Tansley review - popgen.wzw.tum.de€¦ · Tansley review Cospeciation vs host-shift speciation:...

Tansley review

Cospeciation vs host-shift speciation: methodsfor testing, evidence from natural associationsand relation to coevolution

Author for correspondence:D. M. de Vienne

Tel: +34 933 160 282

Email: [email protected]

Received: 22 November 2012Accepted: 19 December 2012

D. M. de Vienne1,2, G. Refr�egier3,4, M. L�opez-Villavicencio5, A. Tellier6,

M. E. Hood7 and T. Giraud8,9

1Centre for Genomic Regulation (CRG), Dr. Aiguader 88, 08003, Barcelona, Spain; 2Universitat Pompeu Fabra (UPF), 08003,

Barcelona, Spain; 3Universit�e Paris-Sud, Institut de G�en�etique et Microbiologie, UMR 8621, 91405, Orsay, France; 4CNRS,

UMR8621, 91405, Orsay, France; 5Mus�eumNational d’Histoire Naturelle, 57 rue Cuvier, F-75231, Paris Cedex 05, France; 6Section

of Population Genetics, Center of Life and Food Sciences Weihenstephan, Technische Universit€at M€unchen, D–85354, Freising,

Germany; 7Department of Biology, Amherst College, Amherst,MA,USA; 8Universit�e Paris-Sud, Ecologie, Syst�ematique et Evolution,

UMR 8079, 91405, Orsay, France; 9CNRS, UMR8079, 91405, Orsay, France

Contents

Summary 347

I. Introduction 348

II. Origin of the cospeciation concept 349

III. Theoretical framework andmethods for testing for cospeciation 349

IV. Studiesofnatural associations reveal theprevalenceofhost shifts 355

V. Relationship between host–symbiont coevolution and symbiontspeciation

378

VI. Conclusion 381

Acknowledgements 381

References 381

Glossary 379

New Phytologist (2013) 198: 347–385doi: 10.1111/nph.12150

Key words: co-cladogenesis, cophylogeneticanalysis, host-jump, host–pathogeninteraction, host-switch, PARAFIT, TREEFITTER,TREEMAP.

Summary

Hosts and their symbionts are involved in intimate physiological and ecological interactions. The

impact of these interactions on the evolution of each partner depends on the time-scale

considered. Short-term dynamics – ‘coevolution’ in the narrow sense – has been reviewed

elsewhere. We focus here on the long-term evolutionary dynamics of cospeciation and

speciation following host shifts. Whether hosts and their symbionts speciate in parallel, by

cospeciation, or through host shifts, is a key issue in host–symbiont evolution. In this review, we

first outline approaches to compare divergence between pairwise associated groups of species,

their advantages and pitfalls. We then consider recent insights into the long-term evolution of

host–parasite andhost–mutualist associationsby critically reviewing the literature.Weshowthat

convincing cases of cospeciation are rare (7%) and that cophylogenetic methods overestimate

the occurrence of such events. Finally, we examine the relationships between short-term

coevolutionary dynamics and long-term patterns of diversification in host–symbiont associa-

tions. We review theoretical and experimental studies showing that short-term dynamics can

foster parasite specialization, but that these events can occur following host shifts and do not

necessarily involve cospeciation. Overall, there is now substantial evidence to suggest that

coevolutionary dynamics of hosts and parasites do not favor long-term cospeciation.

� 2013 The Authors

New Phytologist� 2013 New Phytologist TrustNew Phytologist (2013) 198: 347–385 347

www.newphytologist.com

Review

I. Introduction

Interest in the reciprocal influences between hosts and symbiontshas recently increased because of the need to control devastatingdiseases, to identify or develop biocontrol agents against invasivepests, to improve agricultural production and to decipher theprocesses of diversification in symbiosis as a widespread lifestyle(Poulin&Morand, 2004). Host–symbiont interactions occur overshort time-scales, from a single disease cycle in the case ofopportunistic and transient infections by parasites, to very longtime-scales persisting over multiple host speciation events. Shorttime-scales have been associated with reciprocal selection pressurebetween host and parasite, leading to changes in allele frequenciesover successive generations (i.e. ‘coevolution’ in the narrow sense,Clayton&Moore, 1997; see Box 1 for glossary of terms used in thisreview). By contrast, long time-scales may encompass severalspeciation events. The concomitant occurrence of speciation inhosts and their symbionts is referred to as ‘cospeciation’ (Page,2003). However, the speciation of symbionts may occur indepen-dently of host speciation, often through host shifts as the symbiontcomes to occupy a new host environment in isolation from theancestral lineage. ‘Coevolution’ is used by some authors to describelong-term dynamics as a synonym for cospeciation but this usagemay be misleading, as pointed out by some authors (Smith et al.,2008a). We will therefore use ‘coevolution’ in the narrow sense

here: reciprocal selection pressure and resultingmicro-evolutionarychanges.

The often obligate and specialized interactions between hostsand symbionts suggest that any bifurcation of the host lineage islikely to result in the simultaneous isolation of its associatedsymbionts (Fig. 1a). Thus speciation in one lineage is then peggedto speciation in the other, and this process is referred to ascospeciation. Alternatively, new host–symbiont combinationsmayarise owing to movement and specialization of the symbiont to anew host, on which the symbiont’s immediate ancestor did notoccur. Symbiont speciation subsequent to such movement is oftenreferred to as ‘host-shift speciation’ (Fig. 1b, Agosta et al., 2010;Giraud et al., 2010).

In this review, we aim to: outline the origin of the concept ofcospeciation; provide a description of the various methodsdeveloped for determining whether cospeciation has actuallyoccurred, together with their advantages and pitfalls; criticallyreview recent inferences on the history of host–symbiont associ-ations based on these methods; and examine the relationshipbetween coevolution in its narrowest sense and symbiont specia-tion. We caution against the use of ‘coevolution’ as a synonym forcospeciation because of the implication that short-term dynamicscontributes directly to cospeciation in the long term, although therationale underlying this idea and its potential implications havenever been fully articulated. Indeed, recent studies comparing host

(a)

(b)

(c)

Fig. 1 Cophylogenetic patterns resulting fromdifferent types of parasite speciation. Blacklines represent the host lineages; red and bluelines represent parasite lineages. (a)Cospeciation resulting in congruentphylogenies. (b)Host-shift speciation resultingin congruent phylogenies, but with shorterbranches in theparasite lineages. (c)Host-shiftspeciations, resulting in incongruentphylogenies. (d) Cospeciation occurringtogetherwith intrahost speciation (also knownas duplication) and extinctions, resulting inincongruent phylogenies without any hostshift – a host shift can thus be replaced in areconciliation analysis by several independentevents of intrahost speciation and extinctions.

New Phytologist (2013) 198: 347–385 � 2013 The Authors

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Review Tansley reviewNewPhytologist348

and parasite phylogenies and theoretical developments relating toparasite specialization and speciation seem to argue againstcospeciation being the predominant mode of host and symbiontdiversification, despite the occurrence of reciprocal selection overshort time-scales.

II. Origin of the cospeciation concept

The idea of cospeciation was put forward in pioneering studies onavian parasites, such as those of Kellogg (1913) and Fahrenholz(1913), at the beginning of the 20th century. These authors notedthat closely related avian parasites, with similar phenotypic features,were associated with closely related host species. They proposed thefollowing hypothesis, known today as the Fahrenholz rule: ‘parasitephylogeny mirrors that of its host’ (1913). A similar principle wasproposed by Szidat some years later (1940): ‘primitive hosts harborprimitive parasites’. The idea was that similarity between theparasites of related hosts results from cospeciation (i.e. concurrentand interdependent bifurcation of host and parasite lineages),leading, in turn, to congruent host and parasite phylogenies.

The first studies referring to the Fahrenholz rule did not actuallytest cospeciation as a hypothesis. Without DNA sequencing beingpossible at the time it was therefore very important to obtain otherforms of phylogenetic information. The narrow host distributionof many animal parasites led researchers to use parasites ascharacters for inferring phylogenetic relationships between hosttaxa (Hoberg et al., 1997). Similar hypotheses were proposed forplant parasites (Savile, 1979). Conversely, host taxa were often usedas taxonomic criteria for the classification of parasites (see forexample Downey, 1962). In both cases, the phylogeny of onepartner was used to build the phylogeny of the other, so the twophylogenies tended to be congruent. As congruence between hostand parasite phylogenies was themost widely accepted criterion forinferring cospeciation, this led to the widespread belief thatcospeciation was common.

However, this reasoning is clearly circular and the evidence putforward for cospeciation in host–parasite associations was formanyyears inadequate. It was not until the late 1980s that robustphylogenies, built independently for hosts and parasites, were usedto test for cospeciation in a more specific manner (Hafner &Nadler, 1988).

III. Theoretical framework andmethods for testing forcospeciation

Macro-evolutionary aspects of host–parasite associations cannot beobserved within the lifespan of a researcher. Methods for inferringthe effects of interactions have thus been developed based oncomparisons of the phylogenies of the interacting species. Thesemethods, which are described as ‘cophylogenetic methods’, arebased on the idea that two interacting lineages will have completelycongruent phylogenies if they have diversified exclusively bycospeciation (Fig. 1a). However, it is important to note thatcongruent topologies can also be obtained after host shifts to closelyrelated hosts under certain realistic conditions of time-spanbetween host-switch and subsequent speciation (Fig. 1b, see de

Vienne et al., 2007b for details). Events that reduce the congruencebetween host and symbiont phylogenies include: (1) host-shiftspeciation (Fig. 1c), when a population of the symbiont speciesadapts to a new host followed by speciation (under certainconditions, see de Vienne et al., 2007b for details); (2) speciation ofthe symbiont without speciation of the host or host switching, alsoknown as intrahost speciation or duplication; and (3) symbiontextinction (Fig. 1d).

Cophylogenetic methods can be divided into two main classes(Table 1). The first class encompasses methods aiming to recon-struct the evolutionary history of the host and parasite lineages, toinfer the nature and frequency of different evolutionary scenariosby comparing phylogenetic trees (event-based methods). Diversi-fication by cospeciation is generally inferred if the number ofcospeciation events is significantly greater than the number ofcospeciation events inferred when randomizing the associations,although this merely indicates topological congruence and notnecessarily cospeciation. Significant congruence can indeed beobtained after repeated host shifts, as noted above (Fig. 1b). Thesecond class of methods tests the overall congruence between thehost and parasite phylogenies (i.e. topology or distance-basedmethods using the similarity and/or symmetry in the time ofdivergence between hosts and parasites) and it is generallyconsidered that high levels of congruence provide evidence offrequent cospeciation – although this conclusion may be similarlyunwarranted (Fig. 1b). We will explain these two approaches inmore detail in the following text and provide a brief overview of theexisting cophylogenetic tools (summarized in Table 1). Finally, wewill discuss some of the limitations of these methods in the light ofrecent results on the likelihood of host and parasite treescongruence in the absence of cospeciation.

1. Event-based methods

The first event-based method developed was Brooks’ ParsimonyAnalysis (BPA; Brooks, 1981). It opened the way for such methodsbut considered parasites as character states of the hosts. Theparasitic character states are assigned to each branch in the hostphylogeny and themost parsimonious reconstruction, the one withsmallest number of parasite presence vs absence state changes in thehost phylogeny, is retained. If host and parasite phylogenies aretopologically congruent, then each internal branch in the hostphylogeny is assigned one ‘parasite’ state so that no ‘state’ transitionis required and cospeciation is inferred along the whole phylogeny.Although BPA was widely used in the 1980s and early 1990s, itreceived heavy criticism, particularly because of its requirement fora large number of a posteriori interpretations (Page, 1994).

