Evolutionary Biology of Primitive Fishes Evolutionary Biology of Primitive Fishes Edited by R. E. Foreman Bamfield Marine Station Bamfield, British Columbia, Canada A. Gorbman University of Washington Seattle, Washington J. M. Dodd University College of North Wales Bangor, United Kingdom and R. Olsson University of Stockholm Stockholm, Sweden Plenum Press New York and London Published in cooperation with NATO Scientific Affairs Division Proceedings of a NATO Advanced Resean:h Workshop on Evolutionary Biology of Primitive Fishes, held April 14-17, 1985, at Bamfield Marine Station, Bamfield, British Columbia, Canada, co-sponsored by the Natural Sciences and Engineering Research Council of Canada and the Western Canadian Universities Marine Biological Society Library of Congress Cataloging in Publication Data NATO Advanced Research Workshop on Evolutionary Biology of Primitive Fishes (1985: Bamfield, B.C.) Evolutionary biology of primitive fishes. (NATO ASI series. Series A, Life sciences; v. 103) "Proceedings of a NATO Advanced Research Workshop on Evolutionary Biology of Primitive Fishes, held April 14-17, 1985, at Bamfield Marine Station, Bamfield, British Columbia, Canada"-T.p. verso. "Published in cooperation with NATO SCientific Affairs Division." Includes bibliographies and index. 1. Fishes-Evolution-Congresses. 2. Fishes, Fossil-Congresses. I. Foreman, R. E. (Ronald Eugene), date. II. North Atlantic Treaty Organization. Scientific Affairs Division. III. Title. IV. Series. QL618.2.N37 1985 597'.038 85-31168 ISBN-13: 978-1-4615-9455-0 e-ISBN-13: 978-1-4615-9453-6 001: 10.1007/978-1-4615-9453-6 © 1985 Plenum Press, New York Softcover reprint of the hardcover I st edition 1985 A Division of Plenum Publishing Corporation 233 Spring Street, New York, N.Y. 10013 All rights reserved. No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher PREFACE What, precisely, is a primitive fish? Most biologists would agree that the living cyclostomes, selachians, crossopterygians, etc. cannot be considered truly primitive. However, they and the fossil record have served to provide the information which forms the basis for speculation concerning the nature of the original vertebrates. This symposium of biologists from a variety of disciplines was called together to create collectively, from the best available current evidence, a picture of the probable line of evolution of the prototype primitive fishes. The symposium was designed to follow one that took place in Stockholm in 1967, convened for a similar purpose, with about the same number of participants. It is a matter of interest that almost the entire 1967 symposium (Nobel Symposium 4) dealt only with the hard tissues, whether fossil or modern. In charting the course of the present symposium it was felt that the intervening years have produced numerous lines of new evidence that could be employed in the same way that a navigator determines his position. Each field, be it adult morphology, geology, ecology, biochemistry, development or physiology, generates evidence that can be extrapolated backward from existing vertebrate forms and forward from invertebrate forms. If the intersect of only two lines of evidence produces a navigational "fix" of rather low reliability, then an intersect, however unfocussed, of multiple guidelines from more numerous disciplines might provide a better position from which to judge early vertebrate history. Accordingly, we have recorded here information from behaviorist-ecologists who have tried to see the early vertebrates in their own prevailing environments and subject to the exacting restraints of these environments. The biochemists and immunocytochemists can trace particular peptide combinations from the established vertebrate taxa clear across the terra (or mare) incogllita into the invertebrate domain. Developmental information hopefully supplies even more insight than adult structure, and we have tried to obtain as much of this as is available and appropriate. The large body of accumulated physiological lore now can be drawn upon to give us some understanding of how the early vertebrates may have solved their adaptive functional problems. At any rate, we have here as good a picture as is currently available of the prevailing circumstances and probable structural and functional features of the truly primitive fishes, if that is what these aquatic creatures may be called. For whatever it is worth, we present this crystallization, or condensation, of current information as it applies to early vertebrate phylogeny. v vi PREFACE We gratefully acknowledge the editorial assistance of Dr. William S. Wheeler and Dr. Christine E. Milliken, and typing assistance of Miss Sandra Kschischang and Mrs. Linda Mather. The technical software support group of Lexisoft, Inc. of Davis, California, was always there when we needed their assistance, for which we are very appreciative. We are most grateful to Dr. M. di Lullo, Director of NATO ARW Programme, and the North Atlantic Treaty Organization for their support of the workshop. Financial support was also provided by the Natural Sciences and Engineering Research Council of Canada and the Western Canadian Universities Marine Biological Society. The sponsoring organizations greatly contributed to the success of the workshop, as did Mrs. Linda Mather, Miss Sabina Leader and Miss Anne Bergey. R. E. Foreman A. Gorbman J. M. Dodd R. Olsson September, 1985 CONTENTS Scenarios: Why? C. Gans General Ecology of Primitive Fishes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . II G. Bertmar Facts and Thoughts on Piscine Phylogeny. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 31 H. C. Bjerring Reconstructing the Life Cycle and the Feeding of Ancestral Vertebrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 59 J. Mallatt Habitat, Phylogeny and the Evolution of Osmoregulatory Strategies in Primitive Fishes .... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 69 R. W. Griffith The Brain and Sense Organs of the Earliest Vertebrates: Reconstruction of a Morphotype . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81 R. G. Northcutt The Lateral Line System of Cyclostomes .............................. 113 B. Fernholm Freshwater Parasitic Lamprey on Vancouver Island and a Theory of the Evolution of the Freshwater Parasitic and Nonparasitic Life History Types . .. . . .. .. . . .. . . .. . . .. 123 R. J. Beamish Organ Development and Specialization in Lamprey Species. . . . . . . . . . . . . . .. 141 J. H. Youson Early Development of Oral, Olfactory and Adenohypophyseal Structures of Agnathans and Its Evolutionary Implications ............ 