Comparative Physiology and Evolution of Vision in Invertebrates: A: Invertebrate Photoreceptors

735 Pages·1979·24.88 MB·English

by  H. Autrum

Handbook
of
Sensory Physiology
Volume VII/6A
Editorial Board
H. Autrum R. lung WR. Loewenstein
D. M. MacKay H.-L. Teuber
Comparative Physiology
and Evolution of
Vision in Invertebrates
A:
Invertebrate Photoreceptors
By
H. Autrum M. F. Bennett B. Diehn K. Hamdorf
M. Heisenberg M. larvilehto P. Kunze R. Menzel
W. H. Miller A. W. Snyder D. G. Stavenga M. Yoshida
Edited by
H.Autrum
With 314 Figures
Springer-Verlag Berlin Heidelberg New York 1979
H. Autrum
Zoologisches Institut der Universitiit, Luisenstr. 14, 8000 Miinchen, Germany
ISBN-13: 978-3-642-67001-5 e-ISBN-13: 978-3-642-66999-6
DOl: lO.lO07/978-3-642-66999-6
Library of Congress Cataloging in Publication Data Main entry under title: Comparative physiology and evolution of vision in
invertebrates. (Handbook of sensory physiology; v. VII/6) Bibliography: p. Includes indexes. CONTENTS: A. Invertebrate photore·
ceptors. 1. Vision. 2. Invertebrates-Physiology. 3. Physiology, Comparative. I. Autrum, Hansjochem. II. Series. QP351.H34 vol. 7/6A,
etc. [QP475] 591.1'82'08s 78·21470 (v. A) [592'.01'832]
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Softcover reprint of the hardcover 1st edition 1979
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Preface
In the comparative physiology of photoreception by the Protista and the
invertebrates two aspects are emphasized: (1) the diversity of visual processes in
these groups and (2) their bearing upon general mechanisms of photoreception.
Invertebrates have evolved a far greater variety of adaptations than vertebrates
modifications aiding survival in the remarkably different biotopes they occupy.
The number of species in itself suggests this multiformity; each of them has
peculiarities of its own, in morphology as well as in physiology and behavior. But
these special adaptations are variations on a few great themes.
Although the catalogue of invertebrate species is immense, the literature
concerning them nearly rivals it in extent-even if one considers only that fraction
dealing with visual physiology. Taxonomy proceeds by grouping the species,
categorizing them in genera, families, orders, and progressively larger units.
Similarly, comparative physiology aims at an analogous, more or less compre
hensive, classification. This Part A of Volume VII/6, like Part B that follows it,
emphasizes the broad questions that concern groups larger than the individual
species; in some cases these questions have general applicability. The middle
course between approaches that are too specialized and those that are too general
is often elusive, but here we attempt to follow it. The vast number of special
adaptations-probably, as we have said, as large as the number of species-is
beyond the range even of a handbook.
Comparative physiologists continually ask to what extent the findings in one
species can be generalized? Of the roughly 85,000 known species of Diptera, the
visual physiology of less than half a dozen have been studied intensively. And even
these have been chosen, as a rule, not because they displayed particularly
interesting adaptations, but because they could be raised easily in the laboratory
or were readily obtainable in large numbers. Physiologists have usually tried to
establish the generality of their results by showing that a certain morphologic
structure is associated with a certain function. With this aim geneticists, initially
working with Drosophila, have recently developed new methods (cf. Ch. 12) with
results having implications for animals other than just the insects.
Behavior, physiology, and morphology-the latter ranging from anatomy
down to ultrastructure and even to the configuration of molecules-are insepar
able. Data regarding the anatomic and light-microscopic structure of invertebrate
visual organs are so extensive that in these volumes they can be mentioned only
where they particularly assist in the understanding of physiologic processes and
VI Preface
where the relationship between form and function is especially close. In the
foreground, then, we shall stress biophysics, biochemistry, and behavior.
Nevertheless, the number of species cited as examples is quite large. To guard
against premature generalization, the particular species studied is named in all of
the following discussions; it is clearly a bad habit to speak simply of "the fly". On
the other hand, the available variety of animals should not be used as an excuse for
multiplying the already far too numerous publications by repetitious experiments
revealing only analogous results. Such studies of related species, if they are to be of
interest, must pose new questions of their own-whether the approach employed
derives from ecology, behavior, biochemistry, or biophysics.
Comparative physiology can of course not be limited to the invertebrates. In
many chapters vertebrates are drawn into the discussion, either because they have
evolved comparable structures or functions or because they differ.
Correspondingly, invertebrates are also treated elsewhere in this handbook, in
addition to these two parts of Vol. VII; these articles are listed at the end of the
Preface. In all cases, repetition has been avoided wherever possible.
Part A is concerned primarily with the physiology of photoreceptor cells. It is
impossible to draw a strict boundary between this aspect and the central nervous
processes, for various reasons. First there is the obvious fact that photoreception
does not stop with the photoreceptors. Second, in invertebrates, far more than in
vertebrates, the study of vision has begun with and depends on behavioral
experiments; as a rule, the biochemical and biophysical work has stemmed from
prior analyses of behavioral physiology. Color vision, sensitivity to polarized and
UV light, and extraocular photoreception are examples. Circadian periodicity,
which is treated briefly, does not yet enjoy a genuine causal analysis; as such, it is a
quite distinct behavioral phenomenon.