Another method, ‘reconciliation analysis’, proposed by Page(1990), considers parasites as evolutionary lineages rather thancharacter states. Implemented in the COMPONENT program (Page,1993), it estimates the minimum number of extinctions andintrahost speciations required to reconcile the separate host andparasite phylogenies. Cospeciation is explicitly considered as themost parsimonious hypothesis. Page (1994) subsequently addedhost-shift speciation in the TREEMAP 1 program. This method triesto reconcile host and parasite phylogenies by maximizing the


New Phytologist� 2013 New Phytologist TrustNew Phytologist (2013) 198: 347–385


NewPhytologist Tansley review Review 349

Tab

le1Methodsdev

eloped

forthereconstructionorinve

stigationofthehistory

oftheassociationbetweeninteractinghostan

dparasitespecies(orother

symbionts)

Even

t-based

methods

Basicconcept:consider

cospeciationas

themostparsimoniousexplanationforcongruen

cebetweenhostan

dparasitetrees

Method

Mainfeature

Software/

method

Estimationofthebestreconstruction

Advantages

Disad

vantages

Referen

ces

Availability

†

Brooks

Parsimony

analysis

Considersparasites

ascharacterstates

ofthehosts

BPA

Minim

um

number

of

characterstate

chan

ges

inthehost

phylogen

y(parsimony)

Can

han

dlemore

than

just

1:1

corresponden

cebetweenhostsan

dparasitetips

Multipleeq

uallyparsimonious

reconstructionsforlarge

phylogen

iesan

d/orformultiple

associationsbetweenhostan

dparasiteC

ospeciationconsidered

themostparsimonioushyp

othesis

Brooks

(1981);

Brooks

&McLen

nan

(1991)

Tobeim

plemen

tedby

theuser.Refer

toBrooks

etal.(2001)

fordetails

Reconciliation

analysis

Map

pingofthe

parasite

phylogen

yonto

thehost

phylogen

y.The

bestscen

ario

may

bethat

withthe

minim

um

number

ofeven

tsinferred

ortheleastcostly

Componen

tMinim

izationofthe

number

ofextinctions

andintrah

ost

speciationsan

dmaxim

izationofthe

number

of

cospeciations

Nohostshiftsconsidered

Cospeciationconsidered

themost

parsimonioushyp

othesis

Needs1:1

corresponden

cebetweenhostsan

dparasites

Pag

e(1993)

http://taxonomy.

zoology.gla.ac.uk/

rod/cpw.htm

l

TREEMAP1*

Minim

izationofthe

number

ofhostshifts

andmaxim

izationof

thenumber

of

cospeciations

Hostshiftsare

takeninto

account

Gives

agraphicalrepresentation

ofthehistory

ofthehost-parasite

association

Includes

atestto

assess

whether

thenumber

ofcospeciation

even

tsishigher

than

forrandom

phylogen

ies(thusalso

listedwith

topology-based

methods)


themost

parsimonioushyp

othesis

Thenumber

ofparasites

infecting

ancestralh

ostspeciescanbe

unreasonab

lyhigh

Can

giveavery

largenumber

of

reconstructions

Does

notguaran

teethat

reconstructionsinvo

lvingmore

than

onehostshiftarerealistic

(i.e.theremay

betiming

incompatibilities)

Needsone-to-one

corresponden

cebetweenhostan

dparasitetips

Pag

e(1994)

http://taxonomy.

zoology.gla.ac.uk/

rod/treem

ap.htm

l

TREEMAP2*

Minim

izationofthetotal

costofthe

reconstruction,acost

associated

witheach

even

t

Costisassociated

witheach

even

tImplemen

tationofthe‘ju

ngles’

method(Charleston,1998),an

algorithm

allowingtherapid

iden

tificationoftheoptimal

reconstructionstakingcostsinto

accountan

den

suringthefeasibility

ofeach

reconstruction


themost

parsimonioushyp

othesis

Veryslow

forlargetrees

Charleston(1998)

http://syd

ney.edu.

au/engineering/it/

~mcharles/

software/

treemap

/treemap

.htm

l

TARZAN

Possibility

ofdefi

ningthetimingof

nodes

intheparasitephylogen

yVery

fast

Does

notguaran

teethat

the

solutionisoptimal

Can

notalwaysfindasolution

even

when

thereisone


the

mostparsimonioushyp

othesis

Merkle&

Midden

dorf

(2005)

http://pacosy.

inform

atik.

uni-leipzig.de/

146-0-D

ownload

.htm

l

JANE

Possibility

ofdefi

ningthetimingof

nodes

inboth

theparasitean

dhost

phylogen

ies

Possibility

ofdefi

ningdifferenthost-

switch

costsindep

enden

tlyInteractive

graphicalinterface

Faster

than

TREEMAP2

Possibility

ofdefi

ningthemaxim

um

permittedhost-switch

distance

Slower

than

TARZAN


the

mostparsimonioushyp

othesis

Conowetal.(2010)

http://w

ww.cs.hmc.

edu/~

had

as/jan

e/Jane1

/index.htm

l

Cost-based

methods

Costassociated

witheach

even

t,nographical

representation

TREEFITTER

Minim

izationofthetotal

costofthe

reconstruction,acost

beingassociated

with

each

even

t

Probab

ility

associated

witheach

type

ofeven

tCostsofeach

even

taresetby

theuser


themost

parsimonioushyp

othesis

Cospeciationscannotbemore

costlythan

host-shift

speciations

Possibletimingincompatibilities

lead

ingto

potentiallyerroneo

us

conclusions

Ronquist(1995)

http://sourceforge.

net/projects/

treefitter/




Tab

le1(Continued

)

Even

t-based

methods

Basicconcept:consider

cospeciationas

themostparsimoniousexplanationforcongruen

cebetweenhostan

dparasitetrees

Method

Mainfeature

Software/

method

Estimationofthebestreconstruction

Advantages

Disad

vantages

Referen

ces

Availability

†

Bayesian

methods

Combinationoftw

omodels,one

estimatingthe

probab

ility

ofa

given

evolutionary

scen

ario

andone

usedto

inferhost

andparasite

phylogen

ies

Determines

themost

likelyevolutionary

scen

ario

lead

ingto

the

observed

hostan

dparasiteDNA

sequen

ces,nottheir

phylogen

ies

Does

notconsider

thephylogen

iesof

thehostan

dtheparasites

tobe

known


themost

parsimonioushyp

othesis

Onlyconsidershostshiftan

dcospeciation

Worksonlyfora1:1

corresponden

cebetweenhostan

dparasitetips

Huelsenbecketal.

(2000,2003)

Theo

retically,upon

requestto

author.

Butseem

sunavailable

Topologyan

ddistance-based

methods

Basicconcept:does

notconsider

anyeven

t.Thesearesimpletestsofindep

enden

ceorsimilarity

betweentreesoralignmen

ts

Method

Mainfeatures

Software/method

Inputdata

Advantages

Disad

vantages

Referen

ces

Availability

†

Testof

indep

enden

ceLo

oks

attheprobab

ility

ofobservingacertain

levelo

fcongruen

cebetweentw

otrees

withrespectto

expectationsifthe

treeswere

indep

enden

t

I congindex

Trees.Nobranch

lengths

Norandom

treesneedto

be

gen

erated

fortestingforhigher

levelsofcongruen

cethan

expectedbychan

ce

Worksonlyfora1:1

corresponden

cebetweenhostan

dparasitetipsC

onsiders

treesto

becorrect

deVienneetal.(2007a)

http://m

ax2.ese.

u-psud.fr/bases/

upresa/pag

es/

devienne/

Methodsbased

on

Man

teltestbetween-

distance

matrices

Sequen

cealignmen

ts(converted

into

distance

matrices)

Does

notaccountfor

phylogen

etic

nonindep

enden

ce(Felsenstein,1985)

Hafner

etal.(1994)

Tobeim

plemen

ted

bytheuser.Refer

toHafner

etal.(1994)

fordetails

PARAFIT

Trees

oralignmen

ts(converted

into

distance

matrices)

Notrestricted

to1:1

corresponden

cebetweenhost

andparasitesAllowstestingof

thecontributionofeach

individualhost-parasitelinkto

thetotalcongruen

cestatistic

(takinginto

accountboth

topologicalcongruen

cean

dbranch

lengths)

Does

notaccountfor

phylogen

etic

nonindep

enden

ce(Felsenstein,1985)

Considerstreesto

be

correct(iftreesused)

Legen

dre

etal.(2002)

Methodbased

on

Pearson’scorrelation

analysisbetweenhost

distancesan

dparasite

distances

Trees

oralignmen

ts(converted

into

distance

matrices)

Notrestricted

to1:1

corresponden

cebetweenhost

andparasitesApparen

tlymore

accurate

estimationofthe

contributionofeach

individual

host–p

arasitelinkto

thetotal

congruen

cethan

PARAFIT

Considerstreesto

be

correct(iftreesused)

Hommolaetal.(2009)

http://w

ww1.m

aths.

leed

s.ac.uk/

~kerstin/an

dHommolaetal.

(2009)

MRCAlinkalgorithm

Trees

Applicab

leto

methodslike

PARAFIT:makingitpossibleto

take

phylogen

etic

nonindep

enden

ceinto

account

Considerstreesto

be

correct

Schardletal.(2008)

http://cophylogen

y.net/research.php

TREEMAP1

Trees

Considerstreesto

be

correct

Pag

e(1994)

http://taxonomy.

zoology.gla.ac.uk/

rod/treem

ap.htm

lTREEMAPTREEMAP2

Trees

Based

onthe‘ju

ngles’

method.Severalrandomization

teststatistics

available

Considerstreesto

be

correct

Charleston(1998)

http://syd

ney.edu.

au/engineering/it/

~mcharles/

software/treemap

/treemap

.htm

l





number of cospeciations and minimizing the number of host-shiftspeciations. There are no constraints on the numbers of intrahostspeciations or extinctions or on numbers of parasites present oninternal nodes, so the number of parasites infecting ancestral hostspecies or number of intrahost speciations may be assumed to beunreasonably high (Refr�egier et al., 2008). A graphical represen-tation of the history of the host–parasite association is provided,although this representation is most often unlikely to be correct asexact costs for the events are impossible to assess a priori. TREEMAP 1also determines whether the number of cospeciation events in thehost and parasite trees compared is greater than that in randomphylogenies. This is the most useful part of the program, but it isoften taken as a test for cospeciation, while in fact it is a test oftopological congruence. Indeed, 100% of inferred events will becospeciations in cases of complete congruence, while this can resultfrom host-shift speciation (Fig. 1b, de Vienne et al., 2007b).Overall, reconciliation analyses overestimate cospeciation eventsbecause (1) they assume, a priori, that cospeciation is more likelythan host-shift speciation or other events – this assumption likelybeing unfounded (Ronquist, 1995) – and (2) they interpretcongruence as evidence for cospeciation,while this is not necessarilythe case (Fig. 1b).

The most recent version, TREEMAP 2, more rapidly identifiesoptimal phylogenetic reconstructions and takes into account thetemporal feasibility of each reconstruction (host shifts onlyoccurring between hosts present at the same time; for details onthe method and its implementation in TREEMAP 2, see Charleston,1998; Charleston & Perkins, 2003). Similar methods with fastercomputation have since been developed. TARZAN (Merkle &Middendorf, 2005) handles phylogenies by allowing uncertaintyon the age of parasite nodes (associating each node to a time zone)and selecting the cost of each event. JANE (Conow et al., 2010) takesinto account uncertainty in time for the host phylogeny withoutsubstantially increasing the computation time.

