Environmental Stress, Adaptation and Evolution Edited by R. Bijlsma

v. Loeschcke

Springer Basel AG

Editors:

Dr. R. Bijlsma Department of Genetics University of Groningen Kerklaan 30 NL-975I NN Haren The Netherlands

Dr. V. Loeschcke Departrnent of Ecology and Genetics University of Aarhus Ny Munkegade Building 540 DK-8000 Aarhus Denmark

Library of Congress Cataloging-in-Publication Data Environmental stress, adaptation and evolution: / edited by

R. Bijlsma, VLoeschcke p. cm. -- (EXS; 83)

Inc1udes bibliographical references and index. ISBN 978-3-0348-9813-3 ISBN 978-3-0348-8882-0 (eBook) DOI 10.1007/978-3-0348-8882-0 1. Adaptation (Physiology) 2. Adaptation (Biology) 3. Stress (Physiology) 4. Evolution. 1. Bijlsma, R. (Rudolf), 1945-

11. Loeschcke, V. (Volker), 1950-- . III. Series. QP82.E825 1997 576.8'5--dc21

Deutsche Bibliothek Cataloging-in-Publication Data Environmental stress, adaptation and evolution: / ed. by R. Bijlsma ; V. Loeschcke. - Basel; Boston; Berlin : Birkhäuser, 1997

(EXS: 83)

ISBN 978-3-0348-9813-3 EXS. - Basel ; Boston; Berlin : Birkhäuser

Früher Schriftenrcihc Fortlaufende Beil. zu: Experientia

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© 1997 Springer Basel AG Originally published by Birkhäuser Verlag in 1997 Softcover reprint of the hardcover 1 st edition 1997

Cover design: Eis Meeles, Groningen, The Netherlands Printed on acid-free paper produced from chlorinc-frce pulp

ISBN 978-3-0348-9813-3

987654321

Contents

List of Contributors VII

Preface ...... . ................... XI

R. Bijlsma and Volker Loeschcke Introductory remarks: Environmental stress, adaptation and evolution. . . . . . . . . . . . . . . . . . . . . . . . . . . . . XIII

Extreme environments and adaptation

Mark R. Macnair The evolution of plants in metal-contaminated environments 3

Valery E. Forbes and Peter Calow Responses of aquatic organisms to pollutant stress: Theoretical and practical implications . . . . . . . . . . . . . . . . . . . . 25

Outi A. Savolainen and Piiivi K. Hurme Conifers from the cold ........ . 43

Genetic variation and environmental stress

Paul M Brakefield Phenotypic plasticity and fluctuating asymmetry as responses to environmental stress in the butterfly Bicyclus anynana . . 65

Nicole L. Jenkins, Carla M. Sgro and Ary A. Hoffmann Environmental stress and the expression of genetic variation 79

Wilke van Delden and Albert Kamping Worldwide latitudinal clines for the alcohol dehydrogenase polymorphism in Drosophila melanogaster: What is the unit of selection? . . . . . . . . . . . . . . . . . . . . . . . . . . 97

Andrew G. Clark Stress and metabolic regulation in Drosophila 117

Acclimation and response to thermal stress

Albert F. Bennett and Richard E. Lenski Phenotypic and evolutionary adaptation of a model bacterial system to stressful thermal environments. . . . . . . . . . . . . . . 135

VI Contents

Martin E. Feder and Robert A. Krebs Ecological and evolutionary physiology of heat shock proteins and the stress response in Drosophila: Complementary insights from genetic engineering and natural variation. . . . . . . . . . . . 155

Volker Loeschcke, Robert A. Krebs, Jesper Dahlgaard and Pawel Michalak High-temperature stress and the evolution of thermal resistance in Drosophila . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 175

Stress, selection and extinction

R. Bylsma, Jorgen Bundgaard, Anneke C. Boerema and Ttelam E Tim Putten Genetic and environmental stress, and the persistence of populations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193

Reinhard Burger and Michael Lynch Adaptation and extinction in changing environments. 209

Lev A. Zhivotovsky Environmental stress and evolution: A theoretical study 241

Anders P. Moller Stress, developmental stability and sexual selection . . . . . . . . . 255

Evolution and stress

Franr;ois Taddei, Marin Vulic, Miroslav Radman and Ivan Matic Genetic variability and adaptation to stress . . . . . . . . . . . . . . 271

Peter A. Parsons Stress-resistance genotypes, metabolic efficiency and interpreting evolutionary change . . . . . . .

