Yet another defence of the calcichordates

[(Richard Jefferies) <rpsj@xxxxxxxxx>]

On Thursday 22  May, Dick Jefferies writes: 
  
  The  title echoes  two previous papers  (Jefferies 1981, 1997). 

  I was surprised  to read, in the message from Jo Murukami of 14 May 1997, 
that the calcichordate theory of the origin of chordates had been 
successfully refuted by Claus Nielsen on pp. 377-378 of his 1995 book 
`Animal Evolution - interrelationships of the living phyla'.
  
  This was not what I remembered. However, Claus is a friend of mine and a 
very learned man, so I again  looked  up the pages referred to. I 
still do not think, of course,  that  his  refutation was successful. Let 
me quote the passage in question with my comments enclosed in square 
brackets [].  

Nielsen: "A totally different phylogeny of the deuterostomes, the 
calcichordate theory, has been advocated in a series of recent publications 
by Jefferies (summarised in 1986)."

  [Comment: As Henry Gee has pointed out in his Paleonet message 
of 15 May, the matter has advanced considerably since I published my book. 
Most of what I said in it still stands but we now have much more extensive 
information. Thus, for example, Tony Cripps has worked on the cornute-
mitrate transition (1989a, 1989b, 1990, 1991, Cripps & Daley 1994). Paul 
Daley (1992, 1995, 1996) and I (1990) have  studied the solutes and, by 
implication, the events that occurred when echinoderms and chordates first 
separated from each other. Ian Woods has reconstructed locomotion 
in Cothurnocystis (Woods & Jefferies 1992).  Fritz Friedrich has 
monographed the Cincta (1993). Individual mitrates have been studied by 
Mario Beisswenger (1994), Marcello Ruta (1997a, b) and Adam Craske 
(Craske & Jefferies 1989).]

   [As a consequence of all of this, we can now place all the `carpoid' 
groups (the solutes, cornutes, mitrates, ctenocystoids and helicoplacoids)  
in their broad phylogenetic position as stem-group dexiothetes, stem-group 
echinoderms, stem-group chordates, stem-group acraniates, stem-group 
tunicates or stem-group craniates (Jefferies, Brown & Daley 1996). In that 
same paper I made various guesses about gene expression  in extant 
chordates, mainly on the basis of the theory of dexiothetism i.e. that the 
echinoderms and chordates had in their exclusive common ancestry an episode 
in which a Cephalodiscus-like ancestor lay down on the right side.]

   [In addition, Henry Gee has written an excellent general book (1996) 
which should make the whole problem  more intelligible to interested  
outside readers. Also, Kevin Peterson has published criticism of the 
calcichordate theory (1994, 1995) and I have answered him (Jefferies 1997).]

Nielsen: "It is based  on a very detailed interpretation of the Palaeozoic 
group Carpoidea of Homalozoa, which  by most palaeontologists, such as 
Ubaghs (1975) and Philip (1979), is regarded as non-pentameric echinoderms. 
The more traditional view is that the carpoids had an asymmetrical body  
with a series of openings, which could have housed retractile gills, and 
one articulated arm possibly with tube feet and possibly a feeding organ."

  [Comment: It is totally wrong to think that the views of the opponents of 
the calcichordate theory are consistent with each other. There is no 
generally accepted doctrine accepted by all sensible people, on the one 
hand,  as  opposed to  the cranky opinions of Jefferies & Co. on the other. 
Thus Ubaghs, for example, believes that the jointed appendage of mitrates 
and cornutes was a feeding arm, but Philip does not. In my view, the Ubaghs 
interpretation  is disproved by the solutes which possess an obvious 
feeding arm at one end of the animal and a homologue of the cornute and 
mitrate appendage (for me the tail) at the other end.]

Nielsen: "Jefferies' interpretation of the series of openings is that they 
were gill slits like those of amphioxus and that the long jointed 
appendage was a tail with chorda and neural tube; the body should 
have housed a spacious branchial chamber like that of tunicates and 
cephalochordates. This group of organisms, called calcichordates, 
should then have given rise to the echinoderms and chordates. The theory 
completely disregards the similarities between the gill slits of 
enteropneusts and chordates." 

