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Senescence in natural populations of animals: Widespread evidence and its implications for bio-gerontology

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Senescence in natural populations of animals: Widespread evidence and its implications for bio-gerontology
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  AgeingResearchReviews 12 (2013) 214–225 ContentslistsavailableatSciVerseScienceDirect AgeingResearch   Reviews  journalhomepage:www.elsevier.com/locate/arr Review Senescence   in   natural   populations   of    animals:   Widespread   evidence   and   itsimplications   for   bio-gerontology Daniel   H.Nussey a , b , ∗ ,Hannah   Froy a ,    Jean-Franc¸    ois   Lemaitre c ,    Jean-Michel   Gaillard c ,SteveN.Austad d a InstituteofEvolutionaryBiology,SchoolofBiologicalSciences,UniversityofEdinburgh,Edinburgh,UK  b CentreforImmunity,Infection&Evolution,Schoolof    BiologicalSciences,Universityof    Edinburgh,Edinburgh,UK  c UnitéMixtedeRecherche5558‘BiométrieetBiologieÉvolutive’,UniversitéClaudeBernardLyonI,43boul.du11Novembre1918,69622VilleurbanneCedex,France d UniversityofTexasHealthScienceCenterSanAntonio,BarshopInstituteforLongevityandAgingStudies,DepartmentofCellular&StructuralBiology,SanAntonio,USA a   rti   c   l   ei   nf   o  Articlehistory: Received15May   2012Receivedinrevisedform24July2012Accepted30July2012 Available online xxx Keywords: AntagonisticpleiotropyDisposablesomaEcologyEvolutionFree-livingpopulationsWildanimals ab   s   t   ra   ct Thatsenescence   israrely,if    ever,   observed   innatural   populations   is   an   oft-quoted   fallacywithin   bio-gerontology.   Weidentify   the   roots   ofthisfallacyinthe   otherwise   seminalworks   of    Medawar   and   Comfort,andexplainthat   under   antagonistic   pleiotropy   or   disposable   soma   explanations   for   the   evolution   of senescence   thereisnoreasonwhysenescence   cannot   evolve   tobe   manifest   within   the   life   expectanciesof    wild   organisms.   The   recent   emergenceof    long-termfieldstudies   presents   irrefutable   evidencethatsenescenceis   commonly   detected   innature.   We   found   such   evidencein175   differentanimal   species   from340separate   studies.Although   the   bulkof    thisevidence   comesfrom   birds   and   mammals,   wealso   foundevidencefor   senescence   inother   vertebrates   and   insects.Wedescribe   howhigh-qualitylongitudinalfielddata   allow   us   totestevolutionary   explanations   fordifferences   insenescence   betweenthe   sexes   andamong   traits   and   individuals.   Recentstudies   indicate   that   genes,   prior   environmentand   investment   ingrowth   and   reproduction   influence   aging   rates   inthe   wild.   Weargue   that–with   the   fallacythat   wildanimals   do   not   senesce   finallydeadandburied   –collaborations   betweenbio-gerontologists   andfieldbiologists   can   begin   totestthe   ecological   generality   of    purportedly   ‘public’mechanisms   regulating   aginginlaboratory   models. © 2012 Elsevier B.V. All rights reserved. 