Review
An
Ecological
and
Evolutionary
Framework
for
Commensalism
in
Anthropogenic
Environments
Ardern
Hulme-Beaman,
1,2,*
Keith
Dobney,
1,2Thomas
Cucchi,
1,3and
Jeremy
B.
Searle
4Commensalismwithinanthropogenicenvironmentshasnotbeenextensively
discussed,despiteitsimpactonhumans,andthereisnoformalframeworkfor
assessing thisecological relationship in its variedforms. Here, we examine
commensalism in anthropogenic environments in detail, considering both
ecologicaland evolutionarydrivers.Themanyassumptions about
commen-salism and the nature of anthropogenic environments are discussed and
we highlight dependency as a key attribute of anthropogenic commensals
(anthrodependent taxa). We primarily focus on mammalian species in the
anthropogenic-commensalniche,butthetraitsdescribedandselective
pres-surespresented arelikely fundamentaltomany speciesengagedin intense
commensalrelationshipswithhumans.Furthermore,wedemonstratethatthis
largelyunderstudiedinteractionrepresentsanimportantopportunityto
inves-tigateevolutionaryprocessesinrapidlychangingenvironments.
WhyaFrameworkisNeeded
Commensaltaxa(seeGlossary)havebeenmajorcontributorstothehuman-mediated biodi-versitycrisis[1,2],areimplicatedinzoonoses[3],andwerepossiblesourcesofdomesticates
[4,5];thus, they have a profound impact onlife on Earth. However, many aspects ofthis relationship,andtheecologicalandevolutionaryprocessesassociatedwithcommensaltaxa, aresurprisinglypoorlyunderstood.Thisstemsfromthe seeminglysimpledefinitionof com-mensalism:arelationshipwhereonespeciesbenefits(+)andtheotherspeciesexperiencesno impact(0)[6].Observationsofanimalsbenefittingfromanthropogenicenvironmentsoften leadtotheconclusionthattheseanimalsareundergoingcommensal-specificevolution.There aremanyassumptionsassociatedwiththisevolutionaryprocess,whichwebreakdowninthis paper.Wecontendthatanthropogenicenvironmentsarehighlyunstableanddonotentirely buffercommensal species fromseasonality. Therefore, theevolution of commensal taxa is definedbytheirabilitytobecomedependentontheseunstableanthropogenicenvironments. Observationsofcommensalinteractionshaveledresearchersinfieldssuchasarchaeologyand studiesofdomesticationtocategorisespeciesascommensallydependent,butwithout pro-vidingawiderecologicalcontext.Forexample,becausethereiscurrentlynoadequate ecology-basedframeworkforcommensalevolution,theviewthatferaldogpopulationsarereasonable modelsfor‘proto-domestic’forms(e.g.,[4,7])hasnotbeenassessedwithsufficientrigour.The assumptionthatdomesticdogsderiveultimatelyfromcommensalwolves,thereforeremainsa premiseunderpinningmuchoftheresearchintodogdomestication(e.g.,[8]).Althoughwolves
Trends
The definition of commensal taxa shouldbebasedondependency. Theconceptofanthrodependenttaxa leadstonewspeciescategorisedas commensal.
Commensalsgiveinsightintoselective pressures in rapidly changing environments.
1
DepartmentofArchaeology,School ofGeosciences,Universityof Aberdeen,StMary'sBuilding, Aberdeen,AB243UF,UK 2
DepartmentofArchaeology,Classics andEgyptology,Universityof Liverpool,12–14AbercrombySquare, Liverpool,L697WZ,UK
3
MuséumNationald’HistoireNaturelle, CNRSUMR7209,Paris,France 4
DepartmentofEcologyand EvolutionaryBiology,Cornell University,CorsonHall,Ithaca, NY14853-2701,USA
*Correspondence:
[email protected] (A.Hulme-Beaman).
doengageincommensal relationships with humansas facultativescavengers (e.g., [9]), whetheritispossibleforasubgroupofwolves,priortodirecthumaninteraction,trulytobecome acommensaltaxonintheevolutionarysenseremainsuntested.
ANewFramework:AnthrodependentTaxa
A review of the current usageof the term ‘commensalism’ inanthropogenic environments highlightshowdependenceiscentraltotheunderstandingofcommensaltaxa.Here,weidentify theunpredictabilityandinstabilityoftheanthropogenicnicheastheprimaryselectivepressures involvedintheevolutionofcommensalspecies.Furthermore,wedemonstratethatanecological frameworkisrequiredto:(i)identifytheintensityoftherelationshipinordertodefineataxonas commensal;(ii)assessthecomplexitiesofecologicalsystemsassociatedwithcommensals;and (iii)assessselectivepressuresoncommensaltaxathatdrivetheirevolution.Weproposeanew termfororganismsthatmightrepresentthetypicalcommensalconditioninananthropogenic environment:‘anthrodependenttaxa’or‘anthrodependants’(Box1).
