Global Ecol Biogeogr. 2019;28:1925–1936. wileyonlinelibrary.com/journal/geb  | 1925© 2019 John Wiley & Sons Ltd

Received:2August2019  |  Revised:23September2019  |  Accepted:25September2019DOI: 10.1111/geb.13020

M A C R O E C O L O G Y 3 0 T H A N N I V E R S A R Y

Unifying macroecology and macroevolution to answer fundamental questions about biodiversity

Brian J. McGill1  | Jonathan M. Chase2,3  | Joaquín Hortal4 | Isaac Overcast5 | Andrew J. Rominger6 | James Rosindell7 | Paulo A. V. Borges8 | Brent C. Emerson9  | Rampal Etienne10 | Michael J. Hickerson5,11 | D. Luke Mahler12 | Francois Massol13,14 | Angela McGaughran15 | Pedro Neves10 | Christine Parent16,17 | Jairo Patiño18 | Megan Ruffley17 | Catherine E. Wagner19 | Rosemary Gillespie20

1SchoolofBiology&Ecology,MitchellCenterforSustainabilitySolutions,UniversityofMaine,Orono,Maine,USA2GermanCentreforIntegrativeBiodiversityResearch(iDiv),Halle‐Jena‐Leipzig,Leipzig,Germany3InstituteofComputerScience,Martin‐LutherUniversityHalle‐Wittenberg,Halle(Saale),Germany4DepartmentofBiogeographyandGlobalChange,MuseoNacionaldeCienciasNaturales(MNCN‐CSIC),Madrid,Spain5GraduateCenteroftheCityUniversityofNewYork,NewYork,NewYork,USA6SantaFeInstitute,SantaFe,NewMexico,USA7DepartmentofLifeSciences,ImperialCollegeLondon,Ascot,Berkshire,UK8cE3c–CentreforEcology,EvolutionandEnvironmentalChanges/AzoreanBiodiversityGroup,FaculdadedeCiênciasAgráriasedoAmbiente,UniversidadedosAçores–,AngradoHeroísmo,Terceira,Portugal9IslandEcologyandEvolutionResearchGroup,InstitutodeProductosNaturalesyAgrobiología(IPNA‐CSIC),Tenerife,CanaryIslands,Spain10GroningenInstituteforEvolutionaryLifeSciences,UniversityofGroningen,Groningen,TheNetherlands11DivisionofInvertebrateZoology,AmericanMuseumofNaturalHistory,NewYork,NewYork,USA12DepartmentofEcology&EvolutionaryBiology,UniversityofToronto,Toronto,Ontario,Canada13Univ.Lille,CNRS,Inserm,CHULille,InstitutPasteurdeLille,U1019‐UMR8204‐CIIL‐CenterforInfectionandImmunityofLille,59000Lille,France14Univ.Lille,CNRS,UMR8198‐Evo‐Eco‐Paleo,SPICIgroup,59000Lille,France15DivisionofEcologyandEvolution,ResearchSchoolofBiology,AustralianNationalUniversity,Canberra,AustralianCapitalTerritory,Australia16InstituteforBioinformaticsandEvolutionaryStudies(IBEST),UniversityofIdaho,Moscow,Idaho,USA17DepartmentofBiologicalSciences,UniversityofIdaho,Moscow,Idaho,USA18DepartmentofBotany,PlantEcology&Physiology,FacultyofScience,UnivesityofLaLaguna,LaLaguna,Tenerife,Spain19DepartmentofBotany,UniversityofWyoming,Laramie,Wyoming,USA20DepartmentofEnvironmentalScience,Policy,andManagement,UniversityofCalifornia,Berkeley,California,USA

AbstractThestudyofbiodiversitystartedasasingleunifiedfieldthatspannedbothecologyand evolution and bothmacro andmicro phenomena. But over the 20th century,majortrendsdroveecologyandevolutionapartandpushedanemphasistowardsthemicroperspectiveinbothdisciplines.Macroecologyandmacroevolutionre‐emergedas self‐consciously distinct fields in the1970s and1980s, but they remain largelyseparatedfromeachother.Here,wearguethatdespitethechallenges, it isworthworkingtocombinemacroecologyandmacroevolution.Wepresent25fundamentalquestionsaboutbiodiversitythatareanswerableonlywithamixtureoftheviewsandtoolsofbothmacroecologyandmacroevolution.

CorrespondenceBrianJ.McGill,SchoolofBiology&Ecology,MitchellCenterforSustainabilitySolutions,UniversityofMaine,Orono,Maine,USA.Email:geb@brianmcgill.org

Funding informationUSDAHatchMAFES,Grant/AwardNumber:1011538;sDiv,Grant/AwardNumber:sEcoEvoworkinggroup;NationalScienceFoundation,Grant/AwardNumber:ABIgrant#1660000

Editor:AdamAlgar

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1  | HISTORIC AL CONTE X T

In Darwin's “On the origin of species”(1859),itisimpossibletofindadistinctionbetweenecologicalandevolutionaryprocesses;theyareintertwinedthroughout.AlthoughseveralofDarwin'schaptersaredevotedtowhatwenowperceiveaspurelyevolutionarytopics,suchastransformationsofspeciesinthefossilrecord(Chapters9and10)andhybridism(Chapter8),otherchapterswouldbeassignedtoecology, suchas the struggle for existence,which involves re‐productionandmortality(Chapters4and5).Therearealsoseveralchaptersaddressingtopicsthatarecurrentlyrecognizedascrossingboth ecology and evolution (intraspecific variation in Chapters 1and2;behaviourinChapter7).Equally,Darwinmadenodistinctionbetweenmicro andmacro scales.He interwove the fossil recordwithagriculturalbreedingprogrammes,andalocalentangledbankof interactingspecieswith thebiogeographicaldistributionofor‐ganisms.Similarbreadthcanbeseeninthewritingsofauthorswhopre‐datedDarwin, suchasvonHumboldt (vonHumboldt&Ross,1852).