The attentive reader of the contributions to these volumes will find many
unsolved problems; the further research progresses, the further the horizon
recedes. Untilled fields and even impenetrable jungles come into view. Often the
relationships between particular variants of molecular structure or biophysical
events and the behaviour that must somehow be associated with them are
impossible even to guess at, let alone document experimentally. In the area of
invertebrate photoreception innumerable questions remain unanswered; in parti
cular, though, challenging problems arise as soon as methods and results from
other disciplines are applied to biologic phenomena. Here "interdisciplinary"
implies not only the application of mathematical, physical, and chemical know
ledge and techniques to a special topic, but also the manifold approaches within
the field of biology itself; one may consider a particular phenomenon from several
viewpoints, among them evolutionary origin and adaptation to a given biotope.
Our understanding in this area is so incomplete, and speCUlative interpretations so
outnumber facts and theories, that a consistent, well-founded presentation remains
beyond our reach. No attempt to produce one will be made here.
Almost daily new results are published; some of them open entirely novel
aspects of general significance. In view of this rapid advance, we may well ask
whether a survey of the present state of knowledge in the form of a handbook is
really appropriate. Will such writings not become outdated in a few years, perhaps
even before they have left the author's desk? On the contrary, I think it is precisely
Preface VII
in such periods of tempestuous development that one must from time to time seek
the eye of the storm, taking the opportunity to look the situation over and to see
which problems have been solved and which remain open. A handbook gives us
this chance. To the beginner it opens the way to the earlier literature; those more
advanced may learn the current status of areas related to their own. At the least it
stands as a milestone and a prominence from which we survey both past and
future. A handbook cannot replace the substance of the classical works-those of
Johannes MUller, Exner, Hesse and von Frisch, to name but a few-but it can
point the way to them. In studying such pioneering papers, the reader will find
remarkably clear statements of central problems, hypotheses, theories, and
suggestions. Many a dead-end road, and many a fruitless discussion, would be
circumvented if researchers were more familiar with this early literature. The value
of such familiarity is evident in a number of the points made here. These handbook
volumes, then, serve both as a milestone and as an informative overview; we owe
our special thanks to the publisher for bringing them into being.
MUnchen, den 12. Oktober 1978 H. AUTRUM
Contents
Chapter 1 Introduction. By H. AUTRUM. With 4 Figures . . 1
Chapter 2 Photic Responses and Sensory Transduction in Protists. By
B.DIEHN. With 18 Figures . . . . . . . . . . . . 23
Chapter 3 Intraocular Filters. By W. H. MILLER. With 39 Figures . . .. 69
Chapter 4 The Physiology ofInvertebrate Visual Pigments. By K. HAMDORF.
With 39 Figures . . . . . . . . . . . . . . . . . . . . 145
Chapter 5 The Physics of Vision in Compound Eyes. By A. W. SNYDER.
With 36 Figures . . . . . . . . . . . . . . . . . . . . 225
Chapter 6 Receptor Potentials in Invertebrate Visual Cells.
By M. JARVILEHTO. With 19 Figures . . . . . . 315
Chapter 7 Pseudopupils of Compound Eyes. By D.G.STAVENGA. With
50 Figures . . . . . . . . . . .. ......... 357
Chapter 8 Apposition and Superposition Eyes. By P. KUNZE. With 46
Figures . . . . . . . . . . . . . . . . . . . . . . . . 441
Chapter 9 Spectral Sensitivity and Colour Vision in Invertebrates. By
R.MENZEL. With 14 Figures ............... 503
Chapter 10 Extraocular Photoreception. By M. YOSHIDA. With 39 Figures 581
Chapter 11 Extraocular Light Receptors and Circadian Rythms. By
M.F. BENNETT. With 9 Figures .............. 641
Chapter 12 Genetic Approach to a Visual System. By M. HEISENBERG.
