Untitled

spawning
environment reproduction egg type fertilisation

yolk
type cleavage pattern FW SW Ovp Ovv Vvp B P I E
Myxinlformes meroblastic + + + +
Petromyzontiformes holoblastic + + -1- +
Chondriclidiyes
Holocephali T meroblastic + + + +
Elasmobranchii T meroblastic + + + + + +
.So rcoplerygii
Coelacanthiformes T meroblastic + + +
Lepidosireniformes M semi-holoblastic + + + +
Dipnoi
Osteichtiiyeis
Ceratodont I formes M semi-holoblastic + + + +
Polypteryformes M semi-holoblastic + + + +
Ac ipenseri formes M semi-holoblastic + + + +
Actinopl erygii
Semionotiformes M semi-holoblastic + + + +
Amilformes M semi-hoioblastic + + + +
Ncoptcrygii
Teleostei T meroblastic + + + + + + + + +
Phylogenetic overview of extant fishes showing genome duplication events, type of yolk:
telolecithal (T) ormesolecithal (M), cleavage pattern, spawning environment: freshwater
(FW) or seawater (SW), mode of reproduction: oviparous (Ovp), ovoviviparous (Ow), or
viviparous (Vvp), type of egg spawned: benthic (B) or pelagic (P), and mode of fertilisation:
internal (I) or external (E). * highlights current genome sequencing projects:
Petromyzontiformes: sea lamprey (Petromyzon marinus); Holocephali: elephant shark
(Callorhinchus milii); Elasmobranchii: Little Skate (Raja erinacea); Teleostei: zebrafish
(Danio rerio); Atlantic salmon (Salmo salar); Atlantic cod (Gadus morhua); three-spined
stickleback (Gasterosteusaculeatus); medaka (Oryziaslatipes); Nile tilapia (Oreochromis
niloticus); spotted green pufferfish (Tetraodon nigroviridis) and torafugu (Takifugu
rubripes). » highlights Lepidosireniformes: marbled lungfish (Protopterusaethiopicus) as
containing the largest animal genome (130 000 Mb) known to date; « highlights
Tetraodontiformes: spotted green pufferfish (Tetraodon nigroviridis) as containing the
smallest vertebrate genome (340 Mb) known to date.
FISH
LARVAL PHYSIOLOGY
Taylor & Francis
Taylor & Francis Group
http://taylorandfrancis.com
FISH
LARVAL PHYSIOLOGY
Editors
RNFinn
Department of Biology
University of Bergen
Bergen High Technology Centre
Thormohlensgate 55
N-5008 Bergen, Norway
E-mail: [email protected]
BG Kapoor
Formerly Professor of Zoology
The University of Jodhpur
Jodhpur, India
E-mail: bhagatgopal.kapoor® rediffmail.com
Science Publishers
Enfield (NH) Jersey Plymouth
Science Publishers www.scipub.net
234 May Street
Post Office Box 699
Enfield, New Hampshire 03748
United States of America
General enquiries : [email protected]

Editorial enquiries: [email protected]
Sales enquiries : [email protected]
Published by Science Publishers, Enfield, NH, USA

An imprint of Edenbridge Ltd., British Channel Islands
Printed in India
© 2008 reserved
ISBN: 978-1-57808-388-6
Library of Congress Cataloging-in-Publication Data

Fish larval physiology/editors, R.N. Finn, E.G. Kapoor.
p. cm.
Includes bibliographical references and index.
ISBN 978-1-57808-388-6 (hardcover)
1. Fishes—Larvae—Physiology. I. Finn, R.N. II. Kapoor, E.G.
QL639.25.F567 2008
571.1'7-dc22
2007050712
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, mechanical, photocopying or otherwise, without
the prior permission of the publisher, in writing. The exception to
this is when a reasonable part of the text is quoted for purpose of
book review, abstracting etc.
This book is sold subject to the condition that it shall not, by way
of trade or otherwise be lent, re-sold, hired out, or otherwise circulated
without the publisher's prior consent in any form of binding or cover
other than that in which it is published and without a similar condition
including this condition being imposed on the subsequent purchaser.
Preface
To study physiology is to examine how organisms have evolved solutions

to the business of living in an inanimate world. Our world is and has
always been dominated by physical and chemical forces. A physicist might
tell us that all things are physical, while a chemist is more concerned
with the elementary nature of reactions. A physical chemist sees the
bonds between these views, and a biochemist draws out the organic
symphony of the vital pathways. A structural biologist adds shape to the
chemical building blocks of life, while a molecular biologist tinkers with
these structures. A cell biologist is closely related to a molecular biologist
and cousin to an anatomist that is intrigued by the variety of phenotypes.
Mapping the fabric between these fields is a developmental biologist that
not only seeks to understand the mechanisms of cell signalling and
differentiation, but place them in an evolutionary context. To understand
how an organism functions, and adapts to changes in its external and
internal environment, a physiologist must dabble in each of these fields.
Consequently modern physiologists face a daunting task of acquiring a
rich tapestry of knowledge and methods that will lead them from the
whole organism to the depths of sub-cellular compartments and molecules
responsible for life.
This book is intended as a resource for students and researchers
interested in developmental biology and physiology and specifically
addresses the larval stages of fish. Fish larvae (and fish embryos) are not
small juveniles or adults. Rather they are transitionary organisms that
bridge the critical gap between the single-celled egg and sexually
immature juvenile. Fish larvae represent the stage of the life cycle that is
used for differentiation, feeding and distribution. Like the juveniles and
adults, however, they face the same physical and chemical challenges
Viii Preface
imposed by their aquatic environment, yet lack many of the cells, tissues
or organs present in the more advanced stages to deal with such adversities.
Many fish larvae, particularly those of the marine forms of teleosts, are
small, in fact tiny, necessitating the use of magnifying devices just to see
them. A common size of a newly hatched marine teleost is four mm or
less, the same size as a one month old human embryo. As a consequence
traditional physiological investigation of fish larvae has tended to be of
the "black box" whole organism nature. With the advancement of
molecular tools, and miniaturisation of manipulation instruments,
investigators can now peer deep inside the developing systems and explain
how they work. The genomic revolution might be regarded as the cavalry
in this regard, where physiologists can not only investigate the ontogeny
of expression, but modulate the genes through insertional mutations, or
regulate them via hybridisation techniques. When coupled with more
classical methods, an entirely new level of understanding emerges.
From a biodiversity perspective, fish champion the vertebrates,
accounting for almost half of the known species of craniates. The most
recent count is —28 000 species spread among more than 500 families.
The physiological diversity of fish larvae, in all of their myriad forms, is
only beginning to be chartered. This book aims at providing a single-
volume treatise that explains how fish larvae develop and differentiate,
how they regulate salt, water and acid-base balance, how they transport
and exchange gases, acquire and utilise energy, how they sense their
environment, and move in their aquatic medium, how they control and
defend themselves, and finally how they grow up. We hope that the
reader learns as much from this text as we have editing it.
Roderick Nigel Finn

Bhagat Gopal Kapoor
Contents
Preface vii
Lis t of Contributors xi
Part 1: Ontogeny
1. Pattern Formation 3
Thomas E Hall
2. Pigmentation 27
Robert N Kelsh and David M Punchy
3. Bioluminescence 51
Andrey V Suntsov, Edith A Widder and Tracey T Sutton
Part 2: Respiration & Homeostasis

4. Gas Exchange 91
Bernd Pelster
5. Cardiovascular Anatomy and Physiology 119
Warren WBurggren and Brian Bagatto
6. Osmo- and lonoregulation 163
Toyoji Kaneko and]unya Hiroi
7. Acid-base Balance 185
Colin] Brauner
Part 3: Nutrition and Energy
8. Digestion 201
Ivar R0nnestad and Sofia Morais
9. Nitrogen Excretion 263
Bendik F Terjesen
X Contents
Part 4: Sensory Physiology