Inthefirsthalfofthe20thcentury,awedgebegantoformbe‐tweentheevolutionaryandecologicalsidesofthefield(Figure1).Ontheonehand,ecologistsbecamemoreinterestedinsmaller‐scalephenomena,suchaspopulationdynamicsandspeciesinteractions,andcouldlargelyignoreevolutionaryprocesses(Clements,Weaver,&Hanson,1929;Elton,1927).Ontheotherhand,manyevolutionarybiologists,spurredonbylinkagestogenetics(Morgan&Biologiste,

1925) and the development of theoretical population genetics(Provine,2001),shiftedtheir focusto individualgenesratherthanthewholephenotype.Forexample,thedevelopmentofmathemat‐icalmodels that startwithassumptions suchas “let the fitnessofAAandAabe1andofaabe1−s”tendtounderplaytheecologicalprocessesthat leadtodifferencesinfitnessthatDarwin'swritingsso eloquently merged.

The latter half of the20th century began to see the re‐emer‐genceofaconnection.Someearlydescriptionsofthiscanbeseeninchaptersof theeditedvolume“Evolutionasaprocess” (Huxley,Hardy, & Ford, 1954),where evolutionary processeswere said toleadtocommunitiesofinteractingorganisms(muchlikeDarwin’sen‐tangledbank).Selectioninnaturalenvironmentsbegantobestudied(Ford,1971;Kettlewell,1955). Likewise, theemergenceofquanti‐tativegenetics (Crow&Kimura,1970)andmodelsofevolutionofmultivariatephenotypes(Lande,1979)broughtbackacomplexviewofphenotype.Fromtheecologyside,evolutionaryecologyemergedasafield,inspiredbyHutchinson'smetaphorofthe“ecologicalthe‐aterandtheevolutionaryplay”(Hutchinson,1965)andthemodelsbyMacArthurandcolleaguesthatlookedattheevolutionofecolog‐ically relevanttraits (MacArthur,1961,1962;MacArthur&Levins,1964;MacArthur&Pianka,1966).

The 1970s saw this reconnection of ecology and evolutiondevelop more fully as part of the field of “population biology”,explaining ecological and evolutionary questions through basicpopulationprocessesusingsimpledifferentialequationsinvolving

F I G U R E 1  AbriefhistoryofhowDarwin'sintegrativevisionoforganismalbiologybecamesplitintofirsttwoandthenfourseparatefields:microevolution,macroevolution,microecology(traditionalpopulationandcommunityecology)andmacroecology.Inthebottomrightpanel,effortstolinkmicroevolutiontomacroevolutionandmicroecologytomacroecology(narrowverticalpaths)areongoingbutdifficult.Effortstolinkmicroevolutionandmicroecology(horizontalbroadconnection)havebeenamajorfocusforrecentdecades.Effortstolinkmacroecologyandmacroevolution(missingareashownbyaquestionmark)havebeen,incomparison,muchmorelimitedbutareneededurgently[Colourfigurecanbeviewedatwileyonlinelibrary.com]

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birth,death, immigrationandemigration,andspeciation (Levins,1968;MacArthur&Wilson,1967;Wilson&Bossert,1971).Thispopulation biology framing opened up new fields that com‐bined evolutionary and ecological perspectives spanning a di‐versearrayofquestions,includingevolutionaryecology(Bulmer,1994;Fox,Roff,&Fairbairn,2001), behavioural ecology (Alcock&Rubenstein,1989)andlife‐historytheory(Roff,2002;Stearns,1976). The population biology approach has also seen a resur‐genceover the lastdecadeunder the labelof “eco‐evolutionarydynamics”,whichexplorestheevolutionarydynamicsoftraitsthatplayoutonthesametime‐scalesasecologicalprocesses(Carroll,Hendry,Reznick,&Fox,2007;Grant&Grant,1989;Hendry,2016;McGill & Brown, 2007; McPeek, 2017; Metz, Geritz, Meszena,Jacobs, & Heerwaarden, 1996; Schoener, 2011; Yoshida, Jones,Ellner,Fussmann,&HairstonJr.,2003).

Althoughthepopulationbiologyresearchprogrammesucceededinbringingecologyandevolutiontogether incertainways, itgaveprimacytosmall‐scaleprocesses.Thisisessentiallythephilosophicalnotionofreductionism;explainingasystembybreakingitintocom‐ponent parts and examining their interactions. This presumes theabilitytoscaleupdetailedmodelsofpopulationprocessestoanswermacroevolutionaryquestionsaboutspeciesdiversityandphenotypeevolutionormacroecologicalquestionsabout the spatial variationin diversity and the relative abundance of species. Although suchscalingupisanactiveandinterestingareaofresearch,progresshasbeenslowowingtospecificmathematicalobstacles(McGill,2019;O’Neill,1979).Theresult is thatembracingthepopulationbiologyview, while helping to reunite aspects of ecology and evolution,droveawedgebetweenthemicro‐andmacro‐scaleaspectsofeachdiscipline.

Withmicro‐scale processes predominating in the populationbiology paradigm, this arguably diminished the importance andrelevance of themacro‐scale disciplines. As a result,macroevo‐lution andmacroecology emerged as distinct, separately namedfields (Brown &Maurer, 1989; Stanley, 1975). In evolution, thelineissharpandwidelyagreedupon;studiesofprocesseswithinaspeciesaremicroevolution,whereasmacroevolutionaddressesquestions above the species level (phylogenies and comparativeevolution). In ecology, the line is more blurred. Microecology(more commonly called ecology) studies small scales, involvingphysiology, behaviour, populations and communities, whereasmacroecologystudieslargespatial,temporalortaxonomicscales(Brown, 1995; Gaston & Blackburn, 2000; McGill, 2019). Giventhatbothmacrofieldsspenttheirfirstdecadesestablishingthem‐selves as independent fields, they have not often looked exter‐nally, leading to comparatively few links betweenmacroecologyand macroevolution.