The first series of methods allowing the user to attribute a cost toeach evolutionary event (cospeciation, host-shift speciation, intra-host speciation and extinction) was developed by Ronquist (1995).These ‘cost-based’methods find themost parsimonious scenario byminimizing the total cost. The most popular cost-based method isthat implemented in TREEFITTER software (Ronquist, 1995).TREEFITTER estimates the number of events of each type that couldexplain the observed congruence between the two phylogenies. Itthen associates each event with the probability that it arose bychance, calculated by permutations of the host and/or parasiteleaves on the phylogeny. TREEFITTER finds the optimal numbers ofeach type of event by minimizing the total cost of the reconstruc-tion, but it does not allow cospeciations to bemore costly than host-shift speciation.

All the methods presented consider the host and parasitephylogenies to be known and fully resolved trees, and therefore theyare sensitive to the selection of different optimal trees. The Bayesianmethod developed by Huelsenbeck et al. (2000, 2003) overcomesthis problem. This method aims to determine the most likelyevolutionary scenario leading to the observed host and parasiteDNA sequences, rather than their phylogenies. It is based on twosimple stochastic models: one for host-shift speciations and theT

able1(Continued

)

Topologyan

ddistance-based

methods

Basicconcept:does

notconsider

anyeven

t.Thesearesimpletestsofindep

enden

ceorsimilarity

betweentreesoralignmen

ts

Method

Mainfeatures

Software/method

Inputdata

Advantages

Disad

vantages

Referen

ces

Availability

†

Testofsimilarity

oriden

tity

Estimates

theprobab

ility

ofobservingtheactual

hostan

dparasiteDNA

sequen

cevariation

assumingtheir

phylogen

iesare

congruen

t

Maxim

um

likelihood

method

Sequen

cealignmen

tsDoes

notconsider

thetreesto

be

known

Onlytopologiesare

considered

,notbranch

lengths

Huelsenbecketal.

(1997)

Theo

retically,upon

requestto

author.

Butseem

sunavailable

Bayesianmethod

Sequen

cealignmen

tsDoes

notconsider

thetreesto

be

known

Onlytopologiesare

considered

,notbranch

lengths

Huelsenbecketal.

(1997)

Theo

retically,upon

requestto

author.

Butseem

sunavailable

Secondmaxim

um

Likelihoodmethod

Sequen

cealignmen

tsDoes

notconsider

thetreesto

be

knownTestsfortemporal

congruen

ce,thenull

hyp

othesisbeingthat

the

speciationsoccurred

atthe

sametime

Huelsenbecketal.

(1997,2003)

Theo

retically,upon

requestto

author.

Butseem

sunavailable

*TREEMAPTREEMAPisalso

atopology-based

program.

†Allweb

siteslistedherehav

ebeenve

rified

atthedateofsubmissionofthepap

er.




other for DNA substitutions. The two models are mixed andsubjected to Bayesian analysis.

2. Topology- and distance-based methods

All the methods presented earlier and summarized at the top ofTable 1 are based on the idea that host and parasite phylogeniesshould be identical (congruent) in the absence of host-shiftspeciation, extinction and intrahost speciation. This is a logicalconclusion of the principles first formulated by Fahrenholz (1913)and Szidat (1940) (see Section II, Origin of the cospeciationconcept). Yet, host shifts can also lead to phylogenetic congruenceunder realistic conditions (Fig. 1b, see de Vienne et al., 2007b fordetails). Another set of methods is based on statistical tests forcongruence between host and parasite phylogenies. These methodsdo not directly consider high levels of congruence to constituteproof of cospeciation. Instead, they compare the probability ofobserving a certain level of congruence between two trees, withexpectations based on the independence between trees. By linkingthe results obtained with such methods to the common history ofthe interacting lineages it is possible to obtain an a posterioriinterpretation that is not integral to the test. This approach maythus be considered less biased than event-based or event- and cost-based methods, such as those already presented.

These methods can be assigned to different classes according tothenull hypothesis tested (similarityor independence,Huelsenbecket al., 2003) and the data used for the test (trees, distancematrices orraw sequence alignments; Light & Hafner, 2008). Tests ofindependence are based on comparisons of the topological orgenetic distances of the focal host–parasite association with adistribution of distances computed from a large number ofrandomly generated trees. If the distance of interest is significantlysmaller than expected by chance, the association is considered to besignificantly congruent. This principle is similar to that underlyingthe test implemented in TREEMAP 1.

One of the weaknesses of these methods lies in the large numberof random trees that must be generated de novo for each newcomparison of trees. A test of tree independence has been proposedto overcome this problem, being based on the use of previouslysimulated associations (de Vienne et al., 2007a, 2009a; Kupczok&von Haeseler, 2009).

Tests of independence have also been used to evaluate temporalcongruence in the speciation histories of hosts and parasites.Repeated cospeciation events imply the simultaneous occurrence ofspeciation events (i.e. temporal congruence) and thus proportionalbranch length and identical dates for the nodes in the phylogeniescompared (Fig. 1a). One method (Hafner et al., 1994) testswhether the two species have accumulated similar numbers ofgenetic differences. Input data include host–parasite speciesassociations and the alignment of one specific locus (or severalconcatenated loci) for hosts and parasites. These alignments areused to calculate distance matrices. The significance of thecorrelation between the two matrices is then assessed using aMantel test (Hafner et al., 1994). A second method comparesmatrices of branch lengths from host and parasite trees in the sameway (Hafner et al., 1994; Page, 1996). If molecular clocks are

available for both host and parasite it is possible to compare theestimated absolute ages of the nodes in the two trees. Thedetermination of identical ages for each node is actually the onlyway to establish cospeciation with confidence. Indeed, identicalrelative divergence times, as deduced from proportional branchlengths, may exist in some host–parasite associations in whichspeciation times are not identical. This can be the case whenparasites jump preferentially onto closely related hosts and take atime to speciate that is proportional to the phylogenetic distancebetween initial and novel hosts (Charleston & Robertson, 2002).Furthermore, while Mantel tests account for statistical noninde-pendence in matrices, they do not account for phylogeneticnonindependence (Felsenstein, 1985; illustrated in Fig. 2), in thatthe data for divergence at ancient nodes include the sameinformation as those for divergence at more recent nodes alongthe same branches (Felsenstein, 1985; Schardl et al., 2008). All thepoints used in the distance matrices are thus phylogeneticallynonindependent, which should preclude the use of a Mantel test.

PARAFIT (Legendre et al., 2002) tests the independence of hostand symbiont genetic or patristic distances (patristic distances arecalculated by summing the lengths of the branches in the estimatedtree, joining each pair of taxa). This method is advantageousbecause it can (1) deal with cases in which multiple symbionts areassociated with a single host, or where multiple hosts are associatedwith a single symbiont, and (2) be used to assess the contribution ofeach individual host–symbiont link to the total congruencestatistics. The host sequences and/or tree and the symbiontsequences and/or tree are transformed into distance matrices.A sumof the squared distances gives a value for the overall similaritybetween trees (ParafitGlobal), which is compared with a distribu-tion of ParafitGlobal values obtained by permutations to assesssignificance. The contribution of each individual link to the overallcongruence between trees is assessed by removing the links one byone. However, the problem of nonindependence of phylogenies(Fig. 2, Felsenstein, 1985) also applies to this method.

Hommola et al. (2009) recently introduced a new permutationmethod for evaluating the independence of host and parasitephylogenies. This test is based on the calculation of Pearson’scorrelation coefficients between host distances and parasite

Fig. 2 Illustration of the problem of phylogenetic nonindependence. Blacklines represent the host lineages; color lines represent the parasite lineages.Thephylogenetic distancebetween the taxaaandc is not independent of thephylogenetic distance between the taxa b and c, as a great proportion ofthese distances share an evolutionary history (in green). Similarly, thedistances between c and d, and between c and e count as twice the distancebetween c and the common ancestor of d and e (in blue). Such apseudoreplication can inflate the degree of congruence.





distances, considering all pairs of interacting hosts and parasites.This correlation coefficient is then compared with that obtainedafter random permutations of the data, retaining the observedinteraction links. Thismethod is thus a generalization of theManteltest, making it possible to test data in the absence of a one-to-onecorrespondence between hosts and parasites. This method seems tobe more powerful than PARAFIT, with more accurate estimatedP-values, although this superior performancemay be attributable tothe larger number of permutations performed (100 000, vs only 99for PARAFIT).

Finally, Schardl et al. (2008) proposed a modification forprograms such as PARAFIT, taking into account the nonindepen-dence of pairs of species from the same branch and using a methodsimilar to the phylogenetic independent contrasts (PIC) methodproposed by Felsenstein (1985). The algorithm, MRCAlink(MRCA for Most Recent Common Ancestor), identifies phylo-genetically independent pairs between host and parasite trees andthe reduced host and parasite matrices can then be compared.

3. Pitfalls in the theoretical framework when consideringhost–parasite associations

All the methods presented above and summarized in Table 1 havedrawbacks (Nieberding et al., 2010). These problems includetesting for congruence on the basis of estimated phylogenieswithout taking into account uncertainty in the inference (TREEMAP,TREEFITTER or Icong,which require fully resolved trees), phylogeneticnonindependence (TREEMAP, TREEFITTER), tests considering onlytopologies and thus ignoring branch lengths (Icong, Huelsenbeck’smethods) or underestimation of the potentially high probability ofhost-shift speciations (TREEMAP). A key issue that is rarely discussed(but see Hafner & Nadler, 1988; Hafner et al., 1994) is thecommon but potentially erroneous interpretation of these tests,specifically that congruence between host and parasite phylogeniesresults from frequent cospeciations between host and parasitephylogenies, whereas incongruence results from host-shift speci-ation, extinction, intrahost speciation and other evolutionaryscenarios.

A good illustration of the limitations of reconciliation methodswas provided by Lanterbecq et al. (2010), who reviewed studiesbased on the use of TREEMAP to reconstruct the history of host–parasite associations. Most of the examples in their Table 5(Lanterbecq et al. 2010) refer to studies in which host shifts wereeventually identified because of asynchronous splitting events as themainmode of parasite speciation, whereas the number of host shiftssuggested by TREEMAP was smaller than numbers of cospeciationevents. This was the case, for example, for legume-feeding insectsand plants of the Genistae (Percy et al., 2004), for which 16cospeciations and no host shifts were inferred and for algal andfungal mutualists (lichens, Piercey-Normore & DePriest, 2001),for which 10–11 cospeciations and 3–5 host shifts were inferred.This example also illustrates one of the greatest pitfalls of event-based methods (Fig. 3); the cospeciation events could only beinferred while assuming unreasonably large numbers of intrahostspeciations and sorting events (29 intrahost speciations and 220sorting events for the plant-insect interaction and 7–9 intrahost

speciations and65–81 sorting events for lichens). Similarly unlikelyinferences were also made in a cophylogenetic study betweenneobatrachian frogs and their parasitic platyhelminthes, for which22 cospeciations were estimated for 26 species pairs, but with 10intrahost speciations and 16 extinction events (Badets et al., 2011).The PARAFIT test was not significant and the tree node ages appearedto be inconsistent with cospeciations. The large number ofcospeciation events inferred was thus clearly misleading. Thedefault cost values for cospeciation, host-shift, intrahost speciationand sorting events in reconciliation methods thus bear littleresemblance to the actual probabilities of these events (see SectionIV Studies of natural associations reveal the prevalence of hostshifts). For example, if parasite extinction occurs in a host lineageand this host lineage is then recolonized through host-shiftspeciation, reconstructions by event-basedmethods tend to suggestthe occurrence of intrahost speciations in the distant past, followedby many extinction events (Fig. 1d). This tendency to avoidinferring host shift makes it necessary to include many moreevolutionary steps to reconcile the two phylogenies than recon-structions involving a host shift.