165 A. Gorbman and A. Tamarin vii viii INDEX Immunologic Relations Among Fish Groups ........................... 187 G. T. Rijkers Evolution of Temperature Regulation and of Constancy of Function (Homeokinesis) at Different Temperatures ................. 203 C. L. Prosser Respiration in Phyletically Ancient Fishes ......................... 217 W. Burggren, K. Johansen and B. McMahon Regulation of Blood and Body Fluids in Primitive Fish Groups ......... 253 R. Hinge Evolution of the Renin-Angiotensin System and Its Role in Control of Cardiovascular Function in Fishes . . . . . . . . . . .. 275 H. Nishimura Evolutionary Aspects of Reproduction in Cyclostomes and Cartilaginous Fishes .................................... 295 J. M. Dodd and M. H. I. Dodd On Urea Formation in Primitive Fishes ......................... 321 G. W. Brown, Jr. and S. G. Brown Some Aspects of Hormonal Regulation of Metabolism in Agnathans .... .. 339 E. Plisetskaya Hagfish Insulin: Evolution of Insulin . . . . . . . . . . . . . . . . . . . . . . . . . .. 363 S. O. Emdin, D. F. Steiner, S. J. Chan and S. Falkmer Evolution of Gastro-Entero-Pancreatic Endocrine Systems in Lower Vertebrates ................................... 379 M. C. Thorndyke and S. Falkmer Functional Evolution of Gastrointestinal Hormones ................. 40 I S. R. Vigna Hormonal Peptide Evolution ................................. 413 Y. A. Fontaine Tissue Distribution of Hormonal Peptides in Primitive Fishes .......... 433 M. Nozaki Group Photo 455 Contributors and Participants 457 Index ................ . 461 SCENARIOS: WHY? Carl Gans Division of Biological Sciences The University of Michigan Ann Arbor. Michigan 48109-1048 Introduction In beginning this symposium on the patterns disclosed by primitive fishes, we should perhaps ask what it is that we are trying to achieve. Some of us hope to generate schemes for the taxonomic placement of certain Recent animals and for mapping the shifting pattern of their phenotypes through time. However, another part of our agenda might involve the generation of scenarios, i.e. efforts to reconstruct the functional changes producing the process of vertebrate evolution. Obviously, there are two sets of evidence that can be used to achieve these aims. The first derives from fossils and was emphasized in the previous symposium. The second derives from the Recent and is the topic here. At the start, we may wish to remind ourselves about the guidelines for making decisions about the past events that we wish to reconstruct. Specifically, what is it that we can observe and what is it that we may conclude from it? Obviously, comparison is the key of this symposium, and we hope to enhance the potential for it by assembling specialists on different groups of organisms and of distinct organ systems. We operate less by absolute determinations of conditions in one kind of system or animal, than by analyzing the similarities and differences disclosed by observation of diverse species. Hence, the rules of comparison apply to our system as well as to most others in biology, and we must keep them in mind. Aspects in comparison Animals provide us with three sets of data, their adult phenotype, the pattern by which the phenotype develops after fertilization and the way the phenotype is utilized by the organism. Thus, structure, development and function form three sets of descriptors of currently observable phenomena (Fig. I). These descriptors 2 C.GANS No Fig. 1. Venn diagram to show the three kinds of current similarities likely to be exhibited by organisms and the combined states that these may display. Note that similarity of function is not an aspect generated by the phenotype, but one that is permitted by the phenotype. (After Gans, 1985, Amer. Zool., in press). may be compared, and the similarities and differences thus disclosed may be refined by incorporating more specimens and species and improving the reliability of the observations. However, the similarities and differences obtained by the study of individuals of any single or pair of species may have multiple causes and permit only limited conclusions about affinity. More is needed, because similarities of morphology and physiology may reflect closeness of derivation from a common ancestor, matching of different phenotypes to a common environment or both. Hence analysis of affinity must take into account the potential pitfalls posed by the convergence of characters. This difficulty requires matching our findings against phylogenetic schemes, or cladograms. These let us test whether a particular condition seen in several species represents a single invention (i.e. appears in a single evolutionary line) or whether it has been invented independently a number of times (i.e. it appears in several separate evolutionary lines; Fig. 2). The origin of vertebrates involves another set of complicating problems. There are few obvious "outgroups" against which the vertebrates, and for that matter the chordates, may be compared; too many of the presumably intermediate forms appear to have become extinct. Also, there are no immediately obvious. "ancestors" from which "descendents" are derivable in a single, or relatively few steps. Indeed, we see an array of vertebrate characteristics, all of which are shared and derived, and all of which appear in the fossil record almost simultaneously, not shared with any other group. Such a situation suggests either that much time has passed (with the intermediate forms having all become extinct) or that there may be a common denominator for some of the set. SCENARIOS: WHY? 3 2 3 4 A 2 3 4 B 2 3 4 c f TIME I 2 3 4 1 D TIME I Fig. 2. A set of cladograms labelled and modified to show the pattern of character states of recent organisms (A), and the way this pattern would be modified if the vertical axis is explicitly made to represent time and fossils mapped into the appropriate places (C). The ecological, behavioral, physiological states seen in the Recent have been mapped onto one cladogram (B); whereas, the time-associated diagram indicates the potential for functional (as well as phenotypic) shifts in each line leading to members of a pair of sister groups (D). Obviously, selection for the transition must have been effected by the function-associated demands existing at the time of bifurcation. Common denominators are of interest because it is obviously easier to posit evolution by means of a limited number of changes than by positing multiple, coincident, but supposedly independent, events. Incidentally, this is one reason for