Tosummarize(andadmittedly,tooversimplify),thestudyofor‐ganismalbiologystartedasaunifiedfield,became,formostprac‐titioners, split into distinct fields of ecology and evolution, thenbecamesplitfurtherintofourfields,withmostpractitionersfocus‐ingonmicroversusmacroversionsofeachfield(Figure1).

2  | REL ATIONSHIP OF MACROECOLOGY AND MACROE VOLUTION

Are we on our way to the seamless integration of ecology andevolutionpractisedbyDarwin?Wewould suggest not yet in animportant way. The missing linkage in the history as describedabove is a direct linkage betweenmacroecology andmacroevo‐lution (questionmark inFigure1),despiteseeminganatural linkgiven their strongmatch in embracing large scales.Notably, theverticallinkagesofthetwomacro–microbridgeshaveprovedsur‐prisinglyresistanttoadvances(notwithstandingsomesuccesses;Avise,2000),andwesuggestthattheywillultimatelyprovetobeharderbarrierstocrossthantheecology–evolutiondivide(hencethe thicker line in Figure1) for some specificmathematical rea‐sons (McGill, 2019; O’Neill, 1979). Regardless of one's view onthe feasibility of spanning themacro–micro divide, the indirect,three‐legged route of linking macroevolution to microevolutionto microecology to macroecology is hopelessly unwieldy. Themainthesisofthispaperisthatorganismalbiologyismissing(andbadlyneeds)are‐unificationdirectlybetweenmacroecologyandmacroevolution.

Averysimpleexaminationofthelimitedinteractionsbetweenmacroecology and macroevolution can be made using bibliomet‐ricanalysis,albeitinanecessarilysimplisticfashion.Inparticular,manymacroecologicalandmacroevolutionarypapersoftendonotusethosekeywords (andnecessarilycouldnotbeforethewordswerecoined),meaningthatthisanalysisclearlyomitsrelevantpa‐pers,butwebelieveittobeasamplethatisnotbiased.Ananalysisofwordsfound inkeywordsandabstractsusingWebofSciencewasperformedinMarch2018.Asearchforderivativesofmacro‐ecology (“macroecolog*”) found 1,814 papers going back to thecoiningofthetermin1989(Brown&Maurer,1989)andc.150pa‐pers/yearinrecentyears.Derivativesofmacroevolution(“macro‐evolution*”) found 2,570 papers going back to Stanely's coiningof the term (Stanley, 1975), with c. 220 papers/year in recentyears.Although, again,bynomeansdoes this approachcaptureall macroecological or macroevolutionary papers, these resultssuggest that a substantial sample is obtained in searches usingthesekeywords.Thisanalysissupportsthenotionthatbothofthemacro fieldshavebeengrowing rapidly since their relatively re‐centlaunches.Italsosupportsthenotionthatmacroecologyandmacroevolution are infrequently practised as overlapping fields.Only105papersstartingin2000(c.10papers/year)containbothmacroecologyandmacroevolution(macroecolog*andmacroevo‐lution*).Bythismethod,only4%–6%ofthepapersthatareexplic‐itlymacroecological ormacroevolutionary recognize themselvesas interdisciplinarybetweenbothfields.Thiscrudeanalysissug‐gests that although linkages betweenmacroecology andmacro‐evolutiondoexist,theyarenotyetcommon.Inrecognitionoftheexistenceofsomelinksbetweenmacroecologyandmacroevolu‐tion,Box1givessomewell‐knownexamplesoflinkagesbetweenbothdisciplines.

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Therearegoodreasonsforthisdisconnectbetweenthetwomacro fields. As noted, both fields are relatively new, placinganemphasisonself‐definitionrather thanreachingout tootherfields. Additionally, the two fields operationalize and measuretheir variables differently although they discuss the same con‐cepts (Table 1). This is in part because the sources of the dataare distinct and in part because the perspectives and priorities

are distinct.Macroevolutionists focus on changes through timeandthususeeitherstratifiedfossilsorphylogeniesderivedfromcurrent molecular sequences or both. Macroecologists focuson spaceand thususebiological inventories in thepresentday.Clearly,boththeseperspectivesarecrucialtounderstandingdi‐versityinspaceandtime,butintegratingtheseperspectivespres‐entschallenges.

Box 1 Examples of prominent existing work linking macroecology and macroevolution

• Biogeographyandpalaeontology(andpalaeoecology)arelong‐standingfieldsthatintegrateecologyandevolutionatmacroscales.Palaeontologyisfullofexamples,suchasthestudyofhowextinctionratesdependonbodysize(e.g.,Jablonski&Raup,1995)orhowphenotypechangesthroughtime(e.g.,Foote,1997)orrangesshiftbecauseofclimate(Lyons,2003)orecologicalprocessesinfossilcommunities(Bloisetal.,2014).

• MacArthurwaskeyinre‐introducingevolutionarythinkingintoecology(MacArthur,1961).Examplesthataremoremacroinnatureincludetheideaoflimitingsimilarity(MacArthur&Levins,1967),hisexplorationofthecausesofthelatitudinalgradientinrichness(MacArthur,1969),hisworkonRversusKselection(MacArthur,1962)orevenhisexplicitrecognitionoftheimportanceofevolution‐aryprocessesinthetheoryofislandbiogeography(Chapter7ofMacArthur&Wilson,1967).