1.Introduction:Wildanimalsfailtosenesce– abrief historyofthefallacy  1.1.Medawarandtheoriginsofthefallacy Thenotionthatanimalsinnaturedonotsenesce–thatenvi-ronmentalchallengeswhethertheybepredators,floods,famineorsomethingelsekillallwildanimalsbeforeagingcantakeameasur-abletoll–canbetracedatleastasfarbackasPeterMedawar’sfirstfulltheoreticaltreatmentof    theevolutionof    senescence(Medawar,1952).Thisideais   clearlyfallaciousaswewillshow,undercutbybothsubsequenttheoreticalworkandcopiousempiricaldatafromawiderangeofanimals,yetitwascrucialtothedevelopmentofMedawar’scentralhypothesisaboutthegeneticmechanismbywhichsenescencecouldevolve.Medawar’sparadigm-shiftingcontributionto   theevolutionaryunderstandingofagingwashisinsightthatduetotheinevitabil-ityofdeathfromenvironmentallydrivencauses,theabilityof  ∗ Correspondingauthorat:Instituteof    EvolutionaryBiology,Schoolof    BiologicalSciences,UniversityofEdinburgh,AshworthLaboratories,KingsBuildings,WestMainsRoad,EdinburghEH93JT,UK.Tel.:+440   1316505494;fax:+440   1316506564. E-mailaddress: dan.nussey@ed.ac.uk (D.H.Nussey). naturalselectiontofavourordisfavourgenetically-basedtraitsdependedontheageatwhichthosetraitsappeared.Ashe   phrasedit,“theforceof    naturalselectionweakenswithincreasingage”.Thisspecificinsightformsthebasisofallsubsequentanalysesof theevolutionof    senescence.Basedonthisidea,Medawarpro-poseda   particulargeneticmechanism–thatsenescenceevolvesbytheaccumulationinthegenomeof    harmfulalleles,suchasthosepredisposingtocancer,dementia,orheartdisease,whoseeffectsappearsufficientlylateinlifethat“theforceofnaturalselectionwillbetooattenuatedto   opposetheirestablishmentandspread.”Inotherwords,suchdeleteriousallelescouldspreadonlywhentheprobabilitythattheycouldhaveameasurableeffectonreproductivesuccesswas   verylow.Consequentlyobservablesenescenceshouldonlyoccuratages“whichthegreatmajorityofthepopulationdonot   reach”(allquotesfromMedawar,1952).Onlyunderconditionsinwhichanimalsare   protectedfromnatu-ralhazards,hetheorized,suchthat   theycommonlysurvivetoagestheywouldveryseldomorneverachieveinthewild,wouldsenes-cencebemanifest.Hewas   quitespecificaboutthislatterpoint,repeatingitfourtimesinthesamemonograph.Tociteoneof these,“Whetheranimals can ,   orcannot,revealaninnatedeteriorationisalmostliterallya   domesticproblem;the  fact  isthatunderthe 1568-1637/$–seefrontmatter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.arr.2012.07.004  D.H.Nusseyetal./AgeingResearchReviews 12 (2013) 214–225 215 exactionsofnaturallifetheydo   notdo   so.Theysimplydonotlivethatlong.”–Medawar,1952(italicsinoriginal)As   evidenceforthisclaim,Medawarcitesa   personalcommuni-cationfromfieldmammalogistDennisChitty,in   whichChittystatesthat“wildmammalsof    anyperceptibledegreeof    senility”seldomturnedupinhistraps,andiftheydidheassumedthatsomecauseotherthansenescence(e.g.infection,injury)was   responsiblefortheircondition(Medawar,1952).Forwildbirds,Medawar’ssourcewasDavidLack,thepioneeringfieldornithologist.Lackhadnotedinseveralpapersin   the1940’s,thattheprobabilityofdeathseemedtobeindependentofageinbirdsinnature,implyingthat   senes-cence,atleastin   itsactuarialsense,did   notoccur(Lack,1943a,b).Medawar’sclaimwasrepeatedinthefirstcomprehensiveconsid-erationofsenescenceasa   generalbiologicalphenomenon–AlexComfort’sclassictome, TheBiologyofSenescence (Comfort,1956).Sincethen,theideathat   senescencefailsto   occurin   naturehasbeenoftenrepeatedwithinbio-gerontology(e.g.Hayflick,2000;KirkwoodandAustad,2000;Rose,1991).InMedawarandComfort’stimetherewasinfactscantevidenceforsenescenceinthewildbecausefewdetailedlong-termstudiesofnaturalpopulationsexisted.Thosethatwereavailabletendedtobeshort-term,cross-sectionalandoftendidnot   knowtheexactageof    adultsinthepopulation.Ithassincebecomeapparentthatlong-termstudiesthatmonitormarkedindividualsfrombirthtodeatharerequiredtoreliablydetectandinvestigatesenescenceinthewild.Inanearliermonographonaginganddeathpublishedin   1946,Medawarseemstoacknowledgethis,highlightingtheimportanceof    studiesofexactlythiskind:“No-onehasyetmadeasystematicstudyofwhetherevenmam-mals intheirnaturalhabitat  doindeedlivelongenoughto   reachamoderatethoughcertifiabledegreeofsenility .   .. Thedifficultiesofconstructinglifetablesin   thewildaretechnicallyformidable,buttheymustbesolved.”– Medawar,1946(italicsinoriginal)As   wewilldemonstrate,despiteMedawarandComfort’ssubse-quentassertionsto   thecontrary,therewasneveranytheoreticalreasontoadducetheabsenceof    senescencein   thewild(Williams,1957),andtherehasbeenanavalancheof    recentdatafromwildpopulationsclearlydemonstratingthesenescencedoesindeedoccurcommonlyin   naturalpopulations(BennettandOwens,2002;Brunet-RossinniandAustad,2006;Nusseyetal.,2008a). 1.2.Unravellingthefallacy Quiteprobably,Medawar’sbeliefthatanimalsin   naturefailedtosenesceallowedhimtodismissoneclearimplicationofhisinsight.Whilsthefocusednearlyexclusivelyontheaccumulationof    late-actingdeleteriousalleles,hementionedinpassing–evengivinganexample–thatbecauseofthegradualweakeningstrengthof    nat-uralselectionwithage,“arelativesmalladvantageconferredearly[inlife] ... may   outweigha   catastrophicdisadvantagewithhelduntillater”(Medawar,1952).This,of    course,isasuccinctdescriptionof anideaGeorgeWilliamslaterdeveloped:antagonisticpleiotropy,inwhichalleleswithbeneficialeffectsonsurvivalor   reproductionearlyinlifecanbeactivelyfavouredbynaturalselectiondespitenegativeeffectsonhealthandfitnesslaterinlife(Williams,1957). SoalthoughMedawardescribedantagonisticpleiotropy,hefailedtoappreciateitssignificance.In   summarizingtheimplicationsofhistheoryattheendofhis   1952paper,henevermentionedit,focusinginsteadontheaccumulationof    late-actingallelesandonhypothet-icalmodifierallelesthatmightpostponetheeffectsof    deleteriousallelestoagesatwhichtheywouldbeeffectivelyneutral(Medawar,1952).However,ifantagonisticpleiotropyis   a   commonmechanismofsenescence,thenthereis   nonecessaryexpectationthatwildanimalswillfailtodisplayprogressivedeteriorationof    healthinlaterlifeor   that   suchdeteriorationneedbesubtle.Williams’clearlyappreciatedthis,referringtoComfort’sargumentthatsenescencewas‘outsidethedevelopmentalprogramthatconcernsnaturalselection’,asfollows:“I   believethatthistheoryis   incorrect.Itsfallacyliesinthecon-fusionof    theprocessof    senescencewiththestateof    senility,andinaninaccurateconceptionof    therelationshipofagetoselectionprocesses.”– Williams,1957Bywayof    example,Williamsnotedthatanexaminationofath-leticrecordsreveals‘rampant’senescenceinhumansasearlyastheir30’s,aperiodwhichno-onecoulddisagreehumanscom-monlyreachedevenin   a   stateofnature(Williams,1957).Williams highlightedtwo   crucialpointsthatalterthewaywe   thinkaboutsenescenceinnaturalpopulations.First,inanevolutionarysense,senescenceis   theprogressivephysiologicalprocessofdeteriorationleadingtoa   declineinfitnesswithage,whichisnotsynony-mouswithinfirmityandfrailtyassociatedwithextremeoldagein   humansandcaptiveanimals.Classicalevolutionarytheorydoesnotrefertoor   considera   stateof    senilityinverylateadulthood,ratheritpredictsthatsenescenceshouldbeginattheageof    sex-ual   maturityandprogressfromthatpointastheforceof    naturalselectionweakens(Hamilton,1966;Williams,1957).Second,under antagonisticpleiotropy,naturalselectionisexpectedtofavourtheevolutionof    lifehistoriesinwhichsenescencehasadetectablefit-nesscostwithinthenaturallifeexpectanciesof    organisms,aslongasthegenesassociatedwiththisdeteriorationconfera   sufficientfitnessbenefitin   earlierlife.Kirkwood’s(1977)disposablesomatheoryofsenescenceis   alsocompatiblewiththemanifestationof    