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THE ORIGIN OF THE CHORDATES
By QUENTIN BONE
From the Plymouth Laboratory
(With 2 text-figuree)
Communicated by Professor C.F.A. Pentin, F.R.S.
CONTENTS
......................................................
..........................................................
INTRODUCTION
GENERALCONSIDERATIONS OF THE PROBLEM OB NEOTENY IN THE cHOl€DATE
LINE
Peg13
262
264
THE NATUREOF THE LARVAWHICH QAVE RISE BY NEOTONY TO THE CHORDATE
LINE ..........................................................
266
ANCESTORS............................
268
........................................................
286
THE UROCHORDA
All CHORDATE
THEHEMICHORDA
AS CHORDATEANCESTORS............................ 261
THERELATIONSHIPS
OF THE A c ~ l w r a ..................................
263
ACKNOWLEDOEMENTB
................................................
264
REFEIUZNCES
INTRODUCTION
SPECULATION
upon the origin of the phylum Chordata has in recent years seemed
less interesting to students of evolution than it did in the nineteenth century, partly,
no doubt, because as more has become known of the various invertebrate phyla which
were suggested as candidates for chordate ancestry, their title to this position has
been seen t o be based upon very slender evidence ; suoh similarities as were cited
between these groups and the chordates are seen today t o be analogies rather than
homologies. Few zoologistswould now attempt to uphold the view that the chordates
arose from the h e l i d a OF the Arthropoda.
In part, also, interest has waned in this topic for a very different reason. The
discovery of the ohordate-liketadpole larva of the Ascidiacea, and the demonstration
by Conklin (1905, 1932) that the ascidian fate map was in essential details exactly
equivalent to that of amphioxus and the craniate, seemed to place the tunicates
&mly in the position of the ancestral stock to the chordates ; and (since fossil evidence as to the origin of the Urochorda is lacking) the question has been regarded &s
more or less closed. Many zoologiste believe that it is most reasonable to suppose
that the chordates arose from the Urochorda, but that it is not profitable to disouss
the transformation in detail, for we cannot discover much about it.
However, attempts have been made to disentangle the relationships of the two
groups, and the modern views of chordate origin from the Urochorda (based upon
the ideas of Carstang, 1928), are of much interest. The emphasia which Garstang
placed upon the importance of neoteny (paedomorphosis)in the evolution of new
groups of organisms, and the similarities between adult chordates and the larvae of
the sessile ascidians, naturally led to the rejection of earlier views of the Urochorda
as degenerate vertebrates, and to the modern theories of chordate origins from primitive ascidicbn larvae by neoteny. What may be called the ' ascidian-origin theory of
chordate evolution has been argued at length by Berrill (1955), and most recently,
by Whitear (1967)-these authors either derive the chordates from the tadpole
larvae of early Urochordates, or from the tadpole larvae of early ascidians ; the
Acrania are regarded as of similar (though independent) evolution.
The evidence for this view of chordate origins depends chiefly upon the morphology
of the tadpole larva : in effect, the protagonist of this theory points to the striking
resemblance between the tadpole larva and the adult chordate, and claims that these
correspondences inevitably lead to the conclusion that they arise as a result of the
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THE ORIUIN OF THE CHORDATES
253
origin of the chordates by neoteny from forms similar t o the tadpole larva. The
differences between the various theories of this type, then arise from different views
of the evolutionary stage of the Urochorda a t which the neotenous transformation
is imagined t o have taken place.
The interesting point about many of the theories of the ‘ ascidian-origin ’ type,
is that little attention is paid to the functional basis of the neotenous transformation
leading t o the chordate line ; it suffices to indicate morphological evidence pointing
t o the occurrence of neoteny, without considering the functional difficulties that this
change involves. These difficulties may be considerable ; I shall attempt t o show in
the present discussion of the subject that they rule out the Urochorda as chordate
ancestors. It is interesting that Carter (1957) comes to the same conclusion, on rather
different grounds.
Carter struck a t the base of the ascidian-origin theory by denying that the
hypothesis of neotenic transformations was a necessary one in phylogenetic speculation. He pointed out that the resemblances between the adults of one group, and
the larvae of a related group could be accounted for without invoking the neotenous
transformation of the former from the latter, and suggested that the great majority
of examples of so-called neoteny could be more simply explained by assuming that
the two groups in question shared a common ancestor, whose larva the one group
came to resemble by the retardation of appearance of some of the characters of the
original larva so that they appeared in the adult descendants.
I n my opinion, this rejection of the hypothesis of neoteny is a false economy ;
although the hypothesis has suffered from uncritical use by various authors who
have not sufficiently considered the functional difficulties implied in neotenic: transformations ; there is still a good case for many of the examples of neoteny which
have been suggested. I n particular, I shall try to show that a neotenic transformation
has resulted in the origin of the chordate line, though it did not take place a t the
stage supposed by the protagonists of the ascidian-origin theory.
The argument leading to this conclusion is somewhat complex, and I shall therefore follow Garstang’s example in setting out a summary of the steps involved,
before considering each point in detail.
Summary of Argument
1. General considerations of the problem of neoteny i n the chordate line
(a) Neotenic transformations have been supposed either to be sudden, (by a
‘ macro-mutation ’ affecting the reproductive organs of the larva), or t o be gradual ;
it is shown that the gradual alteration of developmental processes is a much more
probable hypothesis.
(b) If the process leading t o total neoteny was a gradual one, this implies that it
must have been of selective advantage t o the animal becoming modified in this manner.
(c) This consideration makes it unlikely that the ascidian tadpole larva can have
undergone neoteny t o give rise to the chordate line. From the origins of the group,
the tadpole larva was specialized for short range site selection, and its physiological
peculiarities are exactly the opposite of those which would be expected in the form
which is assumed t o have undergone gradual neoteny.
(d) So-called neoteny has taken place in the Urochorda to produce the Thaliacea,
but this is a different process from that which (it is assumed) gave rise t o the chordate
line, and does not argue for the neotenous origin of the chordates from the Urochorda.
2 . The nature of the larva giving rise to the chordate line by neoteny
(a) Two typea of larvae are recognizable in the Protochordate groups ; those
living for a long period in the plankton where they feed and increase in size, and those
which are specialized for a short free-swimming period, during which they do not
feed.
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(b) The former type of larva is suggested t o have undergone neoteny to give rise
to the chordate line as a consequence of selection increasing the larval life in the
plankton.
(c) It is suggested that the larval period in the plankton was lengthened t o enable
the larva t o exploit the rich food supply a t the sea surface.
3. The Urochorda as chordate ancestors
(a) Thc Ascidiacea can be disregarded since their larvae are specialized away
from the physiological type which is assumed t o have given rise t o the chordate line.
(b) These arguments apply to the Urochorda also, from the origin of the group.
(c) It is suggested therefore, that the Urochorda have inherited the tadpole larva
from an earlier group, and have lost their claim t o chordate ancestry by adopting a
sessile habit and consequently specializing their larvae for site-selection.
(d) It is therefore necessary t o consider the adult animals which possessed tadpole-like larvae, and gave rise to the chordates by neoteny. It is supposed that they
were semi-sessile, reasons are given for rejecting the alternative view that they were
free-swimming and gave rise t o the chordate line without neoteny.
4. The Hemichorda as chordate ancestors
(a) The homologies of the head coeloms and their connexions and derivatives
definitely implicate the Hemichorda in chordate ancestry.