• Theexplorationofadaptiveradiationsinisland‐likesystemshaslongnecessitatedthecombinationofmacroecologyandmacroevolu‐tion(Grant&Grant,1989;Schluter,2000).Thestudyofecologicalmorphotypesandtheirevolutionacrossmanyislandsisarelatedexample(Gillespie,2004;Losos,2011).

• Ecologicalneutraltheorywithspeciation(Hubbell,2001)clearlylinksthetwofields.Moregenerally,withgrowingrecognitionoftheimportanceoftheregionalpoolofspeciesforecology(Ricklefs&Schluter,1993a,1993b),therehasbeenincreasedinterestinexplor‐ingthemacroevolutionofregionalpoolsofspecies,whichthenconstrainlocalcommunityassembly(Mittelbach&Schemske,2015;Ricklefs,2015).Alsorelatedarestudiescomparingtheassemblyofcommunitiesthroughcolonizationversusspeciation(Rummel&Roughgarden,1985).

• Likewise,phylogeneticcommunityecologyhassoughttounderstandhowthemacroevolutionaryhistoryoftheregionalpoolinteractswithecologicalandbiogeographicalprocessestoproduceobservedassemblagesofco‐occurringtaxa(Webbetal.,2002;Emerson&Gillespie,2008;Cavender‐Bares,Kozak,Fine,&Kembel,2009).

• Nicheconservatismisexplicitlyanevolutionaryhypothesisaboutanecologicalconcept(thatnichesevolveslowlyandthusshowcon‐servatismoveraphylogeny;Ackerly,2003;Peterson,Soberón&Sánchez‐Cordero,1999;Wiens&Graham,2005).

• Ricklefandcolleagueshavestudiedtaxoncyclesonislands(Ricklefs&Cox,1972)andtheroleofdistinctmacroevolutionondifferentcontinentsinspeciesrichness(Latham&Ricklefs,1993),writtennumerouspapersattheinterfaceofniche,communityandmacroevo‐lution(Cox&Ricklefs,1977;Ricklefs,2010,2011)andmademultiplecallsfortheimportanceofmergingecologicalandevolutionarythinking(Ricklefs,2007;Ricklefs&Schluter,1993a,1993b).

• Rosenzweig'sexaminationofcompetitivespeciation(ecologicalconditionsleadingtosympatricspeciation;Rosenzweig,1978)andthestudyofincumbentreplacement(increaseddiversificationratesaftercompetitorsgoextinct;Rosenzweig&McCord,1991)arealsoexamples.

TA B L E 1  Comparisonofmacroecologicalversusmacroevolutionaryviewsofdifferentvariables

Variable Macroecology Macroevolution

Diversity Richness,evenness,abundance(oftenofpolyphyleticgroups)

Richness(typicallywithinamonophyleticclade)

Traits Morphospace;traitvolumesandnichesacrossan assemblage;functionaldiversity

Evolutionofmorphospace,traitvolumesandnichesacrossaphylogeny

Diversification Phylogeneticdiversityindices Speciation,extinction,diversificationrates

Distribution Rangesize,habitatpreferences Biogeographicalprovince

Speciesinteractions(e.g.,competition,predation,parasitism)

Interaction webs Co‐evolution

Abiotic environment Climatevariationacrossspace;staticviewofsoils/topography

Climatevariationacrosstime;geologicalchangeintopography

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Thekeyvariablethatbothfieldsshare isan interest inspeciesrichness,althoughmacroevolutioninitiallyseesthisasanoutcomeof speciation and extinction through time,whereasmacroecologyinitiallyseesthisasanecologicaloutcomeofdispersalandofpastandpresentclimaticconditions(Belyea&Lancaster,1999)varyingacrossspaceatonepointintime(butasourpaperhighlights,eco‐logical conditions anddiversification are not independent of eachother;alsoseeRicklefs&Schluter,1993b).Moreover,macroevolu‐tiontendstofocusontherichnessofamonophyleticgroupofspe‐cies(e.g.,aspecificcladeoffrogs),whereasmacroecologytendstofocusontherichnessofanassemblage (e.g.,all trees) thatcanbepolyphyletic.

Such differences extend to other variables of interest. Bothareasfocusonphenotype.Macroecologistscanfocusonacom‐plexmultivariatesetoffeaturesbutarelimitedtoapointintime.Macroevolutionists bring a temporal perspective but are limitedto a simpler view of phenotype owing to the limitations of fos‐sils and phylogenetic methods. Likewise, both fields focus onabundanceanddistribution.Butabundance isnotestimatable inphylogeniesandisspottilypreservedinthefossilrecord,anddis‐tributionscanonlybeapproximatedfromfossilandphylogeneticinference,leadingtoaverycoarseviewofhistoricaldistribution.Macroecologistscanmeasurethesewithmuchmoreprecisionatfine‐grainedspatialscalesbutfailtoseeabundanceanddistribu‐tionasdynamicandchangingthroughevolutionarytime.Finally,bothfieldshavenotionsofcolonization,butmacroevolutionlooksatrarevicarianceorfoundereventsacrossbiogeographicalprov‐inces,whereasmacroecologylooksmoreatthescaleofmetapop‐ulation dynamics.

Aswe have shown, the overlap in concepts of interest tobothmacroecology andmacroevolutionhides deeper divides.Methodological challengesexistowing to theirdisparatedatasources. Butmore fundamentally, there is also a key concep‐tual difference. Macroevolution tends to focus on temporalprocesses, whereas macroecology tends to focus on spatialprocesses. Core questions in macroevolution tend to centreon questions of rates (speciation, extinction and net diversi‐fication)andhowtheserateschangethroughtimewithinandacrossclades.Corequestions inmacroecology tend tocentreon levels (not rates), such as abundance, richness, range sizeandtraits,andhowtheselevelschangeacrossspaceandacrosstaxa.