10. Mechanoreception 305
Patricia M Pankhurst
11. Chemoreception 331
Kjell B D0ving and Alexander O Kasumyan
12. Photoreception 395
Ellis R Loew and Christina M Wahl
13. Electroreception 425
Frank Kirschbaum and Jean-Pierre Denizot
14. Magnetoreception 461
Krzysztof Formicki
Part 5: Movement
15. Buoyancy 495
John J Gowni and Richard B Forward ]r
16. Swimming and Muscle 523
UlrilceKMuller
Part 6: Control and Defense

17. Enteric Control 553
Anna Holmberg, Susanne Holmgren and Catharina Olsson
18. Immunology 573
Agustin G Zapata and Alfonso Cortes
Part 7: Functional Changes in Form

19. Metamorphosis 607
DM Power, N Silwz and MA Campinho
20. Smoltification 639
Sigurd O Ste/ansson, Bjorn Th Bjornsson, Lars OE Et>t>esson and
Stephen D McCormiclc
Glossary 683
Species Index 693
Common Name Index 703
Subject Index 715
List of Contributors
Bagatto Brian
Department of Biology, University of Akron, Akron, OH 44325, USA
Bjornsson Bjorn Th
Fish Endocrinology Laboratory, Department of Zoology/Zoophysiology,
Goteborg University, Box 463, S40530, Goteborg, Sweden
Brauner Colin J
Department of Zoology, University of British Columbia, 6270 University
Blvd., Vancouver, BC, Canada, V6T 1Z4
Burggren Warren
Department of Biological Sciences, University of North Texas, Denton,
TX 76205, USA
Campinho MA
Comparative Molecular Endocrinology Group, Marine Science Centre
(CCMAR), Universidade do Algarve, FERN, Campus de Gambelas,
8005-139 Faro, Portugal
Cortes Alfonso
Department of Cell Biology, Faculty of Biology, Complu tense University,
28040 Madrid, Spain
XJ J List of Contributors
Denizot Jean-Pierre
C.N.R.S., Unite de Neurosciences Integratives et Computationnelles,
91198 Gif-sur-Yvette, Cedex, France
D0ving Kjell B
Department of Molecular Bioscience, University of Oslo, PO Box 1041
Blindern, N-0316 Oslo, Norway
Ebbesson Lars OE
Department of Biology, University of Bergen, Bergen High Technology
Centre, N-5008 Bergen, Norway
Formicki Krzysztof
University of Agriculture in Szczecin, Department of Fish Anatomy
and Embryology 4 K. Krolewicza St. 71-550 Szczecin, Poland
Forward Jr Richard B
Duke University, Nicholas School of the Environment and Earth
Sciences, Marine Laboratory, 135 Duke Marine Lab Road, Beaufort,
NC 28516-9721, USA
Govoni John J.
US Department of Commerce, National Oceanic and Atmospheric
Administration, National Ocean Service, National Centers for Coastal
Ocean Science, Center for Coastal Fisheries and Habitat Research,
101 Pivers Island Road, Beaufort, NC 28516-9727, USA
Hall Thomas E
Victor Chang Cardiac Research Institute, 384 Victoria Street,
Darlinghurst, Sydney, NSW 2010, Australia
Hiroi Junya
Department of Anatomy, St. Marianna University School of Medicine,
Miyamae, Kawasaki, Kanagawa 216-8511, Japan
List of Contributors XIII
Holmberg Anna
Department of Zoophysiology, University of Goteborg, Box 463, SE 405
30 Goteborg, Sweden
Holmgren Susanne
30 Goteborg, Sweden
Kaneko Toyoji
Department of Aquatic Bioscience, Graduate School of Agricultural
and Life Sciences, University of Tokyo, 1-1-1, Yayoi, Bunkyo, Tokyo
113-8657,Japan
E-mail: kaneko31 ©marine.fs.a.u-tokyo.ac.jp
Kasumyan Alexander O
Department of Ichthyology, Faculty of Biology, Moscow State
University, R-l 19991, Russia
Kelsh Robert N
Centre for Regenerative Medicine, Department of Biology and Biochemistry,
University of Bath, Claverton Down, Bath BA2 7AY, UK
Kirschbaum Frank
Leibniz-Institute of Freshwater Ecology and Inland Fisheries,
Miiggelseedamm 310, 12587 Berlin, Germany
Institute of Animal Sciences, Humboldt-University Berlin, Berlin,
Germany
Loew Ellis R
Cornell University, Department of Biomedical Sciences, Ithaca, NY
14853, USA
McCormick Stephen D
USGS, Conte Anadromous Fish Research Center, Turners Falls, MA
01376, USA
XJV List of Contributors
Morals Sofia
(CCMAR), Universidade do algarve, FERN, Campus de Gambelas,
Miiller Ulrike K
Department of Biology, California State University Fresno, 2555 E San
Ramon Avenue, Fresno CA 93740, USA
Olsson Catharina
30 Goteborg, Sweden
Pankhurst Patricia M
School of Tropical and Marine Biology, Faculty of Science, Engineering
and Information Technology, James Cook University, Townsville,
Queensland 4811, Australia
Parichy David M
Department of Biology and Institute for Stem Cell and Regenerative
Medicine, University of Washington, Seattle WA 98195
Pelster Bernd
Institut fur Zoologie, Universitat Innsbruck, TechnikerstraBe 25,
A-6020 Innsbruck, Austria
Power DM
R0nnestad Ivar
List of Contributors XV
Silva N
Stefansson Sigurd O
Suntsov Andrey V
Northwest Fisheries Science Center, National Oceanic and
Atmospheric Administration, Newport OR 97365 USA
Sutton Tracey T
Harbor Branch Oceanographic Institution, Fort Pierce FL 34949 USA
Terjesen Bendik F
AKVAFORSK, Institute of Aquaculture Research, N-6600,
Sunndals0ra, Norway
Wahl Christina M
Wells College, Department of Biological and Chemical Sciences,
Aurora, NY 13026, USA
Widder Edith A
Ocean Research & Conservation Association, Fort Pierce FL 34949
USA
Zapata Agustin G
Department of Cell Biology, Faculty of Biology, Complu tense University,
28040 Madrid, Spain
Taylor & Francis
PARTI
Ontogeny
Taylor & Francis
CHAPTER
Pattern Formation
Thomas E Hall
INTRODUCTION
Pattern formation during development refers to the processes by which the structure of
the organism is spatially and temporally organised. On a cellular level, this requires the
management of cell activities within the embryo so that a well-ordered structure
develops. These processes begin prior to fertilisation, during oogenesis, and eventually
result in the differentiation of the tissue and organ systems essential for homeostasis in
complex organisms.
The fishes are a large and diverse group containing approximately half of known
craniate species (Nelson, 1994). Early ontogeny varies substantially be tweenclades,
although this diversity is partly artifactual, since fish are a paraphyletic taxon (Collazo
et al, 1994). As such, this chapter concentrates on the Actinopterygii (ray-finned
fishes) and mainly on the group Teleostei, which benefits from a number of well-
studied models such as the medaka (Oryzias latipes) and zebrafish (Danio rerio). In
addition, the rise of intensive aquaculture in recent years has fuelled much
developmental research on commercially important species.
Author's address: Victor Chang Cardiac Research Institute, 384 Victoria Street, Darlinghurst,
Sydney, NSW 2010, Australia.
4 Fish Larval Physiology
EARLY PATTERN FORMATION

