Table Of ContentBefore the Backbone
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Before the Backbone
Views on the origin of the vertebrates
Henry Gee
CHAPMAN & HALL
London • Weinheinn • New York • Tokyo • Melbourne • Madras
Published by Chapman & Hall, an imprint of Thomson Science, 2-6
Boundary Row, London SEl 8HN, UK
Thomson Science, 2-6 Boundary Row, London SEl 8HN, UK
Thomson Science, 115 Fifth Avenue, New York, NY 10003, USA
Thomson Science, Suite 750,400 Market Street, Philadelphia, PA 19106, USA
Thomson Science, Pappelallee 3, 69469 Weinheim, Germany
First edition 1996
Reprinted 1998
© 1996 Henry Gee
Thomson Science is a division of International T (^TM 1>
Thomson Publishing ••• Vi/ ''
Typeset in 10/12pt Palatino by Saxon Graphics Ltd, Derby
Printed in Great Britain by St Edmundsbury Press, Bury St Edmunds, Suffolk
ISBN 0 412 48300 9
All rights reserved. No part of this publication may be reproduced, stored in a
retrieval system or transmitted in any form or by any means, electronic,
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permission of the publishers. Applications for permission should be addressed
to the rights manager at the London address of the publisher.
The publisher makes no representation, express or implied, with regard to
the accuracy of the information contained in this book and cannot accept any
legal responsibihty or liability for any errors or omissions that may be made.
A catalogue record for this book is available from the British Library
Library of Congress Catalog Card Number: 95-72203
To the memory of David Lanning, who first taught me
which cranial nerve was which.
Contents
Preface ix
Acknowledgements xix
1 Introduction 1
1.1 Our own corner of creation 1
1.2 Multicells make metazoa 4
1.3 Protostomes and deuterostomes 5
1.4 Problems with protostomes 8
1.5 Willi Hennig's systematics 11
1.6 The principle of parsimony 15
1.7 Chordate characteristics 16
1.8 What makes a craniate? 17
1.9 Deuterostomes: dramatis personae 19
1.10 Vertebrate development in perspective 70
1.11 The gap between hemichordates and chordates 73
1.12 Echinoderms, chordates and hemichordates 75
1.13 Chordates and vertebrates 77
1.14 A deuterostome phylogeny 78
2 The origins of vertebrates 84
2.1 Vertebrate origins before Garstang 84
2.2 Garstang 106
2.3 Gislen and carpoid echinoderms 143
3 Head to head 160
3.1 Heads and tails 160
3.2 The metameric vertebrate 161
3.3 Romer's somaticovisceral animal 162
3.4 A new head 170
3.5 Head segmentation 170
3.6 Genetic patterns 171
3.7 Head to head 191
3.8 Tails 194
4 Jefferies' Calcichordate Theory 201
4.1 Carpoids revisited 201
4.2 Calcichordates, ball by ball 221
viii Contents
5 Conclusions 287
5.1 Apologia 287
5.2 The higher protosomes 288
5.3 The tunicate tadpole larva 289
5.4 Calcichordates 291
5.5 Recent and fossil forms 292
5.6 The Cambrian Explosion 293
5.7 Diversity and disparity 295
5.8 Depauperate deuterostomes 299
5.9 Two persistent problems 301
5.10 The way out 302
References 305
Index 337
Preface
We cannot catechise our stony ichthyolites, as did the necromantic
lady of the Arabian Nights did the coloured fishes of the lake which
had once been a city, when she touched their dead bodies with
her wand, and they straightaway raised their heads and rephed to
her queries. We would have many a question to ask them if we
could - questions never to be solved.
Hugh Miller, The Old Red Sandstone
When I started this book in 1991, the subject of vertebrate origins was
fusty and unfashionable. Early drafts for this preface read like an extend
ed complaint at the lot of traditional morphologists, cast aside by the
march of modern molecular biology.
But no longer - this book should reach you at a time of renewed inter
est in the origin of the vertebrates, our own particular corner of creation.
For although the topic has excited interest for well over a century, molec
ular biology has only lately achieved the maturity necessary to test its
predictions. As a legitimate field of study, it is fashionable again.
It has been a long time coming. Most people remember William Bateson
as one of those who rehabilitated Mendelian inheritance at the turn of the
century, an act that paved the way for the Modern Synthesis. They will
also be familiar with the name of Thomas Hunt Morgan, a pioneer of the
genetics of the fruit fly Drosophila melanogaster, and thus much of modern
genetics. The unit of recombinational distance is named after him.
Less well known is that both men contributed to the debate on verte
brate origins through early studies on the acorn worm Balanoglossus
{=Saccoglossus), a member of the group of animals known as hemichor-
dates. The noted palaeontologist William King Gregory takes up the
story (Gregory, 1946).