Peter R. Sheldon The Plus 9a change model: Explaining stasis and evolution

..... 291

in response to abiotic stress over geological timescales . ..... 307

Subject index ............................. 321

List of Contributors

Albert F. Bennett, Department of Ecology and Evolutionary Biology, Uni­versity of California, Irvine, CA 92696, USA.

R. Bijlsma, Department of Genetics, University of Groningen, Kerklaan 30, NL-9751 Haren, The Netherlands.

Anneke C. Boerema, Department of Genetics, University of Groningen, Kerklaan 30, NL-975 1 Haren, The Netherlands.

Paul M. Brakefield, Institute of Evolutionary and Ecological Sciences, Leiden University, P.O. Box 9516, NL-2300 RA Leiden, The Netherlands.

J0rgen Bundgaard, Department of Ecology and Genetics, University of Aarhus, Ny Munkegade, Building 540, DK-8000 Aarhus C, Denmark.

Reinhard Biirger, Institute of Mathematics, University of Vienna, Strudl­hofgasse 4, A-I 090 Wien, Austria.

Peter Calow, Department of Animal and Plant Sciences, The University of Sheffield, Sheffield S 10 2UQ, UK.

Andrew G. Clark, Department of Biology, 208 Mueller Laboratory, Pennsylvania State University, University Park, PA 16802, USA.

Jesper Dahlgaard, Department of Ecology and ,Genetics, University of Aarhus, Ny Munkegade, Building 540, DK-8000 Aarhus C, Denmark.

Martin E. Feder, Department of Organismal Biology and Anatomy, The Commitee on Evolutionary Biology, and The College, The University of Chicago, 1027 East 57th Street, Chicago, IL 60637, USA.

Valery E. Forbes, Department of Life Sciences and Chemistry, Roskilde University, P. 0. Box 260, DK-4000 Roskilde, Denmark.

VIII List of Contributors

Ary A. Hoffmann, School of Genetics and Human Variation, La Trobe University, Bundoora, Victoria 3083, Australia.

Paivi K. Hurme, Department of Biology, University ofOulu, P.O. Box 333, FIN-90571 Oulu, Finland.

Nicole L. Jenkins, School of Genetics and Human Variation, La Trobe Uni­versity, Bundoora, Victoria 3083, Australia.

Albert Kamping, Department of Genetics, University of Groningen, Kerk­laan 30, NL-975I Haren, The Netherlands.

Robert A. Krebs, Department of Organismal Biology and Anatomy, The Commitee on Evolutionary Biology, The University of Chicago, 1027 East 57th Street, Chicago, IL 60637, USA.

Richard E. Lenski, Center for Microbial Ecology, Michigan State Uni­versity, East Lansing, M148824, USA.

Volker Loeschcke, Department of Ecology and Genetics, University of Aarhus, Ny Munkegade, Building 540, DK-8000 Aarhus C, Denmark.

Michael Lynch, Department of Biology, University of Oregon, Eugene, Oregon 97403, USA.

Mark R. Macnair, Hatherly Laboratories, University of Exeter, Department of Biological Sciences, Prince of Wales Rd, Exeter EX4 4PS, UK.

Ivan Matic, Laboratoire de Mutagenese, Institut Jacques Monod, 2 Place Jussieu, F-75251 Paris, France.

Pawel Michalak, Department of Ecology and Genetics, University of Aar­hus, Ny Munkegade, Building 540, DK-8000 Aarhus C, Denmark.

