Convergence in Multispecies Interactions

12 Pages·2016·2 MB·English

by  Leonora S. Bittleston

Review
Convergence in Multispecies

Interactions
Leonora S. Bittleston,1,2,* Naomi E. Pierce,1,2

Aaron M. Ellison,1,3 and Anne Pringle4

The concepts of convergent evolution and community convergence highlight
Trends
how selective pressures can shape unrelated organisms or communities in
Wepresentaframeworkforexploring
similar ways. We propose a related concept, convergent interactions, to
how selection shapes multispecies

describe the independent evolution of multispecies interactions with similar associations.

physiologicalorecologicalfunctions.Afocusonconvergentinteractionsclari-
We provide examples of functional
fies how natural selection repeatedly favors particular kinds of associations
convergenceinspeciesinteractions.

among species. Characterizing convergent interactions in a comparative con-
Convergent interactions can be used
textislikelytofacilitatepredictionoftheecologicalrolesoforganisms(including
to predict the ecology of unknown
microbes)inmultispeciesinteractionsandselectivepressuresactinginpoorly sy mbioses .

understood or newly discovered multispecies systems. We illustrate the con-
Convergentinteractionscanhelpelu-
cept of convergent interactions with examples: vertebrates and their gut bac-
cidatetheecologicalrolesofmicrobes.
teria; ec tomycorrhiz ae;insect–fu ngal –bacterial i nteractions; pitc her-p lant food

webs; and ants and ant–plants.

Convergence in Evolution and Ecology

Thewordconvergencetypicallydescribesconvergentevolution,theindependentevolutionof

similartraitsindifferentlineagesresultingfromstrongselectivepressures:‘[a]nimals,belonging

totwomostdistinctlinesofdescent,mayreadilybecomeadaptedtosimilarconditions,andthus

assumeacloseexternalresemblance’[1].Althoughconvergentevolutionisprimarilyadescrip-

torofmorphologicalfeaturesofanimalsandplants,itcanbeusedtodescribemicrobesand

physiologicalprocessesaswell(e.g.,convergentevolutionoftranscriptionalregulationofgene

circuits in bacteriaandfungi; see[2]).

Convergenceisalsorecognizedinecologicalassemblages;forexample,inhigh-altitudeplant

communities of the Andes, Alps, and Himalayas [3]. The homogeneity of vegetation in geo-

graphicallydistantbiomeswasdiscussedearlyinthehistoryofecology[4,5].Theresemblance
1DepartmentofOrganismicand
of high-altitude plant communities, or whole communities of plants, birds, and lizards in the Evolutionary Bio logy,Harva rd

Mediterranean climates of California, Chile, South Africa, and the Mediterranean Basin, are University,16DivinityAvenue,
examples of co mmunity co nvergence, define d as the physio gnom ic s imilarity of asse mblage s of 2CMamusberuidmgeo ,f MC Ao m02p1a3ra8 t,i vUeSZAoology,
co-occurringplantsoranimalsresultingfromcomparablephysicalandbioticselectivepressures HarvardU niv ersity,26Ox fordStreet,
[6–8].Comm unityc on vergenc efocuses onc ommunitys tructure and functi onaltraits butdoes Cambrid ge,MA021 38 ,USA
3HarvardFo rest ,Harvar dUniversity,
notexplicitly investigateinteractions amongspecies.
324NorthMainStreet,Petersham,MA

01366,USA
Convergent Interactions 4Depar tmentsofBacteriologyand
Wedefinecon vergentinteractionsastheindependentemergenceofmultispeciesinteractions Botany, Unive rsit y of Wiscons in–
Madison,430LincolnDrive,Madison,
with similar physiological or ecological functions. We define ecological function as the role a WI53706 ,US A

speciesplaysinaninteraction,community,orecosystem;forexample,theexcretionofessential

aminoacidsbyanendosymbioticbacteriumorthedecompositionofdeadleavesbyaninsect
detritiv ore.O ur de finitionofconve rgentinter act ions ispurposefully b roada ndcan b eu sedto *Correspondence:
[email protected]
generate hypotheses about many kinds of ecological relationships. The concept might be (L.S.Bittleston).

TrendsinEcology&Evolution,April2016,Vol.31,No.4 http://dx.doi.org/10.1016/j.tree.2016.01.006 269

©2016ElsevierLtd.Allrightsreserved.
especially useful when thinking about symbioses and microbes; for example, the ecology of

microbial gut communities in independently evolved herbivores with similar gut morphology,

includingkangaroosandbighornsheep[9].Usingconvergentinteractionsasaframeworkfor

studyingassociationsislikelytobringnewclaritytonascentanddynamicstudiesofsymbioses

among microbesandotherorganisms(reviewed in [10]).