senescenceinthewild.Devel-opedfromadifferenttheoreticalframework–optimizationtheoryasopposedtopopulationgeneticstheory–thedisposablesomatheorymakeslargelysimilarpredictionsto   antagonisticpleiotropy.Briefly,ithypothesizesthatbecausecriticalresourcessuchasenergyarelimited,naturalselectionwilladjusttheallocationof cellularandphysiologicalresourcesbetweenthefundamentalpro-cessesof    somaticmaintenanceandreproductionappropriatelyforanorganism’secologicalcontext(Kirkwood,1977;KirkwoodandRose,1991).Sincenaturalselectionisexpectedtoweakenwithage,selectionwilltendtofavourinvestmentin   earlyreproductionoverlong-termsomaticmaintenance,andsenescencewillresult(KirkwoodandRose,1991).Antagonisticpleiotropyanddisposable somatheories,oftenreferredtotogetheras‘lifehistory’theoriesof    aging(PartridgeandBarton,1996),nowformthebasisofthe majorityof    theoreticalworkontheevolutionof    aging.Thisemerg-ingbodyof    evolutionarytheorynowclearlydemonstratesthatselectioncanfavoursenescenceoccurringwithina   species’nat-urallifeexpectancy,andthatthepatternof    senescencecanvarydependingonthespecificsoforganism’slifehistory,ecologyandtheinterplaybetween“intrinsic”and“extrinsic”factorsinfluencingmortality(e.g.AbramsandLudwig,1995;Baudisch,2008;Cichon, 2001;Mangel,2008;McNamaraetal.,   2009;WilliamsandDay,2003).Currentempiricalsupportfrommodellaboratoryorganismsfordisposablesomatheoryandantagonisticpleiotropyasmechanismsof    senescenceis   dramaticallystrongerthanformutationaccumu-lation.Forinstance,manysinglegenemutationsknownto   extendlifein   modellaboratoryorganismshavedetrimentaleffectsonearlycomponentsofDarwinianfitness(Table1).Topick   oneilluminatingexample,a   partiallossof    functionmutationin daf-2 ,the Caenorhab-ditiselegans orthologof    thevertebrateinsulin/IGFreceptor,doublesthelongevityof    wormsinthelaboratory,yetitsdepressiveeffectsonearlyreproduction(Chenetal.,2007)causeittobequickly  216  D.H.Nusseyetal./     AgeingResearchReviews 12 (2013) 214–225  Table   1 Asamplingofantagonisticpleiotropyinlong-livedgeneticallymodifiedmodelorganisms.Notethatallgeneticmanipulationswhichlengthenlifealsodecreaseoneormoremeasuresofearlylifefitness.“ ox -”   prefixindicatesover-expressionof    thegene.Species/modificationLongevityincreasePleiotropyeffectReference Caenorhabditiselegans daf-2112%   Reducedreproductiverate Jenkinset   al.(2004)clk-1   27%ReducedreproductiverateChenet   al.(2007)age-1   50%Reducedreproductiverate a Walkeret   al.(2000)Mit   mutants( atp-3 , nuo-2,issp-1 ,   cco-1 ,    frh-1 )60–70%Reducedfecundity, reduced eggviability,delayeddevelopmentReaetal.(2007)Fruitfly( Drosophilamelanogaster  )chico 40–50% Reducedfecundity/sterility Clancyetal.(2001)inR 48%Reducedfertility/sterilityTataret   al.(2001)indy   90%Reducedreproductiverate b Mardenet   al.(2003) ox -FOXO(fatbody)20–40%ReducedreproductiverateGiannakouetal.(2004)Mouse   ( Mus   musculus )Ames(prop1 df  )35–70%Reducedreproductiverate,delayedmaturationBartke(2005)Snell(pit1 dw )42%Reducedreproductiverate,delayedmaturationLittle(GHRHR  lit )24% c Reducedfertility,enhancedinfectiousdiseasesusceptibilityChubb(1987)Altetal.(2003)GHRKO40–55%Reducedfertility,delayedmaturation ox -  MUPA20%Reducedreproductiverate,cognitiveimpairmentMiskinandMasos(1997) ox -klotho19–31%ReducedfertilityKurosuetal.(2005) a Onlyundercyclicalstarvation(asexperiencedinthewild). b Onlyunderreducedfoodintake. c Lowfatdietonly. eliminatedwhendirectlycompetedagainwormscarryinga   wild-typeallele( Jenkinsetal.,   2004).If    antagonisticpleiotropyanddisposablesomaare   themainmechanismsresponsiblefortheevo-lutionofsenescenceandthemaintenanceofgeneticvariationinagingandlifespan,we   shouldexpectto   observesenescenceinthewild. 