Anders P. M011er, Laboratoire d'Ecologie, CNRS URA 258, Universite Pierre et Marie Curie, Bat. A, 7eme etage, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 5, France.

List of Contributors IX

Peter A. Parsons, School of Genetics and Human Variation, La Trobe Uni­versity, Bundoora, Victoria 3083, Australia. For correspondence: 21 Avenue Road, Glebe, NSW 2037, Australia.

Miroslav Radman, Laboratoire de Mutagenese, Institut Jacques Monod, 2 Place Jussieu, F-7525l Paris, France.

Outi A. Savolainen, Department of Biology, University of Oulu, P. O. Box 333, FIN-90571 OuIu, Finland.

Carla M. Sgro, School of Genetics and Human Variation, La Trobe Uni­versity, Bundoora, Victoria 3083, Australia.

Peter R. Sheldon, Department of Earth Sciences, The Open University, Milton Keynes MK7 6AA, UK. e-mail: P.R.Sheldon@open.ac.uk

Fran~ois Taddei, Laboratoire de Mutagenese, Institut Jacques Monod, 2 Place Jussieu, F -7 5251 Paris, France.

Wilke van Delden, Department of Genetics, University of Groningen, Kerklaan 30, NL-9751 Haren, The Netherlands.

Welam F. Van Putten, Department of Genetics, University of Groningen, Kerklaan 30, NL-9751 Haren, The Netherlands.

Marin Vulic, Laboratoire de Mutagenese, Institut Jacques Monod, 2 Place Jussieu, F-75251 Paris, France.

Lev A. Zhivotovsky, Vavilov Institute of General Genetics, Russian Academy of Sciences, 3 Gubkin St., Moscow 117809, Russia.

Preface

Considering environmental stress from an evolutionary viewpoint almost naturally leads to a definition of stress as an environmental factor that impairs Darwinian fitness. Even if the occurrence of stress is only a rare event not necessarily experienced by each individual in its lifetime, or if stress can be avoided behaviourally most of the time, stressful conditions may have a huge impact on evolutionary change if stress-resistant organisms are the only survivors on these rare occasions. Environmental stress, e.g. in the form of extreme temperatures or humidity, may also set limits to species distribution and abundance and therefore have a decisive role in shaping the composition of biological communities. All organisms have apparently evolved mechanisms to cope with stress or to reduce its negative impact on fitness. For example, in response to extreme temperatures (and many other stresses), organisms express a suite of proteins called heat shock proteins or stress proteins that prevent the damaging impact of thermal stress.

We invited as authors scientists whose emphases reflect their varied approaches to the study of environmental stress - from molecules and proteins to individuals, populations and ecosystems - with the aim of ex­ploring how organisms adapt to extreme environments, how stress changes genetic structure and affects life histories, how organisms cope with ther­mal stress through acclimation, and how environmental and genetic stress induce fluctuating asymmetry, shape selection pressure and cause extinc­tion of populations. Finally, we asked the authors to discuss the role of stress in evolutionary change, from stress-induced mutations and selection to speciation and evolution at the geological timescale. The authors were asked to review their field but also to include their latest and often not yet otherwise published research and to identify lines of future research activ­ities. The book therefore contains reviews as well as novel scientific results on the subject and will be of interest to both researchers and graduate students and may also serve as a text for graduate courses. Some of the papers were presented at a symposium on stress and evolution held at the Fifth International Congress of Evolutionary Biology and Systematics, Budapest, Hungary, in August 1996. We are grateful to those who contrib­uted for sharing their goals and perspectives with us, and to the reviewers of the manuscripts for their prompt and helpful advice.

Kuke Bijlsma and Volker Loeschcke

Groningen, The Netherlands, and Aarhus, Denmark, January 1997.