Convergentinteractionsareoftenassociatedwithconvergentlyevolvedmorphologicalstructures

andspecializedmorphologiescanaidintheidentificationofecologicalfunctions.Forexample,any

fungusforminga‘Hartignet’withinaroottipislikelytobeparticipatinginanectomycorrhizal(ECM)

mutualismwithaplant[11].Moreover,researchonconvergentinteractionsinonelocationcan

illuminatesimilarreciprocalselectivepressuresactinginanalogoussystems.Forexample,experi-

mentswithantsandant–plantsinAfricaarelikelytoinformourunderstandingofindependently

evolved ants and ant–plants in South America or Asia, not unlike using a ‘prior’ in Bayesian

inference.
Wesuggestthatexplicitlyrecognizingconvergentinteractionswillprovideaheuristicmethodto

predict: (i) the functions of multiple associated species, such as the metabolic capacities of

microbesinaherbivoregut;(ii)theecologicalroleofasymbiosisinvolvingnewlydiscoveredor

poorlydescribedspecies,suchasanECMsymbiosisrecentlyfoundinatropicalhabitat;and(iii)

selectivepressuresactinginonesystembasedondatafromadifferentsystem,suchasamong

ant–plantsfoundondifferentcontinents.Althoughconvergenceofmultispeciesinteractionshas

beenimplicitlydiscussedinrecentpapers(e.g.,[12–14]),theconcepthasneverbeforebeen

explicitly definedorformally explored.

Situating Convergent Interactions

Ouruseofconvergentinteractionsdiffersfromcurrentusesofconvergentevolutionandcommu-

nityconvergence.Convergentevolutionisdefinedstrictlybyphylogenyandconcernsindividual

species,notinteractions.Bycontrast,convergentinteractionsfocusontheecologyandbehaviors

ofmultipleinteractingspecies;moreover,theindependentevolutionofalloftheinteractingspecies

isnotrequired.Forexample,symbiosesoftwooakspecieswithdistantlyrelatedandindepen-

dentlyevolvedlineagesofECMfungi(e.g.,trufflesandboletes)canstillbeconsideredconvergent

althoughthecapacityoftheoakstoformECMassociationsisasynapomorphy:theassociated

fungievolvedtheECMhabitindependently.Communityconvergencedescribessimilaritiesinthe

distribution,diversity,andmorphologiesofgeographicallydisparatesetsofco-occurringspecies

inrelationtosimilaritiesoftheirhabitats(e.g.,shrubsorlizardsfromCaliforniaandChile[6,7])but

doesnotspecificallyaddressinterspecificinteractions.Typically,communityconvergencefocuses

onaparticularguild.Bycontrast,convergentinteractionsemphasizerelationshipsamongmultiple

organisms and trophic levels and often across different kingdoms. In certain circumstances,

convergentinteractionscanappearascommunityconvergence;forexample,ifthemammalian

gut is defined purely as a habitat and not as part of an organism. However, we think that an

association among living organisms (e.g., bacteria and a human gut) will have fundamentally

different evolutionary dynamics than an association of organisms with an abiotic environment

(e.g.,bacteriaandasewerpipe),becauseofthepotentialforcoevolution.

Adifferentframework,thegeographicmosaicofcoevolution,isusefulforunderstandinghow

natural selection and coevolutionary processes differ among populations [15]. By contrast,

convergentinteractions encompassinteractionsamonggroupsofdifferentspecies emerging

independently from different lineages and in different regions of the world (e.g., ant–plant

interactions in Africa, Southeast Asia, and South America). Convergent interaction takes a

broaderperspectivethanthegeographicmosaicofcoevolutionbecauseitcomparesdifferent

groups of species across regions; however, geographic mosaicsare likely toact within each

group ofspecies in aregion (e.g., within Kenyanant–plantinteractions).

270 TrendsinEcology&Evolution,April2016,Vol.31,No.4
(A) (B)

Figure1.ConvergentInteractionsin Ectomycorrhizaeand Ant–Plants.(A)Examplesofectomycorrhizalsym-

bioses.Left:Apinetree[Pinus(agymnosperm)]andthebasidiomyceteAmanita.Right:Southernbeech[Nothofagus(an

angiosperm)]andtheascomyceteElaphomyces.Althoughneitherthetreesnorthefungiarecloselyrelated,theroottips

(enlargedincircles)ofbothsymbioseshavesimilarmorphologies:amantleoffungalhyphaecoveringtheroot,highly

branched structures between root cells (the Hartig net), and extraradical mycelia extending from the mantles into
surroundin gsoils.(B) Examples ofa nt–pla ntsa ndplan t–ant s.Le ft:Macarang a(Malpig hiales)and Crem atog aster(My rmi-

cinae).Right:Cecropia(Rosales)andAzteca(Dolichoderinae).Althoughneithertheplantsnortheantsarecloselyrelated,

bothtreeshavedomatiainhollowstemswhereantsrearlarvaeandtendhemipteransandbothproducefoodbodies

consumedbyants.Inturn,theantsprotecttheirtreesfromherbivores.IllustrationsbyL.S.Bittleston.

Last, convergent interactions also differ from analyses of phylogenetic community ecology.

Phylogenetic community ecology examines how species are phylogenetically and phenotypi-

cally clustered or over-dispersed within a community and typically explores whether these

patternsarecausedbycompetitionorevolutionaryconvergenceofsimilartraits[16].Analysesof

phylogenetic community ecology are normally performed within one phylogenetic clade and

mostoftenwithinaparticularregion;oaktreesinFloridaisasalientexample[17].Bycontrast,an

analysisofconvergentinteractionsmightcomparetheinterspecificinteractionsoforganismsof

differentphylogeneticcladesacrossgeographicallydistantsystems;forexample,amongtrees

andECM symbionts fromNorth AmericaandAustralia(Figure1A).