2.Senescenceinwildanimals–   an   evidentiaryreview  Duringthelasttwodecadesanavalancheof    empiricalevidenceforsenescenceinwildanimalshasaccumulated(TableS1,Fig.1).However,atleastonepieceof    publishedevidenceforsenescenceintheformofincreasingmortalitywithagealreadyexistedforwildmammalsatthetimeof Medawar’s1952monograph.Morethan600DallsheepinAlaskahadtheiragesatdeathestimatedbyannualgrowthringsontheirhorns,revealinga   clearincreaseinmortalitywithage(Deevey,1947).Inbirds,Lack’scontention– citedbyMedawar–thatbirdsdidnotshowactuarialsenescencecontinuedtobetheconventionalwisdomamongornithologistsatleastuntil1974,whenBotkinandMillerpointedoutthatif mortalitywereindeedindependentof    ageinbirdsthenanum-beroflong-livedseabirdssuchasgullsoralbatrossesshouldreachagesof200–400years,manytimeslongerthanappearsrealisticgivenwhatweknowabouttheagedistributionof    suchpopulations(BotkinandMiller,1974).Furthermore,a   visionary18-yearstudyof yellow-eyedpenguinsin   NewZealandpublishedin   1957providedclearevidencefordeclinesin   somereproductivetraitswithageinawildbird(Richdale,1957).Overa   decadelater,compellingevi-denceemergedforbothactuarialandreproductivesenescenceinawildpopulationofa   muchshorterlivedspecies,thegreattit( Parusmajor  ),   basedonlong-termfielddatafroma   studythatLackhim-selfstartedinthe1940s(Perrins,1979).Adecadeorsolater,severalstudiesusedlifetableinformationfromwildbirdsandmammalstosuggestthatmortalityratesincreasedwithage(Finchetal.,   1990;Nesse,1988;Promislow,1991),althoughtheinferencesthatcanbe madeaboutsenescencefromsuchvertical(orstatic)lifetablesareknowntobelimited(Gaillardetal.,   1994; Jonesetal.,2008).Morerecently,thematurationof    numerouslong-term,individual-basedstudiesofwildvertebrateshasprovidedunequivocal,longitudinalevidenceforage-relateddeclinesin   survival,reproductionandphysiologicalfunctioninbirdsandmammals(Brunet-RossinniandAustad,2006;Clutton-BrockandSheldon,2011; Jonesetal.,2008) and,toa   lesserdegree,reptilesandinsects(BondurianskyandBrassil,2002;Massotetal.,   2011;Sherrattetal.,   2010).Supplementarymaterialrelatedtothisarticlefound,intheonlineversion,athttp://dx.doi.org/10.1016/j.arr.2012.07.004.Togivesomeideaofthescopeofcurrentknowledge,wesur-veyedtheliteratureforstudiesprovidingevidenceofsenescenceinfree-livinganimals,theresultsofwhicharepresentedinFig.1(andlistedindetailin   TableS1).Usingpreviousnon-exhaustivereviewsofbirds(BennettandOwens,2002)andbothbirdsandmammals (Brunet-RossinniandAustad,2006)asa   basis,we   includedstudiesof    free-livingpopulationsthat   documentedage-relatedchangesinadulthoodconsistentwithsenescentdeterioration,notingwhetherthechangeswereinsurvivalprobability,reproductiveperformancetraits(e.g.fecundity,offspringsize,offspringsurvival),orotherphysiologicalorbehaviouraltraits(e.g.foragingefficiency,immu-nity,bodymass).Althoughnosuchsurveywilleverbeexhaustive,wehavemadeourbesteffortstolocateandincludestudiesdoc-umentingage-relatedchangesconsistentwithsenescenceinthewild.Wehaveincludedonlystudiesthat   analysedprimaryfielddatainoursurvey;comparativestudiesanalysingpreviouslypub-lishedlifetableswereexcluded.Whilstthevastmajorityofstudieswereongenuinelywildpopulations,we   alsoincludedahandfulof ‘semi-natural’studiesin   whichanimalswerekeptinsomeformof protectiveenclosurebutwerestillexposedtosomeformsofnat-uralenvironmentalstressorsandmortalityrisk(e.g.Hruskaetal.,2010;Zajitscheketal.,2009a,andotherstudiesdenotedwitha   “$”inTableS1).We   found340studiesof    