Pre-cleauage Patterning
Typically, teleosts are externally fertilising (oviparous), and the entirety of embryonic
development occurs outside the mother's body. The eggs are supplied with a large yolk
volume to sustain early development in the absence of direct maternal nutrition. In the
unfertilised egg, the yolk and cytoplasm are intermixed (Leung et al, 2000). The first
patterning information is apparent even at this early stage as the animal/vegetal axis
can be predicted on the basis of the localisation of specific maternal mRNAs (Howley
& Ho, 2000). Following sperm entry and extrusion of the second polar body, the
cytoplasm and yolk begin to separate, forming a single blastomere at the animal pole,
sitting atop a continuous acellular yolk mass. In many species (e.g. the zebrafish;
Kimmel et al, 1995) streaming of cytoplasmic constituents to the animal pole maybe
observed directly under the light microscope. An actin microfilament network drives
this movement (Leung et al, 2000).
Cleavage
All teleosts show a discoidal meroblastic cleavage pattern, where the large yolk volume
restricts cell division to a small area at the animal pole. The early embryo forms as a
small disc sitting atop the large yolk. Holoblastic cleavage, where division splits the
entire mass, is thought to be the ancestral condition, and is common in many
invertebrate chordate phyla, as well as the lampreys. However, it appears that most
animals with telolecithal eggs (those with a high ratio of yolk: cytoplasm) have evolved
the meroblastic "shortcut". A meroblastic cleavage pattern allows cell division to proceed
rapidly, and avoids the need for synthesis of large amounts of new cell membrane.
Indeed, meroblastic cleavage has evolved independently at least five times within the
craniates (once in each of the lineages leading to the hagfish, elasmobranchs,
coelacanths, teleosts and amniotes; Collazo et al, 1994). Interestingly, present-day
mammals show a reversion to holoblastic cleavage, possibly as a result of gaining nutrition
directly from the mother, rather than having to lay down copious quantities of yolk.
The first divisions are vertical and there is no cytoplasmic growth during this period,
resulting in a decrease in blastomere size with each successive division. Early cleavages
tend to be incomplete, and the initial blastomeres maintain cytoplasmic bridges with
the yolk cell. Cleavages occur synchronously between embryos and the first cell cycles
are easy to follow within clutches. Mitotic spindles can often be seen as the disc cleaves
to form two distinct cells (Kimmel et al, 1995; Hall et al, 2004). The second cleavage
is also horizontal and results in a 2x2 array. Timing of the cell cycle during the first
cleavage events is highly synchronous, with each cycle having approximately the same
length (Marrable, 1965; Kimmel et al, 1995). Around the 16 to 32 cell stage however,
the mass of cells (the blastodisc), becomes stratified into more than one layer. In most
species the blastomeres are regular in size and shape. However, inter- and intra-specific
variation exists on the general pattern. In the Atlantic cod (Gadus morhua) horizontal
Thomas E Hall 5
stratification of the cell mass usually occurs at the sixth cleavage, between the 32 and
the 64 cell stages, but is frequently observed at the previous or following cleavage (Hall
et al, 2004). In the medaka, the first horizontal cleavage is the fifth, occurring between
the 16 and 3 2 cell stages (Iwamatsu, 1994) and in the ice goby (Leucopsarion petersii) it
occurs even earlier, between the 4 and 8 cell stages (Nakatsuji et al, 1997). Unusually
within the teleosts, eggs of the wolffish (Anarhichas lupus), have unequal blastomere
sizes during early divisions (Pavlov et al., 1992). During later cleavages it is only the
marginal blastomeres (sometimes called Wilson cells), positioned on the periphery of
the cell mass (now called the blastodisc), which maintain their cytoplasmic bridges
with the yolk.
The Early Blastula and the Yolk Syncytial Layer

Loss of cytoplasmic bridges coincides with the formation of the yolk syncytial layer
(YSL; Trinkaus, 1992). Around the ninth and tenth cleavages, the marginal blastomeres
collapse into a single large, multinucleate (or syncytial) cell (Kimmel & Law, 1985).
The YSL is an organ unique to teleosts that no longer undergoes cytoplasmic cleavage.
The nuclei, however, continue to divide mitotically, and spindles may be seen in the
cytoplasm as the YSL spreads beneath the blastodisc, separating the true blastomeres
from the yolk. Around the 12l cleavage the YSL nuclei become post-mitotic (Kane
et al, 1992). Three cellular layers are now visible in the blastula; an enveloping layer
(EVL) constituting the most external cells, which is epithelial in nature and covers the
blastoderm; a middle layer of deep cells which will become the embryo proper, and the
YSL lying between the deep cells and the yolk. The YSL is continuous with the yolk
cytoplasmic layer (YCL), a thin layer of anuclear cytoplasm surrounding the yolk. The
YSL itself is often described as possessing two domains, the internal YSL, which spreads
beneath the blastodisc, and the external YSL which lies around the circumference.
Tight junctions between the YSL and the overlying blastomeres mark the boundary
between the internal and external domains. The thinner internal YSL (beneath the
blastodisc) is populated by nuclei derived from the external YSL (Kimmel & Law,
1985).
In the early development of many animals, the initial rapid cleavage stages are
followed by a period where the cell cycle lengthens, the embryo begins to transcribe its
own RNA, and the cells of the blastula become motile, in preparation for gastrulation.
This is termed the mid-blastula transition (MET; Kane & Kimmel, 1993). The teleost
MET begins around cell cycle eight-ten (cycle ten in the zebrafish and the Atlantic
cod). From around the seventh cleavage, the cells begin to show metasynchrony in
their divisions, and within a further two or three cell cycles, cleavage events cannot be
distinguished. In contrast to the early cleavages when there was little net cell movement,
cell divisions now often spread daughter cells more than a cell diameter apart, causing
a mild dispersion of progeny and intermingling of distant cell lineages (Kimmel & Law,
1985). Pseudopodia are also present, consistent with the activation of cell motility.
However, the fate map in the early blastula is non-determinative; the progeny of any
blastomere may contribute to all tissues in the embryo. Cell movements at this stage are
not "directed or coherent" (Kane & Adams, 2002). Interestingly, the onset of cell
cycle lengthening at the MET is correlated not with cleavage number, but with
nucleocytoplasmic ratio (Kane &Kimmel, 1993).
EPIBOLY AND GASTRULATION

Gastrulation is effectively a way of organising the developing embryo into the three
primordial tissue layers, moving the endoderm and the mesoderm inside the ectoderm
(Kimelman & Schier, 2002). The ectoderm will form the epidermis and neural tissue,
and organs such as the ears and eyes; the mesoderm will form organs such as the
muscle, bone, heart, kidney and vasculature; and the endoderm will form the lining of
the alimentary canal, the swim bladder and organs such as the liver and pancreas.
Note that the EVL, considered an extra-embryonic tissue, will form the first skin of the
embryo, the periderm (Kimmel et al, 1990). Nuclei of the YSL, also considered an
extra-embryonic tissue, have not been tracked beyond the end of gastrulation (D'Amico
&Cooper,2001).
The process of gastrulation in teleosts is associated with a cell movement called
epiboly, where the blastoderm spreads over the yolk from the animal pole, eventually
enveloping the entire mass. Strictly, epiboly begins before the onset of gastrulation,
with the thinning of the blastodisc. The YSL appears to drive epiboly via a microtubule
dependant process, and if the blastoderm is removed, continues to move autonomously
(Trinkaus, 1951). The YSL undergoes a mitotic arrest shortly before epiboly in zebrafish
and killifish (Fundulus heteroclitus), possibly because the simultaneous use of
microtubules in both mitosis and motility is likely to be mutually exclusive (Kane &
Adams, 2002).
Shortly after the onset of epiboly, and prior to gastrulation, the fate map becomes
restricted at the tissue level. Cells within only a small number of cell diameters from the
margin of the blastoderm will become endodermal and mesodermal tissues (the
"mesendodermal" compartment). Cells close to the margin, but outside of this domain,
will become purely mesodermal tissues. Cells further towards the animal pole, will
become ectodermal tissues (Fig. la). The onset of gastrulation itself begins with
involution. Involution is a movement within the deep cell layer, whereby cells on the
periphery of the blastodisc "roll underneath" the blastoderm lip (which is advancing
towards the vegetal pole), and move back in the direction of the animal pole. The
resulting thickening around the edge of the blastodisc is known as the "germ ring".
The involuted layer, termed the hypoblast, is specified as mesoderm and endoderm.
By the end of gastrulation, the outside layer, the epiblast, is composed of ectodermal
cells. There is some variability in the timing of the beginning of involution with respect
to percent epiboly between species. In the Atlantic cod, medaka and common carp
(Cyprinus carpio), hypoblast formation starts early and coincides with the thinning of
the blastodisc at the very beginning of epiboly. In killifish, hypoblast formation begins at
approximately 25% epiboly and in the zebrafish, does not start until 50% epiboly (Hall
etol.,2004).
Thomas E Hall 7
Historically, there has been debate over the dynamics of hypoblast formation during
teleost gastrulation. There are two models as to the manner in which the marginal cells
internalise; ingression, where cells "sink" as individuals from the epiblast to the hypoblast,
and involution, which specifically refers to the rolling of a sheet of cells around an
edge. Early studies in the rainbow trout (Oncorhynchus mykiss), (formerly Salmo gairdneri),
found no evidence of involution (Ballard, 1966). Similarly, in killifish, the classical
process of involution appears to be absent (Trinkaus, 1984). However, hypoblast
formation in the zebrafish (Warga & Kimmel, 1990), and the rosy barb (Puntius
conchonius; Wood &Timmermans, 1988) has been clearly described as an involuting
cellular sheet. A unifying model of these processes has since been proposed. In small-
egged teleosts such as the zebrafish and rosy barb, where cell density is relatively high
at the onset of gastrulation, cell movements to form the hypoblast do involve the
internalisation of individual cells by a process of, or a process similar to, ingression. The
passage of deep cells into the hypoblast layer is indeed confined to those cells at the
blastoderm margin, and initially all cells appear to be moving together. However, as the
cells begin to descend, they seem to be moving as individuals, often changing places
with their neighbours and extending active protrusions. The close proximity of so many
cells undergoing this movement within one or two cell diameters of the margin, gives
the appearance of a flow of cells into the hypoblast (Kane & Adams, 2002).
Mesodermal and Endodermal Specification