3  | RE A SONS WHY A UNIFIC ATION IS NEEDED

Scientificinquirydoesnotdivideitselfarbitrarilyintospatialques‐tionsversustemporalquestions.Nordoesscientificinquirylimitit‐selftoasinglesourceofdataatatime.Thesearebarrierscreatedbyhumans.Althoughtheremighthavebeenpragmaticreasons(includ‐ingsocialandcomputational limits)thathaveslowedthecoopera‐tionofmacroecologyandmacroevolution, theconceptualbarriers

arereadilyovercome.Indeed,althoughwehaveemphasizedthedif‐ferences and challenges thus far, the overlap in topics of interestbetweenmacroecologyandmacroevolutionisstriking(Table1).Tothedegreethatlargespatialprocessesplayoutacrosslongtempo‐raltime‐scalesandviceversa(Levin,1992;Stommel,1963;Wiens,1989),macroecologyandmacroevolutionwillalsonaturallylookto‐wardseachotherratherthantowardsthe“micro”versionsoftheirfields. In fact,we suggest thatmacroecology andmacroevolutionurgentlyneedtocooperate,becausethereareobviousandimpor‐tantquestions thatcombinemacroecologicalandmacroevolution‐aryvariablesandperspectives.

Figure 2 gives a conceptual framework that suggests manyoverlappingquestions,25ofwhicharethenlistedinmoredetail

F I G U R E 2  Therelationshipsbetweenmacroecologyandmacroevolution.Therowscontainpossibleexplanatoryvariables(labelledandcategorizedattheleft).Thecolumnscontainpossibledependentvariables(labelledandcategorizedatthetop).Someofthesevariablesareecological(inblue)andsomeareevolutionary(inred).Diversityandtaxonomicgrouparesharedbetweenecologyandevolution(inpurple).Abioticvariablesareshowninitalics,whereasbioticvariablesareshowninbold.Eachintersectionorgridcellisapotentialquestionoftheform,“HowdoesXaffectY?”.Historically,macroecologyfocusedpredominantlyonintersectionsofvariablesthatwereecological,whereasmacroevolutionfocusedonvariablesthatwereevolutionary,althoughthisdivisionhasneverbeenabsolute(Box1).Questionsinvolvingecologicalvariablesimpactingevolutionaryvariablesandviceversa(lightpurpleregions)representtheemergingsynthesisbetweenmacroecologyandmacroevolution,asarguedforhere.Thefactthatdiversityandtheimportanceofdistincttaxonomicgroupsissharedbetweenmacroecology and macroevolution creates a boundary region (darkpurple).Notethat“diversity”appearsasasinglefactorinthediagrambutcouldrefertotaxonomic,functionalorphylogeneticdiversityandcouldequallyrefertoalpha,betaorgammadiversity.Numbersinthegridcellsrepresentquestions,whicharelistedinTable2.Boldnumbersrepresentcasestudies,whichareexpandeduponinthispaper,andtheirsuperscriptletterindicatesthecasestudy(A–F)towhichtheyrefer.Abioticvariablesaffectingabioticvariablesareearthsciencequestionsandnotincludedhere.Onecanplacealliedfields,suchasbiogeography,asastripespanningtheabioticvariablesrunningacrossthewidthofthediagramandpalaeontologyacrossthebottomrow.Thisplacementshowsthatthereisclearlyoverlap,butthesefieldsdonotcoverthefullrangeofwhatweproposehere[Colourfigurecanbeviewedatwileyonlinelibrary.com]

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in Table 2. All these questions are “big” questions in the sensethat they have long been speculated about, in some cases for>100 years. For example, the question, “are closely related spe‐cieslikelytohavesimilarnichesandcompetemoreintenselywitheachother?”(Question15inTable2)washypothesizedbyDarwin(1859). All the listed questions remain largely unanswered (butseeBox1),becausescientistshavenotyetbridgedthedividebe‐tweenmacroecologyandmacroevolutionmethodologically.NotethatthestructureofFigure2naturallydividesthequestionsintothreecategories:wherecausalityflowsfromecologytoevolution,wherecausalityflowsfromevolutiontoecology,andcross‐cuttingquestionswheretheflowofcausalityisbidirectionalorcomplex,andTable2isorganizedaccordingly.Inthenextsection,wegivesomecase studiesof a subsetof thequestions toprovidemoredepth.

4  | C A SE STUDIES

Itisbeyondthescopeofthispapertoreviewexistingliteratureandhighlightthekeypathsforwardforall25questionslistedinTable2(andthecountlessothersthatwehavenotidentified,butwhichareequallyimportant).However,toprovidesomedepthandmakeourclaimofimportanceforthesemostlyunansweredquestionsmoreconcrete,wehighlightsixofthesequestions(inboldinFigure2andTable2,alsoseeFigure3)andbrieflyaddressthemascasestudies.

4.1 | Case study A (Question 1, Figure 3a): What ecological conditions enable radiations?

What ecological conditions promote or inhibit evolutionary di‐versification? Adaptive radiations occur when a clade rapidly

TA B L E 2  Alistof25importantquestionsattheinterfacebetweenmacroecologyandmacroevolution