ANotSoSimpleRelationship
Theterm‘commensal’,denotingarelationship,hasastraightforwardmeaning[6].However, whenthetermisappliedtoataxon(e.g., torodents[10] ortoaso-called‘proto-domestic’ species[4]),itoftenmeanssomethingmorecomplex,reflectingboththeacquisitionofanew capabilitytoexploittheanthropogenic environmentandanassociatedrelianceuponit. Fur-thermore,astherelationshipbecomesmoreintense(oneofdependence),these‘commensal
Glossary
Adaptation:anevolutionaryprocess wherebyorganismsbecomebetter suitedtotheenvironmentsthey occupy.
Anthropogenicenvironment:an environmentthatiscreatedand maintainedbyhumans,suchthat naturalfluctuationsandseasonal changesarealtered.
Communitycomposition:therange ofspeciesthatcomprisea
communityoforganismsinanygiven environmentorecosystem. Facultativescavenger:ananimal thatoccasionallyandopportunistically partakesinscavenging;theyarenot dependentonscavengingfor survival.
Homerange:thearearegularly travelledbyananimalaspartofits routinebehaviour(i.e.,foraging, feeding,sleeping,andmating). Naturalenvironments:
environmentswherespeciesusethe environmentandfluctuateinnumbers inawayexpectedintheabsenceof orunderlittleinfluencefromhumans (notingthatalmostallenvironments arenowinfluencedbyhumans) Plasticity:aresponsetochanged environmentorcircumstancesthatis notfixedbythebiologyofthe organism(i.e.,byitsgenotypeor anatomy).Thiscanincludenotonly behaviouralchangesinanimals,but alsophysicalchangesdueto changesindevelopmentinresponse toenvironment.Aplasticresponse mightbeafirststageinadaptation. Selectivepressure:theextentto whichtraitsarefavoured(selected for)ordisfavoured(selectedagainst) inanygivenenvironment,resultingin adaptation(seeabove).
Taxon(plural:taxa):anevolutionary unit,suchasaspecies,family,or order.
Box1.Previously Used Definitions ofSpecies in AnthropogenicEnvironments (with Our Proposed
NewCategory*)
Commensaltaxa(com-:sharingand-mensa:table)
Commensalisminitsoriginalandsimplestformspecifiesarelationship,representedas+/0,wherebyoneorganism benefits(+) fromanotherwithoutcausing deleteriouseffectstotheother(0)[6].Asappliedtotaxa,ratherthan relationships,itoftenreferstospecieslivingwithinhouses[10,12].Moreprecisely,‘truecommensals’liveentirelyin houses,‘occasionalcommensals’movebetweenhousesandoutdoorhabitats,and‘obligatecommensals’arethose thatcanonlysurviveinanareabecauseoftheirabilitytooccupyhouses(e.g.,blackratsinnorthernEurope). Synanthropicandsynurbantaxa(syn-:together)
Thesetermsareusedinstudiesofspeciesthatcontinuetoliveinareasthatareoccupiedandalteredbyhumans[83,84]. Theycanincludebothobligate-commensalspeciesandalsospeciesnotdependenton,orevenparticularlybenefiting from,humans[83].Thesesynanthropicspeciesshowachangedlifestyleassociatedwithlivingincloseproximitywith humans(affectingbreedingcycles,territorialbehaviour,foragingbehaviour,diet,etc.[85,86]).Synanthropicisalsoused todescribeproto-commensalspeciesinarchaeology(e.g.,[87]).
Anthropophilictaxa(-phile:loverof)
Traditionallyappliedtoectoparasites,thistermhasincreasinglybeenusedinarchaeologytoindicatespeciesattractedto humanenvironmentsandactivities[4,88,89].Thiscanincludenotonlycommensalspecies,butalsospecies oppor-tunisticallybenefittingfromhumans,withoutdependence[90].
Domestictaxa(domus-:house)
Humansactivelybufferthesetaxafromexternalselectivepressures,enhancingsurvival,andbreeding.Therefore, humansreduceandsometimesremoveimpactsofnaturalevolutionaryprocessesonthesetaxaand,atmoreadvanced stagesofdomestication,humansdirectlycontroltheselectivepressures.
*Anthrodependenttaxa
Weproposethistermtorefertothosetaxathatmighthavehad,andcontinuetohave,acommensalrelationship(+/0), butaredefinedbytheirdependenceonanthropogenicresources,whichinsomecasescanhaveanegativeimpacton theironcecommensalpartner.
taxa’rarelyhaveaneutralimpactonhumans;forexample,theyconsumecrops,stealfood,and/ orharbourdisease[3,11](Box2).
Taxa categorised as ‘commensal’ are reasonably assumed to be exposed to selective pressuresrelatingtotheirexploitationoftheanthropogenicniche[12].However, justwhat the main characteristics of the anthropogenic niche are (beyond a simplistic view that it represents a concentration of resources associated in some way with humans) remains unexplored,andthishasledtofurtherbroad assumptionsbeingmadeaboutevolutionary pressuresonproposedcommensaltaxa(e.g. [8]).Beyondtheobvioussettingsof human-madestructuresandurbanenvironments,itmustalsoberecognisedthatagricultural environ-mentsarealsosubjecttounpredictableandunseasonalhumanactivity,resultingin‘unnatural’ availabilityofresources.Thesetoohavearangeofassociateddependenttaxa,often consid-ered‘pests’.Atlowdensities,suchtaxamightbeconsideredtoholdcommensalrelationships, but, as densities become higher, they might be viewed as competitors, although these categoriesare largely subjective. From an ecological and evolutionaryperspective, these competingtaxainhabitanunpredictableandfluctuatinganthropogenicenvironmentsimilarto thatexperiencedbymanycommensalsand,therefore,canbeconsideredanthrodependent withacommensalorigin.