  [Comment: This last sentence seems to refer to the classical comparison 
between the gill slits of amphioxus, on the one hand, and those of the 
enteropneusts on the other. I dealt with this on pp. 25-27 of my 1986 book. 
In both groups the gill slits are fundamentally U-shaped, ciliated, 
supported by cartilage, crossed by trabeculae and associated with coeloms 
in the gill bars. However, the U-shape is a fairly obvious adaptation to 
increase the length (and therefore the number of cilia) of each slit. It 
could easily have evolved  twice. Moreover the supporting cartilages are 
not in detail comparable and the trabeculae are an  obvious strengthening 
device, easily acquired twice. Also the coeloms of the two groups  differ 
in their relation to the gill bars - in amphioxus the primordial bars 
(between the U's) have coeloms and  the tongue bars do not, while in 
enteropneusts the  converse is true. Additionally, the ontogenetic 
development of the gill slits is different. It is very complicated in 
amphioxus: there is a primary left set in the larva, a secondary right set 
that appears suddenly at metamorphosis and a tertiary set added throughout 
the later life of the animal, at right and left behind the primary and 
secondary sets already present. There is no such complexity in 
enteropneusts where new  slits are simply added posteriorly, symmetrically 
on right and left. I conclude that there is no good reason for regarding 
the detailed structure of the gill slits as being homologous between 
amphioxus and enteropneusts. I might add that the structure seen in 
acraniates such as amphioxus (Branchiostoma and Epigonichthys (=
Asymmetron)) is never seen in other chordates, so I do not see why it is 
regarded as so important as an indication of what primitive chordate gill 
slits were like.] 

Nielsen: "The interpretation of the gill slits is proposed axiomatically : 
`Since the openings suggest outlet valves, they can plausibly be seen as 
gill slits.' (Jefferies 1986, p.197). However, it is very difficult to see 
how the pharynx of the reconstructed cornutes (for example Cothurnocystis; 
Jefferies 1986, Fig. 7.6) can be compared to the gill chamber of a living 
tunicate or cephalochordate; both of these types have a gill chamber with 
large areas of gills, which both carry the ciliary bands creating the water 
currents and support the mucus net which is the filtering device. If the 
mucus filter extended only across the row of gill slits in the cornute, the 
filtering area would have been disproportionately small both in relation 
to the size of the pharynx and  to the size of the whole animal when the 
living organisms are considered. A possibility not considered by Jefferies 
is of course that the `gill slits' were merely exit openings for the 
filtered water and that the filter was a more extensive structure 
somewhere else in the `pharynx', but this brings the speculations into the 
realm of fantasy."  

  [Comment: Fossil evidence does not answer all questions but has been  
too easily dismissed. It is  much better than no evidence. This is 
particularly true for the mitrates, with their very complicated informative 
skeletons. In them the pharynx can be reconstructed rather fully. In 
several, often asymmetrical, details it compares with the pharynx of 
tunicates. These statements are  based on interpretation of fossil  
evidence, not `fantasy'.]

  [Thus in the mitrates Mitrocystites, Mitrocystella and Placocystites 
plausible positions can be found for the right and left peripharyngeal 
bands, the ciliated organ (situated near where the peripharyngeal bands 
meet dorsally as in tunicates), the dorsal lamina (sloping downwards and 
rightwards in transverse section as in tunicates), the opening of the 
oesophagus (right of the mid-line as in tunicates), the posterior end of 
the endostyle, the retropharyngeal band (passing from the right posterior 
corner of the endostyle towards the opening of the oesophagus as in 
tunicates),  the pharyngo-epicardial openings (right and left of the 
retropharyngeal band as in the tunicate Ciona) and  the epicardia 
(situated posterior to the pharynx as in tunicates). Moreover, in the 
mitrate Placocystella the whole extent of the endostyle is indicated (Ruta 
1997a). Also there is clear evidence, in all mitrates, that the left 
pharynx preceded the right pharynx in ontogeny, as in amphioxus. I have 
argued all this in several publications (e.g. Jefferies 1981).]