Even Bateson (1884, 1885), in his younger, more liberal days at
least, contributed through his studies on the embryology of the
X Preface
acorn worms (Balanoglossus) to the contemporary wide interest in
the problem of the origin of the vertebrates. But after he had experi
enced the satisfactions of experimental science, Bateson (1914)
formed a poor opinion of those who indulged in what he regarded
as idle speculations and held them up to ridicule, comparing their
attempts to explain 'adaptations' with the optimistic vaporings of
Voltaire's Dr. Pangloss.
He continues:
Bateson's American colleague T. H. Morgan, although he had also
contributed to the knowledge of the development of Balanoglossus
... likewise encouraged a sceptical attitude toward supposedly out
worn theories of the origin of the vertebrates and toward all a pri
ori [sic] reasoning without benefit of experimental science ... In that
period of brilliant and far-reaching successes in the genetic and
experimental fields and in the application of statistical methods and
mathematical analyses to the problems of growth and form, it was
inevitable that the problem of the origin of the vertebrates, dealing
with a very distant event by means of qualitative analysis of mor
phological patterns, should come to be regarded in many quarters
as of less than academic importance. [1946: p348]
Bateson's reservations were justified given the once widespread misuse
of Darwinian ideas to justify morphological just-so stories. Haeckel - an
ardent fan of Darwin - perfected the idea of recapitulation. As Garstang
(1922) showed, recapitulation has many good things to say provided that
it is not taken too literally. Which is, of course, how it was generally taken.
Again, Gaskell's defence of his idea that vertebrates came from a crus
tacean-like ancestor (in Gaskell et al, 1910) is less reprehensible for its
morphological content than for its basis in a mode of evolutionary
thought that owed more to pre-Darwinian ideas than natural selection.
Morphologists in the Garstangian tradition, notably Berrill (1955), veered
the other way in their promotion of a panselectionist view, in which
absolutely everything could be explained by the agency of natural selec
tion.
Bateson, Morgan and their colleagues were powerful people, and - as
Gregory (1946) further shows - they used their influence actively to dis
courage the teaching of old-style morphological argument, replacing it
with modern experimental science.
Matters have now come full circle, and, thanks to the experimental
biology of the kind championed by Bateson and Morgan, the subject has
been revitalized. Although a consensus about the relationships of verte
brates with invertebrates has yet to emerge, progress in molecular biolo
gy suggests that the answers will be with us soon.
Preface xi
When discussing the origin of vertebrates, it is often more correct to
use the term 'craniate' than Vertebrate' (Janvier, 1981). Chordates are
those animals in which (among other things) the primary axis is support
ed by a stiffening, rod-like structure called a notochord. Craniates
include those chordates in which the brain and organs of special sense
are housed in a special protective box, or 'cranium'. Vertebrates, which
are all craniates, include animals in which, in addition to the notochord,
the spinal column is composed of a segmental series of vertebrae, which
may supplant the notochord entirely. However, some animals - the hag-
fishes - contrive to be craniates, because they have skulls; but not verte
brates, because their notochords are not replaced by vertebral discs.
Strictly speaking, then, hagfishes are craniates but not vertebrates.
However, for the sake of not replacing a familiar term with an unfamiliar
one, in this book I consider hagfishes as at least honorary vertebrates, at
least when the term 'vertebrate' is used casually. So, most of the time it's
safe to read 'craniate' when I write 'vertebrate', unless otherwise indicat
ed.
In the conventional textbook scheme, as taught to generations of stu
dents, the closest living relatives of the craniates among the chordates are
generally held to be the lancelets, technically known as the cephalochor-
dates. Lancelets are small, superficially fish-like creatures which have a
notochord and many other craniate-like features, but they lack organs of
special sense and the cranium necessary to contain them (hence an alter
native name for the group, the acraniates).
The sea-squirts, otherwise known as tunicates or urochordates, are also
chordates. They are usually sessile creatures, in which the notochord is
confined to a short-lived larval stage, and in sessile forms, atrophies on
settlement. Some urochordates, though, retain the notochord and a
propulsive tail throughout life. Urochordates are usually placed slightly
more distant from the craniates and cephalochordates.
The craniates, cephalochordates and urochordates constitute a larger
group, the phylum Chordata, on the basis of certain attributes (such as
the notochord) which they share.
The textbook view of the position of hemichordates (Bateson and
Morgan's Balanoglossus and its allies) is that they are probably the closest
relatives of chordates, if they are not actually chordates themselves. Of
more remote alliance are the echinoderms; the spiny-skinned starfish,
sea-urchins, crinoids and their allies.
All these groups - the chordates, hemichordates and echinoderms -
constitute a distinct branch of the animal kingdom, known as the
deuterostomes, defined largely on embryonic features (Schaeffer, 1987).
They are distinct from other major groups of animals, such as arthro
pods, segmented worms and molluscs, which share a different set of
embryonic features.