(b) The modern tornaria type of larva is supposed t o be ancestral for the group,
from it, a tadpole-like larva was evolved (following Garstang) as a n adaptation for
increasing the planktonic life of the larva.
(c) From this larva, the chordate line arose by gradual neoteny, and the abandonment of the hemichordate adult structure.
(d) It is suggested that the modern Pogonophora throw some light on the question
of this original adult structure.
5 . The relationship of the Acrania
(a) The Acrania are considered to represent the early paedomorphosed chordate
type, which have lost their claim t o chordate ancestry by the adoption of a semisessile habit (and the secondary acqui8ition of a larval stage).
(b) Amphioxus is more definitely sessile than the Asymmetrontids, its larva is
reduced compared with other larvae known in the group and i t is suggested that it
is being reduced t o a short range site-selector as in the Ascidiacea.
(c) The amphioxides type of larva, on the other hand, lives for long periods in
the plankton and may possess developed gonads ; it seems that it is recapitulating
the evolutionary history of the chordates a t the present time !
GENERALCONSIDERATIONS
OF THE PROBLEM
OF NEOTENY
IN THE CHORDATE
LINE.
It is curious that the process of neoteny (usually agreed t o have played a n
important role in the production ofthe chordate line, but see p. 260) has not been
comidered in detail. Whilst it is easy t o suggest points of resemblance between, say,
the amphioxus larva or adult, and the tunicate tadpole larva, i t is very much more
difficult t o envisage the process whereby the larval form of the one became transformed into the adult of the later type.
It is clear that this process could be brought about in two different ways. It is
possible that the new adult form might arise directly a t a single step, by some fundamental alteration of the relative rates of development of the gonads and of the somatic
characters. I n this way, many of the later appearing characters of the ancestral
adult form would be missed by the new form, or even, if the gonads matured in the
larva before metamorphosis, the new form would lose all trace of the characters of
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255
the ancestral adult. The transformation of this tadpole larva to the vertebrate involves an alteration of this latter kind.
The objections to such a sudden step as this appear almost insuperable. Many of
the objections that have been urged against the appearance of new bi-sexually reproducing organisms by polyploidy apply with equal force in this case. The difficulty
of such a view, is with what type of animal does the newly produced neotenous form
reproduce ? Without considering the extreme unlikelihood of a " macro-mutation
sufficient t o cause neoteny resulting in an animal able to survive, let alone an animal
capable of reproducing itself; it is very difficult to see how this sort of mutation
(which is affecting the reproductive mechanism) could spread in the population.
In the modern Ascidiacea, Carlisle (1951) has shown that special mechanisms
exist for the simultaneous release of gametes from a number of individuals ; it is
likely that similar mechanisms are found in the Acrania. It is thus not probable that
a larva living in the surface layers, which has been produced by a large mutation
sufficient that its gonads are mature a t this stage, could produce gametes that would
be able to come into contact with those produced by the sessile adult forms from
which the larva arose. It does not seem likely that the timing of gamete release of
the neotenous larva could be correctly ' geared ' with that of the original adults ;
such mechanisms for the correlation of gamete release are necessary because of the
short period of viability of the free gametes in tho sea.
)
the transformation of the early Urochordate
However, Whitear ( 1 ~ 8regards
larva t o the chordate as a sudden step ; but it is probable that most speculations
upon the role of neoteny in evolution have been concerned with a much more ' gradual '
type of neoteny although thia is not usually explicitly stated.
That the neotenous change was a gradual process, taking place over many
generations, so that the gonads became functional earlier and earlier in ontogeny (or
alternatively, that the larva spent longer and longer of its life afloat, so that the
gonads appeared in larval life), finally becoming functional in larval life with the
production of a new, neotenous form-is a much simpler process t o imagine. If the
neoteny arose in this manner, then not only would the larva be gradually adapting
t o life in the surface plankton, developing larval adaptations fitting it for such a life,
but also, it is understandable that many larvae would be undergoing this process
concomitantly so that when total neoteny eventually took place, i t would occur in
a population (thus being perpetuable by reproduction within this group) and not, as
in the view of sudden neoteny, taking place in a single larva only.
Such a view of the neoteny of the early larva t o the chordate adult implies that
the process of gradual neoteny must have been of selective advantage t o the larvae
that were gradually becoming neotenous-it is this aspect of the problem that is
illuminating when speculating upon vertebrate origins.
Berrill has convincingly shown that the modern tadpole larva of the Ascidiacea
is a highly specialized organism, specialized for short-range site-selection. In his
analysis of the structural and behavioural peculiarities of the various types of modern
tadpole larvae, he has shown that they are adapted for a short larval life, and for the
selection of sites of attachment for the new adult, close t o the parent form.
There can be little doubt that the selective forces acting upon the modern tadpole
larva, resulting in the specialized larva seen today, have been acting from the origin
of the Ascidiacea as a group ; there is no reason t o suppose that the larva of the
present-day Ascidiacea is a much compressed version of the earlier larva of that
group (whether or not the larva first arose within the group). This conclusion is
supported by consideration of the structure of the pelagic tunicate Doliolum.
It is generally agreed that the Doliolids have been produced from sessile Ascidiaceans that have failed t o settle and have become adapted t o a pelagic life. From
the Doliolids, the Larvaceans are then derived by neoteny.
Now, as Whitear points out, the discovery by Lohmann (1922) of a n apparently
modern Larvacean (Oesia) in a middle Cambrian deposit, implies that a t this time
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the Doliolids had already been produced from the Ascidiacea ; the point of interest
in the present conncxion is that the cell numhers of the modern Doliolid tail (resorbed
before the oozooid hatches) are those of the tail of the modern tadpole larva, 80 that
this larva can scurccly be regarded as a modern specialization.
The next point in the argument, is that stage at which the tadpole larva evolvcd,
in the history of the Urochordates.
Reasons have been given above t o indicate that from the origin of the Ascidiacea
as a group, the+ larvir WILB of the modern type. If, as Berrill supposcs, this tadpole
type of larva is an Ascidiacean invention, then, on this view, it cannot be regarded
as a vertcbratc ancestor. From its origin, it was being selected for short-range site
selection, and thus selected in exactly the opposite direction t o that which would
lead to gradual ncotcny.
This type of larva is not a suitable one from which to derive the chordates by
neoteny. It is the result of selection maintaining and specializing a short larval phase,
and is physiologically quite unlike the type of larva which underwent neoteny, whose
whole history must have been of longer and longer periods spent in the plankton whilst
the rieoteny gradually appeared.
The fundamental difference between this type of larva characteristic of the
Ascidiacea, and the latter type, which i t is here suggested gave rise by neoteny t o
the vcrtcbrates, will be discussed in the next section. Before considering this other
type of larva, it is necessary to consider an objection which may be raised against
the summary rejection of the tadpole larva as EL form which can undergo neoteny.
The difficulties of neoteny in the tunicate line, that have been emphasized above,
may be thought to be not insuperable, for Garstang himself has sufficiently shown
that neoteny has taken place several times in the tunicate line-resulting in the
various groups of pelagic tunicetes. The process that upon Carstang’s view has taken
place in the production of these groups is however, of a different kind from that which
may be supposed t o have taken place in the production of the chordate line. The
hyppthesis is that for some reason or othcr, the tadpole larva which gave rise to the
Doliolids, fuiled to settle, (possibly because of a failure of development of its sensory
apparatua), and went on t o fecd and adopt a pelagic life. From Doliolids formed in
this way, further stages lead on to the Larvaceans.