Experimental and theoretical studies have shown that congru-ence between host and parasite phylogenies can be achieved in theabsence of cospeciation if there is a preferential host shift towardsclosely related hosts (Charleston & Robertson, 2002) and undercertain conditions of time lag between the switch and the followingspeciation (Charleston & Robertson, 2002; de Vienne et al.,2007b; Fig. 1b). Preferential host shifts towards related hosts havebeen found using experimental cross-inoculations in many host–parasite associations (Gilbert & Webb, 2007; de Vienne et al.,2009b) and the possibility of topological congruence withoutcospeciation highlights the importance of testing temporalcongruence between host and parasite phylogenies, as only suchtests can validate the occurrence of cospeciation events (Charleston& Robertson, 2002; Hirose et al., 2005; Mikheyev et al., 2010).

Another pitfall of cophylogenetic studies is the failure to delimitspecies correctly as this may lead several methods to artificially

Fig. 3 Illustration of the recommended approach and pitfalls to avoid forinferring the history of host–parasite associations.




inflate congruence when generalist species are found on closelyrelated hosts (Refr�egier et al., 2008). Indeed, species delimitation inparasites is often difficult and generalist symbionts often infectclosely related hosts; congruent intraspecific nodes then artificiallyincrease the number of cospeciations inferred (Fig. 4). Multipleindividuals per parasite species are often included in analyses,particularly when these species are generalists (Light & Hafner,2007; Bruyndonckx et al., 2009), which can cause the same biastowards congruence.

A last issue in cophylogenetic studies is the frequent use ofmtDNA phylogenies. It is increasingly recognized that a singlemarker cannot reliably be used to reconstruct species phylogenies,and this is particularly true for mtDNA, which is more prone tointrogression than nuclear DNA (Coyne &Orr, 2004) and can besubject to strong selective pressures and low recombination rates(Balloux, 2010).

We present the approach we recommend to test for cospeciationin Fig. 3, to avoid as much as possible the different pitfallsdiscussed.

IV. Studies of natural associations reveal theprevalence of host shifts

The methods described earlier have been used in diverse host–parasite associations to test cospeciation hypotheses. After > 50 yrof research, convincing examples of cospeciation between host andsymbiont seem to be the exception rather than the rule. We haveperformed an extensive search in ISI Web of Knowledge, and wesummarize in Table 2 and Fig. 5 the studies reporting cophylogenyanalyses. We include the system and its type of symbiosis, theconclusion inferred by authors, the type of phylogenetic data, theresults of cophylogenetic analyses, the results of the test fortemporal congruence (when available) and our own conclusions.Convincing cospeciation between host and symbiont trees isseldom found except for a few mutualist associations, most ofteninvolving vertically transmitted symbionts. Host-shift speciationhas been recognized for some time as the main mode of speciationin many systems involving plant viruses, plant fungi, plant

parasitoids and animal viruses (Table 2, Fig. 5). Host shifts arealso frequent in phytophagous insects (for an extensive review seeNyman, 2010). In addition, we show here that even in associationswhere cospeciation has been claimed to occur together with otherevents, host shifts may be the only convincingly demonstratedmode of speciation. Indeed, in all these cases where absolute datescould be obtained, they indicated more recent speciation bysymbionts, even when cophylogenetic analyses suggested cospeci-ation as the major mode of diversification. Furthermore, thenumber of duplications inferred is more often unrealistically high,casting doubt on the conclusion of cospeciation (Table 2, Fig. 5).Indeed, when host-shifts are considered costly, theywill be replacedin most reconstructions by duplications and extinctions (Fig. 1d).

Examples in the literature are also found illustrating thatsignificant congruence between host and symbiont phylogeniesmay occur without cospeciation, by the preferential occurrence ofhost shifts between closely related hosts under certain conditions oftime lag between host shift and subsequent speciation. Indeed,most of the few studies in which absolute node dates were inferredhave shown the dates of speciation to be incongruent for theinteracting host and parasite species, despite the inference ofcospeciation events by topology-based analyses (Charleston &Robertson, 2002; Sorenson et al., 2004; Huyse & Volckaert,2005). Good illustrations are also found for our claim that merecorrelations between branch lengths without absolute calibrationsbased on fossils are not sufficient to show temporal congruence. Ina study analysing codivergence in a tritrophic association betweenPiper plants, Eoismoths and their Parapanteles parasitoids (Wilsonet al., 2012), the branch lengths of the phylogenies were found tobe significantly correlated, but dating analyses revealed that thecorrelation resulted from host conservationism (i.e. the mothradiated preferentially on closely related hosts after host shifts orclosely related moths radiated on the same hosts) rather thancodivergence. Another study has shown that correlations betweenbranch lengths of the phylogenies of Caryophyllaceous plants andtheir anther smut fungi most likely result from host shiftsoccurring preferentially between closely related hosts (Refr�egieret al., 2008).

The well-known association between pocket gophers and theirchewing lice (Hafner et al., 1994, 2003) remains the ‘textbookexample’ of cospeciation, and it played a central role in thedevelopment of themethods presented here. Interestingly, the highlevel of cospeciation in this system may be linked to the life historyand ecology of these parasites and their hosts: pocket gophers(Rodentia: Geomyidae) are herbivorous rodents that spendmost oftheir life in tunnels that they do not share with other individuals.Species of pocket gophers are mostly allopatric, decreasing thelikelihood of their parasites shifting to other hosts. Moreover, thechewing lice (family Trichodectidae) are obligate parasites thatspend their entire life on the host, with no dispersal stage (Reed &Hafner, 1997; Clayton et al., 2004). Experimental studies haveshown that lice can colonize new gopher species, suggesting thatlimited dispersal is the main constraint preventing host shifts. Thecombination of the solitary and allopatric host lifestyle and thelimited dispersal ability of the parasite may account for the rarity ofhost-shift speciation in this system (Clayton & Johnson, 2003;

Fig. 4 Illustration of the problem of sampling multiple individuals per(cryptic) species. Black lines represent the host lineages; red lines representthe parasite lineages. Host shifts are prevalent and result in incongruentphylogenies. However, the intraspecific nodes increase the congruencewithout representing cospeciation, only intraspecific divergence.





Tab

le2Literature

review

ofstudiesreportingcophylogen

yan

alyses,w

iththetypeofassociationas

weinferred

it,thehost–sym

biontsystem

,thetypeofsymbiont(parasiteormutualist),thenumber

of

taxa

analysed

,themethodsusedfortestingtopologicalincongruen

ce,themainconclusion(cospeciationvs

hostshift),thepercentageofcospeciationev

entsinferred

,datausedforthehostan

dsymbiont

phylogen

ies,temporalcongruen

ceforthenodes

ofthetw

ophylogen

iesan

dreference

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

1a

Dev

escovinid

flag

ellates

(Devescovinaspp.)

andBacteroidales

ectosymbionts

Codivergen

ceMutualisticterm

itegut

flag

ellatesan

dtheir

bacterialsymbionts

7pairsof

Dev

escovina

flag

ellatesan

dBacteroidales

ectosymbionts

TREEMAPTREEMAP

100%

codivergen

ceSS

UrRNAfor

flag

ellates.Fo

rbacteria:16S

Verygood

correlationofthe

hostan

dsymbiont

coalescenttimes

(r2=0.98),butno

absolute

calibration

Desaietal.

(2010)

1a

Trichonymphater

mitegutflag

ellates

andCan

didatus

bacteria

Codivergen

ceMutualisticterm

itegut

flag

ellatesan

dtheir

bacterial

endosymbionts

Flag

ellate

and

bacteriafrom

11

term

itespecies

TREEMAPTREEMAP

7/11cospeciation

even

tsFo

rboth:S

SUrRNAgen

esNottested

Iked

a-Ohtsubo&

Brune

(2009)

1a

Brachycaudus

aphids

andBuchnera

aphidicola

bacteria

Codivergen

ceVertically

tran

smitted

mutualisticbacteria

of

aphids

56specim

ensof

thehost

Brachycaudus,

representing27

species

TREEMAPTREEMAP

and

PARAFIT

34cospeciation

even

ts,1hostshift;

PARAFIT,also

indicated

significant

codivergen

ce

Forthebacteria:

TrpBan

dtw

ointergen

icregionsFo

rthe

host:CytB,COI

andITS2

Strongcorrelation

betweenthe

divergen

cesin

the

twolinea

ges,

(R=0.9455),the

y-intercep

twas

not

significantlydiffer

entfrom

0

Jousselin

etal.

(2009)

1a

Leafhoppers

(Cicad

ellinae

)an

dtheirtw

omain

symbionts:Sulcia

(Bacteroidetes)an

dBaumannia

(Prote

obacteria)

Codivergen

ceLe

afhoppersan

dtw

oen

dosymbiont

species

providingnutrients

29leafhoppers

speciesan

dtheir

symbionts

Parsimony-

based

ILD

test,

Shim

odaira–

Haseg

awa

test

and

TREEFITTER

Theresultsofalltests

suggestthat

the

diversificationof

both

endosymbiontswas

largelyoren

tirely

dep

enden

tonthe

phylogen

etic

history

oftheirhost

leafhoppers

Host:COI,COII,

16SrD

NAan

dH3.F

orthe

symbionts:16S

rDNA

Like

lihood-ratiotest

toassess

whether

the16SrD

NAof

Baumannia

and

Sulcia

were

evolvingwitha

constan

trate

across

differenthost-

associated

linea

ges

Tak

iyaetal.

(2006)

1a

Plataspidae

Stinkb

ugsan

dc-

Proteobacteria

Strict

cospeciation

Stinkb

ugsofthefamily

Plataspidae

,andtheir

highlyspecific

mutualisticgut

endocellularc-

Proteobacteria.

Bacteriave

rtically

tran

smitted

Threegen

era,

sevenspecies,

and12

populationsof

stinkb

ugsan

dtheirbacteria

TREEMAPTREEMAP

Strict

congruen

ce(6

codivergen

ceev

ents)

Forthehost:

mitochondrial

16SrRNAgen

eFo

rthebacteria:

16SrRNAgen

e

Nottested

Hosokawa

etal.(2006)




Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

1a

Cockroaches

(Polyphag

idae

,Cryptocercidae

and

Blattidae

)an

dtheir

Blattabacterium

bacteria

Cospeciation

Blattabacterium

verti-

cally

tran

smitted

intracellularmutual-

ists

(that

presumab

lyparticipatein

the

recyclingofuricacid)

that

are

locatedin

specialized

cells

ofcockroaches

Fourcockroach

speciesan

dtheir

Blattab

acterium

bacteria

Componen

tLite,

Tem

pleton

testan

dSh

imodaira

and

Haseg

awa

test

Hostan

dsymbiont

topologieswere

foundto

behighly

similar,an

dtests

indicated

that

they

werenot

statistically

different

Forthebacteria:

16SrD

NA.Fo

rthehost:18S

rDNAan

dmitochondrial

COII,12SrD

NA,

and16SrD

NA

combined

with

morphological

dataalread

ypublished

Congruen

ceof

divergen

cetimes

Lo(2003)

1a

Dee

pseaclam

s(V

esicomya,

Calyptogena,

and

Ectenagena)

and

bacteria

Cospeciation

Vesicomyidclam

sdep

endsen

tirelyon

theirsulfur-oxidizing

endosymbiotic

bacteria

16clam

species

andtheirassoci

ated

bacteria

Kishino–

Haseg

awa

criteria

Thetopologiesare

notsignificantly

different

Bacteria:

16S

rDNA;Clams:

16San

dmtD

NA

COI

Congruen

tdates

based

onfossils

Pee

ketal.