The mesoderm and endodermal tissues of the hypoblast are first specified by inducing
signals, released in a ring by the external edge of the YSL, affecting the overlying
blastomeres (Mizunoetal., 1996;Rodawayetal., 1999).Thenodal-relatedmorphogen
squint (Sqt) is one of the signals, inducing its own expression, and that of the related
factor cyclops (Cyc) in the involuting cells. Cyc and Sqt show substantial functional
redundancy, and are essential for the formation of all mesoderm and endoderm other
than tail mesoderm, which is induced directly by an unknown TGF-f3 like signal from
the YSL (reviewed by Schier, 2003).
In the zebrafish fate map (and almost certainly in those of other teleosts), there are
relatively few endodermal progenitors compared to ectodermal and mesodermal
progenitors (Warga &Stainier, 2002). The endodermal progenitors occupy the most
marginal positions prior to involution. All endodermal cells are derived from clones
situated within four cell diameters of the blastoderm lip, and are among the first to
involute during gastrulation. However, in the early blastula, cells from this domain may
also give rise to mesoderm, suggesting some indeterminacy in cell fate. Marginal cells
situated further from the blastoderm lip give rise exclusively to mesoderm (Warga &
Nusslein-Volhard, 1999). As the endodermal progenitors begin to involute, a number
of endodermal genes become active, such as casanova (cos), bonnie and clyde (ban) and
faust (fau/gata5; reviewed in Warga & Stainier, 2002). By the end of gastrulation,
endodermal cells maybe distinguished on the basis of morphology, as a monolayer of
large flat cells with numerous filopodia lying against the yolk (Warga & Nusslein-
Volhard, 1999). The mesodermal component of the hypoblast, in contrast, has limited
contact with the yolk and shows less marked changes in cell morphology. There is
increasing evidence that nodal signalling not only specifies the involuted cell
compartment, but is also involved in patterning it. It is likely that there is a nodal-
activity gradient along the animal-vegetal axis, with the highest levels at the blastoderm
margin producing endoderm, prechordal plate and ventricular progenitors, lower levels
producing notochord and other mesodermal fates, and the absence of nodal signalling
allowing neural and tail specification (reviewed in Schier &Talbot, 2005).
Convergent-extension and the Fish "Organiser"

The third major cell movement that occurs during teleost gastrulation, (in addition to
epiboly and involution/ingression), is convergent-extension. Convergent-extension
breaks radial symmetry by the convergence of cells to the dorsal side of the embryo,
and results in its animal/vegetal extension. The dorsal accumulation of cells is known
as the embryonic shield, and defines the axis of the embryo. All three germ layers
participate in the underlying cellular movements. As in the African clawed frog
(Xenopus laevis), a major driver of teleost convergent-extension is mediolateral
intercalation of cells (Concha & Adams, 1998; Glickman et al, 2003). However,
active cell migration is also important in patterning the shield. Around mid-gastrulation,
cells of the hypoblast, which are moving animal-ward on individual, meandering paths,
acquire a directional bias towards the future dorsal side (Sepich & Solnica-Krezel,
2005; Sepich et al, 2005). Depending on location along the animal-vegetal axis, cell
migration occurs at different rates, resulting in a "fanning out" of cell trajectories, and
the antero-posterior extension of the tissue layer. It is likely that convective or passive
cell movements also contribute to convergent-extension, perhaps by adhesion to the
epiblast or YSL (D'Amico & Cooper, 2001).
The concept of the organiser was introduced by Spemann (Spemann & Mangold,
1924; but see Gilbert & Raunio, 1997). The initial experiments, in amphibians,
demonstrated that cells from the dorsal lip of the newt gastrula, when transplanted to
a host of the same developmental stage, were able to elicit the formation of a secondary
axis. The structures of the secondary axis, such as the somites, secondary notochord,
and in some cases gut, were derived not from the grafted tissue but from host cells that
normally would not participate in formation of these structures. These cells were
subsequently referred to as the "Spemann organiser" (a functionally equivalent domain
known as "Hensen's node" was later described in the chick; Hunt, 1929). There is
some evidence that the embryonic shield in zebrafish is analogous to the Spemann
organiser in amphibians. Transplantation of the shield can generate a complete
secondary axis (Saude et al, 2000). In addition, it appears that there are distinct cell
populations within the shield, with grafts from deep regions of the shield preferentially
inducing anterior structures, whilst the superficial region tends to induce posterior
structures. Although the transplant experiments appear conclusive, the results of shield
ablation experiments are more ambiguous. It appears that the shield does not define
the organiser per se, but that the organiser forms earlier and over a wider region than
the shield (reviewed by Hibi et al, 2002).
Thomas E Hall 9
DIFFERENTIATION OF THE GERM LAYERS