TheNeedforaScalableTerm
Otherdiscrepanciesindefinitionsstemfromaresearchbiastowardssmall-bodiedanimalsliving inhuman-madestructures[10,12].Occupationofsuchstructuressetsanarbitrarydefinitionof ‘commensaltaxa’withtheresultthatcomparisons ofsimilarevolutionary processes experi-encedby large-bodiedspeciesareoverlooked.In thisway,aunifyingdefinitionand under-standing is needed of ‘commensal taxa’ that allows an evolutionary understanding and is transferablebetween taxa(withvarying bodyandhome-rangesizes) thatoccupy different anthropogenicenvironmentsandexploitdiverseanthropogenicresources.
Farmoreusefulistoconsidercommensalism(andotherrelatedtypesofspeciesinteraction)in terms of the degreeof dependence upon an anthropogenic niche (Figure 1). Dependency comeswithbothbenefitsandcosts,whichinturndrivetheevolutionofanthrodependenttaxa
[5].Examiningtheselectivepressuresstemmingfrombothbenefitsandcostsprovidesamore appropriate framework that allows detailed insight into evolutionary processes specifically associatedwithpast,present,andfutureanthropogenicenvironments.Onlybyinterrogating thearchaeologicalrecordwillwegainafullerunderstandingofthewaysuchtaxaevolveand adapt[13].
Box2.TheNatureofaRelationship:‘CommensalNeutrality’
Manyso-called‘commensal’specieshaveanythingbutaneutralrelationshipwithhumans[3].Theirroleasdisease vectorsmightbeconsideredakeynegativeimpact[11],butitisentirelyindirect,giventhatessentiallynoenergyis expendedtospreadthedisease(althoughparasite-inducedbehaviours exist [91]). Competitionforresources is understoodtobea–/–relationship[6],withmoreobviousdirectinteraction.However,thecomparisonbetweenthe impactofdiseaseandthedamagefromcompetitionisdifficulttoquantifyandmightsuggestthat,whenpresent,the indirectpathogen impact has a greater andmore acuteeffect than thedirectcompetition resulting from crop consumption[3].Also,shouldwetakeintoaccounttheabilityofhumanstomitigatesuchimpactswhenconsidering whetherarelationshipislargelyneutralorotherwise?Anotherquestionthatisraisedbythequantificationofinteractionsis whethernegativeinteractionsareoverridingandadditiveorwhethertheycanbebalancedbybeneficialactivities.Feral catsareapossiblecommensalspecies;theycarrytoxoplasmosis,adiseaseknowntoaffecthumans[91],buttheyalso consumeandregulatepopulationsofotherspeciesknowntocarrymanymorediseases[11].Feralcatsconsume competitorsofhumans(rodents),soifdiseaseisnotconsidered,doesthatthenmaketherelationshipmutual?Doesthe perceivedbeneficialbehaviourofferalcatsmitigatethenegativeimpacttheycanhaveonhumans?Ultimately,this extremelycomplexsetofimpactsaffectstheevolutionofallorganismsinvolvedbut,onanevolutionaryecologyscale,itis currentlyunquantifiable.Asaresult,itmightbebesttosimplycategorisetheseinteractionsasfluctuatingandcomplex ratherthantryingtodefinethemasnegativeorneutral.
Ability to compete in
local natural environments
Home-range anth ropogenic envir onment over
lap Anthropogenic resourceconsum
pon Hom e-range anthropogen ic environmen t overlap Anthropogen ic resource consumpon Hom e-range anthropogen ic environmen t overl ap Ant hropogenic re source consump on Home-ran ge anthr opogenic environmen
t overlap Anthropog enic resource consumpon
Ability to compete in
local natural environments
Ability to compete in
local natural environments
Ability to compete in
local natural environments
Anthropophilic populaons
(C) (D)
(A) (B)
Synanthropic populaons Anthropophobic populaons
Commensal and anthrodependent populaons
–
0
(E)
Consume resources and transmit diseases No impact or
factors balance
Nature of relaonships between anthrodependants and humans
Figure1.TheWayinwhichSpeciesInteractwithAnthropogenicEnvironmentsisBestConsideredata
PopulationLevel.Asaresult,differentpopulationsofthesamespeciescanholddifferentpositionswithinthis
con-ceptualisedschematicofinteractionswithanthropogenicenvironments.(A)Thedark-shadedcuberepresents obligate-commensalpopulationsthatarewhollydependentonanthropogenicenvironments,whilethelightercuberepresents commensalpopulationsthatarecompetitivelycapableinnaturalenvironments.(B)Anthropophilicpopulationsinclude facultativescavengers,whichregularlyconsumeanthropogenicresourcesbutdisplaybehaviourtosuggesttheyarenot whollydependentonhumans.(C)Synanthropicpopulationshavehomerangesthatoverlapextensivelywithanthropogenic environmentsbutotherwisedonotinteractgreatlywithanthropogenicresources.(D)Anthropophobicornatural popula-tionsavoidhome-rangeoverlapwithhumansanddonotconsumehumanresources.Thelightercubemightbeconsidered naturalspecialists,whilethedarkcubearenaturalgeneralists.(E)Thenewcategoryofcommensaltaxathatwepropose, anthrodependants,canaffecthumansindifferentways;weightingthenegativeandpositiveimpactsmightbedifficult.Here weproposehowanthrodependenttaxamightfallonascale.