(1998)

1b

Crematogasteran

tsan

dMacaranga

plants

Cospeciation

Highlyspeciesspecific

mutualistic

interaction

between

Crematogasteran

tsan

dMacaranga

plants,

buttw

oan

tspecies

hav

emultiplehosts

NineMacaranga

plantspecies

andfourspecies

of

Crematogaster

ants

TreeMap

ping

in Componen

t

Thecongruen

ceof

thetw

ophylogen

ies

isstatistically

significantalthough

thereisamajor

disag

reem

ent

Fortheplant:

phylogen

yalread

ypublished

based

onmorphology

andthenuclea

rITS.Fo

rthean

ts:

COI

Tertiaryclim

atean

dtherestrictionof

Macarangato

sea

sonalforestssug

gestthat

thisplant

clad

ediversified

inthelate

Tertiary,

whichcorresponds

tothediversifica-

tion

periodofthean

ts

Itinoetal.

(2001)

1b

Cam

ponotusAnts

andtheirbacteria

(Can

didatus

Blochmannia)

Cospeciation

Mutualism

betwee

nan

tsan

dtheir

bacterial

associates,that

are

locatedwithin

bacteriocytesan

dare

tran

smittedvertically

althoughsome

horizontal

tran

smissionhas

bee

nsuggested

16hostspecies

andtheir

bacteria

Shim

odaira–

Haseg

awa

test

Noconflictonwell-

resolved

nodes

Forthebacteria:

16Sribosomal

DNA[rDNA],

groEL

,gidA,and

rpsB.Fo

rthe

host:thenuclea

rEF

-1aF2

and

mitochondrial

COIa

ndCOII

Correlated

ratesof

synonym

ous

substitution(dS)

inthetw

ophylogen

ies

Deg

nan

etal.

(2004)





Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

2Tep

hritinae

fruitflies

andbacteria

(Can

didatusspp.)

62.5%

of

nodes

with

codivergen

ceinferred

Mutualistic

relationships

betwee

nfruitfliesan

dtheir

extracellularbacterial

symbionts(some

vertically

tran

smitted)

33Tep

hritinae

fliesspeciesin

17

differentgen

era

TREEMAP,PARAFIT

and

Shim

odaira–

Haseg

awa

likelihood-

based

test

Amax

imum

of20

codivergen

ceev

ents(=

10

cospeciations),

from

6to

17

losses,1to

6sw

itches

and12to

14duplication

even

ts

Forthehost:16S

rDNAan

dCOI-

tRNALeu-C

OII;

forthe

symbiont:16S

rDNA

Nottested

Mazzonetal.

(2010)

2Mak

ialginemites

(Acari,

Psoroptidae

,Mak

ialginae

)an

dGalag

alges

primates

Mainly

cospeciations

and

duplications

Perman

entan

dhighly

specialized

ectoparasitemites

Fortheparasite:

9taxa

TREEFITTER

and

TREEMAP

4/5

cospeciation,but

atleastas

man

yduplicationev

ents

ascospeciation

even

ts

Morphological

traits

Nottested

Bochko

vetal.(2011)

2Crinoids

(Echinodermata)

andmyzostomids

(Myzostomida,

Annelida)

Mainly

cospeciation

andlosses

Obligatean

dhighly

specificcommen

sal

marineworm

s

16speciesof

crinoids

(belongingto

6different

families)an

dtheir16

associated

myzostomids

(belongingto

15

species)

TREEMAP,PARAFIT

andKHan

dSH

tests

8or9cospeciations,

but7–1

0losses

and

3–4

hostshifts

Forcrinoids:18S

rDNA,an

dCOI;

formyzostomid:

18SrD

NA,16S

rDNA,an

dCOI

Nottested

Lanterbecq

etal.(2010)

2Roden

ts(M

uridae

:Sigmodontinae

)an

dtheir

hoplopleurid

suckinglice

(Phthirap

tera:

Anoplura)

Cospeciation

butwith

preva

lent

host

switching

Gen

eralistparasitic

suckingliceof

roden

ts

15distinct

louse

speciesan

d19

roden

tspecies

TREEMAPan

dTREEFITTER

TREEMAP:12–2

0codivergen

ces,

10–1

4duplications,

12–1

5ex

tinctions,

3–4

host

switchings.

TREEFITTER:6–9

codivergen

ces,0

duplications,0–3

extinctions,6–1

0hostsw

itchings

Fortheparasite:

CO

Ian

dEF

1a

Nottested

Smithetal.

(2008b)




Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

2Figtree

s(M

oraceae,

Ficus)an

dfig

wasps

Significant

cospeciation

butwithhost

shiftsan

dduplications

Pollinatingan

dnonpollinatingfig

waspsan

dFicus

23figspecies

TREEMAPan

dPARAFIT

Pollinators:no

significant

cospeciationin

the

tree

withallspecies,

butsignificant

cospeciationin

the

combined

tree

with

fewer

species.Non

pollinators:

significant

cospeciation,but

withalmostas

man

yduplications

needed

ascospeciation

even

ts

Figs:tw

onuclea

rDNAfrag

men

ts(ETSan

dITS).

Wasps:28San

dITS2

Significant

correlationof

MRCA,with

intercep

tat

0but

slope<1

Jousselin

etal.

(2008)

2Geomydoecus

liceon

Cratogeomys

pocket

gophers

Codivergen

ceChew

ingparasite

licean

dtheir

pocket

gopher

hosts

Fortheparasite:

41specim

ensof

chew

inglice

from

seven

species.

Gophers:16

individualsfrom

3species

TREEMAP,PARAFIT,

KHan

dSH

tests,

TREEMAP:significant

cophylogen

ybetwee

nhostan

dparasites,16

codivergen

ceev

ents,6–8

duplications,3–4

extinctions,3–4

hostsw

itches

Louse:C

OIan

dEF

-1aFo

rthe

host,COI

Reg

ressionan

alyses

ofestim

ated

branch

lengthsin

gophers

andliceshowed

intercep

tsthatwere

notsignificantly

differentfrom

zero

Light&

Hafner

(2007)

2Figs(Ficusspp.,

Moraceae

)an

dwasps(H

ymen

op

tera,Agao

nidae

,Chalcidoidea)

‘Diffuse

coev

olution’

Hostspecific

mutualistic

pollinatoran

dnonpollinator

waspsoffigs

411individuals

from

69

pollinatingan

dnonpollinating

figwaspspecies,

17speciesof

Urostigmafigs

TREEMAPan

dPARAFIT

Significant

congruen

ce.Host-

switchingan

dmultiplewasp

speciesper

hostare

howev

erubiquitous;1–6

cospeciations,1–1

0duplications,4–6

8sortingev

ents,0–1

hostsw

itch

Waspphylogen

ybased

onCOI

Nottested

Marussich&

Machad

o(2007)





Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

2Pelecan

iform

birds

andPectinopygus

lice

Significant

congruen

cebutwithhost

shifts

Host-specific

parasitic

licethat

infect

asingleorder

of

birds

(Pelecan

iform

)

17Pectinopygus

speciesan

dtheir

pelecan

iform

host

TREEFITTER,

TREEMAP,ILD,

and

PARAFIT

Significantoverall

congruen

ce.

However,without

invo

kingan

yhost

switching,TREEMAP

had

tointroduce

10–1

1cospeciation

even

ts,5–6

duplications,an

d19–2

4sorting

even

ts.Allowing

hostshifts:10–1

1cospeciations,5–6

duplications,3–1

9losses,an

d0–6

switches

Fortheparasite:

mitochondrial

12SrRNA,16S

rRNA,COI,an

dnuclea

rwingless

andEF

l-agen

e.Fo

rthehost:

mitochondrial

12SrRNA,COI,

andATPases

8an

d6gen

es

Significant

correlation

between

coalescence

times

(r=0.94).The

intercep

tofthe

slopeispositive

but

notsignificantlydif

ferentfrom

zero

Hughes

etal.

(2007)

2W

ingliceofthe

gen

usAnaticola

(Is

chnocera)an

dsev

eralgen

eraoffla

mingoes

andducks

Cospeciations

andhost

shifts

Parasiticliceinfecting

flam

ingoes

andducks

43gen

eraof

avianlice

TREEMAP

Codivergen

ces=

4–5

,duplications=

5–6

,losses

=1–3

2,

hostsw

itches

=0–6

Fortheparasite:

nuclea

rEF

-1a,

mitochondrial

12San

dcytochrome

oxidaseI(COI).

Avian

phylogen

yalread

ypublished

Nottested

Johnsonetal.

(2006)

2Polyomav

iridae

(polyomav

iruses)

andve

rteb

rates

(avian

and

mam

mals)

Codivergen

ceParasiticdouble-

stranded

DNA

viruses,which

arewidely

distributedam

ong

verteb

rates;av

ian

virusesinfect

abroad

erhostrange

than

thehighly

specificmam

malian

polyomav

iruses

72fullgen

omes:

ninemam

malian

(67strains)an

dtw

oav

ian

(5strains)

polyomavirus

TREEMAP

Codivergen

ces=12,

duplications=8,

losses

=2–1

3,host

switches

=0–4

Forthevirus:the

mainfive

gen

esofthegen

ome

(VP1,V

P2,VP3,

largeTan

tigen

,an

dsm

allT

antigen

)

Nottested

Perez-Losada

etal.(2006)




Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

2Mea

lybugs

Hem

iptera

(Subfamily

Pseudococcinae)

anden

dosymbiont

bacteria

Codivergen

cean

dsorting

even

ts

Hem

ipterans,

mea

lybugsan

dtheir

obligateintracellular

bacterialsymbionts,

thoughtto

bestrictly

verticallyinherited

21hostmea

lybug

taxa

andtheir

bacterial

symbionts

TREEMAPan

dSO

WHtest

TREEMAP:14

codivergen

ces,0–3

duplications,7–1

2sortingev

entsan

d2–5

hostshifts.

Significantly

congruen

t

Forthe

mea

lybugs:

EF-1a,

28San

d18S.

Forthe

endosymbionts:

16San

d23S

rDNA

Strongcorrelation

betweenbranch

lengthsin

hostan

dsymbionttree

s(r=0.785,

P<0.001)

Downie&

Gullan

(2005)

2Plants(Fab

acea

e,Asteracea

e,Rosa

ceae

,Cyp

eracea

e)an

dgall-form

ing

nem

atodes

(Tylen

chida:

Anguinidae

)

Cospeciation

Gall-form

ing

nem

atodes,o

bligate

specialized

parasites

of

plants

58nem

atode

samplesfrom

53

populations

TREEMAP

12cospeciations,

4–6

duplications,

1–4

hostsw

itches.

Theleve

lof

cospeciationwas

estimated

as60%

Fortheparasitic

nem

atode:ITS1

,5.8San

dITS2

.Fo

rtheplant:

ITS1

andITS2

Nottested

Subbotin

etal.(2004)

2Dove

san

dpigeo

ns

(Ave

s:Columbiform

es)

andfeather

licein

thegen

us

Columbicola

(In

secta:Phthirap

tera)

Cospeciation,

butalso

significant

leve

lof

incongruen

cean

dhost

switches

Vertically

tran

smitted

parasiticliceof

pigeo

ns

anddove

s.So

me

speciesarehost

specific,other

are

foundonmultiple

host

species

27hostspecies

andtheir

associated

15

licespecies

TREEMAPan

dTREEFITTER

9cospeciation

even

ts,11

duplicationsan

d61

sortingev

ents.Up

to3hostsw

itches

under

certaincosts.