Organogenesis in the Mesoderm
The processes of organogenesis begin during late gastrulation or shortly after, when
cells from the three tissue layers start to differentiate into specific structures. At this
time, precursors of different cell types are arranged along the dorso-ventral and antero-
posterior axes (Fig. Ib). It should be noted at this point that classical developmental
periods such as gastrulation, segmentation, neurulation and organogenesis tend to
show some overlap in teleosts, to a greater or lesser extent depending on species.
The mesoderm consists of three domains, the head, trunk and tail. Each of the
three domains is specified early to produce different structures. Following gastrulation,
the head domain (prechordal and head mesoderm) specifically expresses the marker
goosecoid (gsc). Trunk and tail specification appear to be under the control of fibroblast
growth factor (FGF) signalling, through the downstream genes no tail (ntl) and spade
tail (spt). In the zebrafish, if FGFs are blocked, no trunk or tail mesoderm is formed
(Griffin et al, 1995). In the ntl and spt mutants, ntl has no tail mesoderm and spt has
severely defective trunk mesoderm. The double mutant (ntl/spt), phenocopies the
effect of blocking FGF signalling (reviewed by Sakaguchi et al, 2002).
The first organ to delineate physical boundaries in the early embryo is the notochord.
Two longitudinal furrows appear dividing the axial chorda mesoderm (which expresses
the marker floating head, flh; Melby et al, 1997) and the paraxial segmental plate
mesoderm (which will become the somites). The process is driven by differing rates of
convergent-extension between the two tissues. Cells in the presumptive notochord
extend several times faster than those in the adjacent paraxial mesoderm, resulting in
shearing along the boundary (Glickman et al, 2003). As development proceeds, the
furrows extend posteriorly down the axis of the embryo either side of the midline. The
central cells of the notochord are known as chordoblasts, and each develops a large,
fluid-filled vacuole. Vacuolisation is associated with the deposition of a surrounding
thickened sheath of tissue which, together with the core, imparts the rigidity and axial
support necessary for early swimming movements (Adams, 1990;Koehletal., 2000).
Shortly after the notochord furrows become visible, the first somite furrow appears
perpendicularly in the paraxial mesoderm, marking the beginning of segmentation (so
called because of the repeated nature of the somites). The process of somitogenesis is
similar to that in amphibians, birds and mammals (Stickney et al, 2000). It involves a
mesenchymal-epithelial transition of cells within the paraxial mesoderm, to surround a
central space, the somitocoele, which contains a loose meshwork of mesenchymal
cells. In rainbow trout, the epithelial cells of the somite express collagen-1 (Rescan
et al, 2005). Somites are added posteriorly in a temporally linear, reiterative fashion until
the final number is reached (for this reason somite number is the most useful staging
tool in fish embryonic development). Final somite number is extremely variable within
the teleosts, ranging from 18 in the ocean sunfish (Mola mold} (Brainerd et al., 2001) to
over 200 in some eels (Richardson et al, 1998). As with the onset of gastrulation, there
is some variability as to the beginning of segmentation. For instance, the first somite
furrow in the Atlantic cod is formed at approx 45% epiboly. In contrast in the zebrafish,
common carp, medaka and killifish, somitogenesis is not initiated until well after the
completion of epiboly. Development of tissues from the onset of somitogenesis tends to
proceed temporally in a rostral-caudal wave, with the most well developed structures
towards the anterior, and the least developed towards the posterior. The process of
vertebrate segmentation itself seems to be under the control of a segmentation clock,
involving an intrinsic oscillator within the pre-somitic mesoderm, revealed by the
expression of "cycling genes". The clock appears to function in parallel with a wavefront
of differentiation involving FGF signalling, whose progression determines the correct
position of somite boundaries (Dubrulle et al, 2001; Sawada et al, 2001; Freitas
etol.,2005).
Somites contain cells that will become a variety of mesodermal derivatives. The
majority of the somite in fish becomes the myotome, and will form the body musculature.
There are however, a number of other cellular compartments within the somite. The
most ventral zone of the somite is the sclerotome, which will form the cartilage, and
later the bone of the animal (Morin-Kensicki & Eisen, 1997). Fish, which exist within
an aqueous medium, exert a lesser demand on the axial skeleton for maintenance and
locomotion than terrestrial vertebrates, and possess an increased requirement for axial
(swimming) muscle (Bone, 1966). As a result, the sclerotome in amniotes occupies a
much larger area and is situated adjacent to the notochord. In teleosts, the sclerotome
is a relatively small compartment, and is initially located ventrally within the somite.
Only later in development do these cells undergo a dorsal-ward migration and position
themselves adjacent to the notochord. The mechanism of vertebral formation is also
fundamentally different. In amniotes the vertebral body rudiments are formed in
cartilage and are derived from adjacent half-somites. In contrast, the development of
teleost vertebrae involves the development of specialised notochordal structures called
chordacentra, which first form as acellular calcified "rings" within the notochord
sheath. The sclerotomally-derived bone is then deposited through direct ossification
on the outside of the chordacentra and notochord, without the prior formation of
cartilage (Grotmol et al., 2003).
The structure of the body musculature in teleosts is peculiar within the vertebrates,
in that the fast- and slow-twitch muscle fibres are spatially separated, with the slow
muscle being confined to a relatively thin layer on the periphery of the myotome, and
the fast fibres forming the bulk of the deep myotome (Bone, 1978). This peculiarity is
reflected in myotomal ontogeny. In the undifferentiated somite, most cells are
mesenchymal in nature. However, adjacent to the notochord lie a group of large
cuboidal cells known as adaxial cells, so called because of their proximity to the midline
(Felsenfeld et al., 1991). Towards the end of somitogenesis, in response to the expression
of hedge hog proteins from the notochord (Blagdenetal., 1997), these cells begin to
express slow myosin heavy chain. They then perform an astounding migration, moving
laterally through the overlying somitic cells, whilst elongating and fusing into the first
myotubes (Devoto et al., 1996). It has recently been shown that this migration is driven
Thomas E Hall 11
by cell sorting behaviour in response to laterally radiating waves of expression of the cell
adhesion molecules n- and m-cadherin (Cortes et al, 2003). A subset of these cells,
which lie at the horizontal myoseptum, are known as the muscle pioneer cells (Felsenfeld
et al., 1991). They are distinct both morphologically and genetically, spreading laterally
from the notochord to the myotome surface, and expressing the nuclear protein Engrailed
(Roy et al., 2001). Following adaxial cell migration, sclerotomal cells from the ventral
somite migrate dorsally to occupy their position adjacent to the notochord, adopting
the positional relationship seen in amniotes. Adaxial cell migration through the myotome
also appears to be necessary to "prime" the myotome for invasion by the primary motor
neurons (Zeller et al., 2002). As the slow muscle cells reach the periphery of the
myotome, the deeper, fast fibres begin to fuse and differentiate. Further fibre recruitment
occurs from zones at the peripheries of the myotome, and at the horizontal myoseptum
(reviewed by Johnston & Hall, 2004).
Other than the myotome and the sclerotome, cellular compartments within fish
somites have not been extensively characterised. In amniotes, the dorsal epithelium of
the somite is referred to as the dermomyotome, and is a multipotent tissue, able to give
rise to dermis, vascular endothelia, trunk muscle fibres, and the muscles of the limbs
and ventral body wall (intercostal muscles; Scaal & Christ, 2004). It has been shown
that cells of the zebrafish somite can give rise to blood vessels (Morin-Kensicki & Eisen,
1997), and that muscle fibre recruitment occurs in the teleost myotome throughout
life. In addition, the presence of so-called "external cells", a non-continuos layer of
flattened mitochondrion-dense cells outside the slow muscle layer has been noted by
many investigators (Waterman, 1969; van Raamsdonketal., 1978; Felsenfeld etal,
1991) and this has been claimed represent the teleost dermomyotome (Devoto et al.,
2006). However, there is little functional evidence for this.
The heart, blood and kidney all form from more lateral non-somitic mesoderm (see
Fig. Ic). Fate mapping studies have revealed that heart progenitors, giving rise to both
myocardial and endocardial lineages, are clustered into two laterally located groups in
the mesendodermal cell layer (reviewed by Stainier, 2001). By early somitogenesis,
they are located close to the future hindbrain as two populations, either side of the
embryonic midline. Within these populations the myocardial progenitors are located
more laterally and the endocardial progenitors more medially. At this time, the pre-
cardiac field is defined by the expression of the marker nlcx2.5, which is conserved
throughout the vertebrates (Schwartz & Olson, 1999). By mid-somitogenesis, the
heart progenitors have migrated as far as the midline, and merge at the posterior to
form a horseshoe-like structure, and then a shallow cone, with the apex being located
more dorsally (Yelon et al, 1999). During the latter period of somitogenesis, the apex of
the cone tilts posteriorly and to the right, before its extension to form the heart tube.
The tube consists of an atrial anterior end, to the left of the midline, and a posterior
ventricular end, to the right, and is lined with endocardial cells. Subsequent
morphogenetic events result in cardiac looping, and the formation of an organ with the
ventricle positioned to the right of the atrium. It is noteworthy that the teleost heart
tends to begin beating before the development of haemoglobin, and before the
Fig. 1 Arrangement of presumptive tissue types in the zebrafish (Danio rerio) at the onset
of gastrulation (a), shortly before the end of gastrulation (b), and early segmentation (c).
Modified from Schier & Talbot (2005).
Thomas E Hall 13
development of functional gills. It is likely that the function of this early circulation is
nutritional, and for the distribution of the yolk substrates rather than gas exchange.
Development of vasculature during the embryonic stages is highly variable between
species and often reflects egg and larval size. For instance, in the salmonids, the entire
yolk sac becomes vascularised early in development, in contrast to species with smaller
embryos such as the Atlantic cod or zebrafish (Gorodilov, 1996; Hall et al, 2004). It is
thought that both vascular and haematopoietic cells originate from common progenitors
known as haemangioblasts, present adjacent to the presumptive kidney at the end of
gastrulation. All of the earliest forming blood vessels in teleosts appear to have direct
homologues in other vertebrates, and the overall pattern changes little before first-
feeding (YelonetoJ., 2002).
The embryonic kidney is the pronephros, which consists of two fused glomeruli
situated ventral to the notochord at the approximate position of the first somites,
sprouting a pair of laterally projecting pronephric tubules, each adjoining a pronephric
duct running posteriorly above the alimentary canal (Serluca & Fishman, 2001). It
arises from cells adjacent to the somitic mesoderm, and later in development, during
the juvenile to adult transition, a more complex, mesonephric kidney arises (Drummond
etol.,1998).
Organogenesis in the Ectoderm