Environmental Stres~ Adaptation and Evolution ed. by R. Bijlsma and V. loeschcke © 1997 Birkhauser Verlag BasellSwitzerland

Introductory remarks: Environmental stress, adaptation and evolution

Kuke Bijlsma I and Volker Loeschcke 2

1 Department of Genetics, University ofGroningen, Kerklaan 30, NL-9751 NN Haren, The Netherlands 2 Department of Ecology and Genetics, University of Aarhus, Ny Munkegade, Building 540, DK-8000 Aarhus C, Denmark

There is a growing awareness that environmental stress may play and may have played a significant role in the evolution of biological systems, from the level of the gene to that of ecosystems. Historically, environmental stress has not been considered important in the development of evolution­ary theories. Although the adaptation of an individual to its natural physi­cal and biotic environment is central to Darwin's theory of evolution as expressed in On the Origin of Species by Means of Natural Selection (1859), he thought intra- and interspecific competition to be much more significant than environmental stress. A comprehensive overview and the historical role of stress in evolutionary thinking can be found in Hoffmann and Parsons (1991). Since the 1940s, for Drosophilists starting with the publication of Timofeeff-Ressovsky (1940), there has been increasing interest in linking environmental stress with natural selection for stress resistance and adaptation. Recently, an accumulating number of data do suggest that environmental stress may have a considerable impact on the evolutionary and ecological processes that affect and shape the genetic structure and evolution of populations (Calow and Berry, 1989; Hoffmann and Parsons, 1991), and may even playa significant role in the process of speciation (Parsons, this volume; Sheldon, this volume).

Most biologists are familiar with the word "stress" , but it is used in many different ways and different contexts for several reasons. First, as pointed out by Hoffmann and Parsons (1991), two components are involved in deal­ing with stress, "the external and internal forces that are applied to orga­nisms or other biological systems, and changes in biological systems that occur as a consequence of these forces". Both are clearly interdependent, and the degree of stress caused by an environment can only be valued in relation to the organism or population experiencing this environment (see e.g. Zhivotovsky, this volume). Although the term "stress" is often used to designate either the environmental component or the biological com­ponent, from an evolutionary perspective the environmental force and the biological response should be viewed as integrative.

XIV R. BijIsma and V. Loeschcke

Second, stress is level-dependent: it can be viewed at different biological levels, e.g. at the molecular, physiological, organismal and populational level. Responses at one level do not necessarily have to become manifest at another. For examle, phenotypic plasticity may prevent biochemical changes from being revealed at the organismallevel, although this process itself may be costly and may be revealed as a change in fitness.

Third, the term "stress" is often associated with the intensity of stress. Often the environment is considered to be stressful only if the response it causes exceeds an arbitrary threshold, e.g. when more than a certain frac­tion of the population is affected. Others consider the intensity of stress to be continuous, including zero.

Given the foregoing problems, it is not surprising that many different definitions of stress have been formulated. Biological definitions, general­ly, fall into two classes. The first class of definitions considers stress in a physiological context. These definitions focus mostly on the physiological effects of stress on the individual. Selye (1973), for example, defined stress as a syndrome of physiological responses to environmental stresses that affect the well-being of individuals. In this view, these stresses are non­specific, and various stresses can cause a similar syndrome at the physio­logical level.

The second class of definitions considers stress in an evolutionary con­text. Most of these definitions focus on both environmental forces and the specific effect of stress on the biological system. For example, Sibly and Calow (1989) defined stress as "an environmental condition that, when first applied, impairs Darwinian fitness" . Koehn and Bayne (1989) defined it as "any environmental change that acts to reduce the fitness of an orga­nism". Definitions of this type and many more can be found elsewhere in this volume, and have in common that they emphasize the reduction in fitness caused by the environmental factor. As such, the organism or popu­lation may respond to stress phenotypically and/or genetically, and evolve adaptive mechanisms to overcome it. All contributors to this book, either explicitly or implicitly, consider stress in this manner, and aim to under­stand the impact of stress on biological systems from an evolutionary perspective.