What is significant, is that there are dcfinite signs of a metamorphosis in Doliolids,
which has been reduced and suppressed ; similarly, in Yyrosorna, although development is much altered, the end result is the formation of Ascidiaeean-like adults,
although fixation has not talcen place and the colony is pelagic. It seems most reasontthle therefore, t o regard the process that has given rise t o the pelagic tunicates,
as different in kind to that which may have given rise to the chordate line : total
neoteny has not, in fact, taken place. What has happened in this case is that settlement of the metamorphosed larva has not taken place, a new organism has been
produced hy the modification of the free-floating aduIt organism. Such a view of the
origin of the pelagic tunicates does not involve any alteration in the developmental
ph ysiology or behavioural peculiarities of the tadpole larva-so far from this larva
giving rise t o a new form by neoteny, it gives rise to a free-floating adult and is itself
almost immediately suppressed, for i t is n o longer required by the new pelagic adult.
The neotenous origin of the chordate line from the tadpole larva is a very different
type of process, it has been suggested above that this process is very much more
difficult t o imagine.
I n the next seotion, the nature of the larva which gave rise t o the chordate line
will be discussed, and the problem of the adult form that possessed this larva will be
studied.
THE NATUEE
OF THE LARVA
W I ~ C I GAVP,
I
RISE BY NEOTENY
TO THE CHORDATE
LINE.
It is clear that in the living forms that have been considered RS more or less closely
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THE ORIOIN Or THE CHORDATES
257
related to the chordate ancestor, there are two types of larvae, recognizable by their
very different developmental physiology ; although they are morphologically diverse.
On the one hand, there is the tunicate tadpole larva which lives free-swimmingfor a
period of hours only, and metamorphoses near the parental site. On the other, are
the larvae of the Echinoderms, Enteropneusta, and the amphioxides larva of the
Acrania. These larvae spend many weeks or even months free-swimming in the
surface layers, and then undergo a sudden metamorphosis to an adult which may take
up life very far from the parent site. In these larvae, which drift for long periods in
the plankton, there is no question of short range site selection (as in the Ascidiacea),
and the selective forces acting upon such larvae are very different from those acting
upon the tadpole larva. It is worth noting in this connexion, that the adults of the
second group of larval types, are not strictly ' sessile ' as are the Ascidiacea, and thus
the difficulties of site selection are not placed upon the larva to such an extent as
they are upon the tadpole larva.
feeding and growth in
plankton
metamorphosis
I
Tunicate tadpole larva
Larvae of Echinoderms;
Hemichordates. and some
Acraniates
FIQ. I.-Diagrtun ihStr8thg different life-histories of the two hrval types.
It is of course true that the substrate does affect larvae of the second type, in their
settlement (e.g. the metamorphosis of Polychaete worms, studied by Wilson (1955))
but the requirements for successful metamorphosis and adult life are very muoh less
stringent than they are in the Ascidiacea.
The larvae of the second group, adapted to spending a long feeding period in the
plankton, growing and increasing in size, Bhow many special features which aid them
t o maintain their position in the surface layers. Such for example, are the muscuIar
lobes of the larva of the asteroid Luidia, the complexity of the ciliated bands of the
larger tornaria larvae, or the complex feeding arrangements of the amphioxides larva.
The difference between this type of larva and that of the tunicate tadpole may be
diagrammatically illustrated as in Fig. 1.
It is from larvae of the second type, physiologically adapted to a long pelagic
larval life, with various special adaptations fitting them to maintain their position,
and to feed in this position, that the gradual neoteny producing the chordate type is
to be supposed to have taken place. In such larvae, the pressure of selection operates
in the opposite direction to that in the Ascidiacean line, towards the prolongation of
the larval phase ; it is possible to imagine the way in which, as the larva spent longer
and longer in the surface plankton, its gonads became functional in the larval stage,
and already adapted to life in the plankton, it could survive and reproduce as a new
form.
Not only is this process possible to imagine, but it mema that a t the present time
it can actually be observed to be taking place ! In the emphioxidea larvae of the
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Acrania (first studied by Goldschmidt (1905)), gonad rudiments appear before the
metamorphosis, and the larvae live for a t least several months in the plankton
before metamorphosing, (it was in fact, at firs6 supposed that they were adult animals).
The position of these larvae has been misinterpreted by earlier speculators, it is
certain that they are not ‘ doomed t o an eventual death as a larva ’ as Berrill supposed, (see Bone (1957) for a brief discussion of this point). The acrania are a special
caw, their status in phylogenetic speculation will be discussed in detail below, nevertheless, the dramatic recapitulation by the amphioxides larva of the neotenic origin
of the chordate line, makes it very probable that they are the closest representatives
living of the ancestral type of protochordate larva.
In the view put forward above, it is suggested that the larvae of the second type
have spent longer and longer in the plankton ; that selection upon this larva acted
to prolong larval life, and finally neoteny took place to the chordate line rather as
a by-product of the pressure of selection maintaining and increasing the larval freeswimming phase.
It is therefore necessary t o consider what selective advantage the increase of
pelagic life may have conferred upon such a larva. It is clearly unwise t o press the
argument too far, when there are few facts upon which t o base any speculation which
we may wish to make ; however, the following facts are available, and enable a
reasonable suggestion t o be made.
Firstly, the production of forms which are free-swimming in the plankton is a
process that seems to have taken place several times in the groups that are being considered. The arguments of Garstang upon the production of the pelagic tunicates
have already been referred to. It is likely that the amphioxides larva represents a
stage in this process. Amongst the Echinoderms, there are pelagic species (eg.
Uintncrinus, Eldonia and Pelaqothuria), although these are apparently excessively
rare in the group, Secondly, the production by bottom-living animals of free-swimming
forms seems to have taken place in several quite unrelated groups, such as the
Polychaeta (Tomopteris) ; Nemertina (Pelagonemertes); and perhaps the Crustacea
(Copepoda from Decapoda, Gurney (1942)). It is, of course, true that the reverse
process is equally common. Thirdly, the animals whose larvae have been considered
are all sessile or semi-sessile bottom dwelling forms, depending at least to some extent
upon their larvae for distribution. Lastly, all feed (with the exception of the modern
tadpole larva) upon small particles of food which they filter out of the water.
These considerations, and the fact that the greatesb concentration of food particles
is found a t the surface of the sea, suggest that the production of forms living in the
plankton, in the rich food layer a t the surface of the sea, is a direct response t o the
availability of this rich food supply-the neotenio transformation has taken place
indirectly as a result of the exploitation of this food supply by the larva. It is no
coincidence that quite unrelated groups have produced neotenous forms exploiting
the surface layer in the same manner.
These considerations have been very general ; specific groups have not been
implicated in the consideration of the type of larva that underwent neoteny in the
surface layers, save that reasons have been given for rejecting the Ascidiacean tadpole larva.
I n the next section, the evidence that exists as t o the adult forms (whose larva
has been discussed) will be considered.
THEUROCRORDA
AS CHORDATEANCESTORS
Berrill’s view of the Ascidiacea as vertebrate and Acraniate ancestors can be
discounted upon consideration of the peculiarities of the tadpole larva, and from the
arguments that Whitear adduces.
Whitear’s own view, that it was the larvae of an early Urochordate which gave rise
t o the vertebrate line, before the origin of the Ascidiacea as a group, has much to
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THE ORIGIN OF THE CHORDATES
259
commend it. There are however, some serious objections which may be put forward
(as there are t o any view of chordate origins), and these hinge upon two points. The
first, is the nature of the early Urochordate larva.