TheAnthropogenic-CommensalNiche
Humanshavebeenactivelyalteringtheenvironmentaroundthemforthousandsofyearsinwhat canbeconsideredaformofnicheconstruction[14].Itisthisconstructedenvironment,andthe abundanceofresourceswithinit,towhichanthrodependenttaxahaveadaptedandthrived.The extentofanthropogenicenvironmentshasincreasedthroughtime[14],ashastheprevalenceof commensaltaxa[15].Theabilityofataxontomaintainaccesstoanthropogenicenvironments dictatesitssuccessandevolutionasananthrodependant.Inparticular,thisenvironmentisoften characterisedbyextremeandunpredictablefluctuationsofresourceavailabilityandnestsites
[12,16],characteristicsthatarefrequentlyoverlooked.
CostsinAnthropogenicEnvironments:WhyStorageDoesNotMitigateSeasonalityfor Anthrodependants
Itis oftenassumed that anthropogenic environmentsare morestable interms ofresource availabilitythanarenaturalenvironments[17].Thisisnotalwaysthecase[12];neitherwasit likelytohavebeensothroughoutthepast,whenwildorganismsfirstenteredtheanthropogenic niche[13,15,18].Humansradicallymodifytheirenvironmentatfrequentintervals,amplifyingthe seasonalvariabilityofagriculturallandscapesandquicklychangingurbansettingsin unpredict-ableways(Box3).
Agriculturalresourceavailabilityistiedtoseasonalcyclesandassociatedprocesses,suchas harvest,storage,andtrade(e.g.,[19]).Thesefactorsrapidlyaccentuateandthendramatically depleteresourceavailability.Harvestingresultsinrapiddepletionandrelocationofresources, whilestorageleadstotheirmassconcentration.Othermorecomplexsocioculturalfactors(e.g., tradeor conflict) can even removethe resource entirely and unpredictably (e.g., [20]). For humans,thesefactors(combinedwithsocialdistributionnetworks)helptomitigateseasonal fluctuationsinresourceavailability.Theconverseistrueforanthrodependants(particularlyona localscale) where these factors createan unstable and fluctuatingenvironment that affect animalsofvaryingbodysizesanddifferinggenerationtimesindifferentways.Forexample,a small number of house mice (Mus musculus) occupying an empty barn and feeding on resourcesinneighbouringareasmusthavethebehaviouralplasticitytocompeteandsurvive whenthereisamassinfluxofthesameorotherspeciesduringperiodsofstorage.Therefore, althoughagricultureandstoragemightappeartoalleviatefluctuationsintheenvironment,they
Box3.FluctuatingResources
Humanactivityinthelandscapegreatlyaltersthenormalseasonalcycleofresourceavailability,inbothagriculturaland urbanenvironments.Howthesefluctuationsquantitativelycomparewithnaturalenvironmentsshapesselective pres-suresoncommensalspecies.Withinurbanenvironments,refusefromhumansprovidesaregularsourceoffood[92].For example,perpersonperyearinNewYorkCity,peopledropapproximately2.6kgoffoodlitterinthestreets[76]and householdfoodwasteisrecordedtobeaminimumof50kgperpersonperyear[93],anunknownproportionofwhichis consumedbycommensalspecies.Fromagriculturalenvironments,cerealproductionatharvestiscarefullyrecorded (e.g.,bytheWorldBanki
),andstudiesestimatebothpre-andpost-harvestconsumptionofcerealby‘pest’speciesison average5–15%(e.g.,rodentdamage[3]).Withinnaturalenvironments,dataformast-fruitingyearsversus non-mast-fruitingyearsareavailableforvarioustreespecies(e.g.,beech[94]andoak[95]),asonespecificexampleofanaturalfood sourceforrodents.Innon-mastyears,fruitisscarcebyJanuary,whereasduringmastyears,storesoffruitlastthrough thewinteruntilthefollowingsummer.Mast-fruitingallowsyear-roundbreedingforsomespeciesofrodent[95].Asa generality,wesuggestresourcesfluctuateasfollows:
Urban(FigureIA):theseenvironmentsusedtovarysubstantiallybetweensettlementsbuthavebeenstabilisingover recentcenturies;havegreateravailabilityoffoodthaneitheragriculturalornaturalenvironments;produceaconstant leveloffoodwaste;andcanbeunpredictablyandrapidlydepletedatalocallevel.
Agricultural(FigureIB):theseenvironmentsusedtovarysubstantiallybetweenregionsbuthavebeenstabilisingover recentcenturies;accentuateseasonalvariationbetweensuperabundanceandcompletescarcity;producemorefood thannaturalenvironments;anddiversityofcropsand/orbiodiversityislow,whichresultsinshorterperiodsof resourceavailability.