The ectodermal layer which, following gastrulation is the outermost tissue layer of the
embryo, gives rise to the neural tissues, sensory organs, pigment cells, placodal tissues
and the epidermis. Prior to organogenesis, the thickening of the ectoderm above the
presumptive notochord and somites is known as the neural plate.
Towards the end of epiboly, neural plate cells above and dorso-lateral to the
presumptive notochord extend ventrally, forming a deepened keel. This is quickly
overridden by adjacent epidermal cells, and becomes a solid rod. A central lumen, the
neurocoele, originates by cavitation, turning the neural rod into a tube. This mechanism,
known as secondary neurulation, contrasts with the infolding mechanism (primary
neurulation) observed in amniotes (Papan& Campos-Ortega, 1994).
Soon after the beginning of somite formation, the anterior neural tube swells and
distends, but is subdivided by a number of constrictions (Kimmel, 1993). Initially,
around ten swellings are apparent, and the rostral-most three of these become large
and prominently sculpted. The rostral-most two swellings correspond to the subdivisions
of the forebrain, the telencephalon and the diencephalon. The third makes up the
midbrain. The seven smaller, more caudal bulges, termed "rhombomeres" make up the
hindbrain (reviewed by Hjorth & Key, 2002). During their morphogenesis, a subset of
cells located between the developing diencephalon and telencephalon, move laterally
to form the optic primordia, which subsequently detach and invaginate (Easter &
Malicki, 2002). The first neurons of the developing brain, known as primary neurons,
arise in bilateral clusters, close to the centre of each rhombomere. The earliest axons
extend between the clusters of cells in bundles, forming a stereotypically patterned
scaffold. Primary neurons typically have larger soma, which extend axons long distances,
and often pioneer pathways. The smaller secondary neurons develop later, utilising the
initial scaffold laid down by the primary neurons.
The extent of the neural tube posterior to the brain differentiates into the spinal
cord, and lies dorsal to the notochord. The first neurons in the spinal cord arise in a
segmental pattern corresponding to the somites. In the zebrafish, each segment contains
approximately 11 neurons; three primary motor neurons, three primary sensory Rohon-
Beard neurons, and five intemeurons (Kuwada & Bemhardt, 1990). The first neurons
to develop are the dorsally located Rohon-Beard neurons, closely followed by the
intemeurons and the ventrally located motor neurons. The three primary motor neurons
are located in stereotypical patterns relative to the somite boundaries, and are known
as the rostral primary (RoP), middle primary (MiP) and caudal primary (CaP) neurons.
The CaP axon pioneers the common pathway of motor axons to the horizontal
myoseptum. All three axons extend to the muscle pioneer cells at the periphery, before
growing along separate pathways to their final targets (Hjorth &Key, 2002).
One of the most fascinating cell types in the developing embryo is the neural crest.
This population of relatively large cells is present at the border of the neural plate and
the future epidermis, prior to formation of the neural tube (Thisse etal., 1995). Neural
crest cells are unusual in that they delaminate from the neuroepithelium during
neurulation, and undergo long-range migrations throughout the embryo to form a
variety of cell types, such as most of the peripheral nervous system, all epidermal
pigment cells and much of the head skeleton. Cell types derived from vertebrate
neural crest are as diverse as sensory, sympathetic and enteric neurons, glia, melanocytes,
smooth muscle, dermis, connective tissue, cartilage and bone (reviewed by Baker &
Bronner Fraser, 1997; Halloran & Bemdt, 2003; see also Kelsh & Parichy, this volume).
Cranial neural crest cells are those which emanate from the early brain to populate the
anterior region of the head and pharyngeal arches. In the trunk region, individual
trunk crest cells migrate ventrally, following either the "lateral pathway", between the
lateral border of the somite and the overlying epidermis, or the "medial pathway",
between the medial border of the somite and the neural tube. Cells that migrate along
each pathway appear to have different fates. Medial pathway cells form sensory and
sympathetic neurons, Schwann cells and pigment cells, whereas cells utilising the
lateral pathway (which begin their migration later) make only pigment cells (Eisen &
Weston, 1993). In birds and mammals, establishment of the medial migration pathway
pattern in the trunk region is dependant upon sclerotomal cells, which occupy positions
adjacent to the notochord. In teleosts however, the sclerotome is initially confined to
the ventral aspect of each somite, and whilst sclerotomal cells do eventually migrate
dorsally to meet crest cells at the dorso-ventral midline, this occurs later in development.
Recent evidence suggests that the adaxial cells, which begin their movement shortly
after the initiation of neural crest migration, are more important in the regulation of
crest cell migration (Honjo & Eisen, 2005). In addition to cranial and trunk cells,
cardiac crest cells derived from the caudal hindbrain and the pre-otic region of the
neural tube, contribute to all segments of the myocardium (Sato & Yost, 2003).
Thomas E Hall 15
Following neurulation, the placodes are first visible as thickenings of columnar

epithelium in the non-neural ectoderm, which will go on to form the paired sense
organs (olfactory, otic and lateral line placodes), the lens of the eye (lens placode), the
anterior lobe of the pituitary gland (adenohypophyseal placode) and essential
components of some ganglia (epibranchial and trigeminal placodes). It is believed that
all of the seven vertebrate placodal tissues form from a common group of cells called
pre-placodal ectoderm (PPE), located lateral to the neural crest and neural plate (see
Fig. Ib). The PPE is characterised by the expression of six and eya genes, and is later
regionalised by downstream transcription factors (reviewed by Baker & Bronner-Fraser,
2001; Schlosser, 2005). The lens placode is the only entirely non-neurogenic placode
and gives rise to the lens of the eye.
The otic placode is first visible lateral to rhombomeres three-five, and approximately
halfway between the eyes and the first somite in zebrafish (Kimmel et al., 1995). The
central fluid-filled chamber is formed by cavitation, rather than by invagination as in
other vertebrates (Whitfield et al, 2002). Now called the otic vesicle, this hollow ball of
epithelium gives rise to all structures of the membranous labyrinth and the neurons of
the statoacoustic ganglion. The dorsal part of the epithelium thins, whereas the ventral
portion thickens, marking the future site of the sensory patches (maculae and cristae)
which contain the hair cells. Cells of the statoacoustic ganglion are derived from the
otic epithelium. These neuroblast cells undergo an epithelial to mesenchymal transition,
and accumulate beneath the rostral half of the vesicle, where they differentiate into
neurons (Haddon & Lewis, 1996). The adult ear contains three otoliths, one associated
with the maculae of the utricle, saccule and lagena. Initially, only two otoliths form in
the embryo, at the rostral and caudal ends of the vesicle. The third otolith forms much
later, well into the larval period (Riley & Moorman, 2000).
Each olfactory placode is initially a homogeneous mass of cells. As the placode
differentiates, the basal cells, sensory cells and support cells characteristic of the adult
olfactory epithelium become apparent. However, before these develop, a class of pioneer
neurons have been shown to extend path-finding axons to contact the telencephalon,
before undergoing apoptosis (Whitlock & Westerfield, 1998). The sensory neurons of
the olfactory placode then extend axons along the same path. Once within the CNS,
the axons segregate into glomeruli, clustered within the developing olfactory bulb.
The first neuromasts of the lateral line system are also placodally derived. They are
deposited by migrating primordia first detectable in the otic region through expression
ofcadherin 6 (Liu et al, 2006). The neuromasts of the head form the anterior lateral line
system (ALL) and are innervated by a ganglion located between the ear and eye. The
neuromasts of the body and tail form the posterior lateral line system (PLL), whose
ganglion is just posterior to the ear. Each neuromast is comprised of hair cells which
resemble those of the inner ear, surrounded by support cells (see Pankhurst, this volume).
In some species, through specialisation of the hair cell receptors, it has evolved into an
electro-sensory system (Dambly-Chaudiere et al, 2003; see Krischbaum &Denizot,
this volume). The PLL primordium is the most extensively studied of the two, and in
the zebrafish the extent of its migration is used as a staging tool (Kimmel et al, 1995).
From its initial position posterior to the otic vesicle, the primordium migrates to the
horizontal myoseptum. The most rostral of the cells become the innervating ganglion,
whereas the most caudal cells migrate posteriorly, along the entire length of the
horizontal myoseptum. The cells continue to divide as they migrate, to replace
the periodically deposited neuromasts. It has recently been shown that migration of the
PLL occurs along a pathway marked by the chemokine Sdfla, and that its receptor
Cxcr4 is expressed by the PLL cells. Furthermore, neuromast deposition appears to
depend on HGF signalling from the myosepta, through the c-met tyrosine kinase
receptor, also expressed by the PLL (Haines et al, 2004). Despite major differences in
the adult pattern of the lateral line system, it appears that the early migratory processes
involved in migration and neuromast deposition are highly conserved, even between
species such as the Mexican blind cave fish (Astyanax fasciatus) and the medaka
(Sapedeetal., 2002).
Organogenesis in the Endoderm

