Thermal Adaptation: A Theoretical and Empirical Synthesis

304 Pages·2009·6.21 MB·English

by  Michael J. Angilletta Jr.

ThermalAdaptation
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Thermal Adaptation
A Theoretical and
Empirical Synthesis
MichaelJ.AngillettaJr.
1
3
GreatClarendonStreet,Oxfordox26dp
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ISBN 978–0–19–857087–5 978–0–19–857088–2
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ToAmy, Taylor, and Kyle,
for your exceeding tolerance of my wild ideas.
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Preface
ThefirstbookthatIreadasagraduatestudentwas from the paucity of quantitative models of ther-
Foraging Theory (Stephens, D. W., and J. R. Krebs. maladaptation.Thermalbiologistshavedescribed
1986, Foraging Theory. Princeton, Princeton Uni- patterns and documented effects to the point that
versityPress).Atthetime,Iwasplanningtostudy empirical knowledge has far outstripped theoreti-
the evolution of foraging behavior in snakes, and calunderstanding.Mostpapersinthermalbiology
thus wanted to acquire a conceptual background focus on empirical descriptions or rely on verbal
for this work. As fate would have it, my subse- arguments about adaptation. In comparison, con-
quentresearchdidnotfocusonforagingbehavior siderthedisciplineofforagingbiologythatIreferred
(orsnakes),butthebookmadealastingimpression toabove;hereinliesatroveofquantitativemodels
on me anyway. The authors laid out a compre- andexperimentaltestsaboutevolutionaryhypothe-
hensiveandinsightfultheory,movingfromsimple ses.Thebasicideasabouttheevolutionofforaging
modelstocomplexones,whiledrawingonrelevant behavior were formulated in the 1960s and have
empirical data. The book culminated in a rigor- been gradually developed to the point that the
ousappraisalofthefield’saccomplishments,driven evolutionary impacts of many factors—from con-
by the match between theoretical predictions and straints on digestion to risks of predation—have
empiricalobservations. HadIpursuedmyinterest beenexploredingreatdetail.Fewevolutionarypro-
in foraging biology, the book would surely have cessesinthermalbiologyhavebeenmodeledtothe
become my academic bible. Instead, I soon devel- samedegree, andnomajorsynthesisofevolution-
oped a greater interest in thermal biology, only to arythermalbiologyhasemerged.Myaimisnotto
discoverthatnoanalogousresourceexistedforthis castblame(forIwouldcertainlyshareinthisblame).
discipline. Rather,Iwanttoseethermalbiologykeeppacewith
Idon’twanttogiveyoutheimpressionthatlittle otherbiologicaldisciplines.Andtodoso,wemust
wasknownaboutthermalbiologyorthatnoonehad developaquantitativetheoryofthermaladaptation.
attemptedaconceptualsynthesis. Neitherimpres- Uponcloserinspection,awealthofevolutionary
sionwouldbeaccurate. Inmanyrespects, thermal modelsliewaitingforthermalbiologiststoadoptas
biology has progressed tremendously, as one can theirown.BeginningwithLevins(Levins,R.1968,
conclude from reading an early synthesis of this EvolutioninChangingEnvironments: SomeTheo-
topic(seeCossins,A.R.,andK.B.Bowler.1987,Tem- reticalExplorations.Princeton,PrincetonUniversity
peratureBiologyofAnimals.NewYork,Chapman Press), biologists have been modeling the evolu-
and Hall). In other respects, though, thermal biol- tionofquantitativetraitsinvariableenvironments
ogy continues to lag behind other disciplines. Let for more than four decades. With the growth of
me explain. When it comes to documenting pat- thistheory,anincreasingemphasishasbeenplaced
terns,fewdisciplineshavemademoreprogressthan on genetic, developmental, and ecological issues.
thermal biology. But if we judge progress by our Manyofthemodelscanbeappliedtounderstand
understandingoftheprocessesthatgeneratethese aspects of thermal adaptation. Although some of
patterns, then we have much progress to make. these models are mathematically intense, I have
While proximate explanations abound, ultimate distilled from them the essence of what they tell
explanations remain scarce. This problem stems us about adaptation to temperature. For thermal
vii
viii PREFACE
biologists,thisbookcontainsasynthesisoftheory BrandonCooper,LisaCrozier,MarcinCzarnołeski,
that should guide research in the coming decade. WilfriedGabriel,GeorgeGilchrist,LumírGvoždík,
For evolutionary biologists, the book contains an Gabor Herczeg, Luke Hoekstra, Ray Huey, Jose
evaluationofcurrentmodelsofevolutioninvariable Martín, Bill Mitchell, Mike Sears, Ben Williams,
environments. andRobbieWilson.Theirsuggestionsandinsights
