Oxidative Stress and Hormesis in Evolutionary Ecology and Physiology: A Marriage Between Mechanistic and Evolutionary Approaches

359 Pages·2014·6.92 MB·English

by  David Costantini (auth.)

David Costantini
Oxidative Stress
and Hormesis
in Evolutionary
Ecology and
Physiology
A Marriage Between Mechanistic and
Evolutionary Approaches
Oxidative Stress and Hormesis in Evolutionary
Ecology and Physiology
David Costantini
Oxidative Stress and
Hormesis in Evolutionary
Ecology and Physiology
A Marriage Between Mechanistic
and Evolutionary Approaches
123
David Costantini
Department of Biology
Universityof Antwerp
Wilrijk
Belgium
and
InstituteforBiodiversity, AnimalHealth
andComparative Medicine
Universityof Glasgow
Glasgow
UK
ISBN 978-3-642-54662-4 ISBN 978-3-642-54663-1 (eBook)
DOI 10.1007/978-3-642-54663-1
Springer Heidelberg NewYork Dordrecht London
LibraryofCongressControlNumber:2014934114
(cid:2)Springer-VerlagBerlinHeidelberg2014
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To my mother
Preface
Research programmes on oxidative stress and hormesis are wide ranging. Bio-
medicalandtoxicologicalscienceshavetraditionallycentralisedsuchresearch,but
in the last years we have seen the merger of laboratory-based biochemical and
physiologicalapproachestothestudyofoxidativestressandhormeticmechanisms
withethological,ecologicalandevolutionaryprinciples.Althoughresearchinthis
area is still in its infancy, many new fields of research are emerging from the
marriagebetweenthesemechanisticandfunctionalperspectives.Whatiscritically
lackingyetisasynthesisgearedtowardsevolutionaryecologists,ecophysiologists
and behavioural ecologists that seeks to consolidate a vast body of literature
whilst,atthesametime,remainssensitivetoreaderswhomaynothavethedepth
of knowledge often necessary to navigate new fields of scientific enquiry. This
book seeks to fill in this gap. Its goal is to synthesise and integrate research on
oxidativestressandhormesis,butasseenfromtheperspectiveofanevolutionary
ecologistorphysiologist.Workinthisareacanopennewfrontiersforresearchto
further our understanding on how and why biological diversity has evolved. This
book does not have, however, the presumption to claim that oxidative stress or
hormesis are vital, nor does it wish to fully describe biochemical mechanisms.
Ratheritwishestoemphasisethatoxidativestressandhormesisaremissingpieces
ofacomplexbiologicalpuzzle.Focussingonthesemissingpiecesandintegrating
them with other biological features can provide fascinating insights into how
organisms work, how they evolve to sustain physiological function under a vast
array of environmental conditions and why they work the way they do.
The book is organised into ten chapters. Chapter 1 provides general historical
information, definitions and background of research on oxidative stress physiol-
ogy, hormesis and life history; Chaps. 2–10 analyse how oxidative stress and
hormesis have influenced many aspects of life, from the incipient stages of
development to the strategies of reproduction and the ways organisms age. While
everychapterdealswithaspecifictopic,itshouldnotbeforgottenthattheyareall
related to each other. For example, when interpreting the effect of reproductive
effortonoxidativedamage,itisalsoimportanttoconsiderthatsucheffectwillbe
possibly dependent on other aspects, like early life experiences, predation risk, or
food quality and quantity. Moreover, the physiological machinery in turn may
influence the way a specific factor impacts on the individual. For example, over
evolutionary time, diet has been likely adjusted to the physiological needs of an
vii
viii Preface
individualorspecies,whileatthesametimethephysiologicalstrategieshavebeen
adjusted to make use of what is present in the diet itself. We clearly need to
integrateallthisinformationinordertofurtherourunderstandingofhowvariation
in physiological systems and life history strategies comes out. In this regard, the
term adaptation has been used in a general way throughout the book, including
both real adaptations and exaptations. For a character to be regarded as an
adaptation, it must be a derived character that evolved in response to a specific
selective agent. The emergence of an antioxidant mechanism could have been
maintained, for example, by natural selection because it confers current selective
advantage, but this is not evidence of why it has been evolved. This means that
protection against oxidative stress may not be the primary reason for why all
antioxidantmechanismshavebeenevolved,butevolutionofacertainantioxidant
mechanism could have provided secondarily a selective advantage.
Opportunities for studying truly natural processes are diminishing because
pristine or near-pristine environments are rapidly shrinking and becoming more
difficulttoreach.Thisshouldremindusthatweneedtoknowmoreabouthowthe
changing and emerging environments are influencing natural animal populations.
The many examples reported throughout the book will actually show how oxi-
dative stress and hormesis can represent two important links between environ-
mental changes and evolutionary fitness, hence they can represent two relevant