175differentanimalspeciesthatpro-videdevidenceofsenescencein   thewild(Fig.1AandB;TableS1).Ofthese,thevastmajoritywerebirdsandmammals–149studiesof    75birdspeciesand165studiesof79mammalspecies.Table2spreadstheevidenceforsenescencein   thewild(TableS1)acrosstheordersof    birdsandplacentalmammals.Thisservestoillustratethattheevidenceisreasonablywelltaxonomicallyspread.Indeed,oursurveyof    theliteraturesuggeststousthat   wheresenescencehasbeenlookedforwithdetailedlongitudinaldatainwildbirdsandmammalsitis   usuallyfound.However,Table2alsoclearlyshowsthattherearemany,manyordersandgeneraforwhichdataare  D.H.Nusseyetal./AgeingResearchReviews 12 (2013) 214–225 217  Table   2 Phylogeneticdistributionof    studiesdocumentingevidenceof    senescenceinwild   populationsof    birdsandplacentalmammals.Notethatan   absenceof    evidenceforsenescencewithin   ordersorgeneramostlikelyreflectsecologicalignoranceregardingthetaxainquestion,ratherthanevidencethatsenescencedoesnotoccur.BirdsPlacentalmammalsOrderNumberof generaNumberof    generawithevidenceof senescencePercentageof    generawithevidenceof senescenceOrderNumberof generaNumberof    generawithevidenceof senescencePercentageof    generawithevidenceof senescenceStruthioniformes 15 0 0Edentata15   0   0Tinamiformes900Pholidota1   0   0Galliformes 8434Lagomorpha12   0   0Anseriformes52713   Rodentia49141Podicipediformes700Macroscelidea4   0   0Phoenicopteriformes 3 1 33 Primates 74 11 15Phaethontiformes 1 0 0 Scandentia 5 0 0Pteroclidiformes 2 00Chiroptera20910Columbiformes 4600Dermoptera2   0   0Caprimulgiformes2200Insectivora73   23Apodiformes12811Carnivora12615   12Opisthocomiformes100Artiodactyla9017   19Gruiformes4200Cetacea40410Cuculiformes3200Tubulidentata1   0   0Gaviiformes100Perissodactyla6   117Sphenisciformes 6 3 50 Hyracoidea3   133Procellariiformes26623   Sirenia2   0   0Ciconiiformes 600Proboscidea2   2100Pelecaniformes3526Charadriiformes9599Passeriformes1290202Psittaciformes8800Accipitriformes 74 45Coliiformes200Strigiformes 2927Trogoniformes700Piciformes7100Coraciiformes 35 0 0 lacking.Itisveryimportantto   beawarethatin   Table2anabsenceofevidenceforsenescencereflectsecologicalignoranceregardingthetaxainquestion,ratherthanevidencethatsenescencedoesnotoccur.Itis   notablethat   twoparticularlyspeciosemammalianorders,thebats(Chiroptera)androdents(Rodentia),whichcon-tainboththemainmammalianlaboratorymodelorganismsforthestudyofaging(mice)andlong-livedspeciesof    growinginter-estinbio-gerontology(batsandnakedmolerats,Austad,2010),arepoorlyrepresentedinour   surveyof    theliterature.Gapsofthiskindare,atleastinsomepart,dueto   challengesstudyingparticu-larkindsofanimalsin   thefield(e.g.subterranean,aquatic,highlymotileandnocturnalspecies),andthefactresearchefforthasbeengeographicallyfocusedinEuropeandNorthAmerica.However,thisservestohighlightthatwe   areverymuchswimmingintheshal-lowswhenitcomestounderstandingthenaturaldiversityof    agingpatternsacrossavianandmammaliantaxa.Althoughcomparativestudiestestingevolutionarytheoriesof senescencehavetendedtofocusonage-relateddeclinesinsur-vivalprobability(Promislow,1991;Ricklefs,1998,2010,although see Jonesetal.,2008),survivalis   onlyonecomponentof    anorgan-ism’slifetimereproductivesuccess(PartridgeandBarton,1996).AsFig.1Cillustrates,thenumberof    studiesdocumentingage-relatedmortalityrateincreasesinthewildis   well-matchedbyevidenceof    declinesintraitsassociatedwithreproductivefitness,suchasfecundity,offspringsize,offspringsurvival,spermfunctionandsecondarysexualcharacteristics(TableS1).   