If i t is supposed that the tadpole larva of the Ascidiacea is not a n invention of
that group, but is in fact a reduced version of an earlier Urochordate larva, then it
is possible to imagine that the early Urochordate larva could have been of the second
physiological type (discussed in the previous section), and could therefore, by reason
of its developmental physiology, have been selected for life in the surface layer, and
eventually have given rise t o the chordate line. This larva would have been somewhat similar to that of the present day acraniates, i.e. fairly large in size, with a simple
pharyngeal arrangement, feeding as a larva, and with a long larval life. Whitear
supposes that it possessed coelomoducts, but does not suggest exactly what the
conditions of the coelom may have been.
The objection to this view is simply that if the assumption is made that the larva
is an Urochordate invention, and that this larva when it first arose was of the second
type, then this view is perhaps the simplest t o take-but these assumptions are not
likely to be correct. Firstly, considering the adult of the early Urochorda, it is probably correct t o follow Whitear, and consider a form much like a small modern Ciona,
with a simple pharyngeal arrangement, with a coelom, and with little test. Such an
animal would almost certainly be absolutely sessile. There does not seem t o be any
obvious reason why the arguments for larval selection for site-selection should not
apply also t o the larval form of this small simple pre-ascidian. It is true that competition for sites may have been less intense in the Pre-Cambrian (or whenever one
may wish such an animal to have lived), but this is not the primary reason why the
larva selects the site with such care ; unless the larva settles in a place suitable for
the adult’s feeding method, (i.e. upon a firm substrate, where there is a sufficient, but
not too great water current, and where there is a reasonable concentration of food
particles in the water), the adult will not be able t o survive and grow. From the origin
of the Urochorda as e group then, it seems that selection of the larva for short-range
site selection has taken place, the pressure of selection being much what it is for a
modern tadpole larva.
It is of course, simply a matter of opinion what the condition of the pre-ascidian
larva may have been. But if it is assumed t o be a n Urochordate invention, then if
the argument above is agreed, it is difficult to see why it should have been very
different, from its origin, from the modern type of Ascidiacean larva. Even if it was
a much larger version of the present larva, then the same argument applied, and it
would have been in the condition of being selected towards the modern type and
unsuitable, therefore, as a chordate ancestor.
Secondly, there is the question of the origin of this larva. I s it in fact reasonable
t o suppose that it is an Urochordate invention ? If this assumption is made, then, as
has been suggested above, it it difficult to see (from the function that it fulfils in the
group) in what way it could have become neotenous and given rise via the second type
of larva to the chordate line. If on the other hand, it is supposed t o have been inherited from a n ancestral group to the Urochordates, as Carter suggests, this difficulty
is avoided, for we may derive the chordate line from that group rather than from
the Urochorda a t any stage in their evolution.
This view implies that the characters that the tadpole larva shares with the chordates are the result of the common inheritance of these features (notochord, tail
muscles, dorsal nerve tube etc.) from a group which possessed larvae with these
features ; giving rise independently to the chordate line on the one hand, and to the
Urochordates on the other. The features which the Urochordate retained in its larva,
are those which adapt the larva t o its function of site selection for a completely sessile
adult.
It is precisely these features which still indicate the relationship of the Urochorda
t o the chordates, and which still result in the fate map of the Ascidiacean egg being
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almost exactly equivalent (allowing for the smaller cell number) to that of amphioxus
and the vertebrate (Conldin, (1905) ; (1932)). That is t o say, the Urochordate inherits
a larva of the second physiologied type, with notochord, myotomes, a dorsal nerve
cord operating this system, and a sensory system (which it specializeswith sense organs
useful in site selection) a t the front end of the nerve cord-these features of the ancestral larva arc useful in the new role of the larva whose adult had become completely
sessile, and are thus retained even today in the modern Ascidiacea. It is not surprizing
that the Aseidiacean fate map should be so similar t o that of the chordates, because
its bitsic features are those which thc tadpole has inherited from the common ancestor
with the vcrtebratcs, even though the tadpole larva puts these features t o a rather
different use.
Thc argument may be stitted briefly thus. If thc tadpole is an Urochordate invtmtitrii, then it is not easy to see in what w a y it ever became much largor and longer
lived than the modern Ascidincean tadpole larva, nnd thus suitable for the ncotenous
trensformntion leading to thc diordat o line. If' the larva is inherited from another
group, then it still retains its basic ' chordate-like ' character, for i t is precisely this
ehmicter which enables it to carry out its function as a larva ; arid it becomes
possible to derive the chordate line from animals which were not absolutely sessile,
and were thus able to specialize their 1:~rv;~e
for life in the surfwe layers.
We may now corisider these adult animals which we assume to have given rise
to the chordates on the one hand, and the TJrochorda on the other. They possessed
a tadpole-likc larva, rather larger and less simplified than the present-day tadpole
larva, and not specialized for short range site selection. It seems most probably that
they were not aholutely sessile, for had they been, thcy would have been obliged t o
specialize their larva. for site-selection, and, moreover, as Carter pointed out, the
bilateral symmetry of the chordate line does not suggest a sessile stage in their
ancestry.
Thus fiir, we have reached a position similar t o that adopted by Carter, in assuming that the tadpole larva was inherited from an earlier group by the Urochordn, and
that this earlier group was not a sessile one. We cannot follow Carter further. He
assumed that these ancestral adult animals were free-swimming and were similar t o
their Iarvw (though larger and more complex). Since h e supposed the adult t o be
similar t o tho tadpole larva (hence, t o the chordate) he did not need t o assume that
neotrny had taken place, and suggested that the gradual modification of this protochordate adult led directly to the chordate line.
This view is attractive in its simplicity, but it seems necessary to reject it for
several rat'hcr different reasons. Firstly, we may reasonably ask why i t should be
suppowd that the protochordate adult should have been free-swimming ? Carter
suggested that the possession of an atrium by this form was an adaptation strengthening the body wall weakened by the gill slits, but in the life history of amphioxus
the atrium appears only upon metamorphosis and the adoption of life in the sand.
It is dific~ilt~
to see why a free-swimming adult should have possessed a free-swimming
tadpole larva, for, as Carter himself admits, development is likely to have been direct
primitively. A free-swimming adult animal does not require a free-swimming larva
for its distribution ; the pelagic Thaliacea have abandoned the larval stage although
signs of i t still persist in ontogeny. It seems more reasonable to infer that the ancestral
adult protochordate animal was semi-sessile, and required a free-swimming larval
phase for its distribution.
Secondly, there are signs that neoteny does take place in the lower chordate
groups, and it is not unreasonable to suppose that it may have taken place in the
origin of tho group. I n both Acrania (the amphioxides larva), and Agnatha (the
ammocoete larvae described by Zanandrea, 1957) larvae are known where the gonads
are well developed. It is not known whcther in either group, forms exist where the
gonads have matured in the larval phase, resulting in the production of a new type
by neoteny.
=nl
THE ORIGIN OF THE CHORDATES
261
Lastly, it is difficult upon Carter’s view, t o explain the position of the Hemichorda.
The affinities of this group with the echinoderms on the one hand, and the Acrania
and chordates on the other, are certainly remarkable, they have always been a stumbling block to theories of the ascidian-origin type, and appear equally difficult of explanation upon Carter’s scheme. These affinities will be discussed in the next section.