With 1 Figure 665
Author Index . 681
Subject Index . .707
List of Contributors
AUTRUM, H., Zoologisches Institut der UniversiHit, Luisenstr. 14, 8000 Miinchen,
Germany
BENNETT, M.F., Department of Biology, Colby College, Waterville, Maine 04901,
USA
DIEHN,B., Department of Chemistry, University of Toledo, 2801 Bancroft Street,
Toledo, Ohio 43606, USA
HAMDORF, K., Tierphysiologisches Institut der Ruhr-UniversiUit, Postfach 2148,
463 Bochum-Querenburg, Germany
HEISENBERG, M., Institut fUr Genetik und Mikrobiologie der UniversiHit, Rontgen
ring 11, 8700, Wiirzburg, Germany
JXRVILEHTO, M., Department of Physiology, University ofOulu, Kajaanintie 52 A,
90220 Oulu 22, Finland
KUNZE,P., Biologisches Institut der Universitat, Ulmer Str. 227, 7000 Stuttgart 60,
Germany
MENZEL, R., Freie Universitat FB 23, Institut fUr Tierphysiologie, Grunewald
straBe 34, 1000 Berlin 41, Germany
MILLER, W. H., Department of Ophthalmology and Visual Science, Yale Uni
versity School of Medicine, New Haven, Conn. 06510, USA
SNYDER,A. W., The Institute of Advanced Studies, Research Schools of Biological
and Physical Sciences, Australian National University, Canberra, Australia
STAVENGA,D.G., Department of Physics, Laboratorium voor Algememe Natuur
kunde, Rijksuniversiteit Groningen, Westersingel 34, Groningen, The
Netherlands
YOSHIDA,M.*, Tamano Marine Laboratory, 2-3-3 Shibukawa, Tamano, Okyama,
Japan 706
* The name and the address of the Laboratory from August 1979: Ushimado Marine Laboratory,
Kashino, Ushimado, Okayama, Japan 701-43
Chapter 1
Introduction
H. AUTRUM, MUnchen, Germany
With 4 Figures
Contents
A. Comparative Physiology and Evolution 2
I. The Darwinian Way ...... . 2
II. The Way of Comparative Physiology 2
B. Invertebrates and Vertebrates: Comparative Physiology and Evolution. 3
I. Variability of Ecological Adaptations. 3
II. Structural Types of Visual Cells . 6
1. Visual Cells with Cilia . . . . . . 7
2. Visual Cells with Rhabdomeres . . 7
3. Photoreceptors with Neither Cilia nor Rhabdomeres 8
4. Comments on the Evolution of Photoreceptors 8
III. Primary Processes. . . 10
1. Visual Pigments. . . . . . . . . . . . . . 10
2. Receptor Membranes . . . . . . . . . . . 12
a) Permeability (Resting Potential and Receptor Potential) . 12
b) Lipid Content and Fluidity. 13
c) Membrane Protein Turnover . . 13
d) The Ca2+ Ions . . . . . . . . 13
3. Rhodopsin Content and Sensitivity. 13
C. Conclusions and Summary. 15
References. . . . . . . . . . . . . . . 16
"One might say that nature has taken delight in accumulating contradictions."
H. v. Helmholtz
Comparative physiology is the biologic science which begins with man, in
order to understand man. To understand man (biologically) means to know how
evolution has brought him into existence, to reveal the functions of organs, their
mechanisms of operation and their roles as parts of the organism, and to satisfy
the human urge to discover the laws of nature and to create order where diversity
prevails, whether for the sake of the laws themselves or for the sake of the power
that knowledge brings.
2 H. AUTRUM: Introduction
A. Comparative Physiology and Evolution
I. The Darwinian Way
The history of man goes back more than 3 x 109 years. Neither the character
istics man has in common with other organisms nor those that set him apart can
be understood except through comparisons. This was the method DARWIN and
HAECKEL used, proceeding from the early, simple species to late, more complex
forms; although DARWIN in 1859 (in The Origin of Species) did not yet dare to
include man in this evolution, he gave a hint of things to come: "Much light will
be thrown onthe origin of man and his history."
II. The Way of Comparative Physiology
The way of comparative sensory physiology is not that of comparative mor
phology. The former discipline begins with man. It is initially from our own
experience that we know what purpose sense organs serve, what their functions
and roles are. Our knowledge of the human eye begins with what we perceive
directly - that it is used for seeing, that it discriminates colors, detects forms and
movements, assists spatial orientation, and mediates in our relationship with the
environment and our recognition of friends and enemies. The method of compar
ative physiology moves outward from man, following a retrograde path in both
anatomy and physiology via the complicated sense organs of the vertebrates to
single sense cells like those in the skin of annelids (Lumbricus: HESSE, 1896;
Pontobdella: HESSE, 1897). In these cases and many others, comparative physiolo
gists discovered responses to light long before comparative morphologists had
found the visual cells themselves; DARWIN (1881, and others before him) observed
that earthworms respond to light. On the other hand, when HEssE (1897) discov
ered the striated border in the visual cells of several annelids and APATHY (1902)
made a similar discovery in the Hirudinea, anatomical analysis was far in advance
of physiologic study. In fact, many morphologic properties of visual organs were
discovered and described long before their physiologic significance became
known; in some cases, it is still not known [see, e.g., F AHREN BACH (1975); the
ciliary structures in sense organs are discussed, for example, by ATEMA (1973)].
But the physiologic properties found in advance of their morphologic sub
strates were many - and, again, in some cases the morphology is still unclear. In
1882 LUBBOCK discovered that ants (Formica, Lasius) respond to UV light, and
FOREL (1886; rev. see FOREL, 1910) showed that they detect it with their eyes.
KUHN (1927) and KUHN and POHL (1921) showed that for bees UV has the
quality of a color; AUTRUM and VON ZWEHL (1964) found bee visual cells that
were sensitive only to UV; and finally HAMDORF et al. (1971) demonstrated that
there is a particular rhodopsin in insects ( Ascalaphus) that is specifically sensitive
to UV. Sensitivity of the eyes to UV occurs in both vertebrates and invertebrates,
but only in the latter are there UV-specific receptors (see this Volume, Chs. 4, 9,
and 10).