Number

of

cospeciationev

ents

higher

than

expectedbychan

ce

Fortheparasite:

COIan

dthe

nuclea

rEF

-1a.

Forthehost:

mitochondrial

cytb,C

OIan

dthenuclearFIB7

Nottested

Johnsonetal.

(2003)

2Fe

ather

mites

(Subfamily

Ave

nzoariinae

)an

dbirds

(Charad

riiform

es,

Procellariiform

es,

Pelecan

iform

es,

Ciconiiform

es,a

nd

Falconiform

es)

Cospeciation

Mostlycommen

sal

and

someparasiticmites

of

birdsfrom

the

Subfamily

Avenzoariinae

26mitespecies

TREEMAP

12–1

3cospeciation

even

ts,6–7

duplications,2host

shifts,an

d26–2

9sortingev

ents

Mitephylogen

ybased

on41

morphological

charactersan

dmtD

NA.Fo

rbirds,phylogen

yconstructed

from

several

published

phylogen

ies

based

on

morphological

andmolecular

data

Nottested

Dab

ert

(2001)





Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

2Se

abirds

(Procellariiform

esan

dSp

hen

isciform

es)

andlice

(Phthirap

tera)

Cospeciation

Seab

irdsan

dtheir

parasiticlice

11species

ofseab

irds

from

the

sphen

isciform

gen

eraan

d14

speciesoflice

from

sixgen

era

TREEMAP

Onehost-switching,

9cospeciation,3–4

intrah

ost

speciation,

and11–1

4sorting

even

ts

Fortheparasite:

12SrRNA.Fo

rthehosts:12S

ribosomalRNA,

isoen

zyme,

and

beh

aviorald

ata

Nottested

Paterson

etal.

(2000)

3Threetrophicleve

ls:

geo

metridmoths

(Eois),braconid

parasitoids(Para

panteles)an

dplantsin

the

gen

usPiper

Hostshifts

andhost

conservatism

(shiftsto

closely

relatedhosts)

inEois

Herbivore

moths,

specialistmoth

parasitoid

wasp

N=94(>

13spp.)

forEois,N=38

(>10spp.)for

Parapanteles

N=52forPiper

Permutation

testof

Hommola

(nonrandom

associationof

matrices)

NASignificant

correlation

betwee

nthebranch

lengths,

butdueto

host

conservationism

COIandEf1-a

for

Eois;ITS1

and

ITS2

forPiper;

COIan

dtw

onuclea

rgen

esforParapanteles

Fossilcalibrationfor

thePiper

andEois

tree

s,molecular

clock

estimatefor

theParapanteles

tree

:lack

of

temporal

congruen

ce

Wilsonetal.

(2012)

3Neo

batrachian

anurans(frogsan

dtoad

s)an

dPlatyhelminthes

(Monogen

ea)

Hostshifts

Parasiticrelationship:

flatworm

andan

urian

26parasite

species,23

anuranspecies

TREEMAP,PARAFIT,

DIVAan

alysis

4hostshifts,22

codivergen

ces,10

duplications,an

d16ex

tinction

even

ts;

Parafi

ttest

nonsignificant

Fortheparasite:

18San

d28S.Fo

rthehost:

Rhodopsinan

dmitochondrial

(12San

d16S)

No:Inferred

datations

inconsisten

twith

codivergen

ce

Bad

etsetal.

(2011)

3Chew

inglice

(Pappogeomys)

and

Geomydoecus

pocket

gophers

Preva

lent

cospeciation

Highlyhost-specific

parasiticchew

ing

liceonpocket

gophersoccurring

onasingle

pocket

gopher

species

orsubspecies

57individuals

from

the

Geomydoecus

bullerispecies

group

TREEMAPan

dPARAFIT

12cospeciation

even

ts,4

duplications,1loss,

and2hostsw

itches

COIforchew

ing

lice.

Phylogen

yofthehost

previously

published

based

onmtD

NACytb

andCoIan

d1

nuclea

rgen

e(b-fib)

Absolute

time

congruen

cenot

tested

,butthe

estimated

molecular

substitutionrate

isfourfold

higher

inlicethan

inhosts

under

assumed

codivergen

ce

Dem

astes

etal.(2012)




Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

3Cyttaria

fungio

nsouthernbee

chtree

s(N

othofagu

s)

Codivergen

ce,

butalso

host

shiftsan

dextinction

even

ts

ObligateAscomycete

fungip

arasites

of

trees

12speciesof

Cyttariaan

dtheirhosts

PARAFIT

Significant

cophylogen

etic

structure

with

Parafi

t;reconstructionof

thehistory

byhan

dwith7–8

codivergen

ce,1–2

duplications,1–2

hostshifts

Cyttaria

phylogen

ies

alread

ypublished

.Fo

rNothofagus:

cpDNA,rbcL,

nucITS,

rRNA,

cpDNAatpB-

rbcL

intergen

icspacer

and

morphological

data

BEA

STcalibrated

withfossils

inferred

amore

ancien

tdivergen

ceofthe

fungusthan

Nothofagus

Peterson

etal.

(2010)

3Nosema(M

icrospori

dia:Nosematidae

)an

dbees(H

yme

noptera:Apidae)

Cospeciation

andhost

shifts

Microsporidian

parasites

inbee

s4hostspeciesan

d4parasite

species

TREEMAPan

dTREEFITTER

0–1

cospeciation,

1–2

hostshifts

Fortheparasite:

LSan

dSS

rRNA.

Forthehost:

cytochromeb

Nottested

Shafer

etal.

(2009)

3W

hea

t,barleyan

doat

(Poacea

e)an

dW

hea

tdwarf

viruses(W

DV)

(Mastrevirus)

Codivergen

ceforsome

virusesbut

notforothers

ParasiticDNAviruses

Fullgen

omes

of

46isolatesof

Whea

tdwarf

virus

TREEMAP

6codivergen

cesan

d2hostjumps

Forviruses:

Phylogen

etic

tree

sconstructed

usingfull

gen

omes.Host:

rbcL

Correlationbetween

hostlinea

gean

dW

DVdivergen

ceestimates.

However,assuming

codivergen

ce,the

inferred

rate

of

substitutions

impliedstronger

constraintsag

ainst

chan

gethan

by

other

methods

Wuetal.

(2008)

3HeteromyidRoden

ts(Roden

tia:

Heteromyidae)an

dFahrenholzia

suck

inglice(Phthirap

tera:Anoplura)

Codivergen

ceRoden

tsan

dtheir

perman

entan

dobligateectoparasitic

suckinglice

43heteromyid

specim

ensan

dtheirlice

PARAFIT,TREEMAP

PARAFIT:39ofthe44

host-parasitepairs

weresignificant.

TREEMAP:26

codivergen

ces,14

duplications,23

extinctions,1host

switching

Hostan

dparasite

phylogen

ies:

COI

Correlationbetween

branch

lengths,but

riswea

k(r=0.7)

andtheslopeis2.8,

interpretedas

dif-

ferentratesofsub-

stitutionsin

lice;

intercep

tsignificantly<0,

indicatingdelayed

divergen

cein

lice

relative

tohostdivergen

ce

Light&

Hafner

(2008)





Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

3Lice

(Pediculus,

Pedicinus,Pthirus)

andprimates

(Homo,Pan,

Gorilla)

Significant

cospeciation,

butalso

parasite

duplication,

extinction,

andhost

switching

Highlyspecialized

and

perman

entobligate

ectoparasites

of

primates

5speciesoflice

from

primates

andonespecies

from

roden

tsas

outgroup

TREEMAP

TREEMAP:5

cospeciationev

ents

andonehostsw

itch

1duplicationan

d2

losses.Significantly

greater

similarity

betwee

nthehost

andparasitetrees

than

expectedby

chan

ce

Forthelice:

mitochondrial

Cox1

and

elongation

factor1alpha

(EF-1a)

gen

e

Divergen

cedate

estimates

showthat

thenodes

inthe

host

andparasitetree

sarenot

contemporaneo

us

Ree

detal.

(2007)

3Simianfoam

yviruses

andprimates

(Hominoidea

and

Cercopithecoidea

)

Cospeciation

Non-pathogen

icRNA

retrovirusesinfecting

mam

mals

55primate

speciesan

dvirusesisolated

from

44primate

species

TREEMAP

Significantsupport

forove

rall

cospeciation(22

even

ts/44),with

someobviouscases

ofsomeinstan

ces

ofcross-species

infections

Forthevirus:

polymerase

gen

e(pol).Fo

rthehost:

mitochondrial

(mtD

NA)

cytochrome

oxidasesubunit

II(COII)

Significantlinea

rrelationship

(r=0.8486)

betweenbranch

lengths.However,

themolecularclock

calibrationsunder

cospeciation

hyp

othesisinfersan

extrem

elylow

rate

ofSF

Vev

olution,

that

would

mak

eit

theslowest-

evolvingRNAvirus

documen

tedso

far

Switzeretal.

(2005)

3Gyrodactylusflat

worm

san

dPomatoschistus

Gobiesfishes

Hostsw

itches

Twotypes

of

platyhelminth

parasites:a

monophyleticgroup

of

host-specificspecies,

mainlyinfectinggills

andasecondgroup

withlowerspecificity,

dominan

tlyfoundon

finan

dskin

15Gyrodactylus

taxa

TREEFITTER,

TREEMAPan

dPARAFIT

Theove

rallfit

betwee

ntreeswas

significant

accordingto

TREEMAP

and

TREEFITTER,but

notaccordingto

the

timed

analysisin

TREEMAPorto

the

PARAFITan

alysis

Fortheparasite:

theV4regionof

the18SrRNA

andthe

complete

ITS

rDNAregion.

Forthehost:the

12San

d16S

mtD

NA

frag

men

ts

Anab

solutetimingof

speciationev

entsin

hostan

dparasite

ruledoutthe

possibility

of

synchronous

speciationforthe

gillparasites

Huyseetal.

(2005)




Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

3Primatelentiviruses

(PLV

)an

dprimates

Hostsw

itches

Parasiticretroviruses

that

hav

ebeencited

as eviden

cefor

codivergen

ce

12primatetaxa

(including

outgroup)an

dtheir

lentiviruses:11

even

ts

TREEMAP

8codivergen

ces

even

tsofapossible

11ev

entsfor

perfectlymatched

trees,butsimulated

phylogen

iesbased

onthehyp

othesis

ofp

referentialshifts

betwee

nclosely

relatedhostswere

mostlycongruen

t,an

dcospeciation

was

inferred

Hostan

dparasite

phylogen

ies

based

ona

number

of

published

studies

Divergen

cetime

incompatible

Charleston&

Robertson

(2002)

3Broodparasitic

finches

(Vidua

spp.)an

dtheir

finch

hosts

(Estrildidae)

Hostshifts

inferred

from

dates

while

cophylogen

ytestspointed

to cospeciations

HostspecificAfrican

broodparasitic

finches

(Viduaspp.)that

mim

icthesongsan

dnestlingmouth

markings

oftheirfinch

hosts

(fam

ilyEstrildidae

)

74estrildids,21

parasiticfinches,

andnineploceid

finches

asthe

outgroup

TREEMAPan

dPARAFIT

Basaldivergen

ces

amongViduaspe

cies

aremore

recent

than

those

among

hostspecies,allow

ingcospeciationto

berejected

,while

testsforcospecia-

tionindicated

significantcongru

ence

betwee

nhost

andparasitetree

topologies

Forhostan

dparasites:most

ofthean

alyses

weredoneusing

mtD

NAdataset,

althoughsome

nuclea

rsequen

ceswere

also

usedin

someclad

es

More

recent

divergen

ceof

parasites

than

hosts

Sorenson

etal.(2004)

3Malariaparasites

(Plasm

odium

and

Haemoproteus)

and

Hae

moproteus

birds

Cospeciation

Plasm

odium

parasites

andHaemoproteus

birds.Individual

parasitespeciesare

thoughtto

be

restricted

tohost

taxo

nomicfamilies

68linea

ges

of

Plasm

odium/

Haemoproteus

recove

redfrom

79speciesof

birdsin

20av

ian

families

TREEFITTER

Significantlymore

cospeciationev

ents

(9–1

6)than

inrandomized

trees;

howev

er,they

required

upto

52

switchingev

entsor

366extinction

even

ts

Fortheparasite:

Cytochromeb.