Ecologicalfactorsaffectingevolution

1 What ecological conditions enable radiations? (Case study A)

2 How do diversification rates scale with topography? (Case study B)

3 Howdoesareaandisolationinfluencerelativeimportanceofspeciationandcolonization?

4 Dodiversificationratesvarywithcommonnessandrarity?

5 Howdoesdispersalaffectdiversification?

6 Doesspatialsortingleadtospeciationofgooddispersersmorethanpoordispersers?

7 Howdotheenvironmentandenvironmentalchangeaffectdiversificationrates?

8 Dotightlycoupledbioticinteractionsleadingtoco‐evolutionreflectasparallelphylogeniesintheinteractingtaxa?

9 Doesevolutionintonewhabitatsoccurfasterorslowerthanvicarianceeventsbetweenislands?

Evolutionaryfactorsaffectingecology

10 How do relative abundance patterns respond to macroevolution? (Case study C)

11 Are ecological interactions determined by shared evolutionary history? (Case study D)

12 Howdoesrelativeabundancepersistorchangethroughgeologicaltimeandacrossthetreeoflife?

13 Howdoesdispersalabilityevolveandchange?

14 Howdoesdiversificationaffectthenumberofinteractionsperspecies?

15 Arecloselyrelatedspeciesmorelikelytobesimilarinphenotypeandniche?

16 Overwhattime‐scalesdospeciesinteractionsremainstrong?

17 Arenichesandphenotypesstatic?Oriftheychangeovertime,dotheychangeinadirectional,randomorothersystematicfashion?

Cross‐cuttingquestions

18 What is the role of evolution in invasion? (Case study E)

19 Does diversity saturate in space and/or time? (Case study F)

20 Howdotherelativeratesofcolonizationversusspeciationinfluencealpha,betaandgammataxonomic,functionalandphylogeneticdiversity?

21 Whatistherelativeimportanceofenvironmentalheterogeneityandbioticheterogeneityinspeciationrates?

22 Doesdiversitybegetdiversity?

23 Howdotherelativeratesofcolonizationversusspeciationinfluencenichepackingandfilling?

24 Doesspeciationcreatenichesordoesemptynichespacedrivespeciation?

25 Whatistheinterplaybetweendiversificationandcoexistencemechanisms?

Note: Questionsinboldarecasestudiesthatareexpandedoninthemaintext.Cross‐cuttingquestionsinvolvediversity,whichistheonevariablecurrentlysharedbetweenmacroecologyandmacroevolution.ThesEcoEvoworkinggroupgeneratedthislistofquestionsduringaworkinggroupatsDiv.

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speciatesanddiversifiesintomanynovelniches,ofteninresponsetoecologicalopportunities(Schluter,2000).Theexistenceofdra‐maticallyspecies‐richadaptiveradiationsraisesthequestion,whatpropertiesofsystemswheretheseradiationsoccurpromotesuchdiversification?Conversely,aresystemswithlowspeciesrichness,often in harsh temperate areas and characterized by a few rep‐resentativesofdistantly relatedclades, limitedbydispersalovergeological time‐scalesor is theevolutionofnovel forms in suchlow‐richnesssystemslimitedbysomepropertyofthesesystems?

One long‐standing hypothesis for adaptive radiations is thattheecologyofinsularsystemsisdefinedbyreleaseofpopulationsfromtheirancestralpredators,parasitesand/orcompetitors(Losos,2010;Mahler, Revell,Glor,& Losos, 2010; Schluter, 2000; Stroud& Losos, 2016). Conversely, increased diversity in the tropics hasbeen attributed to increased, not decreased, interaction intensitybetweenanincreasednumberofinteractors(Gillespie,2004;Nosil&Crespi,2006).Clearly,ecologicaldriversofevolutionaryradiationexist,butwhichdirectionthosedriverspoint(fromincreasedinter‐action to diversity, or fromdecreased interaction to diversity) re‐mains unresolved.

Analternativebutcomplementaryperspectivepositsthateco‐logical stabilitycaneitherpromoteor inhibitdiversification. If thetropicshavemaintainedstableabioticconditions, thismight facili‐tateconsistentaccumulationofspecies(Jetz&Fine,2012;Pianka,1966). By the same argument, temperate areas, with frequent glacial–interglacialdisturbance,inhibitdiversification.Incontrast,ithasbeenhypothesizedrecently(Romingeretal.,2017)thatthenon‐equilibriumdynamicsofecosystemscouldprovidetheopportunity

forevolutionaryradiationstopermittherelaxationofthesystemsbacktoecologicalequilibrium. If insularsystemsquickly losetheirisolation(e.g.,throughhumanintroductionofnewspecies),thenre‐laxationcould insteadbeachievedby invasion (Helmus,Mahler,&Losos,2014).This couldhelp toexplainboth the incredible adap‐tive radiations on islands and the dramatic prevalence of invasivespecies.

4.2 | Case study B (Question 2, Figure 3b): How do diversification rates scale with topography?

Topographiccomplexity(ruggednessandelevationalrange)haslongbeenlinkedtohighstandingdiversityandtoprocessesofspeciation.Forexample,theAndesmountainsarehometothehighestdiversityinSouthAmericaforbothbirds(Rahbek&Graves,2001)andplants(Mutke,Sommer,Kreft,Kier,&Barthlott,),andalupinecladeintheAndeshasspeciatedatratesapproachingthoseofclassicislandra‐diations(Hughes&Eastwood,2006).Thegeologicalprocessesgen‐eratingoceanicislandslikewisecreatediverseandisolatedhabitats,longhypothesized to contribute todramatic radiations (Ricklefs&Cox,1972;Wilson,1961),asdoisolatedcontinentalmountaintops(sky islands; McCormack, Huang, Knowles, Gillespie, & Clague,2009).What ecological processes interactwith topographic com‐plexitytoleadultimatelytochangeddiversificationrates?