Throughout the book, you may notice a taxo- contributed greatly to the final product. Other
nomicbias.Thisbiasstemsfromtwofactors.First, colleagues provided original images or permis-
intentionalbiasresultedfrommyconceptualfocus. sion to adapt figures: Martin Ackermann, Steve
Thebookrevolvesaroundtheconceptofathermal Beaupre, Gabriel Blouin-Demers, Lauren Buckley,
performance curve, which describes the relation- AndyClarke,LisaCrozier,MichaelDillon,Wilfried
ship between body temperature and organismal Gabriel, Ted Garland, George Gilchrist, Bruce
performance. Most of the book draws on studies Grant,BrianHelmuth,RayHuey,JacobJohansson,
of ectotherms because we can measure their per- Joel Kingsolver, Mark Kirkpatrick, Michael Kopp,
formancecurvesmorereadilythanwecanmeasure Sue Mitchell, Carlos Navas, Mark New, Camille
those of endotherms. Students of endotherms will Parmesan, Steve Piper, Mike Sears, Tim Shreeve,
findthemostrelevanttheoreticalandempiricalcon- Gian-RetoWalther,andKazunoriYamahira.Finally,
tentinChapter4,butotherchapterscontainrelevant the preparation of this book was greatly acceler-
theory.Second,somebiasinevitablyresultsfromthe ated by the help of Angela Borchelt and Phaedra
lackofsuitabledataforcertaintaxa.Ineachchapter, Seraphimidi, who obtained copyright permissions
I focused on the data most relevant to the theory. forthefiguresadaptedfromothersources.
Consequently,certainchaptersarerichwithexam- An undertaking of this magnitude requires the
plesinvolvinganimals,plants,ormicrobes,butno supportandencouragementofmanypeople. Iam
chapter contains an even coverage of all of these greatlyindebtedtomycolleaguesatIndianaState
groups.Ihopethistaxonomicbiasreflectsmyeffort University,whopickeduptheslackformeduring
to evaluate the theory more than my ignorance of mysabbatical.Thechairofmydepartment,Charles
the literature (although the latter seems inevitable Amlaner,keptmyteachingloadincheckduringthe
giventheexponentialgrowthofknowledge). remainderofmywriting.TheLillyFoundationand
Aboveall,Itriedtoproducethekindofsynthesis theOfficeoftheProvostatIndianaStateUniversity
that I had longed for when I was a graduate stu- providedfinancialsupport. Ioweanequaldebtto
dent. If I succeeded in this effort, my success was the students who kept my lab productive despite
due partly to the biologists who mentored me in myreallocationofenergyfromresearchtowriting:
myformativeyears:JustinCongdon,ArtDunham, DeeAsbury,BrandonCooper,JoeEhrenberger,Matt
Henry John-Alder, and Peter Petraitis. My views Schuler, Somayeh Semati, Melissa Storm, and Ben
were also shaped by discussions or collaborations Williams. Most of all, I thank my family—Amy,
with George Bakken, Lauren Buckley, Ray Huey, Taylor, and Kyle. They kindly endured my crazy
Rob James, Joel Kingsolver, Bill Mitchell, Carlos workscheduleandmyoccasionalstressresponses.
Navas, Amanda Niehaus, Peter Niewiarowski, Iwouldnothavecompletedthisbookwithouttheir
Warren Porter, Leslie Rissler, Mike Sears, Frank patienceandunderstanding.
Seebacher, and Robbie Wilson. Many colleagues
were kind enough to comment on sections of the MichaelJ.AngillettaJr.
book or provide information about their research: May24,2008
David Atkinson, George Bakken, Lauren Buckley, TerreHaute,Indiana,USA
Contents
Preface vii
1 EvolutionaryThermalBiology 1
1.1 Thechallengeofevolutionarythermalbiology 1
1.2 Thermalreactionnorms 3
1.3 Theroleoftheory 5
1.4 Theoreticalapproachestoevolutionarythermalbiology 6
1.4.1 Optimalitymodels 6
1.4.2 Quantitativegeneticmodels 8
1.4.3 Allelicmodels 10
1.4.4 Thecomplementarityoftheory 13
1.5 Empiricaltoolsoftheevolutionarythermalbiologist 13
1.5.1 Quantifyingselection 14
1.5.2 Experimentalevolution 14
1.5.3 Comparativeanalysis 15
1.6 Conclusions 18
2 ThermalHeterogeneity 19
2.1 Operativeenvironmentaltemperature 20
2.2 Globalpatternsofoperativetemperature 23
2.2.1 Latitudinalclines 23
2.2.2 Altitudinalclines 27
2.3 Quantifyinglocalvariationinoperativetemperatures 29
2.3.1 Mathematicalmodels 29
2.3.2 Physicalmodels 31
2.3.3 Statisticalmodels 32
2.4 Conclusions 33
3 ThermalSensitivity 35
3.1 Patternsofthermalsensitivity 35
3.2 Proximatemechanismsandtradeoffs 40
3.2.1 Thermaleffectsonenzymes(andotherproteins) 41
3.2.2 Membranestructure 43
3.2.3 Oxygenlimitation 44
3.2.4 Conclusionsfromconsideringproximatemechanisms 45
3.3 Optimalperformancecurves 47
3.3.1 Optimalperformancecurves:survivorshipandrelatedperformances 47
3.3.2 Optimalperformancecurves:fecundityandrelatedperformances 51
3.3.3 Contrastingthetwomodels 53
ix