  [It is therefore likely  that mitrates fed, as tunicates do, by a mucous 
filter secreted by the endostyle, held anteriorly by the peripharyngeal 
bands, rolled up in the dorsal lamina and passed rearwards to the opening 
of the oesophagus. There is some evidence that the internal surface of the 
pharynx was corrugated where the mucous filter was situated and such 
corrugations may have served to hold the filter away from the pharyngeal 
wall. Very likely, also the corrugations would be ciliated to provide a 
pump for the feeding current. In that case the functions of the gill slits, 
deduced to have existed, would be simply to let water into the atria.]
 
  [Cornutes would have fed in the same way except that there was 
no left pharynx. The lack of such a pharynx does not prevent feeding in 
larval amphioxus where the endostyle is fully functional (Olsson 1983).]

  [The fact that the cornutes, like larval amphioxus, had left gill 
slits only is a bizarre resemblance. All those who consider, like Claus 
Nielsen,  that the calcichordate theory is fantasy, should contemplate this 
resemblance for a couple of minutes.] 

  [In most mitrates the evidence for gill bars and slits is circumstantial.
However, in two mitrates we now have direct evidence - the stem-group 
acraniate Lagynocystis (Jefferies 1973, 1986; Gee 1996, Fig. 4.14, p. 243)  
and the stem-group tunicate Jaekelocarpus (Jefferies, 1997, Fig. 5, p. 6).]

  Nielsen: "A functionally even more improbable explanation is the 
interpretation of the closely related Scotiaecystis, which had a long 
series of closely fitting, chevron-shaped ossicles in the same position 
as the `gill slits' of Cothurnocystis. These ossicles would appear to 
close the slits, but the following explanation was offered: `When water 
pressure was high inside the head the dorsal integument would inflate 
upwards. The chevron complex, bisecting the integument and therefore 
situated along the line of maximal stretching, would itself be stretched 
and gaps between the chevrons would open, allowing water to escape' 
(Jefferies 1986, p.207). It is unclear how the pressure inside the head/
pharynx would be created. In living tunicates the pharynx/ gill 
chamber is kept expanded by the elastic tunic and the ciliated gill 
bars pump the water through the mucus filter out of the pharynx;  there 
is, accordingly, a slightly higher pressure at the exhalant siphon than 
inside the filter (Riisgard 1988). If the pressure were to have been 
higher inside the pharynx of Scotiaecystis, a mechanism unknown 
in living tunicates or cephalochordates would have been present, 
and the discussion again becomes mere fantasy."

  [Comment: In order to pass water through a mucous pharyngeal filter of  
primitive chordate type there has to be a pump. From the engineering point 
of view, this pump can be located anywhere in the stream. It can be 
upstream of the filter, as with the muscular contractions of salps or the 
velar pump of ammocoete larvae, though such a pump may  require a valve  
upstream to prevent back-flow. Or it  could be downstream of the filter, 
depending on the action of cilia in the gill slits, as in ascidians or 
amphioxus. Or,  conceivably,  it could be between the filter and the gill 
slits, depending on the action of cilia in a  corrugated pharyngeal wall 
as may well have been true in mitrates like Mitrocystella. Pressure will 
be at a maximum immediately downstream of the pump, wherever the latter is 
located, but will decrease by friction wherever the current  passes, or 
passes through,  an obstacle, as with the oral or branchial siphons of a 
tunicate or with   the mucous filter itself. Both in Cothurnocystis and 
Scotiaecystis, the integuments were flexible and probably  muscular and the 
walls of the pharynx in Cothunocystis seem to have been corrugated and may 
have been  ciliated. Upstream  valves could have been present at the mouth 
(closed by a sphincter) and perhaps  at the junction of pharynx and buccal 
cavity (the velum). Consequently muscular or ciliary action, or both, could 
easily have forced water through the mucous filter and opened the gill 
slits by passive response, as their outlet valve structure suggests. Such a 
mechanism  is not fantasy but  reasonable supposition. Contrary to Nielsen, 
there is no reason why the pump should have taken the form of  cilia in the 
gill slits and in the case of Cothurnocystis and Scotiaecystis I have never 
supposed that it did.] 