Convergentevolutionisbestunderstoodinaphylogeneticframework,wheretraitevolutioncan

betracedthroughancestralnodesandtheindependenceofaparticulartraitcanbeexplored

[18,19]. However, the ancestral nodes of entire communities (however defined) cannot be

modeledwithphylogeniesbecauseofthecontinualexchangeofspeciesamonghabitatswithin

aregion[20].Norcaninteractionsbemodeledwithphylogenies,unlesstheinteractionsinvolve

hosts and symbionts with strict vertical transmission [21]. Methods for assessing convergent

evolutionorcommunityconvergencecanbeappliedtoconvergentinteractionsonlywhenone

setofinteractingpartnersisreducedtocontinuoustraits(Boxes1and2).Networkanalyseswith

dynamicmodelsthatallowcoevolutionamonginteractingspeciesmightbeusefulavenuesfor

developing futuremethods toassessconvergentinteractions (Box2).

Examples of Convergent Interactions

Todeveloptheconceptofconvergentinteractions,wediscussfiveexamplesinvolvingmicrobial

symbioses, mutualisms, and trophic interactions. The examples illustrate how convergent

interactions can be used to predict species’ functions, ecological relationships, and selective

pressuresinnovelsystems.Becauseweareinterestedinconvergence,wefocusonsimilarities

among the interactions; however, documenting differences will also be useful, particularly for

understandinghowphylogeneticconstraintsactwithinevolutionarylineages(seeOutstanding

Questions).Wenotethat,inanydiscussionofconvergence,‘similarity’requirescleardefinition

[8]. At fine scales, for example when species are identified, communities might appear to be

random assemblages [22], but at coarser scales, for example when functional groups are

TrendsinEcology&Evolution,April2016,Vol.31,No.4 271
Box1.ToolsandMetricsforIdentifyingConvergentInteractions

Insomecases,differentgroupsofinteractingorganismsdonotsharecommonancestorsandconvergentinteractions
ar eobvi ous.In otherca ses,co nv ergentinte ractionsar ele ss obviou sbutcan beidenti fied usingacom binationof

ecologicalandphylogeneticmethods.

Method1:NaturalHistory

Thesimplestwaytoidentifyconvergentinteractionsistodescribe:(i)theinteraction;(ii)thespeciesinvolved;and(iii)the
relat ionships amo ng species ofeachinte ractinggrou p. Fo rexample ,i nter actionsofa nt– plan ts(from 19differe ntfa mil ies)
andtheirant inhabita nts(from fived ifferentsub families )inv olvethee xchangeof ne stingspac eand fo odforpr otection

fromherbivores.Phylogeneticallyindependentassociationsarefoundondifferentcontinents(Figure1).Thecommon

ancestorofMacarangaandCecropiatreeswasnotamyrmecophyteandthecommonancestorofCrematogasterand

Aztecaantswasnotanobligatetree-associatedant.Eachinteractionevolvedindependently.

Method2:PhylogeneticMolecularDatingAnalysis

Phylogeneticmethodsarecriticalfordatingtherelativeagesofcladesandcanbeusedtoidentifyconvergentinteractions.A

necessarypostulateisthataninteractioncannotevolvebeforetheinteractingorganismsexist.Certaincladesoffungi,for
exampleth eCanthar ell ales, ev olvedbefor etheap pearan ceofpi nes orflowering plantsinth erosi dclade [36](Fig ur eI).Pin es
androsid sd onotsharean ECMan cestor but plantsfrom ea chcla de areECM .There fo rep ine–C anth arella lessym b ioses
mus thave evo lved inde pen dentl yfromro sid– Cantha rellal essym bios es. Aphyl ogenyofa garicomycetefungi andplants
identi fiesat leasteig htindependen torigi nsofassociationsbe tweenAgaric o mycotaand an giospermsand sixin depe ndent

originsbetweenAgricomycotaandgymnosperms[36](FigureI).Phylogeneticdatingisstraightforwardwheninteractions
involve twoorga nismsbutmor edif ficulttousein syste msinv olv ingthreeorm oresp e cies.

Method3:Ordination

Ordinationcanidentifyconvergenceamongmicrobialcommunitiesandtheirhostsbyclusteringcommunitiesaccording

tofunctionalsimilarity(FigureII).Ordinationmethodsrequireinformationabout:(i)hosttaxonomy;(ii)hosttraits(e.g.,gut

morphology,fungalcultivation);and(iii)thepresence,abundance,andfunctionaltraitsofmicrobes.Clusterscanbe
identifiedvisu allyan dtestedusi ngp erm uta tionalmulti variateanalys iso fvariance [77].W h encommu nitiesass ocia ted

withhostsfromdifferentlineagesclustertogetheraccordingtoaconvergenthosttrait,theinteractionsofthehostsand

theircommunitiesarerecognizedasconvergent[14](FigureII).