Forthehost:

phylogen

ies

alread

ypub

lished

based

on

theDNA–D

NA

hyb

ridization

studies

Assuming

codivergen

ce,the

mitochondrialDNA

nucleo

tide

substitution

appears

tooccurab

out

three

times

faster

inhosts

than

inparasites

Ricklefs&

Fallon

(2002)





Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

3Frankia

bacteriaan

dan

giosperm

plants

(Actinorhizae

)

Significanttree

congruen

cebut

incongruen

tdates

Actinorhizae,

mutualisticrelation

betwee

nan

giosperm

rootsan

dnitrogen

fixingFrankia

bacte-

ria

19Actinorhizal

angiosperms

TREEMAP,

Componen

t8ev

entsof

codivergen

cean

d9

duplicationev

ents.

Theprobab

ility

of

eight

coevolutionary

even

tsoccurringby

chan

cewas

about

0.23when

1000

hostan

dsymbiont

treeswere

randomly

associated

Forthebacteria:

nifHan

d16S

rDNA.Fo

ractinorhizal

plants:rbcL

Estimated

divergen

cetimes

among

Frankia

andplant

clad

esindicated

that

Frankia

clad

esdiverged

more

recentlythan

plant

clad

es

Jeongetal.

(1999)

4Sigmaviruses

(Rhab

doviruses)

andDrosophila

fruitflies

Hostshifts

Parasitevertically

tran

smittedRNA

virus

4speciesof

Diptera

Shim

odaira–

Haseg

awa

testan

dRobinson–

Foulds

distance

4/7

RNApolymerase

gen

eforviruses

Nottested

Longdon

etal.(2011)

4Pap

illomavirusan

dmam

mals

Hostshifts

Parasiticdouble-

stranded

DNAviruses

207PVgen

omes

TREEMAP,

TREEFITTER,an

dPARAFIT

1/3

3gen

esfor

Pap

illoma;

68-

gen

esforthe

hosts

Nottested

Gottschling

etal.(2011)

4Gam

maretroviruses

andbats

(Chiroptera)

Hostshifts

Exogen

ousparasitic

retroviruses

tran

smitted

horizontally

11bat

species

TREEMAP

2/7

Viruses:Gag

and

Polp

roteins.

Hosttree

from

thetree

oflife

Nottested

Cuietal.

(2012)

4Lymphocystis

viruses

andfishes

(Paralich

thyidae

)

Indep

enden

tdivergen

ceParasiticDNAviruses

causinglymphocystis

disease

infish

25virusisolates,8

fish

species

TREEMAP

3codivergen

ces,11

duplicationsan

d19

sortingev

ents

Cytochromebfor

thefishes,m

cp

gen

efor

Lymphocystis

Nottested

Yan

etal.

(2011)

4Maculineabutterfly

andMyrm

icaan

tsIndep

enden

tdivergen

ceParasiticrelationship:

caterpillarsneedto

be

adoptedan

dnursed

by

ants

32Maculinea

specim

ens(8

speciesinclud

ingoutgroup),

14speciesof

Myrm

ica

PARAFIT,

TREEFITTER

Ran

dom

association

betwee

nthehost

andtheparasite

COI,tRNA-Leu

,trnL,

COIIan

dElongation

Factorfor

Maculinea.Fo

rMyrm

ica:

COI,

Cytb,28SArgK,

EF1alphaan

dLw

Rh

Nottested

Jansenetal.

(2011)




Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

4Tobam

ovirusan

dplants(m

onocoty

ledonousan

ddicot

yled

onous)

Indep

enden

tev

olution


plantRNAviruses

31speciesof

Tobamovirus

TREEMAP

Lack

ofcongruen

cebetwee

nthehost

andtheparasite

phylogen

ies

Gen

esforthe

virus:CP

(ORF4

).Fo

rthe

plants:rbcL

More

recent

divergen

ceof

virusesthan

oftheir

hosts(BEA

STestimationsfor

viruses)

Pag

� anetal.

(2010)

4Figtree

s(Ficus)an

dfigwasps(Elisab

ethiella,Courtella,

Alfonsiella)

Hostshifts

Mutualisticrelation

betwee

nFicusan

dex

trem

ehost

specificAfrican

figwasps

42wasptaxa

and

26Ficusspecies

PARAFIT,

TREEFITTER

Nonsignificant

Parafi

ttest;Aleast

twiceas

man

yhost

shiftsas

cospeciation

even

ts,

even

withhigh

coststo

hostshifts

EF-1aan

dCytb

forFicusan

dCO1forwasps

Hostshiftsoccurred

laterthan

host

diversification

even

ts,although

ove

rallconfiden

ceintervalsove

rlap

Mcleish

&Noort

(2012)

4Steinernemanem

atodes

andc-Proteo

bacteria(Xenor-

habdus)

Hostshifts

Mutualistic

relationship

betwee

nnem

atodes

andtheirassociated

c-Proteobacteria

30hostspecies

andtheir

associated

bacteria

Tarzan

12cospeciation

even

ts,17host-

switches

and7

occurren

cesof

sorting

Forthe

nem

atode:

28S,

12S,

andCOI.

Forthebacteria:

16S,

RecAan

dSe

rCgen

es

Nottested

Lee&Stock

(2010)

4Picornavirusesan

dan

imals(Avesan

dmam

mals:

Primates,

Roden

tia,

Carnivora,

Perissodactyla,

Certatiodactyla)

Hostshifts

ParasiticRNAviruses

causingabroad

spectrum

ofdisea

ses

in severalordersofb

irds

andmam

mals

752complete

gen

ome

sequen

cesof

piconav

iruses

PARAFIT

Lack

ofcongruen

ce2C,3Cpro,an

d3Dpol

Nottested

Lewis-Rogers

&Crandall

(2010)

4Malaria

(Plasm

odium)an

dprimates

Indep

enden

tev

olution

ParasiticPlasm

odium

andtheirprimate

hosts

18Plasm

odium

species

TREEFITTER

and

PARAFIT

0–5

cospeciations,

butassumingeither

upto

93sorting

even

tsorupto

12

duplicationsorup

to11hostshifts

ForPlasm

odium:

18SrRNA,b-

tubulin,celldivi

sioncycle2,E

F,cytb,m

erozoite

surface;

Host

phylogen

ypre

viouslypub

lished

Nottested

Garam

szeg

i(2009)

4Han

tavirusan

dRoden

ts(Arvicolinae,

Murinae

,an

dSigmodontinae

subfamilies)

Mainlyhost

shifts

Parasiticsingle-

stranded

RNAviruses

Fortheparasite:

65taxa

.Forthe

host:95

sequen

ces

TREEMAP

13–1

4codivergen

ce,

20–2

3hostshifts,

5–7

duplications

and4–1

0sorting

even

ts;Parafi

ttest

nonsignificant

Forthevirus:S,

M,an

dL

segmen

ts.Fo

rthehost:cytb

Ove

rlap

ofthemea

nnodeag

esRam

sden

etal.(2008)





Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

4Candidatus

endobugula

bacte

riaan

dtheirBugula

bryozoan

host

Nosupportfor

ahistory

of

strict

cospeciation

Mutualisticvertically

tran

smittedbacteria

of

bryozoan

Five

hostspecies

andtheir

associated

symbionts

TREEMAP

3cospeciation

even

tsan

d1hostsw

itch,

butthiswas

not

significantlymore

congruen

tthan

expectedbychan

ce

Host:16SLS

UrRNAan

dCOI;

Symbiont:16S

SSUrRNA

Nottested

Lim-Fong

etal.(2008)

4Grasses

(Pooidea

e)an

dEpichlo€ e

fungalen

dophytes

Ove

rallnon-

significant

congruen

ce,

butea

rly

codivergen

cesuggested

Symbiont(from

mutualistto

parasites)

fungalEn

dophytes

ingrasses,mostly

verticallytran

smitted

26grass

species-

Epichlo€ especies

PARAFITan

dMRCALink

Analysisofthe26

associationsdid

not

reject

random

association.W

hen

five

obvioushost

jumpswere

remove

d,the

analysis

significantly

rejected

random

associationan

dsupported

grass–

endophyte

codivergen

ce

Fortheplant:a

trnLintronan

dtw

ointergen

icspacers(trnT-

trnL,

trnL-trnF)

from

cpDNA.

Forthefungus:

tubB(form

erly

tub2)an

dtefA

(form

erlytef1)

Nocorrelation

betweenMRCA

ages

inthe26

speciestree

Schardletal.

(2008)

4Mussels(M

ytilidae

:Bathym

od-

iolinae)an

den

dosymbiotic

bacteria

Incongruen

ceBathym

odiolin

mussels

andtheirassociated

thiotrophic(sulfur-

oxidizing)bacterial

endosymbiont

Forthehost,25

OTU

PARAFIT

Hostan

dsymbiont

tree

topologies

were

notcongruen

t

Forthehost:

ND4,COIan

d28S.

Forthe

parasite:

16S

rRNA

Inferred

time-dep

ths

ofthegen

etrees

wereinconsisten

t(M

antel’s

test)

Wonetal.

(2008)

4Figtree

s(Ficus)an

dtheirassociated

fig

wasps

Incongruen

ceFigsan

dtheir

mutualistic

pollinators

Forthehost:18

neo

tropicalfig

species

TREEMAP

Nosignificant

codivergen

ce.

Reconciliationof

phylogen

ies

inferred

3–5

cospeciations.If

switchingev

ents

areex

cluded

,reconciliation

required

40–4

5losses

Forthehost:

g3pdh,tpian

dtheITS.

Forthe

pollinator:Phy

logen

ybased

on

dataalread

ypublished

Nottested

Jacksonetal.

(2008)




Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

4Chae

todactylid

mites

andlong-tongued

bee

s(Apidae

and

Meg

achilidae)

Infreq

uen

thostshiftsat

ahigher

taxo

nomic

leve

l,an

dfreq

uen

tshiftsat

alower

leve

l

Mites

ofb

eesincluding

mutualists(feeding

onnestwaste),

parasitoids(killing

thebee

eggor

larvae

),commen

salsor

clep

toparasites

230mitespecies

from

1500

museum

specim

ensof

long-tongued

bees

PARAFIT,

DistPCoA,

TREEFITTER

0–3

cospeciation,

5–8

duplications,

0–6

hostshifts,

0–3

5ex

tinctions

Mitephylogen

y:51

morphological

characters.Host

phylogen

ies

alread

ypublished

Nottested

Klim

ovetal.