Natural(FigureIC):theseenvironmentsarehighlyvariablebetweenhabitats;seasonalvariationisgenerally predict-able;mastfruiting(andotherlarge-scaleavailabilityoffood)occursoccasionally;andcatastrophicfluctuationsoccur infrequently.
canalsoexacerbatethemfromtheperspectiveoforganismsthatmaintainterritories,havesmall homeranges,andfarepoorlyunderinter-orintraspecificcompetition.
ResourceFluctuationsinUrbanEnvironments
Equally,urbanenvironmentshaveunnaturalresourceavailability.Althoughresourcesarelikely availableinsuperabundanceacrossseasons,physicalandsocialchanges(e.g.,duetobuilding technology,urbandecay,urbanredevelopment,wastemanagement,anddifferencesin socio-economicwasteproduction)canrapidlydepleteoncesuperabundantresources[2,20–22].By contrast,innaturalenvironmentswithgreaterbiodiversity,resourcesbecomeavailable season-ally.Therefore,speciesoccupyinganthropogenicenvironments(whetheragriculturalorurban) needspecifictraitstocopewithsuchdramaticfluctuationsinresources.
AccessingAnthropogenicResources OccupationDoesNotEqualDependence
If anthropogenic environments have abrupt boundaries, commensal taxa are unlikely to recognisethem.Animalinhabitantsofgardensandfarmlandinteractwithhumanresources
Spring Summer Autumn Winter Spring Summer Autumn Winter Spring Summer Autumn Winter Spring
Fruit-masng event Harvest Localised urban upheaval (C) (B) (A)
Spring Summer Autumn Winter Spring Summer Autumn Winter Spring Summer Autumn Winter Spring Spring Summer Autumn Winter Spring Summer Autumn Winter Spring Summer Autumn Winter Spring
Resources
Resources
Resources
Time
(e.g.,refuseandagriculturalproduce)todifferingdegrees.Therefore,existingdefinitionsof commensaltaxathatarebasedonoccupationofhumanstructuresarelikelytobe inappropri-ate(e.g.,[12]).Theydonotdenotedependency(e.g.,kestrelsroostinginbuildingsarenot dependent on those buildings [23]) and they are restricting whenexamining comparable evolutionary processes. How commensal taxa interact with and behave while accessing anthropogenic resources (e.g., home-range size, territoriality, and movement) provide far greaterinsightintotheirevolution.
ChangingMobilityPatterns:RodentsandFoxes
Aregular observation isthatindividualswithin commensalurban populations havereduced home ranges compared with members of rural populations, likely reflecting relative food availability[24–26].Housemice,thearchetypalcommensalspecies,canliveatextremelyhigh densities and often exclusively occupy human-made structures within urban environments
[12,25].However,thereisgoodevidencethatcropharvestingleadstothemigrationofhouse mice from agricultural environments to storage andurban areas [25], and even woodland habitats[27].Therefore,withmovementandshiftsinhomerange,urban,rural,andagricultural populationscanallactassourcepopulations,andselectivepressuresononegroupcanaffect others.
Largerodentspeciescapableofdispersingsubstantialdistances[e.g.,thebrownrat(Rattus norvegicus)] also have smaller home-range sizes in anthropogenic compared with natural environments [24]. Similar to commensal mice, many rat species migrate and travel long distancestoexploit anthropogenic resources [27].Farmland populations ofbrown rats can behighlydependentonanthropogenicresources,withnightlytrackingdatashowingindividuals travelling3–6kmtofeedatrefusesites[28].Althoughtheseanimalswouldnotbeconsidered commensalusingadefinitionofproximity,ifwerecognisethattheenvironmentandresources they dependupon are unpredictableand determinedby human activity, they can then be consideredanthrodependentorcommensaltaxa.Consideringtheminthiswaygivesusinsights intotheirevolutionandsuccess.
The red fox (Vulpes vulpes) represents a larger-bodied candidate for consideration as a commensalspecies[29,30].Ittooshows substantialvariabilityinhome-rangesizebetween natural,rural,andurbanareas[31].Urbanfoxesoftenhavedensiteslocatedontheperipheries oftheirhomeranges,withnocturnalterritoriesthatincludeurbanareaswheretheyfeed[32,33]. Thisoccursparticularlywherehumansareintolerantoffoxactivity[33].Therefore,urbanfoxes areanexampleofananimaldependentuponrefuseandassociatedvermin,butthatoftendonot occupydensiteswithinhumansettlementsorstructures.
OccupyingbutnotDependent
Dependencyonanthropogenicresourcesremainsakeydistinctionbetweencommensaltaxa andtaxathatmightbeconsideredsynanthropicoranthropophilicbecausetheyoccasionally holdasimplecommensal(+/0)relationship.Gardenbirdspeciesaresynanthropicand occa-sionallyanthropophilic,butdonotnecessarilydependontheanthropogenicenvironmentsince theymovefreelytoandfromneighbouringnaturalhabitats{e.g.,Europeanblackbirds(Turdus merula)[34] andblue tits (Cyanistes caeruleus) [35]}. Some ofthese species show plastic responsestoanthropogenicenvironments,butthesemightnotconstitutedependency(e.g., songpitchwhenexposedtotrafficnoise[36–38]).Thepointatwhichsuchtraitsdriveorganisms tobecome dependentcommensalsis onlynowbeing realisedand explored.For example, changesinreproductivecycleandsedentisminurban-andforest-livingEuropeanblackbirds indicatelocaladaptiontourbanmicroclimates[34].Theseurbanblackbirdsdepositlowerlevels offatthantheirforest-livingcounterparts,makingthemlesssuitedtomigration,butallowing themto reachsexualmaturitymorequickly [34].In thisinstance,it could bearguedthat a
synanthropicspeciesisdevelopingintoananthropophilicone,whichmighteventuallybecome ananthrodependentspecies.