ECM
Separate origins of + - Agaricales
angiosperm ECM in
Agaricomycetes ++ -- Boletales
Separate origins of ++ -- Russulales
A
gymnosperm ECM -- Polyporales ga
in Agaricomycetes ++ Thelephorales rico
m
++ -- Hymenochaetales yce
te
++ -- Phallomyce(cid:2)dae s
++ -- Cantharellales
++ -- Sebacinales
-- Tremellomycetes
A
n
++ -- Rosids gio
-- Rhododendron sperm
++ -- Pinaceae speGyms
-- Ephedra rmsno-
Earliest possible origin
of gymnosperm ECM Earliest possible origin
of angiosperm ECM
Time
FigureI.MultipleIndependentEvolutionsofEctomycorrhizal(ECM)Symbioses.Multipleindependentorigins

of ECM associations between agaricomycete fungi and angiosperms or gymnosperms (yellow or orange stars,

respectively).Rosidsandpinesdonotshareacommonancestorassociatedwithectomycorrhizalfungiandasthese

taxaevolvedaftercertaincladesofectomycorrhizalagaricomycetefungi,thesymbioticinteractionsmusthavearisen

independently.Modifedfrom[36]underCreativeCommonsAttribution(CC-BY)License©2009HibbettandMatheny.

272 TrendsinEcology&Evolution,April2016,Vol.31,No.4
(A)
Pfam
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Hemiptera
Coleoptera (dendroctonus, xyleborinus)
Hymenoptera (attine ants)
Lepidoptera
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Figure II. Functional Convergence in Bacterial Communities of Fungus-Growing Insects. Metagenomic
function al profiles of b acterial commun itie s associat ed with converg en tly evolved insect–fu ngal sym bioses cluster

separately from environmental or other host-associated communities. (A) Principal coordinate analysis of bacterial
community meta genomesanno tate dusin gtheProteinFam ilies(Pfam)dat aba se.(B)Sim plifiedphyl ogenyof sel ectinsect
orders.Ord ersincludingin sectswith insec t–fu ngalsy mbioses shown in(A)are hig hlightedi nblue.Mo dif edfrom [14]
underC reative Common sAttrib ution –Noncommerc ial–ShareA like3.0 U npo rted license© 20 14Ay lwardet al.

identified,convergentpatternsemerge[23].Weidentifytheappropriatescaleandmeasureof

similarity foreachexample.

Ourfirstthreeexamplesfocusonassociationsbetweenmicroorganismsandanimalsorplants.

Moleculartechniqueshavegreatlyincreasedourknowledgeofmicrobialdiversityandfunctions.

Forexample,wenowknowthat:gutbacteriainfluencehumanweight,nutrition,andimmune

function[24];bacterialandyeastendosymbiontsprovideinsectswithnutritionandprotection

(reviewed in [25]); and fungal endophytes deter plant pathogens and herbivores [26–28].

However,mostoftheworld'smicrobes–andtheirinteractionsandfunctions–remaindifficult

tocharacterize.Afocusonconvergentinteractionswillgeneratehypothesestoexplainobserved

patterns ofmicrobial species diversityandfunction.

Bacterial Communities in Vertebrate Guts

Bacterialcommunitiesinvertebrategutsillustratehowconvergentinteractionscanbeused

toestimatecommunitycompositionandfunctionalrepertoirebasedonthemorphologyand

diet of an animal. Gut bacteria living within the digestive systems of animals assist in the

digestion of complex carbohydrates, provide vitamins, detoxify compounds, facilitate the

maturation of the vertebrate immune system, and protect against some pathogens by

interfering with other microbes [29]. Among vertebrates, mammals (especially herbivorous

ruminants)haveparticularlydenseanddiversecommunitiesofgutmicrobes.Theancestors

TrendsinEcology&Evolution,April2016,Vol.31,No.4 273
Box2.PotentialMethodsforExploringPatternsofConvergentInteractions

Withsufficientdata,recentlydevelopedmethodsformappingtraitevolutionontophylogenies[78]orforquantifyingthe

strength of convergent evolution [79] might emerge as useful resources for identifying and measuring convergent
interactio ns .However, tousethe seto ols,o neseto fint eractin gpartners mu stberedefi ned asatraito finterestor

measureofdiversity.Forexample,continuousfunctionaltraits(e.g.,cellulosedegradation)andbacterialgutcommunity

diversitymeasures(e.g.,phylogeneticbetadiversity)couldbemappedontoahostphylogeny(e.g.,mammals)using
SURFAC E[78].SU RFAC Eidentifiesco nverg entevolu tionary re gimesand then u sess imulations totes twhetherth ereis

moreconvergencethanwouldbeexpectedbychance.Usingthisapproach,onecouldtestwhetherherbivoreshave

associatedconvergentlywithbacterialcommunitieshavinghighcellulose-degradationcapacities.Addingtherecently
developed Wheatsheafin dexc anenabl equantificatio nofthe stren gthofconvergenceby measuring phenoty pic similarity

whilepenalizingforphylogeneticrelatedness[79].