It is most probable that the adult protochordate form which gave rise t o the Urochorda and the chordates, was a semi-sessile animal with a tadpole-like larva as the
distributory phase in its life history ; and that the Urochorda are to be derived from
this form by the modification of the adult as a result of the adoption of a completely
sessile habit ; the chordates by the gradual neoteny of the tadpole larva. Carter’s
view that the protochordate adult was free swimming, and that gradual modification
without a neotenous transformation led t o the chordates, has, in my opinion, less to
recommend it.
AS CHORDATE
ANCESTORS
THEHEMICHORDA
The homologies of the tri-partite coeloms of the echinoderms ; hemichordates ;
acraniates ; and chordates are perhaps the most certain that have been found in
the whole of this field of speculation.
They open to the exterior by the premandibular pores, (in the chordate the premandibular coelom opens via the hypophyseal duct, de Beer, 1955), equivalent in
each group. The enteropneusts possess a dorsal pulsating vesicle (the glomerulus)
which is in origin and mode of action directly comparable with that in echinoderms,
and with the dorsal anterior glomerulus of the acraniates.
Lastly, the pharyngeal arrangements of the enteropneusts are closely comparable
with those of the Acrania on the one hand, and the Ascidiacea on the other (KnightJones, 1953) ; not only in the non-adaptive asymmetry of the ciliary apparatus, and
in the mode of control of this apparatus (see also Bone, 1958 a) but also in the possession of a prae-oral ciliary organ, equivalent t o the wheel organ of amphioxus and the
ciliary organ of the Urochordates.
It is not possible to dismiss these features of the Hemiohordates a s the result of
convergence (although this explanation may be true of the gill bars and their mode
of synapticulation, and even of the dorsal tubular nerve cord ; other ‘ chordate ’
features possessed by enteropneusts) : i t is necessary t o consider in what way these
animals have come t o share these features with the other groups discussed.
The chief difficulty in supposing that primitive Hemichordates gave rise t o the
chordate line, and independently, to the Urochorda, lies in their larva, the tornaria.
This is without a notochord, without a dorsal tubular nerve cord, and without myotome segmentation ; it much resembles the auricularia larva of the echinoderms.
These difficulties were partially avoided by Garstang’s well-known and extremely
ingenious theory of the notoneurula larva, fkst put forward in the last century
(Garstang, 1894), and later developed in his 1926 paper (Garstang & Garstang, 1926).
This hypothesis explained in a neat way several features of vertebrate anatomy (such
as the arrangement of the endostyle, the neurenteric canal, and, most strikingly, the
similarities in development of the head coeloms of the Echinoderms and the chordates).
What i t did not explain directly, was the origin of the notochord-myotome system.
These structures were regarded as later acquisitions of the notoneurula larva, resulting
from the pressure of selection towards a longer larval life in the surface layers. It
seems likely on any view that the myotomes did in fact arise in this way (and not, as
Berrill supposed, as the result of the animal trying to make headway up the river
systems), but that the notochord did so also, is perhaps less probable. However, it
seems reasonable to suppose that the notochord and tail muscle somites are closely
linked in origin (as they are in ontogenetic development (Tung, Wu & Tung, 1958))
and are in fact, to be considered as a single functional system. It is therefore possible
that both arose in the pelagic larva, a t one time, as an adaptation for increasing the
JOURN. LINN. S0C.-ZOOLOGY,
VOL. XLIV.
13§§
262
[J.L.s.z.
QUENTIN BONE:
period of larval li€e (the larva increasing in size, maintaining itself in the surface layer
by active swimming). After all, on any theory, whether that of the Urochordate
invention of the tadpole larva ; or that of the invention of this type of larva by an
early Hemichordate, the notochord and myotomes must have arisen a t some stage
de n o w , appearing in a larval type that did not previously possess one-6he difficulty
remains for either view.
Perhaps the simplest view, is that the modern Hemichorda (following KnightJones) are much specialized and paedomorphic representatives of the early Hemichordata ; and that it was the early Hemichorda which gave rise to the tadpole-
Appenaicuiaria
\
\
\
- .
\
Doiiolids
I
amphioxides
larva
\
Acrania
/
/
(secondarily semi -sessile;
redevelopnient of l a r v a )
/
/
GraDtolithina
FIR. 2.-Diagram illustrating the scheme of chordate origins proposed in the preeent account.
Groups assumed to have arisen by total neoteny are indioated by double underlining.
like larva with a notochord, muscle blocks in the tail, dorsal nerve cord and pharyngeal
arrangements of the chordate type. This larva would be physiologically adapted for
a longer and yet longer larval phase in the plankton as has been suggested above.
From this ancestral stock of Protohemichorda, the chordates and Uroohorda
were independently derived. The specializations of the adult form of these organisms,
led t o the Urochordates on the one hand (by adoption of a completely sessile habit,
and the consequent reduction of the larval phase) ; on the other, t o the chordates by
a process of gradual neoteny, and the omission ofthe adult type ; lastly, t o the modern
Hemichorda by the paedomorphosis of the original adult form (this perhaps accounting for the re-appearance of the ancestral larval form, and the absence of any trace
of the tadpole larva).
This view of the relationships of the groups discussed in this paper is illustrated
diagrammatically in Fig. 2.
XLIV]
THE ORIGIN O F TEE CHORDATES
263
Almost nothing is known of the structure of the adults of the eal'iy Protohemichorda, apart from what may be inferred by extrapolation from living Hemichordates, but it may perhaps be relevant to consider the Pogonophora in this connexion,
for although they are evidently peculiar, and bear no close affinities to any group now
living, they show some characters relating them t o the Hemichorda, and may
illustrate something of the character of the early Protohemichordates. Ivanov (1955),
who has studied this group from the most abundant material yet available, comes to
the conclusion that they are related t o the Hemichorda. He lists such points as the
tri-partite body ; unpaired first coelom ; pericardium ; coelomoducts of the first
segment ; dorsal nerve trunk ; and the development of secondary metamerism along
bhe trunk. The larvae of these forms are known only from a single specimen of
igiboglinum (which contained three larvae), recently described by Jagersten (1957)they are tripartite, ciliated and similar in appearance t o the larvae of Echinoderms
and Hemichordates. There are certain peculiarities, such as the yolk-filled gut remnant, and the presence of setae, which indicate that the larvae are not t o be closely
compared with those of other living groups.
Ivanov's account raised some interesting points. The pericardium is absent in
one group of Pogonophora ; the heart is developed along the ventral vessel (unlike
the hearts of the Hemichorda, but like those of the Urochorda and vertebrates).
The point is significant for it indicates that little weight is t o be placed upon the position of the heart in these various groups in deciding relationships. It may be that the
Urochordate heart is anatomically a t the centre of the system simply a s a response
to the needs of the animal with its relatively inefficient reversing circulatory system.
The accessory branchial hearts of the Acrania are obviously secondary developments,
it is clear that any vessel can potentially become contractile and then evolve into a
heart-the Acraniates show this condition in a n interesting stage.
Secondly, these forms have well-developed coelomoduds, which are used as
gonoducts. No trace of these structures is found in any living Urochordate, nor in
amphioxus (where the sexual products are released by rupture of the walls of the
gonad sacs into the atrium). The gonoducts have an excretory function as they have
i n the Pterobranchs. This arrangement would be an ideal starting point for the
vertebrate type of coelomic kidney ; much more suitable than that of the Urochorda.
The absence of gill slits and notochord in the Pogonophora may be regarded as
secondary specializations, consequent upon the loss of the gut, and the tubicolous
habit ; coupled with the development of the extra-ordinary lophophore system and
the highly peculiar method of feeding.