Topographiccomplexityinteractswithtwoecologicalpropertiesof species (dispersal ability and tolerance or niche breadth) to in‐fluenceevolutionaryprocesses.Specifically,moretopographiccom‐plexityandshorterdispersalandnarrowertolerances increasethe

F I G U R E 3  HypotheticalrelationshipsbetweendriverandresponsevariablesforsixcasestudiestakenfromTable2.ThefirstcolumnrepresentsCasestudiesAandB,whereecologicalfactorsprimarilyinfluenceevolutionarypatternsandprocesses.ThesecondcolumnrepresentsCasestudiesCandD,whereevolutionaryfactorsprimarilyinfluencetheecologicalprocess/pattern.Thethirdcolumnrepresentscross‐cuttingCasestudiesEandF,whichaddressecologicalandevolutionaryprocessesandfeedbacks[Colourfigurecanbeviewedatwileyonlinelibrary.com]

(c)(a) (e)

(d)(b) (f)

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possibilityoflocaladaptation,geneticisolationandensuingallopat‐ric speciationprocesses.The interactionsbetweenmountainsandchangingclimate (suchas thePlio‐Pleistoceneglacial–interglacials)can add to the environmental heterogeneity and local adaptationincreasing speciation (McCormack,Bowen,&Smith,2008;Rangeletal.,2018)butsimultaneouslymakeiteasiertotrackclimate,withshort‐range dispersal decreasing extinction risk (Colwell, Brehm,Cardelús,Gilman,&Longino,2008).

4.3 | Case study C (Question 10, Figure 3c): How do relative abundance patterns respond to macroevolution?

Dothediversificationprocessesthatproduceasetofspeciesinflu‐encetherelativeabundances[speciesabundancedistribution(SAD)]ofthosespecies?

ThereareseveraldevelopinglinesofevidencethatsuggesthighlevelsofdiversificationleadtomoreunevenSADs,withafewhy‐perdominantspeciesandmanyveryrarespecies.ThehighlydiverseAmazon rain forest showsextremehyperdominance:1.4%of treespecies in theAmazonaccount for half of all individuals,whereasmost remaining species are extremely rare (Slik et al., 2015; TerSteegeetal.,2013),andona50haplotonBarroColoradoIsland,2.9%ofspeciesmakeupapproximatelyhalfofallindividuals.

Speciesabundancedistributionsalsoseemtochangeshapewithgreatertimeavailableformacroevolution.Proportionatelymorerarespeciestendtobeinmorespecies‐richgeneraandfamilies(Harte,Rominger,&Zhang,2015).Theexactprocessesbywhichthisevo‐lutionary outcome (high standing species diversity) translates tothisparticular formofSAD isanopenquestion.Onepossibility isthat food‐web theorypredicts that higherdominance is expectedtoresultinmorestablecommunities(Emmerson&Yearsley,2004).Conversely, abundancecouldaffect speciation rates (Makarieva&Gorshkov,2004).Buthowalltheseecologicalfactorscause,orarecausedby,theevolutionaryprocesses leadingtohighdiversityre‐mainsanopenquestion.

4.4 | Case study D (Question 11, Figure 3d): Are ecological interactions determined by shared evolutionary history?

Therelativelyhighlevelofspecializationobservedinhost–parasite andplant–herbivoreinteractionnetworksbegsthefollowingques‐tion: at macroecological scales, are ecological interactions con‐strained primarily by their (co‐)evolutionary history or by theirecologicaldistance (i.e., a combinationofgeographical rangesandpreferredenvironmentalconditions)?

Consideringhost–parasiteinteractionsinparticular,ontheonehand, there is evidence that differences in parasite communitiesassociatedwithdifferenthostspeciesaredrivenbyenvironmentaldissimilarity and phylogenetic distances among hosts, but not bygeographicaldistance (Krasnovetal.,2010).This findinghasbeeninterpreted as evidence of environmental filtering acting on the

communityofparasitesatthe“macro”scale(Krasnovetal.,2014).On the other hand, there is evidence that differences in parasitecommunitiesacrosshostsaredrivenbyparasitegeographicalrangesandnotphylogeneticdistance,despiteastrongapparentsignalofphylogeneticconservatism[Calatayudetal.,2016;alsoseesimilarresults in insect–hostassociations(Nylinetal.,2018)].Thefieldofcommunity phylogenetics also touches on interactions betweenspecies basedon the amountof their sharedevolutionaryhistory(Cavender‐Bares,Ackerly,Baum,&Bazzaz,2004;Webbetal.,2002;butseecautionsinMayfield&Levine,2010).

Thiscasestudyisagoodexampleoftheinterrelationshipsamongthequestions.Question11framesthisasevolutiondrivingecology,butQuestion8isqualitativelythesamequestion,withecologydriv‐ing evolution.

4.5 | Case study E (Question 18, Figure 3e): What is the role of evolution in invasion?

Invasivespeciesareamajorcomponentofglobalchange(MilleniumEcosystem Assessment, 2005). Invasion is largely perceived as asolely ecological processdespite evolutionary studies (Roderick&Navajas,2003).Buttherearemanywaysinwhichinvasionandevo‐lutioninteract(Panteletal.,2017;Vermeij,1996),including,before,duringandaftertheinvasionevent.Focusingontheevolutionofacommunity before it is invaded, note that invasion and speciationaretheprimaryalternativesfornewspeciestocontributetofaunalbuild‐up and assembly. Towhat degree does having a communityprimarilyderived from invasiondiffer froma communityprimarilyderivedfromspeciation?