Networkanalysescanalsobeusedtodescribeconvergentpatternsofinteractionsacrossmultispeciescommunities.To

date,analysesexploringconvergenceacrossmultiplenetworkshavefocusedonverybroadnetworkstructure;for
exam ple,when lookingat differentkinds ofnetw orks,pla nt–animal mutua listicnetw or ksare more highlynes tedthanfo od

websregardlessofthetypeofmutualism[80].Withinnetworks,selectiononacomplementarytraitbetweentrophic

levelscanleadtotraitconvergencewithinatrophiclevel[81].Theconnectionbetweencoevolutionandtraitconvergence

inmutualisticnetworksiscomplex,withresultsdependingonthestrengthofselection[82].Similarnetworkapproaches

arelikelytobeextendabletocomparisonsacrossmultiplenetworkstoidentifyconvergentinteractionswheredifferent

speciesindifferentsystemshavesimilarfunctionalroles.Forexample,twosystemswithconvergentinteractionsmight
havene tw orktopo logiestha tare mores imilarthan expe cted bychanc eal one,ifdif feren torganisms fulfillingthe same

ecosystemfunctionexhibitsimilarmeasuresofcentrality.

Advancesinmetagenomicsequencingandstableisotopeanalysis(particularlystableisotopeprobing[83])canprovide
additional inf ormationonfu nctionalgen esa ndtrop hicleve lsforsm all,difficult-t o-obse rveorg anismss uch asm icrobes

andinvertebrates[84,85].Newtechnologiesandemergingprotocolsshouldallowmicrobestobeincorporatedinto

existingfoodwebsofplantsandanimals,whichcanthenbeusedtoexploreconvergenceacrossentireecosystem

networks.
of mammals were carnivorous [30], but the herbivorous habit is extremely successful:80%

of mammals alive today are herbivores, with herbivores present in 11 of 20 mammalian

orders [30].

Communitiesofgutbacteriainmammalsdifferfromfree-livingmicrobialcommunitiesandreflect

phylogenetic history, morphology, and host diet [9,31]. Among herbivorous mammals, gut

morphology is correlated with fecal microbiota composition: foregut and hindgut fermenters

have different microbial communities, regardless of the hosts’ evolutionary relationships [31].

Whileforegutfermentationevolvedseparatelyinungulates,rodents,marsupials,primates,and

birds[30],thebacterialgutcommunityofthehoatzin(theonlyavianforegutfermenter)ismore

similartothegutcommunityofacowthanitistothatofachicken[32].Ant-andtermite-eating

vertebrates similarly show convergence of gut microbial communities; in this case, diet is

probably the major influence [33]. Gut microbiomes are strongly influenced by both gut

morphologyandhostdietanddistantlyrelated hostswithsimilardiets tendtoindependently

acquire organismsfromthe same bacterial phyla[31].

Doesrelatednesstranslatetofunction?Thefunctionalrepertoiresoffecalbacteriaisolatedfrom

herbivores and carnivores can be predicted from phylogenetic measurements of bacterial

species assemblages [12]. Gut microbiota of herbivores predominantly produce enzymes for

aminoacidbiosynthesis,whereasgutmicrobiotaofcarnivoresproducemoreenzymesinvolved

in amino acid degradation. Bacteria from herbivores, even independently evolved herbivores,

generallybuildaminoacids;conversely,bacteriafromcarnivoresgenerallybreakdownproteins

[12].Host dietappears tocause convergenceof functionaswell asidentity.

Convergentinteractionsareabetterdescriptoroftheserelationshipsthancommunityconver-

gence. Analysis with community convergence would omit the functional nature of the inter-

actions while focusing on environmental filtering of otherwise randomly assembled groups of

species.
274 TrendsinEcology&Evolution,April2016,Vol.31,No.4
Ectomycorrhizae
Ectomycorrhizaeillustratehowmorphologiescanbeusedtoidentifyconvergentinteractions,

evenwhentheassociationsinvolveundescribedspecies.Mycorrhizaearesymbiosesbetween

fungiandplants:thefungisupplyscarceresourcestoplantsinexchangeforcarbon[11].ECM

associationsinvolvebothascomyceteandbasidiomycetefungiandarefoundineveryterrestrial

ecosystem.
ECM symbioses evolved as recently as 50Mya [34,35]. The associations evolved repeatedly

andindependentlyintheascomycetesandbasidiomycetes[11];inthelatter,ECMassociations

evolvedatleast14timesinatleasteightorders(Box1).Amongthese14origins,eightofthede

novo symbiosesinvolved angiospermswhereas sixinvolved gymnosperms [36].

Despite their independent origins, and in line with the concept of convergent interactions,

ECMmorphologyisconvergentacrosslineages(Figure1A).ECMassociationsaredefinedby

threefeatures:(i)afungalsheathormantlearoundaroot;(ii)anetworkofhyphae(theHartig

net)withintheepidermalandcorticalcellsoftheroot;and(iii)amyceliumextendingfromthe

rootthroughsoil[11].Oncethediagnosticmorphologiesofectomycorrhizaearerecognized,

broadaspectsoftheplant–fungalmetabolicexchangeareclear,eveniftheparticularspecies

are undescribed. Thus, recognition of ECM morphologies facilitates the discovery of mutu-

alismsinvolvingundescribedspeciesoffungi,especiallywherebiodiversityispoorlycharac-

terized (e.g., [37]).