Studiesdocumentingage-relatedchangesinotherphysiological,behaviouralandmor-phologicaltraitsconsistentwithsenescencein   thewildhavebeguntoemergesincethelate1990s(Fig.1C).Thisreflectsa   grow-inginterestamongevolutionaryecologistsinthephysiologicalprocessesunderpinningage-relateddeclinesinsurvivalandrepro-ductiveperformance(Monaghanetal.,   2008).Thereismountingevidenceforbodymassdeclinesinlatelifein   wildungulates(e.g.Mysterudetal.,2001;Nusseyetal.,2011;Weladjietal.,2010), aswellasevidenceof    muscularsenescenceinsamplesfromadultwild-caughtsealsandshrews(Hindleetal.,2009a,b).Evidencefor importantchangesin   foragingbehaviourwithage–potentiallydueto   lossof    musclefunctionorwiderphysiologicalcondition–is   alsobeginningtoemerge(e.g.Catryetal.,2006;Lecomteetal.,2010;MacNultyetal.,2009).Changesinmarkersof    theimmunesystem,broadlyconsistentwithimmunosenescence,havealsobeendoc-umentedinsomestudiesof    wildbirdsandreptiles(reviewedinPalaciosetal.,   2011),andin   onewildmammalpopulation(Nusseyetal.,   2012),althoughitisnotablethatseveralstudiesinbirdsandreptileshavefailedtofindpatternsconsistentwithage-relateddeclinesinimmunefunction(e.g.Lecomteetal.,   2010;Massotetal.,2011;Palaciosetal.,2011;Schwanzetal.,2011). Evidenceforsenescencein   vertebratesotherthanbirdsandmammalsis   muchhardertocomeby(Fig.1A   andB,   TableS1).Wewereabletofindonlyonestudyof    amphibians,whichsuggestedretinalstructureandfunctionmightbecompromisedinlarger–andthereforeolder–wildtigersalamanders(Townes-Andersonetal.,1998).Similarly,evidenceinwildfishappearedlimitedtostudiesofPacificsalmon( Oncorhynchusnerka ),whichare   semel-parousandshowrapidsenescenceonreturningtotheirnatalfresh-waterstreamsto   breed(e.g.Morbeyetal.,2005),andguppies( Poe-ciliareticulata ;BryantandReznick,2004).Theevidencefromwildreptilesisa   littlehealthier,withparticularlycompellingevidenceof age-relateddeclinesinsurvivalfroma   long-termstudyofcommonlizards( Lacertavivipara ,Massotetal.,   2011).However,long-termstudiesof    two   speciesofturtlesfoundnoevidenceforsurvivalsenescence(Congdonetal.,   2001,2003).Monitoringfecundityand reproductiveperformanceinthewildis   exceptionallychallenginginreptiles(nottomentionfishoramphibians),andmanystud-ieshavecircumventedthisbybringingwild-caughtfemalesintothelaboratorytobreedandsubsequentlyreleasingthemandtheiryoungbackattheiroriginalcapturesite(e.g.Massotetal.,2011;Sparkmanetal.,   2007).Evidencefromstudiesof    thisnaturefor  218  D.H.Nusseyetal./     AgeingResearchReviews 12 (2013) 214–225 Fig.1. Theevidenceinsupportof    senescenceoccurringinwildanimalsis   nowoverwhelming.TheplotsusethestudieslistedinTableS1to   illustratetherapidlyaccumulatingnumberof:   (A)newspeciesinwhichage-relatedchangesconsistentwithsenescencehavebeen   documentedinthewildand,(B)individualstudiesdoc-umentingorinvestigatingsenescencepatternsinwild   populations.Thedataaresplittoseparatelyillustratetheevidenceforbirds,mammals,othervertebrates(fish,reptilesandamphibians),andinvertebrates.Part(C)showsthecumulativenumberofstudiesdocumentingage-relatedchangeinsurvivalprobability,repro-ductiveperformancetraitsandchangeinother,typicallyphysiological,traitswithage   indicativeofsenescence.Notethatmanystudiesdocumentsenescenceinmorethanonetypeof    trait,andthatinallplotsthefirstyear(1976)on   thegraphsincludedthe   handfulofstudiesuptoandincludingthatyear. reproductivesenescenceinreptilesremainsverylimited:commonlizardsshowage-relateddeclinesinfecundityandoffspringsur-vivalwhenkeptin   semi-naturalenclosures(Richardetal.,2005)butstudiesofwildturtlesandgartersnakesshowverylittleevi-denceof    