The importance of these animals in the present connexion, is that they show
several features which relate them t o the Hemichordates, but in which they are more
' chordate-like ' than that group. Perhaps the strong cuticularisation of the body
wall argues a stage in evolution when this could either be altered to form the Urochordate test, or could be lost, as in modern Enteropneusts. If the phylum Pogonophora is correctly regarded as related to the Hemichorda, then the special characters
that the group shows certainly do not argue against the common ancestry of the Urochorda and the Hemichorda from the Protohemichorda, and the development of
the chordate line from this stem-rather, they tend t o support the derivation of these
groups from a semi-sessile Protohemichordate which had not specialized its feeding
mechanism to the lophophore type, had not developed a tubicolous habit, and possessed a tadpole larva.
THE RELATIONSHIPS
OF THE ACRANIA
Finally, on the scheme put forward in the present paper, what are the relationships of the Acrania ? The striking similarities in development between amphioxus
and the Ascidiacea, well-known from Conklin's classical researches, have hitherto
264
QUENTIN BONE :
[J.L.s.z.
been interpreted to mean that the Acrania have been derived relatively recently from
the Ascidiacea (eg. Medawar, 1951).
On the view developed above, they are t o be interpreted a0 the result of common
inheritance from the Protochordate ancestor ; in each group, the ' chordate ' characters of the larva have been retained, for they have been functionally useful in rather
different ways, so that the features of the two fate maps in which striking similarities
are seen are just those features which both groups require in their larvae. It is worth
emphasizing that in the Acrania, the classical amphioxus type of development, that
is given in all texts (from the detailed account hy Willey (1891)),is not necessarily
typical of the group ; it seems probable that the slower ' amphioxides ' type of
dcvrlopment is typical for the Acrania (Fuller, 1957), and that amphioxus itself
(Rmnrhioatoma lanceolatus) shows Acraniate development in a much compressed and
altered form. The typical development for the group shown by the amphioxides
larvae, is rather similar to that postulated for the larva which gradually paedomorphosed to the chordate line ; as we have seen, amphioxides larvae are apparently
recapit,iilnting the evolutionary history u i the chordates a t the present time !
What seems clear ahout the Acrania, is that they represent the early paedomorphosed chordate type of animal, produced from a semi-sessilestock by gradual neoteny ;
and that they have lost their claim t o chordate ancestry by the secondary adoption
of a sessile habit. It is suggestive that the short-lived amphioxus type of larva is
produced (apparently secondarily) by a semi-sessile adult form ; and that the Asymmetrontide (which are less definitely sessile, adults being found a t times in plankton
hauls, Bigelow and Farfante, 1948), produce amphioxides larvae of the longer-living
type. Possibly, therefore, amphioxus is more specialized than are other acraniates,
and is gradually becoming more and more definitely sessile, selection upon the larva
tending in exactly the same direction as that upon the tadpole larva of the Ascidiacea,
towards reduction and compression of the larval phase.
In the view outline above, the Acrania are free-swimming neotenously produced
adult forms, which have secondarily adopted a sessile habit, and thus re-acquired a
metamorphosis (which is the least drastic of any in all the groups that we have
considered).
Attempts to link the metamorphosis of Acraniates with that of Ascidiaceans
(thus explaining the asymmctry of the amphioxus larva) deserve consideration, but
an ecyutdly probable case can he made out for regarding this asymmetry :LS adaptive,
and Hecondary, related t o the peculiar method of feeding of the larva, (Bone, 1958 b ) ,
Tn any case, the total absence of asymmetry in thc development of the chordate
pharynx argues that the asymmetry of the Acraniates is a secondary phenomenon
and that the original Iarvttl form from which the chordates were derived was symmetrical in its pharyngeal arrangements.
Thifipeper is entirely speculative, in the absence of fossil evidence, and the extreme
unlikelihood that we shall ever possess such evidence, different theories of chordate
origins ran oo-exist ; that which is held will be largely a matter of personal preference.
The vicw advanced in the present paper is suggested as an alternative to the more
recently publicized ascidian-origin theories ; it is desirable that if two plausible
alternatives cxist, both be stated.
ACKNOWLEDGMENTS
I am indebted t o Mr. H. K. Pusey and Dr. Mary Whitear for helpful discussion of
several of the points in this paper ; which was written during the tenure of a prize
fcllowship in Zoology a t Magdalen Collegc, Oxford.
XLTV]
THE ORIGIN OF THE CHORDATES
265
LITERATURE
CITED
BEER,G . R. 1955. The continuity between the cavities of the Premandibular somites and of
Rathke’s pocket in T‘orpedo. Quart. J . micr. Sci., 96 : 279-283.
BERRILL,N. J. 1955. T h e Origin of the Vertebrates. Clarendon Press, Oxford.
H. B. & FARFANTE,
L. P. 1948. Fishes of the Western North Atlantic, Mem. I, pt. I.
BIGELOW,
Sears Foundations Mar. Res.
BONE,Q . 1957. The problem of the ‘ amphioxides ’ larva. Nature, L d . , 180 : 1462-1464.
- 1958 a. Nervous control of cilia in amphioxus (Branchiostoma). Nature, Lond., 181 :
193-194.
- 1958 b. The asymmetry of the larval amphioxus. Proc. Zool. SOC.Lo&., 130 : 289-293.
CARLISLE,
D. B. 1951. On the hormonal and neutral control of the release of gametes in Ascidians.
. I . P T D . Biol.. 28 : 463-472.
CARTER,
G. k. 1957: Chordate Phylogeny (review of ‘ The Origin of Vertebrates ’ by N. J. Berrill).
Sust. ZOO^., 6: 187-192.
CONKL&,E. G. 1905. Organization and cell lineage in the Ascidian egg. J . AcacE. nut. Sc. Phila.,
13 : 1-119.
__ 1932. The rmbryology of Amphioxus. J . Morphol., 54 : 69-151.
FULLER,9.
8. 1957. Personal communication.
GARSTASG,
W. 1894. Preliminary note on a new theory of the phylogeny of the Chordata. Zool.
A m . , 17 : 1.
__ 1928. The morphology of the Tunicata, and its bearings on the phylogeny of the Chor.
data. Quart. J . micr. Sci., 72 : 51-187.
GARSTAKG,
S. L. & GARSTANG,W. 1936. On the development of Botrylloides and the ancestry of
vertebrat.es (preliminary note). Proc. Leeds. phil. Zit. Soc., 1 :81-86.
GOLDSCHMIUT,
K. 1906. Amphioxides. 1Viss. h’rgebn. Deutsche Tiefsee Exped. (‘ Valdivia ’), 12 :
1-92.
GURNEY,R. 1942. Larcae of Decapod C:ru,stacea. Ray SOC.Lond.
IVANOV,
A. 1955. The pogonophora as a new phylum. Dokl. Akad. NauE. S.S.S.R.,
100 : 3, 595
(in Russian).
JAGERSTEN, G. 1957. On the larva of Siboglinum. Zool. Bidr. Uppsala, 32 : 67-79.
KNIGHT-JONES,
E. W. 1953. Feeding in Saccoglossus (Enteropneusta). Proc. zool. SOC.Lond.,
123: 637-54.
LOHMANN,
N. H. 1922. Oesia disjicncta Walcott, eine Appendiculerie &usdem Cambrium. Mitt.
-001. St. inst. Ham,b., 38 : 69--75.