Fungus-Growing InsectsandAntibiotic-Producing Bacteria

Insects that grow fungi and use antibiotic-producing bacteria to defend their gardens from

antagonisticorganismsillustratethatthepresenceof‘thirdparties’inasymbiosiscanbeinferred

fromconvergentinteractions.Speciesofants,beetles,termites,andgallmidgesallgrowfungi

asafoodsourceinenclosed‘garden’chambers.Associationsofinsectsandfungihaveevolved

repeatedlyandindependently,acrossdifferentordersofbothgroups[38].Intheseconvergent

interactions,fungiprovidenutritionandanestingsubstratefortheinsectswhileinsectsprovide

material for fungal decomposition, protected growing spaces, and transportation to new

locations.
Antibiotic-producingbacteriaareacommonthirdpartyassociatedwithfungus-growingants,

beetles, and termites. For example, ants have developed associations with Actinobacteria

multiple times, with independent acquisitions in two genera [39,40]. The Actinobacteria are

maintained on the ants’ cuticles and target the garden parasite Escovopsis [39–41]. Two

species of bark beetle also associate with Actinobacteria to suppress antagonistic fungi

[42,43]. A different bacterial lineage appears to play the same role within termite symbioses:

aBacillusspeciesinthephylumFirmicutesappearstoselectivelytargetfungiantagonistictothe

fungalcultivarfarmedbythetermiteMacrotermesnatalensis[44].Thefunctionalgeneprofilesof

thebacteriaassociatedwithfungus-growingants,beetles,andtermitesareconvergent[14]with

roughlyequivalentphysiologicalpotentials,althoughtheinsectsarefromthreedifferentorders

andthe fungalcultivars are fromtwodifferentphyla [14](Box1).

These independently evolved, close associations of fungus-growing insects and antifungal-

producingbacteriaprovideapowerfulmodelthatcanbeusedtounderstandothersymbioses.

Incontrasttothesymbiosesinvolvingants,beetles,andtermites,thefungus-growinghabitof

the gall midges (from the tribes Lasiopterini and Asphondyliini of the family Cecidomyiidae) is

poorlyunderstood.Gallmidgesassociatewithfungiinwhatarethoughttobeobligatenutritional

symbioses[45,46],butgallmidgesandtheir associatedfungiarerarelybeenstudied.None-

theless,convergentinteractionsamongbacteria,fungi,andants,beetles,ortermitessuggest

that selective antibiotic-producing bacteria will also be found in the fungal gardens of gall

TrendsinEcology&Evolution,April2016,Vol.31,No.4 275
midges. In these systems, convergence is defined as hosting bacterial taxa with a common

function: theproduction ofantimicrobial compounds capable ofprotecting a target cultivar.

Food Websin Carnivorous PitcherPlants

Foodwebsincarnivorouspitcherplantsenableustoexploreconvergentinteractionsamong

entire microecosystems. In three unrelated plant families on three different continents, the

pitcher-shaped carnivorous organs are formed from a single modified leaf [47,48]. Pitcher

plantsuseextrafloralnectariestoattractinsectprey.Thepitchershaveslipperyinteriorsurfaces

andenzymeswithinthepitchersdigestpreytoaccessresourcesthatotherwisearescarceinthe

low-nutrient soils where these species grow. Once the pitchers open, food webs of insects,

arachnids,protozoa,rotifers,bacteria,andfungiforminthewater-filledpoolsofmanypitcher

plantspecies [49].

Diverseorganismsliveinthepitchers;althoughmanyarehostspecific[50],theirfunctionsare

oftensimilar.Forexample,bothSarracenia(Ericales:Sarraceniaceae)andNepenthes(Caryo-

phyllales:Nepenthaceae)pitchershostpredators,filterfeeders,anddetritivores[51].Thefood

websofpitchersfromthesedifferentfamiliesondifferentcontinentsaremorelikeeachother

thantheyarelikethefoodwebsofotheraquaticmicrocosms,evenifthemicrocosmsareinthe

same habitat as the pitchers [50]. Convergence might be influenced by the plants’ internal

chemistry,whichissimilaramongallpitcherplantlineagesandiscontrolledtosomeextentby

the plant[51–53].

Pitchers are elegant models that can be used to test for convergent interactions among

microecosystems. For example, knowing that predators, filter feeders, and detritivores are

common to well-studied Sarracenia and Nepenthes species suggests hypotheses about the

presence,absence,andecologicalrelationshipsofcommunitiesnotonlywithinnewlydescribed

orpoorlystudiedpitcherplantspeciesbutalsoinotherphytotelms[54,55].Microbesactively

decomposecapturedpreyinSarraceniapurpureapitchers[52,56],whichislikelytoincrease

availableresources,andwehypothesizethatmicrobeswithsimilarfunctionalrepertoireswillbe

activeinthemicrobiomesofotherSarraceniaandNepenthesspeciesaswellasinthepitchersof

the rarely studied pitcher plant Cephalotus follicularis. As with the insect–fungal–bacterial

associations,convergentinteractionsinthesesystemsaredefinedbythepresenceorabsence

ofspecieswithaspecificfunctioninthefoodweb;likethebacterialcommunitiesofherbivore

guts, similarity can be measured using metabolic capacities, such as microbial enzymes for

protein decomposition.

Ant–Plant Mutualisms

Ant–plant mutualisms result from similar selective pressures. Ants have associated intimately

withplantssinceatleastthediversificationoffloweringplantsalmost100Mya[57,58].Different

groupsofplantshaveevolvedspecializedinteractionswithants,providingfoodandnestsitesin

exchangeforprotectionfromherbivores,pathogens,andcompetingplants[59].Morethan25%

ofallplantfamiliessecreteextrafloralnectarandplantsfromatleast20differentfamiliesproduce

hollowthornsorstems(‘domatia’)thatprovideantswithsuitablenestingsites;manyalsoare

provisioned with foodbodies rich in protein orfat[60].