The growing interest in environmental stress has been stimulated by recent developments in molecular genetics. These have not only made it possible to study stress responses in more detail, but have also revealed that most organisms have evolved sophisticated mechanisms to cope with different environmental stresses, such as heat shock proteins to counter­act thermal and other stresses, mixed function oxidases to degrade xeno­biotics, and the major histocompatibility complex to fight biotic attacks. Additionally, molecular techniques have made it possible to study re­sponses to stress at the molecular level. The finding that thermal stress induces the production of a suite of proteins (heat shock proteins) to pre­vent the damaging impact of high temperatures in most organisms, from

Introductory remarks: Environmental stress, adaptation and evolution xv

bacteria to humans, has evoked a significant increase in stress-related research.

Moreover, the impact of the human population in the last century on the biosphere at a global scale is unprecedented. This has caused and will increasingly cause major environmental changes, such as climatic shifts, chemical pollution and habitat destruction. The size and rate of these changes form an increasing threat for the existence of life on this planet. Global warming may exert thermal stress, the consequences of chemical pollution are yet incalculable and the destruction of habitats has caused an accelerating rate of species extinction. Understanding the nature and con­sequences of these stresses at a global level from an ecological and evolu­tionary perspective is of paramount importance for the development and evaluation of countermeasures.

About the book

Clearly most if not all organisms and populations have to cope with hostile environments that threaten their existence. Their ability to respond pheno­typically and genetically to these challenges and to evolve adaptive mecha­nisms is, therefore, crucial. In this book we focus on understanding, from an evolutionary perspective, the impact of stress on biological systems.

The first part of the book is concerned with the adaptation of species to extreme stresses in their "natural" environment. Macnair reviews the cur­rent information on adaptation to metal-contaminated soils, and discusses both the genetic and physiological mechanisms involved. Interestingly, he shows that only those species that have tolerance genes present in low fre­quencies in normal populations prior to the selective agent being imposed seem to be able to evolve metal tolerance. Forbes and Calow focus on stress associated with exposure to chemical pollutants of marine and freshwater aquatic systems. They emphasize that the study of the response of biologi­cal systems to novel pollutants can provide significant information for addressing fundamental ecological and evolutionary issues, but, converse­ly, that ecological and evolutionary understanding is crucial for effective development of ecological tests and risk assessment models. Savolainen and Hurme discuss the genetic and evolutionary aspects of adaptation of conifers to the harsh environmental conditions of the northern boreal en­vironments of Finland that are characterized by severe cold stress and a short growing season.

The second part of the book is concerned with the effect of stress on the structure and maintenance of genetic variation. Brakefield describes the striking seasonal polyphenism of the African butterfly Bicyclus anynana that reflects alternative evolutionary responses to alternating seasons, one of which is favorable, the other a stress environment. Evolution of pheno­typic plasticity, mediated by hormonal mechanisms, has lead to genetic and

XVI R. Bijlsma and V. Loeschcke

physiological coupling of fundamental life history traits and plasticity in wing pattern. Jenkins et al. study the effect of environmental extremes on the expression of genetic variation of life history and other relevant traits in Drosophila. Their results, among others, suggest that under extreme con­ditions the pattern of genetic variation may be much more complex than under constant laboratory conditions, and that extreme conditions may markedly affect the heritability of important life history traits. Van Delden and Kamping discuss the role of environmental stress, such as toxic con­centrations of ethanol and high temperature, for explaining the worldwide latitudinal cline observed for polymorphism at the Adh locus in Drosophila melanogaster. They also discuss the mechanisms by which the poly­morphism and the cline are maintained. Clark studies the effect of various stresses on a set of metabolic characters in genetically defined lines of D. melanogaster, and describes the observed magnitude of environmental effects and genotye x environment interactions.