BenefitsversusCostsandCompetitionintheCommensalNiche
Foranthrodependenttaxa,exploitationofanthropogenicresourcescannotbethoughtofonlyin termsofbenefits,because,withdependency,theorganismissubjecttomanycosts.Examining benefitversuscostprovidesevolutionaryinsights[12].
Communitycompositionofcommensalsmallmammalsacrosstheurban–rural–wildgradient demonstratesdifferencesintheabilityofspeciestocompetewitheachother[39].Variationin community composition of commensal species in human settlements over the long term illustrateshowchangesinbuildingmaterialsandstoragepracticesfavoursomespeciesover others{e.g.,changesfromwoodtoconcretecorrespondwithchangesinprevalenceofthree majorcommensalspecies:thearborealblackrat(Rattusrattus);thefossorialbrownrat;andthe crevice-dwellinghousemouse[40]}.Thisintensecompetitioninhighlyfluctuatingenvironments resultsinhighpopulationturnover[24,41–43].Therefore,thebenefitsofferedbytheoccasional superabundanceofresourcesareoffsetbytheunpredictabilityoftheenvironmenttheyoccupy andtheconstantandrapidchangeinlevelsandtypeofcompetitionassociatedwithaccessing thoseresources.
Colonisationof AnthropogenicEnvironments InvasiveProcesses
Commensalspecieslivinginanthropogenic environmentsareanalogoustoinvasive species colonisingandoccupyingnewlocations. Thegrowingdisciplineofinvasivebiologyseeksto identify andthen model commontraits among invasive species. Fluctuating anddisrupted environments,withunexploitedorsuperabundantresources,areparticularlypronetoinvasion
[44,45]andsuchcharacteristicsarealso commontoanthropogenic environments. Further-more,followingdisruptionsinanthropogenicenvironments,anthrodependentspecies recolo-nisehabitatssimilarlyto invasivespeciescolonisingnewenvironments. Invasivespeciesare generallyrapidbreederswithhighmortalityandshortlongevity,characteristicsthathelpmitigate againstsmallfoundingpopulations[46,47].Themostsuccessfulinvasivespeciesare consum-ersandoccupiersofmultiplelowertrophiclevels[48].Commensaltaxafitperfectlywiththis description.
InvasiveDoesNotEquatewithAnthrodependent
Most(ifnotall)commensalspeciesarealreadyconsideredhighlyinvasiveand,assuch,have driven studies on the theory behind invasive biology. They oftenbecome invasive in non-commensalenvironmentswhencompetitionislowandresourcesareunexploited(e.g.,rats onPacificislands[49]).However, notallinvasivespeciesarecommensal;therearemultiple invasivespeciesthatweredeliberatelyintroducedashumanfoodsources,forpestcontrol,orfor aestheticreasons,amongothers.Theseinvasivespecieshavelittlenaturalinclinationtoavail themselvesofanthropogenicresources(e.g.,smallIndianmongoose[50],stoat[51],camel[52], orEuropeanrabbit[53]).Studieshaveexamined howexoticspeciesofvarying competitive abilitiessuccessfullycolonise,withtheintroductionstagefoundtobemostcritical[44,54,55]. Theseprocessesarealsoparticularlyimportanttothesuccessofcommensalspecies. TraitSelectionDrivenbytheCommensalNiche
RecolonisationIsKey
Inahighlyfluctuatingenvironment,withintensecompetitionandrapidunpredictablechange, anthrodependenttaxafrequentlyrepopulateorrecoloniselocalenvironments.Therefore, fecun-dity dictates the success of these taxa because they must continually rebound from low numbers in a way that is comparable with the founding stage of invasion [56–58].
Anthrodependenttaxagenerallyconformwithwhatareconsideredr-selectedtraits,withhigh levelsoffecundity,rapidsexualmaturity,andcatastrophicmortality[47].Althoughr/K-selected traitsareasimplificationofreality[59],theextremesofabundanceandfluctuationsin anthro-pogenicenvironmentsleadtoanenvironmentbestsuitedtospeciesthatfittheparadigmof r-selection.
Housemiceareaperfectexample;withyear-roundbreedingandlargelitters[60,61],theyshow highlevelsofmortalityandwidelyfluctuatingpopulationsizes.Unsurprisingly,someofthemost successfulcommensaltaxa(e.g.,rats[2])arealsogeneralistomnivoresanddisplayapropensity fornovelfeedingbehaviour,dietaryplasticity,andconsumptionofarangeoflowertrophic-level resources[62],traitsalsopredictedbyfood-webmodellingofinvasivespecies[63].