Classicexamplesofant–plantsinclude:AfricanVachellia(Acacia)species,whichgrowlarge,

swollenthornstohouseantcolonies[61];SoutheastAsianMacarangaspecies,whichhost

antswithinhollowswollenstems[62,63];andneotropicalAcaciaandCecropiaspecies,which

have either swollen thorns similar to African Vachellia (Acacia) or hollow stems similar to

Macaranga [64] (Figure 1B and Box 1). Ant–plants tend to grow quickly and in high-light

environmentsandtheassociatedantstendtobeaggressivetowardotherorganisms,even

removingnearbyvegetationtoenablethehostplanttocompetemoreeffectivelyforlightand

276 TrendsinEcology&Evolution,April2016,Vol.31,No.4
space [65]. As with our example of convergent interactions among ectomycorrhizae, mor-

phologysignalsaparticularkindofant–plantinteraction:anewlydiscoveredspeciesofplant

withswollen,hollowstems,foodbodies,andextrafloralnectariesisverylikelytobeinalong-

termassociationwithants.

Becausethebenefitsandcostsofant–plantmutualismshavebeendemonstratedexperimen-

tallyinsomesystems,selectivepressuresshapingtheevolutionofant–plantsthathavenotyet

been investigated can be inferred [66]. For example, when the plant–ants Pseudomyrmex

ferrugineaarepresentonVachellia(Acacia)cornigera,theplantsexperiencedecreasedherbiv-

oryandincreasedsurvivalwhiletheantsgainnutritionandnestingspace[67].Antinhabitants

competefiercelyforcontrolofdomatiaandeasyaccesstofoodprovidedbyant–plants[59].

Hostingantscanbecostlyforplantsbecauseoftheresourcesdevotedtoproducingextrafloral

nectarandshelterstructures.Protectingplantsalsocanbecostlyforants.Someantsattack

herbivoressuchaselephantsthattheycannotkillandeat[68].Despitethesecosts,therepeated

evolutionofant–plantrelationshipsinalltropicalregionsoftheworldislikelytobecausedbythe

mutualstrongselectivepressuresofherbivoryonplantsandcompetitionforfoodandnesting

space onants[59].

Mechanisms Mediating the Emergence of Convergent Interactions

Whyandhowdoconvergentinteractionsemerge?Noorganismlivesinisolation,andmost

organismsrequireboththeirowngeneticinformationandfunctionsprovidedbyotherspecies

tosurviveandreproduce[69].Phylogeneticconstraintscanlimitpotentialtraitspace.Insome

circumstances,evolvingacloseinteractionwithanotherorganismwillbesimplerthanevolving

a new metabolic function. For example, prokaryotes are the only organisms able to make

nitrogenases, enabling them to fix atmospheric nitrogen [70]. Plants are generally nitrogen

limitedbuthaveneverevolvedtheabilitytofixnitrogen,probablybecauseofbothphylogenetic

andmetabolicconstraints.Instead,manyplantshaveevolvedsymbioseswithvariousgroups

of nitrogen-fixing bacteria [71] (Table 1). Evolving a symbiosis with bacteria appears to be

simplerthanevolvinganewmetabolicfunction.However,eventheevolutionofthesymbiosis

appearsconstrainedwithinsubsetsofthelargerphylogenyofplants.Althoughgreateraccess

tofixednitrogenwouldprobablyincreasethefitnessofmostplants,onlyfourordersofrosids

associatewithnitrogen-fixingbacteria[72].Constraintsontheevolutionofinteractionsremain

poorly understood (see Outstanding Questions). Dependence on another organism clearly

entailsrisks[73],butincertaincontextsthesamekindsofassociationsemergerepeatedlyand

independently. Exploring convergent interactions is likely to provide new insights into how

phylogenetic constraints have shaped and continue to shape the evolution of multispecies

associations.
Convergent interactions are unlikely to result from neutral, stochastic processes. Losos

discussesthreealternativemechanismsthatwouldresultinapparentconvergentevolution.

Traitsmightbeconvergentasaresultofcoincidence(aspuriouscorrelationduetorandom

chance) or exaptation (a feature that originally evolved in response to a different selective

pressure) or because traits are a correlated response to selection on a different character

(whensimilarconstraintsaresharedbytaxa,responsescanalsobeshared)[18].Anevolved

interaction between species is unlikely to result from random chance. While an interaction

maybeinterpretedasinvolvingexaptation (e.g.,mutualismshaveevolved from parasitisms

[74], symbionts have switched hosts [75]), if the same changes happen repeatedly and

independentlyamongdifferent,geographicallydisparategroupsoforganisms,naturalselec-

tion is likely to be at play. It is also difficult to imagine convergent interactions emerging as

a result of selection on correlated traits. Whether convergent interactions are ever the

result of neutral processes, however unlikely, remains an open question (see Outstanding