After undergoing involution, the endodermal progenitors of the hypoblast sit beneath
the mesodermal and ectodermal cells, on the surface of the yolk mass (Warga &
Stainier 2002). The majority of the endodermal cells will contribute to structures of the
digestive system; the alimentary canal, liver, gall bladder and pancreas. However,
endoderm originating in the dorsoanterior region will also become the pharyngeal
pouches of the head, giving rise to the segmental gill clefts, thymus, thyroid, parathyroid
and parts of the inner ear. Confocal analysis in the zebrafish has shown that at early
somite stages, endodermal cells constrict into a thin ribbon of midline cells, the intestinal
rod, running posteriorly from the level of the first somite (Field et al, 2003a). The liver,
pancreas and swim bladder (which is not part of the digestive system) all develop by a
process of budding from this central tract. Interestingly, the pancreas arises from two
distinct anlagen, a dorsal posterior bud which gives rise only to endocrine cells, and a
ventral anterior bud which gives rise to the exocrine cells, the pancreatic duct and a
small proportion of endocrine cells (Field et al., 2003b). The more anterior regions of
the alimentary canal, the pharynx and oesophagus arise at mid to late somite stages
from a seemingly separate population of precursor cells (Wallace &Pack, 2003). Further
compartmentalisation of the alimentary canal occurs throughout the larval stages (Ng
et al., 2005; R0nnestad &Morais, this volume).
HOX GENES, SEGMENTAL PATTERNING AND THE

EVOLUTION OF AXIAL COMPLEXITY
The homeotic or hox genes were first described in the fruitfly (Drosophila melanogaster)
as key regulators of regional identity along the antero-posterior axis of the embryo.
Eight linked genes were found to make up the homeotic complex (Lewis, 1978).
Mutations in these transcription factors conferred dramatic phenotypes, whereby one
body segment would take on the identity of another. For instance in the mutant
Thomas E Hall 17
antennapedia, legs grow on the head, in place of the antennae. Hox genes also exhibit
"colinearity", meaning that their pattern of expression along the AP axis reflects the
spatial organisation of genes, such that the most 3' genes are activated first, with
sequential activation of more 5' sequences (Duboule, 1998). Complex interactions
occur between adjacent hox genes such as sharing or competing for enhancer elements,
which explains the maintenance of their tight clustering. Hox genes have since been
described in diverse taxa within the bilateria (Balavoine et al, 2002), but there is great
variation in gene number. Interspecies variation reflects two types of gene duplication;
the tandem duplication of genes within a cluster, and whole cluster duplication. Current
models suggest that the single cluster arrangement found in the fruitfly originated by
successive duplication from a single gene. The tetrapods (including mammals, birds,
amphibians and reptiles) all have four hox clusters, consistent with two rounds of whole
cluster duplication (Krumlauf, 1994). It is possible that this is a reflection of two rounds
of whole genome duplication which occurred via polyploidisation during the origin of
vertebrates; the so-called "2R" hypothesis (Sidow, 1996; Holland, 1999). A logical
progression of this argument led to the suggestion that an increase in the number of hox
genes, and/or an associated increase in genomic complexity was permissive for the
evolution of more complex body plans, consistent with the long-standing theory that
gene duplication is an important mechanism for generating genetic novelty in evolution
(Ohno, 1970). Extensive phylogenetic studies have now been carried out to address
this issue. Most surprisingly, an examination of hox genes in the zebrafish revealed the
existence of seven hox clusters (Amores et al., 1998), comprising 47 known genes
(Kurosawa et al., 2006). Furthermore, expanded hox clusters appear to be the common
condition within the teleosts, with the medaka possessing 46 genes in seven clusters,
and torafugu (Fugu rubripes) 48 genes in eight clusters. This reflects a further full-scale
genome duplication, in the common ancestor of teleosts, elegantly demonstrated by
Jaillon et al. (2004), using data from the spotted green pufferfish (Tetraodon nigroviridis)
genome. They demonstrated firstly, that every chromosome was involved in large-
scale duplication, and secondly, a striking pattern of double synteny, with one
chromosomal region in humans matching two in spotted green pufferfish, across the
whole genome. Consistent with these observations, the location of the eighth zebrafish
hox cluster has been identified by synteny comparisons, but it contains no hox-related
sequences, with the exception of a single microRNA (Weltering & Durston, 2006).
The exact point within the actinopterygian lineage at which the duplication event
occurred is unclear, although the available evidence suggests that it occurred shortly
before the origin of the teleosts, since the non-teleost bichir, bowfin and paddlefish
have hox clusters resembling those of the tetrapods (Crow et al., 2006).
Hox genes across the vertebrates fall into 13 paralogue groups, although not all
paralogues are represented in each cluster, due to gene loss since duplication. According
to accepted nomenclature, hox gene loci in vertebrates are referred to as A, B, C and
D clusters. Since the teleost loci are duplicated, they are referred to as hoxAa, hoxAb
etc. (Kurosawa et al., 2006; Finn & Kristoffersen, 2007). Classically, the retention
of a duplicated gene is necessitated by the acquisition of novel functions
(neofunctionalisation; Ohno, 1970), or by the independent loss of regulatory functions