Nielsen: "The reconstructions of notochord and spinal chord with ganglia in 
the articulated extremity and of nerves, ganglia with eyes, even, in the 
head/body of the Middle-Ordovician Mitrocystella and other mitrates, 
interpreted as early vertebrate ancestors, appear as extreme examples of 
wishful thinking."

  [Comment: Such blanket dismissal of fossil evidence is depressingly 
common but  difficult to counter. I assert, however,  that fossil evidence 
is better than no evidence and that there are complicated observed features 
on which the reconstructions are based. My students and I have published 
photographs of the fossil evidence for the nervous system in many places. 
Thus the spinal ganglia of the mitrate Lagynocystis, for example, are shown 
in Jefferies (1973, Pl. 43, figs 45, 46). The spinal ganglia, connected 
with the dorsal nerve cord overlying the notochord, of the mitrate 
Mitrocystites can be seen in Jefferies (1973, Pl. 39, Figs 32, 33). The 
spinal ganglia of the mitrate Chauvelia are to be seen in Cripps (1990, 
Fig. 3i). The bipartite brain of Mitrocystites and Mitrocystella, divided 
into prosencephalon and deuterencephalon with the optic foramen antero-
ventral to the prosencephalon, is shown in Jefferies & Lewis (1978, Pl. 11, 
Figs 110-113, Pl.13, Figs 121, 123). The branching nerves of the palmar 
complex, mainly trigeminal but also optic, can be seen in Jefferies & Lewis 
(1978, Pl.9, Figs 98, 99). Cripps (1990, Figs 12-14)  has demonstrated how, 
in the mitrate Chauvelia, the acoustic and lateralis ganglia are directed 
connected with the part of the brain where, by comparison with modern 
fishes, the acustico-lateralis nuclei ought to have been located.]       

  [The calcichordate theory is not fantasy. It is tied down to fossil 
evidence in hundreds of observed details of which it provides a coherent 
explanation. I cannot understand, therefore, why some dismiss it so easily, 
whereas the  work of Garstang (1928), for example,  is widely accepted 
without any  evidence whatever.] 

Nielsen: "Consequently, I reject the calcichordate theory on functional 
grounds, in accordance with a number of other authors who have rejected it 
on other grounds (Philip 1979, Ubaghs 1975, Jollie 1982)."

  [Comment: The functional grounds are very weak. Also, as already stated, 
it is not true that the cited  authors agree with each other.]

  [Any phylogenetic  argument based on fossils is difficult to present 
because neontologists have no feel or respect for fossil evidence. I 
emphasise, however, that  the calcichordate theory has great explanatory 
power, presupposes the close relationship of chordates with echinoderms 
which is generally accepted, and is based on innumerable detailed 
observations.]

  [In particular, unlike its rivals, it can explain the numerous  
asymmetries of echinoderms and primitive chordates as Haeckelian 
recapitulations. Claus Nielsen, and those who agree with him, should 
confront the fact that the gill slits of Cothurnocystis, like those of 
larval amphioxus, are left gill slits only.]

  [I hope Paleonetters will have some sympathy for my position.]

  [I am grateful to my friend David Hardwick, of the Civil Engineering 
Department, Imperial College, London, for highly professional advice on 
pumps.]

References.

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====================================================
R P S Jefferies
Department of Palaeontology
The Natural History Museum, London SW7 5BD, England

Telephone: +44 (0)71 938 8713
Fax:       +44 (0)71 938 9277
JANET:     r.jefferies@uk.ac.ic.nhm
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