Questions).
TrendsinEcology&Evolution,April2016,Vol.31,No.4 277
Outstanding Questions
Table1.InAdditiontotheFiveExamplesDetailedin theText,Other PotentialExamplesof Convergent
Intera ctio ns Include the Fol lowin g Howcommonareconvergentinterac-
tions ?
Interaction Description

Rosidplantsand Plantsinfourordersoftherosidcladeofangiospermshaveclose,prolonged Whendoorganismsevolvethecapacity
nitroge n-fixin g associ ati onsw ithnitr og en-fi xing bacter ia intheAlphapr oteob acteria , forap art icularfunct ionver sus evolving

bacteria Betaproteobacteria,andActinobacteria[71].Thesingleevolutionofagene aninteractionwithadifferentorganism

necessaryfornodulationislikelytohaveallowedplantstoformassociationswith thatcanalreadyperformthatfunction?

bacteria[72]andthevariousphylaofbacteriaarelikelytohaveacquired

nitrogenasegenesviahorizontaltransmission[70];however,theinteractionsof Howoftenareconvergentinteractions

theplantswithdifferentgroupsofbacteriaseemtohaveemergedindependently. evolutionaryinnovationsandthecause

of increased niche breadth and per-
Differentfunctional Communitiesofparasitoid,pollinator,andgallerwaspsfromdifferentevolutionary
groupso fwasps lineageslivei nfi gsinAustr alia,Africa ,an dSou thAme rica [76]. haps, ultimately, adaptive radiations?
livingw ith infigs
How do the population dynamics of

Spongeswith Thedifferentmicrobialcommunitiesthatassociatewithdivergentgroupsof speciesaffecttheemergenceofconver-

bacterialsymbionts spongesarefunctionallyequivalent[13]. gentinteractions?Thedemographicsof

individuals among populations may
Plantpollination Plantsfromdifferentlineageshaveconvergedonfloraltraitsthatattractparticular
speed or slow the emergence of
syndromes groupsofpollinators.Arecentquantitativemeta-analysisfoundstrongevidence
thatpo llina tionsyndro m espred ictthemost efficientpollin ators,p articul arlywhen interactions.

pollinatorsarebats,bees,birds,ormoths[86].
Whatconstrainstheevolutionofconver-
Plantsproducing Oil-producingflowersevolvedatleast28timeswithin11differentplantfamilies gent interaction s? Does con ve rgence
floralo ilsand andoil-foragin gbehav iorevolv ed atle ast seven times wit hinbees [87]. requ ire particular envir onments; for

oil-collectingbees example, habitats lacking in a key

resource or traits with simple genetic
Manadrinbeio olurmgainneissmcesnt Bevioolluvmedininesdceepnetn sdyemnbtlyioisnefso uwritthel eboascttefirsiah ionr dtheer sV[ib88rio]annadceinaetw faomsiqlyu aidppfaemaril iteos h[8a9ve]. underpin ning s? H ow do org anisms’
developmental and phylogenetic con-
bacteria
straintsaffecttheemergenceofconver-

gentinteractions?

Concluding Remarks Can convergent interactions result

Interactionsw ithindifferentsystemscanbedefinedasconvergentiftheinteractions:(i)evolved solely from neutral processes?

independently;(ii)involveorganismsfromdifferenttrophiclevels;and(iii)arefunctionallysimilar. Whatcanwelearnfromidentifyingdif-

Convergentinteractionsareeasiertoidentifywhentheyarefoundingeographicallyseparated ferences among convergent interac-
ecosystems oroccuram ong organ ism swith conve rgent lye volved m orphologicalor ecological tions; for exampl e, differences among
ectomycorrhizal symbioses that have
traits (e.g., herbivores with hindguts,insects that grow fungi).
evolved independently?
Convergent interactions provide evidence that natural selection can repeatedly favor certain What new methods are required to
types of int erspecific re lationship s, and in fitne ss land scapes in volv ing multiple spec ies key identi fy, und erstand, a nd q uantify co n-
vergentinteractions?
interactions can represent adaptive peaks. Recognizing convergent interactions provides a

framework togenerate hypotheses aboutecological relationships amongpoorly studiedtaxa

andtoidentifypotentialselectivepressuresstructuringthediversityandfunctionofmultispecies

interactionsacrosskingdoms.Extrapolatingfromknowntounknownmightbemoststraight-

forward in systems where natural selection has reciprocally shaped all interacting parties, as

coevolving partners are likely to be exerting specific and similar selective pressures on each

other.
Ourexamplesreflectourownexperiencesworkingwithmicrobes,mutualisms,andfoodwebs,

buttheconceptofconvergentinteractionswillalsobeusefulforunderstandingothertypesof

interactions.Forexample,convergenceappearstobeafeatureofparasiticfigwaspcommuni-

tiesassociatedwithtreespeciesinAfrica,Australia,andAmerica[76](Table1).Speciesrichness

differsamongthedifferentcommunitiesbuttheproportionsofindividualinsectswithinvarious

functionalgroupsaresimilaracrossthecommunities,andthesethreegeographicallyseparated

multitrophic systems fit thedefinitionof convergentinteractions.

Convergent interactions provide a useful framework for interpreting recent discoveries of

functional convergence patterns, particularly those involving microbes and animals. For

278 TrendsinEcology&Evolution,April2016,Vol.31,No.4