reproductiveaging(Congdonetal.,2001,2003;Miller, 2001;Sparkmanetal.,2007).Age-relatedincreasesin   reproductiveperformance,associatedwithindeterminatepatternsofgrowthobservedin   manyfish,reptilesandamphibianshavebeenshowntheoreticallyto   offsettheweakeningofnaturalselectionwithageduetoage-independentenvironmentally-drivenmortality,makingthesetaxapotentiallyveryinterestingasmodelsof    delayed,negli-gibleorevennegativesenescence(Baudisch,2008;Congdonetal.,2003;Sparkmanetal.,2007).Evidenceforsenescencein   wildinsectsisalsoemerging(Fig.1AandB),althoughwe   wereunableto   findevidenceforsenescenceinthewildfromotherinvertebratetaxa   (e.g.molluscs,crustaceansorcephalopods).Thechallengesinvolvedinmonitoringthedemog-raphyandagestructureof    suchsmallanddispersivecreaturesin   thewildareextreme.Studiestodatehavefocusedonspeciesthatformaggregationsof    somekind,sothatindividualscanbemarkedandsubsequentlyrecaptured.In   aground-breakingstudy,BondurianskyandBrassil(2002)individuallymarkedandfollowedmaleantlerflies( Protopiophilalitigata )acrosstheirreproductivelives,whicharespentonthecastantlersof    ungulates.Theirdataonage-specificmortalityandmatingratesprovidesincontrovert-ible   evidenceforsenescenceinthewildinaspeciesthatlivesonlya   fewweeks(BondurianskyandBrassil,2002).Arecentre-analysis ofmark-recapturedatafromwilddragonfliesanddamselfliessug-geststhatsurvivalsenescenceis   commoninthesegroups(Sherrattetal.,   2011).Inaddition,age-relatedincreasesinwingdamageandmortalityrisk,aswellasdecliningforagingperformancewithageindicatesenescenceinworkerhoneybees(  Apismellif-era )foragingin   thewild(Dukas,2008a,b;HigginsonandBarnard, 2004).Recently,methodshavebeendevelopedto   estimatetheagestructureandagingratesintaxalikeinsectsthatarenotori-ouslydifficultto   monitorlongitudinallyinthewild(Careyetal.,2008;Mulleretal.,   2004;Zajitscheketal.,   2009b).Althoughtheyrestonquiterestrictiveassumptions,these   methodshavealreadyprovidedevidenceforsurvivalsenescenceinwildblackfieldcrick-ets( Teleogrylluscommodus ,Zajitscheketal.,   2009b).Researchintosenescenceandlifespaninwildinsectsis   anexcitingareawithuniquepotentialto   linkourunderstandingof    agingin   laboratoryconditionstoagingina   realisticevolutionarycontext(Carey,2011;Zajitscheketal.,2009b).Thedifficultiesassociatedwithdetectingandmeasuringsenes-cenceinthewildaremanifold,andhavebeenwidelydiscussed(Brunet-RossinniandAustad,2006;Gaillardetal.,   1994;Nusseyetal.,2008a).   Forinstance,imperfectrecaptureprobabilitiesof markedindividualscanbias   estimatesofage-dependentsurvivalandreproduction(Bouwhuisetal.,   2012;Gimenezetal.,2008), phenotypicheterogeneityamongageclassesassociatedwithselec-tioncangeneratecross-sectionalagepatternsthatareunrelatedto   underlyingwithin-individualagingpatterns(Cametal.,2002;Reidetal.,2003),andsurvivalcandeclineinyoungor   oldageasa   resultof    costsassociatedwithincreasedinvestmentin   growthorreproductioninsteadof    senescence(BondurianskyandBrassil,2002;Promislow,1991).However,recentstudiesanalysinghigh-qualitylongitudinaldatawithstatisticaltoolscapableofaccountingforselectiveeffectsandrecapturerates,alongsidesimultaneousassessmentof    survivalandreproductivetraits,haveovercometheseissues.Althoughsomemeticulousanalysesof    highqualitydatafromwildbirdandmammalpopulationshavefailedtofindevidenceof    senescence(e.g.Altweggetal.,   2007;Nicholsetal.,1997;Slade,1995),suchcasesarenowintheclearminority.Any debateaboutwhetherwildanimalssenesceornotis   over,quashedbeyondargumentbytheempiricaldatahighlightedinFig.1and
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