent (Figures2,3,4). First, the main part
many ciliary feeders there is no possibility to distinguish of the central nervous system is down in both. The direc-
between dorsal and ventral sides, and regarding pterobran- tion of blood circulation isthe same, and conforms alsowith
chs, enteropneusts, and apparently also cephalochordates, the general protostomian pattern. On the upper side, both
Nielsen is clearly incorrect (see below). cephalochordates and enteropneusts have a pair of folds,
called metapleural folds in the former, genital folds in the
Enteropneusts, protostomes and the latter. In amphioxus (but not generally in vertebrates), the
central nervous system metapleural folds are interconnected by a transverse fold
closing an atrial space around the pharynx. Between the
Vagile protostomestend to haveat leastoneventral nerve foldsarethe pharyngealtremata(gill pores), although in adult
cord, or a pair. An anterior part of it embraces the oesopha- cephalochordates the individual tremata have disappeared
gus. Although deuterostomes are said to havetheir central and there is a single atrial opening posteriorly. The anus is
nervous system dorsally rather than ventrally, enteropneusts on the upperside both in cephalochordatesand inthe larval
in fact have a well-developed ventral nerve cord, from the tailed enteropneust (and in pterobranchs). In cross section,
Jan Bergström
circum-oesophageal
cns
nerve ring
cns
Figure2. Central nervous system and blood circulation in protostomes (A) and deuterostomes (B,C). A,
Onychophora; B, Enteropneusta (with anus in semi-larval position); C, Cephalochordata (amphioxus). With
amphioxus oriented as in nature, there is a basic similaritythroughout. The main blood circulation isforwards on
the dorsal side, backwards on the ventral side. The main stem of the central nervous system is ventral ; in the
anterior end there is acircum-pharyngeal ring except in amphioxus. The absence in amphioxus appearsto be a
secondary condition, since such a ring is known from urochordates {Oikopleura). The dorsal position ofthe anus
in amphioxus has its counterpart in hemichordates (pterobranchians and larval enteropneusts).
there are paired longitudinal muscles in the lower part ofthe animal would immediately be much more ampioxus-like
animal, whereas the reproductive organs are situated in the (although lacking, for instance, muscular segmentation).
upper part. Between the gut and the nerve cord is the However, manyreaders maywonder how itwould havebeen
notochord. Correspondingly there is in some enteropneust possibleforsluggish bottom-livingenteropneust-likeanimals
speciesa pygochord (for instance in speciesofBalanogloss- to develop swimming powers and pelagic habits. Actually,
us ; cf. Figures2,3). This pygochord likely functions as a whereasmanyenteropneustsaredeposit-feeders,othersare
skeleton. The endostyle (and its derivatives), so character- able to collect food directlyfrom the water, and the species
istic of chordates, may correspond to the preoral ciliated Glandiceps hacksi has been observed swarming at the
organ of enteropneusts. surface in shallow water, feeding on phytoplankton (Brusca
This impressive, and previously unexpected, list ofsimilar- and Brusca 1990, p.853).
ities indicates that chordates may have their origin among
animals very similar to extant enteropneusts. With swim-
ming habits, therewould be no needfora proboscis,andthe
Origin of high-rank groups of organisms
reproductive
organ
Figure3. Idealized cross sections through A, enteropneust (Hemichordata) and B, amphioxus (Cephalochor-
data). Both are oriented as in nature, which means thatthe amphioxus is upside-down in comparison with text-
bookillustrations. Thereisaclosecorrespondenceinseveralstructuresandorgans: pharynxwithgillslits, paired
dorsal 'wings' containing gonads (called genital wings for simplicity in amphioxus, their technical term is
;
metapleural folds), ventrally situated longitudinal muscles, main stem of central nervous system ventrally, and a
stiffening rod (pygochord and notochord) between gut and nerve stem. The enteropneust musculature is usually
poorlydeveloped, but is massive in species ofSaccoglossus. The enteropneustpygochord is notwidelydistribut-
ed, but occurs in species of Balanoglossus.
Filter feeding cephalochordates, use of sensory organs including eyes.
macrophagous vertebrates How could a change from a passive filter-feeding organ-
ism to a macrophagous swimmer come about? How does
We haveto acceptthatwe mustorientamphioxuswith its the reversal of body posture fit in, if at all?
neural side down when we compare its anatomywith thatof We do not know why a change came about. For the
protostomes and enteropneusts. Since this is alsothe way moment we just have to accept that it did. For an active
it lives, itwould be no problem, butforonething : doing this, localization of its food the original vertebrate apparently
we placethem upside-down in comparison with vertebrates, needed eyesight, since eyes were developed. Eyes most
and we can hardly accept instead to place a fish or a easily may develop from the light-sensitive nerve cord. For
mammal upside-down in order to facilitate comparison. a primitive chordate without a circum-oesophageal ring and
However, we have localized the place in the evolutionary a cardial-side component of the brain, this means that the
treewhere reorientation must have occurred : it is insidethe eyes take their origin below rather than above the mouth.