MEDAWAR,
P. B. 1951. Asymmetry of larval Amphioxus. Nature, L d . ,167 : 852-853.
TUNC,T. C., WU, S. C . & TUNG,Y. E. 1’. 1958. The development of isolated blastomeres of
amphioxus. Aetae biol. ezp. Sijziea, 6 , no. 1. (In Chinese, with English summary.)
WHITEAR,
M. 1957. Some remarks on the Ascidian affinities of vertebrates. Ann. Mag. nut. Hist.,
(12), 10 : 338-347.
__ 1958. Personal communication.
WILSON,D. P. 1955. The role of micro-organisms in the settlement of Ophelia bicornis Savigny.
J . mar. biol. Ass. [T.K., 34 : 531-543.
WILLEY,A. S. 1891. Tlie later larval development of amphioxus. Quart. J . micr. Sci., 32 : 183335.
ZANANDI~EA,
G. 1967. Neoteny in a lamprey. Nature, Lond., 179: 925-926.
DE
DISCUSSION
A discussion followed the reading of Mr Quentin Bone’s piper which it has been
thought desirable to publish along with it rather than separately in the Proceedings
of the Society.
Dr G. S. Carter, F.L.S. said :I have listened with great interest to Mr Bone’s discussion, none the less for my
inability t o agree with a good many of his conclusions. I am grateful for the
opportunity of stating my position.
First, I should like to make clear what I think about the general question of
neotenic or paedogenetic evolution, for I do not think that Mr Bone appreciates my
position fully. That neoteny occurs in chordates and other animals is, of course, not
disputed-the axolotl is a clear enough example. But that does not establish that
neotenic evolution, by which I mean loss of the original adult and a new evolutionary
line from its neotcnic young, has a real place in the evolution of animals. It seems to
me important t o keep these two conceptions distinct; that we accept the first is
by itself no reason why we should accept the second.
266
QUENTIN BONE:
[J.L.s.z.
When we consider the reality of neotenic evolution, I think it important to insist
that new interpretations should not be postulated unless we are quite sure that the
facts arc not covered by the processes that we already accept-ee?iCia non sunt
multiplicanda praeter necessitatatem-and I emphasise necessitatem. I believe that all
the eiises that have been put forward as examples of neotenio evolution, with perhaps
a very few exceptions, can be covered by the chssiml and gcncrally accepted processes
of rvolution. If 80, there is no reason t o postulate neotenic evolution for them.
To my mind it is in any case not enough in proof of neotenic evolution to show
that the adult of one group has characters which are confined to larval stages in
anothcr group. Both groups may have evolved from a conimon ilncestor that had
these characters in the :Idult, and they may have been lost in the later evolution of
thc group that no longer has them. The adult of the group having them may then
have been evolved by direct, and not neotenic, evolution from the common ancestor
adult into adult and young into young. I think that we should only postulate an
origin by neotenic evolution when the ad:ilt of the group believed to have been so
evolved has rharacters that eaii only have bccn larval in the common ancestor. And
by no means always even then. Take, for instance, the perennibrimchiate Amphibia,
which are often quoted n s one of the clearest cxamples of neotenic evolution. The
argument runs as follows. Their external gills are organs that can only be in place
in aquatic animals, nnd yet we are told that these amphibians are descended from
trrrestrid ancestors. If so, the gills must have been organs of the Iarvee of these
ancestors, and so the perennihnchiates must h&ve evolvcd by neotenic evolution.
Rut we know that movement up and down the life-history of the stages ai which
organs develop occurs commonly in evolution, by hetcrochrony. Surely, the
presence of external gills in the modern adults may have been due ta retardation by
hctrrochrony, and this may also have been true of others of their organs that show
adaptation to their aquatic habit. It seems t o me morc likely that it was.
Evolutionary neoteny is a possible mode of evolution, but it is very difficult t o
prove that it took place in any particulnr instance, though perhaps this can be most
nearly done for the Larvacea. If it did occur there or elsewhere in the ancestry of
the chordates, I should agree that its origin is more likely to have been gradual than
sudden, though even here there may be some reason for doubt ; fcr it seems to me
that a suddcn mutation making the animal bearing it sterile with the surrounding
population can survive provided it is recessive and provided that the inbreeding is
closc. Whether these conditions could hold in the phylogeny we are discussing I
cannot say.
To pass from these generalities to the special case of chordate evolution. I want
to keep my discuesion general so far as that is possible, for I think that in questions of
high phylogeny such as these there are so many opportunities for mistake if we give
weight to details that the discussion is doubtfully worth-while.
1 think that most of the differences between Mr Bone’s interpretation and mine
derive from our different conceptions of what the general course of the evolution is
likely to have been like, I have accepted the modern view that in progressive
groups evolution normally takes the form of a series of radiations of anirnid types
when they become successful, and lretween each pair of radiatioris the evolution of a
new type in one of the radiating lines. I have regarded the Urochordata, Acrania
and Vertebrata as originating by such a radiation from a common ancestral group,
and to have differentiated litter in adaptation to their very different habits of life.
On the analogy of better-known radiations we must regard the separation of the groups
to have been simultaneous rather than successive, and the adaptational characters of
the groups (especially those of metamorphosis) must therefore be irrelevant t o
discussion of the nature of the common ancestor. I have regarded the Heinichordata
as an earlier offshoot of the chordate line of descent, as shown most clearly by the
abeence in them of a dorsal post-anal tail, which seems to me an important character
associated as it is with the overgrowth of the dorsal blastopore lip. If we must
=wl
THE ORIGIB’ OF THE CHORDATES
267
accept that the ancestors of the Hemichordata had a tadpole-like larva that would
only push that type of development further back in the phylogenetic tree. I see no
reason why they should not have had both a tornaria and a tadpole-like larva a t
successive stages of their development. The Pogonophora and the graptolites may
have been other groups derived from the chordate stock a t a very early stage, possibly
in the same radiation as the Hemichordata. I therefore agree with Mr Bone’s
phylogenetic tree except that I place the origin of the Hemichordata earlier than he
does.
We have no evidence of what the common ancestor of the Uro and Euchordates
was like, but it was a primitive animal and it has seemed t o me natural to suppose that
its development would have been direct, since direct development is certainly
primitive and I know no reason to suggest anything else. It would then have had no
metamorphosis and therefore no larval stage, if by a larva we mean a developing
animal adapted to a life different from that of the adult and possessing organs later
lost or modified a t metamorphosis. This adult would have the type of organisation
we know in the larvae of the groups evolved from it, the tadpole-like larvae. It
would be larger and more elaborately organised but not fundamentally different in
its organisation. This I have thought to be the best we can do in trying t o picture
what the adult of the common ancestor was like. If this interpretation is right, there
is no reason to ask for neotenic evolution a t this stage of chordate evolution. All
the groups derived from this ancestor would be evolved directly fiom the adult.
Lastly, I should like t o say why the objections raised by Mr Bone to my interpretation do not seem to me conclusive. First, it is hardly unreasonable t o suggest that a
free-swimming adult should have free-swimming early stages in its development.
Copepods, many fish, whales and planktonic protozoa-to name only a few of the
major groups of free-living marine animals-are all free-living for the whole of their
life-histories. Secondly, the atrium is certainly formed in Amphioxus a t about the
stage of metamorphosis, but that does not prove that it was evolved in adaptation
t o the conditions of metamorphosis ; change of function in evolution is a very
general phenomenon. I suggest that it was evolved in the common ancestor a t the
stage of development when i t was needed t o strengthen the pharyngeal region of the
body as the animal grew and its size increased. This stage may well have been that
which evolved later into the stage of metamorphosis in Amphioxm. Thirdly,
neoteny undoubtedly occurs in chordates, but, as I have said earlier, this is not
evidence for the occurrence of neotenic evolution in them, Lastly, I think that
my scheme accounts plausibly for the relationships of the Hemichordata.