from each gene, resulting in paralogues with distinct but complementary properties
(subfunctionalisation; Force et al, 1999). As to whether duplication of hox genes
allowed the evolution of more complex body plans, the jury is still out. It has been
argued that invertebrates, which possess only a single hox cluster, exhibit by far greater
diversity in terms of species richness and variety of body plans than do vertebrates. In
addition, whilst most actinopterygians exhibit more hox clusters than sarcopterygians,
and greater species diversity, it has been argued that "a zebrafish is not more complex
than a mouse" (Bruce et al., 2001, cited in Crow et al., 2006).
The basic functions of hox genes between Drosophila, mice and teleosts are
conserved; they act as selectors of regional identity along the primary body axis.
Knockout studies in the mouse have demonstrated that hox paralogue groups are
necessary for many diverse aspects of axial patterning including hindbrain specification,
neural crest, pharyngeal and cranio-facial development. Particularly well characterised
are effects on the axial skeleton and vertebrae, due to the ease of recognising
morphological changes in vertebral structure (reviewed by Maconochie et al., 1996).
The hox genes are highly redundant in the mouse, with knockouts in single genes
generally having mild phenotypes, due to compensation by their paralogues. For
instance, the hoxlO and 11 groups each contain three genes: hoxalO, hox-dO, hoxdlO,
and hoxal I , hoxcl I , hoxdl I respectively. In the absence of hox 10 function, no lumbar
vertebrae are formed. Instead, ribs project from all posterior vertebrae, extending
caudally from the last thoracic vertebrae to beyond the sacral region. In the absence of
hoxl 1 function, sacral vertebrae are not formed and instead these vertebrae assume a
lumbar identity. In each case, the redundancy among these paralogous family members
is so great that this aspect of hox patterning is not apparent in mice that are mutant for
five of the six paralogous alleles (Wellik & Capecchi, 2003). Having said this, for most
paralogy groups a degree of subfunctionalisation is evident. In the zebrafish, hox genes
have been shown to be activated in a colinear fashion (Prince et al., 1998a). Genes
from paralogue groups 1, 2,3 and a subset of 4 are expressed within the developing
hindbrain and show many similarities in pattern with those of the mouse (Prince et al.,
1998b). Genes from paralogue group 2 have also been shown to act to pattern the
second pharyngeal arch (Hunter & Prince, 2002). It should be noted at this point that
the axial organisation of tetrapod vertebrae is more complex than that of the zebrafish.
Only two basic classes of teleost vertebrae are recognised: trunk vertebrae and tail
vertebrae, in contrast to the tetrapods' five. Within the zebrafish trunk mesoderm
however, many hox genes are expressed in a segmental manner. In addition, unlike in
tetrapods, regionalised expression within the notochord has been described (Prince
et al., 1998c). The functional roles of these genes are currently unknown, but are likely
to underpin more subtle aspects of regional identity.
FUTURE PERSPECTIVES
The process of early pattern formation in teleosts has been well studied historically.
However, due to the sheer diversity of the lineage, many aspects of cell movement and
Thomas E Hall 19
differentiation, particularly during the later stages, are only documented from a single,
or small number of species. The rise of intensive aquaculture is helping to address this
shortcoming. Using the genetic models of the zebrafish and medaka, we are now
beginning to understand the molecular basis of pattern formation. In addition,
comparative genomics, utilising the zebrafish, torafugu and spotted green pufferfish
genomes is allowing the examination of the very roots of morphological complexity,
through the study of genome evolution.
Acknowledgments
I would like to thank Alison Rutstein and Abigail Gibson for comments on the
manuscript.
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Dambly-Chaudire C. , Sapde D. , Soubiran F. , Decorde K. , Gompel N. , Ghysen A. (2003)
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Devoto S.H. , Stoiber W. , Hammond C.L. , Steinbacher P. , Haslett J.R. , Barresi M.J. ,
Patterson S.E. , Adiarte E.G. , Hughes S.M. (2006) Generality of vertebrate developmental
patterns: evidence for a dermomyotome in fish. Evol Dev 8: 101-110
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Neuhauss S.C. , Stemple D.L. , Zwartkruis F. , Rangini Z. , Driever W. , Fishman M.C. (1998)
Early development of the zebrafish pronephros and analysis of mutations affecting pronephric
function. Development 125: 4655-4667
Duboule D. (1998) Vertebrate hox gene regulation: clustering and/or colinearity? Curr Opin
Genet Dev 8: 514-518
Dubrulle J. , McGrew M.J. , Pourqui O. (2001) FGF signaling controls somite boundary
position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell
106: 219-232
Easter S.S. , Jr ., Malicki J.J. (2002) The zebrafish eye: developmental and genetic analysis.
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Eisen J.S. , Weston J.A. (1993) Development of the neural crest in the zebrafish. Dev Biol
159: 50-59
Felsenfeld A.L. , Curry M. , Kimmel C.B. (1991) The fub-1 mutation blocks initial myofibril
formation in zebrafish muscle pioneer cells. Dev Biol 148: 23-30
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in zebrafish. I. Liver morphogenesis. Dev Biol 253: 279-290
Field H.A. , Dong P.D. , Beis D. , Stainier D.Y. (2003b) Formation of the digestive system in
zebrafish. II. Pancreas morphogenesis. Dev Biol 261: 197-208
Finn R.N. , Kristoffersen B.A. (2007) Vertebrate vitellogenin gene duplication in relation to the
3R Hypothesis. Correlation to the pelagic egg and the oceanic radiation of teleosts. PLoS
ONE 2(1): e169
Force A. , Lynch M. , Pickett F.B. , Amores A. , Yan Y.L. , Postlethwait J. (1999) Preservation
of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531-1545
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Biol 49: 317-324
Gilbert S.F. , Raunio A.M. (1997) Embryology: Constructing the Organism. Sinauer
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notochord. Development 130: 873-887
Gorodilov Y.N. (1996) Description of the early ontogeny of the Atlantic salmon, Salmo salar,
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Haines L. , Neyt C. , Gautier P. , Keenan D.G. , Bryson-Richardson R.J. , Hollway G.E. , Cole
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Hall T.E. , Smith P. , Johnston I.A. (2004) Stages of embryonic development in the Atlantic
cod Gadus morhua. J Morphol 259: 255-270
Halloran M.C. , Berndt J.D. (2003) Current progress in neural crest cell motility and migration
and future prospects for the zebrafish model system. Dev Dyn 228: 497-513
Hibi M. , Hirano T. , Dawid I.B. (2002) Organizer formation and function. Results Probl Cell
Differ 40: 48-71
Hjorth J. , Key B. (2002) Development of axon pathways in the zebrafish central nervous
system. Int J Dev Biol 46: 609-619
Holland P.W. (1999) Gene duplication: past, present and future. Semin Cell Dev Biol 10: 541-
547
Honjo Y. , Eisen J.S. (2005) Slow muscle regulates the pattern of trunk neural crest migration
in zebrafish. Development 132: 4461-4470
Howley C. , Ho R.K. (2000) mRNA localization patterns in zebrafish oocytes. Mech Dev 92:
305-309
Hunt T.E. (1929) Hensens node as an organizer in the formation of the chick embryo. Anat
Rec 42: 22
Hunter M.P. , Prince V.E. (2002) Zebrafish hox paralogue group 2 genes function redundantly
as selector genes to pattern the second pharyngeal arch. Dev Biol 247: 367-389
Iwamatsu T. (1994) Stages of normal development in the medaka Oryzias latipes. Zool Sci
11: 825-839
Jaillon O. , Aury J.M. , Brunet F. , Petit J.L. , Stange- Thomann N. , Mauceli E. , Bouneau L. ,
Fischer C. , Ozouf-Costaz C. , Bernot A. et al ., (2004) Genome duplication in the teleost fish
Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431: 946-957
Johnston I.A. , Hall T.E. (2004) Mechanisms of muscle development and responses to
temperature change in fish larvae. In: Govoni J.J. (ed) The development of form and function
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spawning

environment reproduction egg type fertilisation

Petromyzontiformes holoblastic + + -1- +

Ac ipenseri formes M semi-holoblastic + + + +

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To study physiology is to examine how organisms have evolved solutions

Roderick Nigel Finn

Part 2: Respiration & Homeostasis

Part 3: Nutrition and Energy

Part 4: Sensory Physiology

Part 6: Control and Defense

Part 7: Functional Changes in Form

EARLY PATTERN FORMATION

The Early Blastula and the Yolk Syncytial Layer

EPIBOLY AND GASTRULATION

Mesodermal and Endodermal Specification

Convergent-extension and the Fish "Organiser"

DIFFERENTIATION OF THE GERM LAYERS

Organogenesis in the Ectoderm

Following neurulation, the placodes are first visible as thickenings of columnar

Organogenesis in the Endoderm

HOX GENES, SEGMENTAL PATTERNING AND THE

(neofunctionalisation; Ohno, 1970), or by the independent loss of regulatory functions

Osmo- and Ionoregulation

Swimming and Muscle

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