chordatetree, aftercephalochordates(amphioxus) branched For food search along the bottom this situation is inconve-
off. Vertebratesobviouslyaretheonlyupside-downdeuter- nient. The simplest way to solve the problem would be a
ostomes, the only real Notoneuralia. reversal of body posture. We can now see that nature
Cephalochordates have several peculiarities of their own, found this solution. Reversal would shift the mouth to the
butthey are also similartovertebrates in many respects, for new ventral side. It is of course possible that the order of
instance in having a segmented musculature. One differ- events was just opposite, with reversal preceeding eye
ence, however, is that they lack eyes, whereas vertebrates development.
have a pair of anterior eyes. They have light-sensitive How likely is itthataswimming proto-vertebratewould be
spots in the central nervous system which helps them able to shift to an upside-down life? We can get some
determinethe correctburrowing depth, buttheycannotspot ideafrom astudyoflivingamphioxus. Myownobservations
their food, and they do not need to because they are still of Branchiostoma lanceolatum indicate that it easily turns
filter-feeders like most hemichordates and urochordates. around when it meets a hindrance, such as aquarium glass.
On the contrary, vertebrates find their food actively by the It turns immediately 180°, and does not swim on its side.
. -
Jan Bergström
mouth
gill pore
genital
wing
genital
wing
gill pore
Jtfïeîf)
Figure4. Ventral viewsofanteriorbody parts ofenteropneusts(Hemichordata)andamphioxus(Cephalochor-
data). A, The enteropneust Balanoglossus, cardial (dorsal) side. B-C, Larval and adult amphioxus (Branchio-
stoma), cardial (so-called ventral) side. Note the general similarity, partly disguised by asymmetry in the larval
amphioxus and lossof individual gill pores in adultamphioxus. The genital wings ofthe enteropneustare similar
to the metapleural folds in amphioxus and similarly enclose the gill pores. A, modified from Ruppert & Barnes
(1994); B-C, modified from Herdman (in Harmer and Shipley 1932).
After a second or two, it turns over again—and then over fore, one orthe otherside up does not mean any impossible
again. When hiding inthebottomshell sand, itusuallyrests difference.
with the neural side down, but in exceptional cases it We have some idea on when it happened. The great
appearsto bethe otherway around. To amphioxus, there- radiation within coelomate phyla started around 540-530
Origin of high-rank groups of organisms
million years ago, at the beginning of the Cambrian. The functional mouth in vertebrates is a new penetration.
oldest known cyclostomes lived during the Early Ordovician This is of course possible, but from a functional point of
eayneds.areThsleighctolnyoldeosnstthaannim5a0l0s mmiulslitonhayevaersbealgoong;etdhetyohtahde avnioetwheitrahpapseaervsollviekdelyfrtohmatthteheolnd.ewWmeouktnhowintohanteinwamyanoyr
vertebrate side of the evolutionary tree (see below). The enteropneusts the pharynx is divided into upper and lower
oldestdefiniteconodontanimalswe knowoflived duringthe portions by lateral infoldingsofthe pharynxwall. The upper
Late Cambrian, some 505 million years ago. Inversion and channel leads water to the pharyngeal tremata ('gill' pores),
the vertebrate eye thus are some 505-530 million years old. while the lower channel conveys food backwards to the
midgut. A similar division could have separated the anter-
Embryology iormost part of the vertebrate forebears into an upper naso-
pharyngeal tube and a lower mouth cavity, both opening
Reversing the adult means that also the egg and embryo posteriorly into the pharynx. This appears to be the situa-
have to be turned around 180°. Surprisingly, the edges tion that is still present in myxinids (hagfishes), while in
closing the neural tube then must be considered as the lips petromyzontids the upper tube is closed at the rear to form
of the urmund. In urochordatesthe definite mouth formsat a nasal sack.
the neuropore, that is, justatthe anteriorend ofthe urmund. The situation in cephalochordates is lesseasyto interpret.
This makes urochordates indistinguishable from protostomes Ontogeneticallythedefinitive mouthformsasanewopening
in this allegedly profound character (Figure5). on the left side of the head, only to move later to the upper
In cephalochordates and vertebrates the situation is more (so-called ventral) midline. This shift serves two purposes.
derived because of a secondary displacement ofthe mouth. First, it 'has to' move from its original position on the lower
However, it is notablethatthe nasal sack still formsfrom the (so-called dorsal) midline to let the notochord grow to the
neuropore, and that this sack is continuous with the gut in anterior end of the animal, where it serves as a support
hagfish. Could it be the original mouth? Arendt and during burrowing. Second, for an animal concealed in the
Nübler-Jung (1996, p.258) found neural evidence that it bottom sediment its position should be as high as possible,
corresponds to the original mouth, and thought that the thus on the upper side. As for vertebrates it appears most
future mouth
neuropore;
mouth in
urochordates
neural fold
blastopore lip
future anus
Figure5. Idealizedviewsofembryosfromtheneural side: left, protostome; right,urochordatedeuterostome.