CopingwithHighDensity
Highpopulationdensitycharacterisesoccupationofanthropogenicenvironmentsby commen-salspecies[25].Thishighpopulationdensityrequiresplasticityofterritorialbehaviour(Box4)and nest-siteselection [57]. Commensaltaxa,suchas house mice,display arange of different
Box4.TerritorialBehaviour
Withfluctuatingavailabilityofresources,commensalspeciesthatdonottypicallyformfixedfeedingterritorieswouldbe expectedtobeatanadvantage.Whenresourcesareinsuperabundanceandpopulationsreachcorrespondinglyhigh density,commensalrodentscanexhibitterritorialbehaviour,therebymonopolising resources[12].However, this behaviourisplasticand,atlowdensity,territoriesdissipate[12].Behaviourwillvarybetweenspeciesinthecommensal niche,butmaintainingforagingmobilityislikelytodictatetheviabilityofacommensalpopulationanditshouldnotbe assumedthatcommensalspeciesarehighlysedentary(e.g.,urbanfox[32,96]orbrownrats[28]).
Feralcatsanddogsdemonstratetheimportanceofterritorialbehaviourinacommensalsetting.Feraldogpopulationsin thecommensalniche(particularlythosecomprisingstraysandtheiroffspring)displaybothfeedingandbreedingterritorial behaviour(FigureIA),butshowlittle within-groupcooperationorsocialorganisation [9].Consequently,resource exploitationispoor,breedingisextensive,andpregnantfemalesandpupsreceivenopreferentialaccesstoresources [9].Thesepopulationsareonlymaintainedbyrecruitmentofnewstrays[9].Conversely,themostsuccessfulcommensal feralcatpopulationsshowadifferentsetofbehaviours:socialdominanceismaintainedbasedonindividualinteractions; grouplivingismaintained,andterritorialbehaviourisnotshownwithinthegroup[97](FigureIB).Youngandpregnant femalesaregivenpriorityaccesstofoodandshowngreatertolerance[97].Theseexamplesofferalcommensal populationsprovidemodelsforfurtherinvestigationintotheeffectsofbehaviouronspeciesoccupyingacommensal niche.Thedifferentstrategiesofferaldogsandcatsmightbesuccessfulunderdifferentcircumstances,accordingtothe rateofinterloperinfluxandlevelofresourceavailability.Exploringthecircumstancesunderwhichspeciescanbe successfulcommensalswillprovidewaystoassessthefeasibilityofthecommensalpathwaytodomesticationforthese species.Furthermore,exploringsuchdynamicscanhelpexplainwhysomesmallmammals identifiedasancient commensals(e.g.,specieswithintheCricetidaeandSoricidae[15])werelateroutcompetedbywhatarenowmodern commensalspecies(e.g.,housemice).
Key:
Building Refuse
FigureI.Territorialversus NonterritorialBehaviouralStrategies.(A)Territorial:withindividualshavingstatic
behaviours at different densities, from nomadism at low density to the formation of male-dominatedterritoriesathighdensity[12].Similarly,urbanfoxesadoptgrouplivingbehaviour athighdensity[64].Solitaryspecies(orthosethatcannotliveathighdensityduetoterritorial behaviour)areunlikelytofaresowellinfluctuatinganthropogenicenvironments.Behavioural traits, suchasgroup foragingand feedingplasticity,arealso highlyadvantageous(e.g., as observedinbrownandPacificrats[65,66]).
GeneticSignalsandSelectivePressuresof theCommensalNiche
Investigationof changing selectivepressures oncommensal taxa can beexploredthrough identificationofdiscretegeneticmarkersthroughtime,andthisiswheredetailedinterrogationof thearchaeologicalrecord(specificallyancientDNA)willproveinvaluable.However,itisunlikely traitswillbeidentifiableasmonogenic, sincemanylociaremorelikelyinvolved.Asaresult, genomeanalysisofcommensalspecies(incorporatingarchaeologicalmaterialwherepossible) willprovidethemostrobustandexplicitevidenceforadaptationtocommensalism. RapidlyChangingandLocalisedSelectivePressures
Anthropogenicenvironmentshavechangeddramaticallythroughtime,fromamosaicofdifferent croptypesandbuildingmethods[67]tomodernhomogeneousbuildingstyles[2]and large-scalemono-cropping[68].Therefore,itislikelythatanygeneticchangeslinkedwithadaptations tothecommensalnichemightvarybetweenlocalities,reflectingregionalhumanbehaviours, cultures,andtechnologies[2].However,manysynanthropicoranthropophilictaxawill experi-encesimilarlocalselectivepressuresasthosethataffectcommensaltaxa,sospecificgenetic signalsmightnotbeexclusivetocommensalspecies.Therefore,analysesincorporatingchange throughtimewillbeimportanttodistinguishbetweendifferentcategoriesoftaxaassociatedwith anthropogenicenvironments.