Rummel and Roughgarden ( , 1985) suggest that invasion‐ structuredcommunitiesaremoretightlypackedinnichespacebutless stableandmoreopen to invasion. In contrast, thedistinctionbetweeninvasionandevolutioninplacehasbeenoneofthemainargumentsinsupportofthenotionthatremoteislands(withbiotaassemblyprimarilydrivenbyspeciation)aremoresusceptibletoin‐vasion,althoughtestsofhighislandinvasibilitysuggestthatitmightberestrictedtotropicalislands(Turbelin,Malamud,&Francis,2017).Lookingat theroleofevolutionduring invasion,manyhavenotedthat thedegreeof fit of the invading species into theestablishedmorphospace(Moulton&Pimm,1983),thephylogeneticpositionoftheinvaderrelativetospecieswithwhichitwill interact(Pearse&Altermatt,2013)andthephylogeneticclade(Binggeli,1996)canallbepredictiveof invasionsuccess.Therearealso interestingques‐tionsconcerningtheevolutionaryresponseoftheinvaderandtheinvadedcommunityafteraninvasionevent.Forexample,ithasbeensuggestedthatinvasivespeciesmightbefreedfromtheirpredatorsand parasites (the ‘enemy release’ hypothesis; Keane & Crawley,2002), leading to potential evolutionary opportunities, includingthe possibility of “evolution of increased competitive ability” orEICA(Blossey&Notzold,1995),althoughtheevidenceisnotcon‐clusive (Willis,Memmott,&Forrester,2000).Theactofbeing in‐vasivemightalsoselectforindividualsthataresuccessfulinvaders,includingincreaseddispersalability(Phillips,Brown,Webb,&Shine,

     |  1933MCGILL et aL.

2006)or thenotion thatselectionduringan invasionmaybespa‐tiallystructured(e.g.,differentattheinvasionfront;Shine,Brown,&Phillips,2011)oradmixtures(geographicalhybrids;Krehenwinkel& Tautz, 2013). The species in the invaded community may alsoshow an evolutionary response to the invader (Goergen, Leger,&Espeland,2011)or exploit an invader as a resource (Carroll et al.,2005).Manyofthesequestionsarealsohighlyrelevantasclimatechangerearrangesspeciesthatco‐occurandleadstonon‐analoguecommunities.

4.6 | Case study F (Question 19, Figure 3f): Does diversity saturate in space and/or time?

Bothmacroecologyandmacroevolutionask thequestion, is thereanupperlimittodiversity?Macroecologiststendtofocusonspatialpatternsasanindicatorofsaturation(Figure3e).Oneclassicalap‐proach has been to ask how the size of the regional species poolinfluencesdiversityatlocalscales(Alroy,2018;Cornell&Harrison,2014; Harmon & Harrison, 2015; Mittelbach & Schemske, 2015;Pärtel,Zobel,Zobel,vanderMaarel,&Partel,1996;Ricklefs,1987).Incontrast,macroevolutionarystudiestendtofocusonsaturationof diversity through time (Etienne & Haegeman, 2012; Moen &Morlon,2014;Phillimore&Price,2008).Inthiscontext,saturationisrevealedbyaplateauofdiversityoverlongtime‐scales(Rabosky,2013;Rabosky&Lovette,2008;Sepkoski,1978),althoughaplateaucouldalsoindicateanequilibriumofspeciationandextinctionratesnotcausedbysaturation(Wagner,Harmon,&Seehausen,2014).Aunifiedapproachtosaturationoverspaceandtimewillrequirethefull integration of both ecological and evolutionary perspectives.Perhaps,forexample,localcommunitiescanbesaturatedovershorttime‐scales,butsuchsaturationbreaksdownoverlongtime‐scales,as evolution of novel traits and lifestyles allow coexistencewhennonewaspossiblebefore.

Wesuggestthatfuturestudiesshouldconsidersaturationfromboth temporal and spatial perspectives, unifying macroecologicalandmacroevolutionaryapproachestothiscrucialquestion.Twore‐centpapers,asimulation(Herrera‐Alsina,vanEls,&Etienne,2018)andanempiricalstudyofthefossilrecord(Closeetal.,2019),sug‐gest thatecologicalprocessesat localscalesmightconstrainmac‐roevolutionary processes of diversification and macroecologicalfactors,suchasspeciesrangesizes, takingplaceover largespatialandlongtemporalscales.

5  | CONCLUSIONS

The modern push to reconnect ecology to evolution (Hendry,2016;McPeek,2017) isoccurringpredominantlyatmicroscales,connecting microevolution (e.g., intraspecific phenotypic evolu‐tion)withmicroecology(e.g.,predator–preyspeciesinteractions).Darwinwouldneverhave attempted tounderstandonewithouttheother.Yetmacroecologyandmacroevolutionhavedevelopedlargelyindependently(butseeBox1)sincetheirconceptualization

(1975and1989,respectively).Giventhattherootsofthetwofieldshavebeensodistinctindataandquestions(Figure2;Table1),thefieldshavelargelyfunctionedindependently.However,aswehaveargued(Figure3;Table2),manyofthemostinterestingandimpor‐tantquestions spanboth fields andwill require synthesizing thedata,toolsandperspectivesofthetworesearchfieldstoproceed.We see signs of this happening. The British Ecological SocietySpecial InterestGrouponMacroecologyopenlyencouragespar‐ticipationby,andcontributionsfrom,bothmacroecologyandmac‐roevolution,asdoesthisjournal.Wehopethisconceptpiecewillprovidefurtherencouragementtothismuchneededunification.

ACKNOWLEDG MENTS

This paper is a joint effort of the working group sEcoEvo, kindlysupportedbysDiv,theSynthesisCentreoftheGermanCentreforIntegrativeBiodiversityResearch (iDiv),Halle‐Jena‐Leipzig, fundedby the German Research Foundation (FZT 118). Brian McGill ac‐knowledges US Department of Agriculture Hatch grant toMaineAgricultural and Forestry Experimental Station #1011538 andNationalScienceFoundationAdvances inBiological Infrastructuregrant#1660000.

ORCID

Brian J. McGill https://orcid.org/0000‐0002‐0850‐1913

Jonathan M. Chase https://orcid.org/0000‐0001‐5580‐4303

Brent C. Emerson https://orcid.org/0000‐0003‐4067‐9858

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How to cite this article:McGillBJ,ChaseJM,HortalJ,etal.Unifyingmacroecologyandmacroevolutiontoanswerfundamentalquestionsaboutbiodiversity.Global Ecol Biogeogr. 2019;28:1925–1936. https://doi.org/10.1111/geb.13020