tools of investigation for conservation biologists, as well.
The book is not exhaustive, hence many relevant studies have not been
included. The book has also never taken into consideration discussion of meth-
odological approaches to quantify reactive species production, antioxidants or
damage levels. Obviously, methods for the quantification of components of the
redox machinery have to satisfy specific technical criteria. We have to recognise,
however, that each method has limits; hence using a combination of more oxi-
dativestatusparametersisessential.Itisalsocrucialthatthebiochemistryofwhat
is being measured is taken into consideration when interpreting experimental
results.Wehavenottolosesightofthefactthattherearealsospecificrestrictions
inherenttomanyecologicalresearchprogrammes,suchastheavailabilityofonly
small amounts of blood and the requirement of non-terminal sampling.
The biological meaning of many mechanisms or molecules that are currently
measured to quantify damage or antioxidant defences is often hard to gauge,
because most in-depth information about the physiological functions of many of
them come from studies on a limited number of taxa. We also do not know in
many cases what differences in oxidative stress mean; this is because we still do
not know whether the impact on evolutionary fitness differs among oxidative
damage parameters. Consequently, any generalisations and extrapolations about
function should be made with considerable caution. Focusing too much on the
limited array of model organisms generally used, and on highly conserved path-
ways, narrows our understanding of what works under what circumstances. We
needtoappreciatethatevolutionhaslikelymodifiedorchangedthebasicdefence
toolkitandthatunderstandinghowdifferentorganismshavesolvedthechallenges
posed by their environments and lifestyles is interesting and important.
Preface ix
The complexity and diversity of the natural world is a powerful experimental
resourcethatisoftenforgottenbymanyscientificdisciplines.Appreciatingsucha
complexity will be instructive and will offer us new opportunities for exploring
new frontiers of biological research.
David Costantini
Acknowledgments
Above all I want to thank very much indeed Nadia Macciocchi, Fernando and
SerenaCostantini,LiviaandFernandoCarello,whosupportedandencouragedme.
I would like to thank very much Gianfranco Brambilla, Claudio Carere, Mauro
Carratelli,GiacomoDell’Omo,AlbertoFanfani,NeilMetcalfeandPatMonaghan
for valuable advice and support over my career. I also thank very much the
following colleagues for providing material or comments that helped me to
improve the quality of the book: Doris Abele, Carlos Alonso-Alvarez, John
Armstrong, Michaël Beaulieu, Emiliano Bruner, David Bruno, Claudio Carere,
Caterina Ferrari, Christopher Guglielmo, Fabrice Helfenstein, Mia Hoogenboom,
Valeria Marasco, Scott McWilliams, Anders Pape Møller, Etsuo Niki, Michalis
Nikolaidis, Kristin M. O’Brien, Rolf Peterson, Maria Savini, Shona Smith,
Gabriele Sorci, Carl Soulsbury and John Speakman. Finally I thank for financial
supportofmyresearchtheNaturalEnvironmentResearchCouncil(NERC)ofthe
UnitedKingdom,theResearchFoundationofFlanders(FWO),theSwissNational
Science Foundation and the Italian association Ornis italica.
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Contents
1 Historical and Contemporary Issues of Oxidative Stress,
Hormesis and Life-History Evolution . . . . . . . . . . . . . . . . . . . . . 1
1.1 The Great Oxidation Event: From a Reducing
to an Oxidising World. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1.2 Reactive Species, Antioxidants and Oxidative Stress. . . . . . . . 2
1.2.1 On the Nature of Free Radicals and Other
Reactive Species . . . . . . . . . . . . . . . . . . . . . . . . . . 2
1.2.2 Antioxidant Mechanisms. . . . . . . . . . . . . . . . . . . . . 5
1.2.3 Oxidative Stress. . . . . . . . . . . . . . . . . . . . . . . . . . . 13
1.2.4 Biochemical Integration and Modularity
of Redox Systems. . . . . . . . . . . . . . . . . . . . . . . . . . 16
1.3 Hormesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
1.3.1 Historical Scenario: Birth, Death and Resurgence
of Hormesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
1.3.2 Types of Hormesis . . . . . . . . . . . . . . . . . . . . . . . . . 21
1.3.3 Quantitative Features of Hormesis and Problems
with Its Detection. . . . . . . . . . . . . . . . . . . . . . . . . . 24
1.3.4 Hormesis and Evolutionary Fitness. . . . . . . . . . . . . . 26
1.4 Life-History Evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30
2 Early-Life Hormesis and Oxidative Experiences Fine-Tune
the Adult Phenotype. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39
2.1 Early Environment and Phenotypic Development. . . . . . . . . . 39
2.2 Pre-natal Maternal Effects: How Mothers Use Hormones
to Shape Their Offspring. . . . . . . . . . . . . . . . . . . . . . . . . . . 41
2.2.1 Effects of Maternal Androgens:
Examples from Birds . . . . . . . . . . . . . . . . . . . . . . . 42
2.2.2 Stress Hormones and the Developmental
Programming Hypothesis. . . . . . . . . . . . . . . . . . . . . 44
2.3 Epigenetic and Transgenerational Hormetic Effects . . . . . . . . 49
xiii