Manyoftheseadaptationsarecurrentlybetterknown fromsynanthropicandanthropophilic speciesthanforcommensals.Theseincludeimmunesystemresponsesinhigh-density pop-ulations[69], resistanceto pollutants andpoisons [70–72],anddietary [8] andbehavioural changes (e.g., to superabundance of food and high-densitypopulations [73]). Other traits specifictothecommensalniche(suchasthoseassociatedwithfecundity)willlikelybeselected for,butmanywillnotbemonogenic.Geneticvariantsassociatedwithspermquantityandquality willlikelybestronglyselectedforfromtheearliestdevelopmentofintensecommensal depen-denceduetohighpopulationdensities(e.g.,[74]),anaspectworthyoffurtherinvestigation. EffectsofHuman-MediatedDispersal
Itshouldalsobeexpectedthatcommensalspecies(particularlythoseofsmallbodysize)are likelyto exhibitincreased levels ofgene flow (where populations arelinked through human transport)thanthesameorsimilarspeciesoccupyingnaturalenvironments[75].Duetothese same transport networks, and the resulting regularity with which commensal species are introduced to new regionsand environments, it is likely thatmost commensal populations areexposedtointenseselectivepressuresrelatingtolocalenvironmentsandclimates(e.g., introductionoftropicalR.rattustotemperateclimatesofnorthernlatitudes[3,49]).Asaresult, examiningcommensalgenomesthroughtimewillalsoprovideinsightsintoadaptiveresponses torapidclimatechange.
DegreesofSeparation: CommensalCarnivoresandInsectivores
Theabilityofhighlycarnivorousspeciestooccupyanddependonacommensalnicheraisesa particularlyinterestingsetofquestions.Withcommensalpopulationsreachinghighdensitiesin man-madeenvironments,othertaxacanalsoexploitthatnichebypredatingthem.Sincethese predatorsaredependentonthisanthropogenicniche,theyshould(byextension)beconsidered anthrodependenttaxabyadegreeofseparation.Theybenefitfromthesuperabundanceofprey
inanthropogenicenvironmentsand(astheirpreyfluctuates)experiencethecostsof depen-denceonanthropogenicresources;asaresult,theylikelyundergosimilarselectivepressuresto anthrodependants.Forexample, anthropogenic habitatsalso attractmany arthropods[76], whicharereadilyconsumedbyinsectivores{e.g.,theAsianhouseshrew(Suncusmurinus)[77]}. Thisspeciesisgenerallyregardedascommensalduetotheiroccupationofhouses,butthey alsoexhibitasimilarsuiteoftraitstoothercommensalstomaintaindependencyonthisniche
[78].Bycontrast,urbanfoxesaregenerallyconsideredfacultativescavengers,buttheyalsohunt othercommensal taxaand, as previously demonstrated,might alsobe considered anthro-dependants[79].
Commensalrelationshipsbetweenhumansandcarnivores,intheformoffacultativescavenging, certainlydoexist(e.g.,wolvesscavengingrefuse[80]).Insomecases,carnivores(e.g.,cats[81]) mightbehighlydependentonhuntingothercommensalspecies.Thishas beenaparticular focusofarchaeologicalendeavour,specificallyinstudieswherecommensalismisproposedas an important pathway to animal domestication [4,5,8,81]. Assessing the intensity of that commensalrelationshipthroughearlyprehistory willbeimportanttoestablishwhetherthose relationshipswereopportunistic(and,therefore,anthropophilic),requiringdirecthuman involve-menttotransitiontodomestic,orwhethertheanthrodependenttaxonevolvedtoan intermedi-ate(‘proto-domestic’)stage.
ConcludingRemarks:ChangingFaceof Commensalism
Adependencyonanthropogenicenvironmentscanbeconsideredthebestindicatorof com-mensalstatusfortaxa.TheonsetofwhatisconsideredtheAnthropocenedemonstratesthe importanceofunderstandingthehumanroleincreatingandinfluencingenvironments[82],the natureofwhichneedsfurtherinvestigation.Whichmammalianspeciescomprisethedominant commensaland‘pest’species(i.e.,blackrats,brownrats,andhousemicetoday[3])hasthe potentialtochangerapidly,dependingonchangesinagriculturaltechnology,building technol-ogy,andclimate,andthis shouldbeexploredthrough adeeper temporal contextwith the archaeologicalrecord.Asanthropogenicenvironmentsbecomegloballymorehomogeneous, theymightenteranew,morestablephase,wherespecialistscanstarttoappear.However,for the moment, thosespecies that canbreed rapidly, liveat high density, and are generalist omnivoresappeartohavethegreatestadvantage.
Thereisgreatpotentialforadvancingourunderstandingofmultipleaspectsofecologicaland evolutionaryprocessesthroughthecomparativestudyofmodernandarchaeological commen-saltaxaandothertypesofanalysis(seeOutstandingQuestions).Commensaltaxarepresenta uniquetoolwithwhichtoinvestigateintenseselectivepressuresonspeciesinrapidlychanging environments.
Acknowledgements
WewouldliketothankJean-DenisVigne,membersoftheSearlelab,andSNEEBatCornellUniversityforastimulating environmentandmanyearlydiscussionsandcomments.WewouldalsoliketothankMaeveMcMahonforcommentson themanuscript.
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Dotheselectivepressuresassociated withdependencyonurbanandrural environments have commonalities and how docommensal and ‘pest’ speciesrespondtothem?
Howhasthecommensalcommunity compositionchanged overtime and canwepredicthowitmightchange inthefuture?
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