The third part of the book focuses on the evolutionary response to ther­mal stress and the role of acclimation, a special case of phenotypic plasti­city. Bennett and Lenski report the evolutionary adaptation of Escherichia coli to thermal stress during thousands of generations. Their results show that fitness significantly increased in adapted populations compared with the ancestral clone, but that this improvement was achieved by several distinct pathways for the different replicates. Contrary to expectations, adaptation did not result in a change in the thermal niche, and acclimation to heat stress seemed not to increase, but rather to decrease, fitness. Feder and Krebs present a combined molecular and evolutionary approach to study the adaptive significance of acclimation and the concurrent produc­tion of heat shock proteins (Hsps) for the hsp70 gene in Drosophila. Their results suggest that increasing the number of copies of this gene results in elevated levels of heat shock proteins after acclimation, and consequently in increased thermotolerance. Loeschcke et al. review the evolution of thermal resistance in Drosophila and discuss the contribution of acclima­tion and heat shock proteins to this process. Their experimental results suggest that several other mechanisms may also playa significant role in the evolution of stress tolerance.

The fourth part of the book focuses on the importance of the level and structure of genetic variation within populations for adaptation to changing environmental conditions and their impact on population extinction. Fur­thermore, the role of different models of selection in the process of adapta­tion is discussed. Bijlsma et al. study the consequences of genetic stress, i.e. loss of fitness due to an increase in homozygosity caused by genetic drift and/or inbreeding, for the fitness and persistence of small D. melano­gaster populations under both optimal and stressful conditions. Their results suggest that genetic stress and environmental stress both increase the extinction risk of small populations and, more important, that both stresses are not independent but can act synergistically. Burger and Lynch

Introductory remarks: Environmental stress, adaptation and evolution XVII

review theoretical models concerning the vulnerability of small popula­tions to demographic stochasticity and directional changes in the environ­ment, and study the effect of mutation and genetic variability for the per­sistence of populations in relation to the rate of environmental change. Zhivotovsky studies theoretically the evolution of the level of stress ex­perienced by a population evolved in a homogeneous "home" environment, when it is exposed to a "foreign" environment, and he analyses the factors involved in this process. One of the interesting results of his model is the observation that a population will not adapt to a foreign environment when the frequency of occurrence of this environment is rare. Meller discusses how sexual selection may give rise to an increase in the general stress levels experienced by individuals of both animal and plant species, and the role of secondary characters and developmental stability in this process. Both Meller and Brakefield discuss the possible importance of fluctuating asymmetry for assessing the level of stress experienced by individuals or populations.

The final part of the book is concerned with the role of environmental stress in the process of speciation and evolution. Taddei et al. present evidence from bacterial systems that stress can induce greatly elevated mutation rates by activating a mutagenic response and by inhibiting anti­mutagenic mechanisms like the mismatch repair system. They argue that such stress-induced mutations not only accelerate the adaptation process but also may lead to a burst in speciation. Parsons argues that organisms have to cope with abiotic stresses far more than with biotic variables, and discusses the role of abiotic stresses in shaping species life histories and in speciation. Sheldon discusses the finding that morphological stasis seems to be the usual response to widely fluctuating physical stresses over a geo­logical time scale. His explanation of this observation is that fluctuating environments could have given rise to generalist species that could survive these fluctuations for millions of years. On the other hand, more stable environments may be characterized by specialization and gradualistic evolution.

References

Calow, P. and Berry, R.J. (1989) Evolution, Ecology and Environmental Stress. Academic Press, London.

Darwin, C. (1859) On the Origin of Species by Means of Natural Selection. Murray, London. Hoffmann, A.A. and Parsons, P.A. (1991) Evolutionary Genetics and Environmental Stress.

Oxford University Press, Oxford. Koehn, R.K. and Bayne, B.L. (1989) Towards a physiological and genetical understanding of

the energetics of the stress response. Bioi. J. Linn. Soc. 37: 157 -171. Selye, H. (1973) The evolution of the stress concept. Amer. Scientist 61 :629-699. Sibly R.M. and Calow, P. (1989) A life cycle theory of response to stress. BioI. J. Linn. Soc.

37: 101-116. Timofeeff-Ressovsky, N.W. (1940) Mutations and geographical variation. In: J. Huxley (ed.):

The New Systematics. Clarendon Press, Oxford, pp. 73 -136.