In a protostomethe future mouth is said to be formed by oratthe anteriorend ofthe closing blastopore, although
thereare numerousexceptions. Theventral nerve cordformsalongthefused blastopore lips. Inadeuterostome
the central nerve cord similarlyforms along apairoffusedfolds, which in urochordatesextend betweenthefuture
mouth and anus. The similarity between thetwo embryotypes is striking, but has notbeen appreciated because
students 'knew' they were looking at opposite sides of the embryos.
10 Jan Bergström
likely that the mouth is not a completely new opening from that the supposed gills have a ventral position, whereas the
an evolutionary point of view, but has shifted position. It gill pores in deuterostomes (other than vertebrates) have a
may have moved over the anterior tip of the animal. If so, decidedly dorsal position. Moreover, Shu et al. (1996)
the lateral formation ofthe mouth may be a lateradaptation, pointed out that the supposed notochord is filled with gut
perhapsto lying down on one side, orto rotational swimming contents.
in the larvae for more effective ciliary feeding. Shu er al. (1996) recently described Cathaymyrus diadexus
from the Chengjiang fauna as a cephalochordate. The
Fossil deuterostomes singlefossil specimen preservesapossiblealimentarycanal,
a possible notochord, a possible pharynx perhaps with gill
Apartfrom echinodermsand vertebrates, nodeuterostome slits, andtransverse bandsthatare interpreted asmyomeres.
group has yielded fossils useful for softpart reconstruction. No fins are visible. According to the authors the animal is
The only other group that is abundant as fossils is the judged to be a relative of amphioxus. This is not obvious
graptolites,towhichthetwogeneraofliving pterobranchians from the illustrations. Additional material is needed before
should be counted. Unfortunately the Palaeozoic anywell founded judgementonthe significanceofthisfossil
graptolites are known only from their colonial skeletons. can be made.
The Lower Cambrian Chengjiang fauna of China has The Middle Cambrian Pikaia gracilens is more easily
yielded the worm-like animal Yunnanozoon lividum. In their accepted as a chordate. It has the general appearance of
original description, Hou et al. (1991) regarded it as slug- an eel larva(Figure6A). Itappearsto be segmented and to
shaped. Bolder interpretations and reconstructions have have typically V-shaped myotomes, a key character of
been issued since. Dzik (1995) and Chen er al. (1995) cephalochordates and vertebrates. However, as long as it
suggested thatthe animal isadeuterostome,thesegmented is unknown if it has eyesorjaws(teeth) itcannotbedecided
bands being myomeres of the type found in cephalochor- ifitisacephalochordateoravertebrate. Thisdiminishesits
dates and vertebrates. I hesitate to accept this interpreta- value in the discussion. Itdoes notseem to be a conodont
tion. There are several reasons for this. For instance, the animal, since it is likely that the conodont teeth would be
supposed myomeres lack the V-shape characteristic of easily preservable and visible. On the other hand, the
segmented chordates. Theyarealso notablydark, which is absence of shell sand inthe BurgessShale indicatesthat its
difficult to explain if they were myomeres. It is even more mode of life was differentfrom that of modern cephalochor-
remarkable that there is occasionally a small overlap dates.
between adjoining 'segments'. Such an overlap is hardly Thesefossilsapparentlycan notgive us much information
compatible with the idea that the 'segments' are massive aboutthe origin and earlyevolution of deuterostome groups.
muscle blocks. At the edge the 'segment' in front occa- The conodont animals, or conodontophorids, are now
sionally stands out a little over the successive one. These known to have had a pair of eyes and a body musculature
features indicate that the 'segments' are not muscle blocks divided into V-shaped myomeres (Figure6B Purnell 1995).
;
at all, but sclerites in the skin ofthe animal. Such sclerites It is quite obvious thatthey are segmented chordates. The
are unknown in marine deuterostomes. It can be added possession of eyes and teeth demonstrates that they were
'
^
jälJ'Jll'll
^
\\\\\\\v
Figure6. Fossil segmented chordates, both oriented with the neural side up. A, Pikaia gracilens, a possible
amphioxus relative from the Middle Cambrian Burgess Shale. Length about 4cm. Drawn from Conway Morris
(1982, PI.S). B, Clydagnathus windsorensis, a conodont animal from the Carboniferous of Scotland. Its eyes
reveal that it belongs to the vertebrate lineage. Length about 4cm. Simplified from Purnell (1995, Figure1).