I agree that it is unlikely that we shall ever reach general agreement on these
questions of high phylogeny. But I do not think that that means that they have lost
their interest. It is good t o have the opinions of zoologists concerning them
reconsidered from time t o time in the light of increasing knowledge, however various
the conclusions may be.
Dr Mary Whitear said :-
My remark on a ‘ sudden step ’ in the origin of the vertebrates, which Mr Bone
referred to, concerned a change in the length of the notochord, which is a necessary
part of a transformation from Urochordate to Vertebrate.
While I agree with Mr Bone on the distinction between first and second types
larvae, there is no objection to my early Urochordate larva being of second type and
feeding. As the trend in modern Ascidians is towards a n abbreviation of larval life,
one might expect the larvae of ancestral forms to spend longer in the plankton.
Mr Bone’s ‘ family tree ’ of Chordates is not so very unlike mine ; the main
difference is that he has written ‘ Protohemichorda ’ where I would write ‘ early
Urochordate ’. My objection to his version is that the vertebrate ancestors must have
had a notochord, and, if the Protohemichordates had a tadpole larva, why is there no
268
QUENTIN BONE :
[J.L.s.z.
notochord in any surviving Hcmichordate? I should put the Hemichordates where
Dr Carter puts them, lower down.
My only comment on Dr Carter’s remarks is that neoteny is such a useful
concept, as (L means of escaping from specialization, that it would be a waste riot to
use it. Carstang’s idea of a neotenous tadpole larva (not his ‘ Notoncurula ’) seems
to me the most economical view.
Dr P. H. Whiting said :Dr Bone has not mentioned the recent note by Wickstead and himself. It seems
relevant to his argument and some of hiN audience may not have seen it. It is in
12th December number of Nature, 1989, and is headed Ecology of Acrmiate larvae.
I do not think an attempt t o elucidate the relationships of the chordate animals
should be termed ‘ unimportant ’. I n research of any sort it is not possible t o say
beforehand what will be discovered or estitblished that is a t present unlmown, still
less that what will be learned will finally prove ‘ important ’ or ‘ unimportant ’.
As to the lineage of Amphioxus, I prefer to kccp an open mind in spite of the
considertitions Dr Bone has put forward. Rut in some respects I think he hais hardly
done justice to the weight of thc evidence given by Professor Berrill.
In particular Dr Bone has not mentioned the experiments of Grave and others,
qiioted by Berrill, in which ii change in the environment of the ascidian tadpolealteration in pH, or in copper or iodine content-were found to produce marked
changes in the rate of metamorphosis and on the form of the animal. Such effects
might occur naturally and might have great importance in producing great changes
in the life-history.
Also I think Dr Bone has not considered the possibility of there being fuio larval
utages developed in the life-history of a ‘ Tunicate ’ line giving rise to the Cephielochordates. Two contrasting larval stages are not after all so uncommon-for
example, the proammocoetc and the ammocoete larval stages of the lampreys.
Thirdly, the similarity between the awidian tadpole and thc young Amphioxus
and young vertebrate is greater in some ways than has been stated by Berrill. The
swimming muscle in the tail of the ascidian tadoplc is usually described 8s
lying against the sides of the notochord and being unsegmentcd. But the embryo
dogfish has myofihrils, not conforming to ti segmental pattern, a t the sides of the
notochord in a long slender ‘ precocious band ’ which was first noticed by F. M.
Balfour. There is also a band of endoderm running below the notochord in the
ascidian tadpole in the position of the Amphioxus and vertebrate alimentary canal.
This is described but not figured by Berrill.
On a small and separate point, I believe Dr Bone placed some weight on an opening to the exterior of the coelom of the premandibular pair of somites. I thought
recent work [Wcdin, R. 1952. K m . Ned. Akad. Proc., 55, C. : 4161 had cast some
doubt on the reality of such a conncction.
Professor E. J. W. Barrington, P.L.S. said :I should like to throw the endostyle into the arena! I
know that this is only a
single element in the situation, but it is one which must find a place in any complete
picture of vertebrate origins, and it is important because our interpretation of it will
affect our ideas on the origin of the thyroid gland. It is very well known that this
organ is already present in lampreys, and that it develops from the endostyle a t the
metamorphosis of the ammocoete larva. We now know that the larval endostyle is
capable of binding iodine organically, and that it synthesises thyroxine and probably
also triiodothyronine, and we also know that it is not, as one might expect, the
glandular tracts which do this but actually the simple epithelium which forms the
wall of the endostylar chamber. Now the endostyles of Amphioxus and Ciona can
also bind iodine, and we know that thyroxine is certainly synthesised in Ciom as a
result of this, and that it is probably formed also in Amphioxus. Moreover, the
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&HE ORIGIN OF THE CHORDATES
269
whole situation is remarkably like that found in the ammocoete, for in both genera
there are specialised iodine-binding cells in the epithelium above the glandular tracts
and i t is doubtful whether the latter are involved at all. I should find it very difficult
t o accept that these very close similarities could have arisen independently, and I
should prefer to believe that there must have been a common ancestor in which an
iodine-binding endostyle was already present. The Hemichordata can hardly be
said to fill this place, and in this respect, therefore, I find myself more in agreement
with the views of Carter. Certainly a t this stage I should be most unwilling to
remove the Tunicata from the main line of vertebrate evolution.
Dr L. B. Tarlo said :I n any discussion of the origin of the vertebrates it is necessary to consider the
fossil evidence, as I have recently done in a paper now in press (Proc. Int. Pal. Union,
Int. G e d . Congr. Copenhagen, 1960). Most of the fossils which have previously been
considered relevant can now be dismissed. The supposed appendicularian tunicate
Oesia from the Middle Cambrian is in fact an annelid, and Janioytius from the
Silurian which was considered a naked form has, on further development, been shown
t o possess scales ornamented like those of the Anaspid ostracoderms.
The only unequivocal fossil evidence of prevertebrate chordates comes from the
Tremadoc (lowest Ordovician). Kozlowski (Palaeontologia Polonica Vol. 3, 1949)
described a varied fauna of sessile benthonic graptolites, pterobranchs, acanthastids
and many other groups, and at the same time he firmly established their hemichordate affinities. It is thus clear that early in the palaeozoic era the hemichordates
were undergoing a considerable evolutionary radiation. Qarstang (1928) demonstrated the potentialities of larval evolution, thus enabling us to consider sessile
benthonic animals as likely ancestral adults which could have produced ' tadpole
larvae ' and hence the vertebrates.
Mr Bone derives the first vertebrates from a ' proto-hemichordate ', whilst Dr
Mary Whitear derives them from a ' proto-sscidian ', but as she has stated (1957) if
one extrapolates the ascidian line backwards one arrives a t an animal very like a
pterobranch hemichordate. I n my opinion there is a t this stage no essential
difference between a ' proto-hemichordate ' and a ' proto-ascidian '-it is merely a
question of terminology. Whatever term is used one can expect the vertebrates to
have emerged out of such a host of evolving forms as Kozlowski described, rather than
from any isolated genus.
The President, summing up the discussion, thanked Mr Bone for his stimulating
paper and also the members and others who had contributed to the discussion.