(2007)

4Polyomav

irusin

human

populations

(Homosapiens

sapiens)

Noev

iden

cefor

codivergen

ce

Double-stran

ded

DNA

virusestran

smittedin

a quasi-ve

rtical

man

ner

(from

paren

tto

child

postnatally)

333viral

gen

omes

and

158human

mitochondrial

sequen

ces

TREEMAP

<10codivergen

ceev

ents

Viralgen

omes

and

mitochondrial

human

sequen

ces

Thean

alysissuggests

that

thisvirusmay

evolvenea

rlytw

oordersof

mag

nitude

faster

than

predictedunder

the

codivergen

cehyp

othesis

Shacke

lton

etal.(2006)

4Pen

guins

(Sphen

isciform

es)

andchew

inglice

(Phthirap

tera:

Philopteridae

)

Incongruen

ceinterpretedas

causedby

failure

tospeciate

(parasites

not

speciatingin

response

totheirhosts

speciating)

Multihostparasites,all

speciesofchew

ing

lice

areparasites

ofan

entire

hostorder

15speciesof

chew

inglice

parasitizingall

17speciesof

pen

guins

TREEFITTER,

TREEMAPan

dPARAFIT

Noev

iden

ceof

extensive

cospeciationbut

supportfor

significant

congruen

cebetwee

nthe

phylogen

ies

interpretedas

possiblefailure

tospeciate

even

ts

Fortheparasitic

lice:

mitochondrial

12San

dCOI

regions.Host

phylogen

ybased

on70

integumen

tary

andbreed

ing

characters

Nottested

Ban

ksetal.

(2006)

4Urophora

insects

(Diptera:Tep

hriti

dae

)an

dplants

(Cen

taureinae)

Noev

iden

ceforove

rall

congruen

ce

Herbivorousinsects

fruitflygen

us

11Eu

ropean

Urophora

taxa

TREEMAP

Thenumber

of

cospeciationev

ents

(3an

d4)did

not

differfrom

random

expectation

Fortheherbivore:

allozyme

freq

uen

cydata

from

20loci.

Hostphylogen

yalread

ypublished

based

onallozymes

Inferred

divergen

cetimes

indicated

that

thesplit

ofinsect

taxa

lagged

beh

ind

thesplit

oftheir

hosts

Br€ andleetal.

(2005)





Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

4Anther

smutfungi

(Microbotryu

m)

andtheirhost

plants

(Caryo

phyllaceae

)

Hostshifts

between

relative

lyclosely

related

species

Microbotryum

com

plex:

Parasitic

sexu

ally

tran

smittedan

dspe-

cies-specificfungio

fthe

Caryo

phyllaceae

21hostplantsan

dtheirfungal

parasites

TREEMAP,

TREEFITTER,

Max

imum

Agreem

ent

Subtree

s(Icongindex),

PARAFIT

Ove

rall,results

suggestthat

cospeciationisnot

therulein

the

Microbotryum–

Caryo

phyllaceae

system

,that

host

shiftswereperva

sive,b

utthat

fungal

speciescould

not

shiftto

toodistant

hostspecies

Forthehostplant:

ITSan

dcpDNA

(trnLan

dtrnF).

Fortheparasite:

b-tubulin,c

-tubulin

and

Elongation

factor1a

Nottested

Refr� egier

etal.(2008)

4Achrysocharoides

parasitoid

wasps,

Lepidoptera

insects

andplants(Rosales,

Sapindales

and

Fabaceae)

Incongruen

cebetweenthe

three

phylogen

ies

Achrysocharoides

parasitoid

wasps,

highlyhost-specific

andattack

leaf-

mining

Lepidoptera

andthe

planthostof

Lepidoptera

larvae

15 Achrysocharoides

species

TREEMAPto

comparethe

three

phylogen

ies

pairw

ise

Noev

iden

cethat

the

phylogen

ieswere

more

congruen

tthan

expectedby

chan

ce

Forthe

parasitoid:

cytb

sequen

ces

and28S.

For

the

Lepidoptera

andtheplant

host,

phylogen

ies

alread

ypublished

Nottested

Lopez-

Vaa

monde

etal.(2005)

4Glochidiontreesan

dEpicephala

moths

Noperfect

congruen

ceObligatespecies-

specificpollination

mutualism

between

plantsan

dtheirseed

-parasiticpollinators

18Glochidion

species.Fo

rthe

pollinatorasin

gleindividual

from

each

ofthe

18morphologi

cally

delim

ited

species

TREEFITTER,

TREEMAPan

dPARAFIT

Greater

congruen

cebetwee

nthe

phylogen

iesthan

expectedin

arandom

association.

Perfect

congruen

cebetwee

nphylogen

iesisnot

found,whichlikely

resulted

from

host

shiftbythemoths

Fortheplant:the

entire

ITS-1,

5.8SrD

NA,an

dITS-2regions

andtheen

tire

intergen

icspacer

region

between28S

and18SrD

NA

includingET

SFo

rthemoth:

CO1,ArgKan

dEF

-lox

Nottested

Kaw

akita

(2010)




Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

4New

World

aren

aviruses

(NW

A)

androden

ts(subfamilies

Sigmodontinae

and

Neo

tominae

)

Hostsw

itches

Single-stran

ded

parasiticRNAviruses.

One-quarterofthem

infect

multiplehosts

andone-thirdofthe

hostspeciescanbe

infected

bymore

than

oneNW

Avirus

21hosttaxa

and

22viraltax

aParafi

t22of31host–virus

associationswere

notsignificantly

congruen

t

Forthevirus:

complete

coding

region

sequen

cesof

GP,N

P,Lan

dZ

proteins.Fo

rthe

host:

mitochondrial

cytochromeb

Nottested

Irwin

etal.

(2012)

4Se

abirds

(Procellariidae)an

dlice(Phthirap

tera:

Ischnocera)

Codivergen

cean

dhost

switches

Parasiticlicefrom

seab

irds(petrels,

albatrosses,an

dtheir

relative

s)withahigh

deg

reeoflinea

ge

specificity

39licespecies

from

diverse

hosts.Thelouse

tree

was

broke

ninto

four

subtree

san

dan

alysed

separately

TREEMAP

Mixture

of

cospeciationan

dhostsw

itching,w

ith

someclad

esoflice

showingclose

fidelityto

their

hosts(high

codivergen

ce)

andother

clad

esshowinghigher

leve

lsofhost

switching

Fortheparasite

12SrRNAan

dCOI.Previously

published

elongation

factor1a.

For

thehost,

phylogen

yconstructed

usinga

published

datasetbased

on

cytochromeb

Correlationbetween

sequen

cedivergen

ces

Pag

eetal.

(2004)

4Decacremaan

tsan

dMacarangatree

sLa

ckofove

rall

phylogen

etic

congruen

ce

Highlyspecific

mutualistican

tsthat

inhab

its

anddefen

ds

treesin

Southea

stAsia

Decacremaan

tsfrom

262trees

corresponding

to22Macaranga

species

TREEMAPan

dPARAFIT

TheParafi

tan

alysis

suggestsonly

partial

congruen

cebetwee

nan

tsan

dplants.No

cospeciationev

ents

wereinferred

by

TREEMAP

Forthean

tphylogen

ybased

onCOI.

Macarangaphy

logen

ybased

on

morphological

charactersan

dnuclea

rITS

alread

ypub

lished

Nottested

Quek

etal.

(2004)

4Avian

malaria

parasites

(Plasm

odium)an

dbirds(Ave

s)

Hostshifts

Birdparasites

vector-

tran

smittedparasites

from

thegen

us

Plasm

odium

and

Haemoproteus

65parasite

linea

ges,4

4host

species,an

d121

host–p

arasite

links

Componen

t,TREEFITTER

and

PARAFIT

Lack

ofsignificant

congruen

ceFo

rtheparasite

andthehost:

cytochromeb

Nottested

Ricklefsetal.

(2004)





Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

4Austrophilopterus

chew

inglicean

dRamphastos

toucans

Hostsw

itches

Chew

inglice,parasites

oftoucans,

considered

tobehostspecific

26Austrophil-

opteruslicecol

lected

from

10

Ramphastos

toucansan

d7

Pteroglossus

toucans

TREEMAPan

dTREEFITTER

Ove

rall,

TREEMAP

indicated

lack

of

cospeciation.

Analyses

iden

tified

onepotential

cospeciationev

ent

butthen

required

3duplicationsan

d17–2

2sorting

even

ts.TREEFITTER:

0–2

cospeciation

even

tsan

d6host

switches

Forparasiticlice:

COIan

dEF

-1a.

Forthetoucans:

phylogen

yalread

ypublished

based

ondifferent

sequen

cessuch

asmitochondrial

COIan

dCyt

b

Nottested

Weckstein

(2004)

4Drosophilafruitflies

andHowardula

nem

atodes

Hostshifts

Howardula

nem

atodes,

horizontally

tran

smit

tedparasites

of

Drosophila

Alm

ostallknown

Drosophila

hostsof

Howardula

TREEMAP

Hostan

dparasite

phylogen

iesarenot

congruen

t.The

reconstructionwith

thefeweststep

syielded

3cospeciation

even

ts,

5hostsw

itches,0

duplicationev

ents

and25sorting

even

ts

Fortheparasite:

rDNA:18S,

ITS1

andCOI.Fo

rthe

host:COI,COII,

COIII

Nottested

Perlm

anetal.

(2003)

4Dee

psea

vestim

entiferan

tubew

orm

san

dbacteria

Noev

iden

cefor

cospeciation

Vestimen

tiferan

tubew

orm

relyingon

intracellularsulfide-

oxidizingbacteria

locatedin

specialized

tissues

15 Vestimen

tiferan

taxa

andtheir

symbionts

TREEMAP

Noev

iden

cefor

cospeciation

Forthesymbiont:

16Sribosomal

gen

e.Fo

rthe

host:COI

Nottested

McM

ullin

etal.(2003)

4Fishes

(Sparidae

)and

monogen

ean

parasites

Lamellodiscus

Associations

considered

tobeduemore

toecological

factorsthan

to cospeciation

Fish

hosts(Sparidae

)an

dtheirhighlyhost

specificmonogen

ean

parasites

(Lamellodiscus)

20described

Lamellodiscus

speciesan

d16

Sparidae

TREEFITTER,

TREEMAPan

dPARAFIT

Allmethodsag

reed

ontheab

sence

of

widespread

cospeciationifthe

costofa

hostsw

itch

isnotassumed

tobe

very

high

Fortheparasite:

18SrD

NA.Fo

rthehost:

mitochondrial

cytban

dpreviously

published

16S

mtD

NA

sequen

ces

Nottested

Desdev

ises

etal.(2002)




Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

4W

olbachia

andfig

wasps(H

ymen

op-

tera)

Incongruen

tphylogen

ies

Mainlyvertically(and

pervasive

horizontally)

tran

smitted

Wolbachia

bacteria

in figwasps

70individuals

representing22

waspspecies

andtheir23

speciesof

associated

Wolbachia

TREEMAP

Thetotaln

umber

of

matches

between

thetw

oclad

ograms

(7cospeciation

even

ts)was

not

signican

tlydifferent

from

random

expectation

Fortheparasite:

wsp

gen

e.Fo

rthehost:phy

logen

yalread

ypublished

based

onpartialCOI

andCOII

sequen

ces

Nottested

Dew

ayne

Shoem

aker

etal.(2002)

4Brueelialicean

dbirds

(Passeriform

es,

Trogoniform

es,

Piciform

es,Coracii

form

es,P

sittacifor

mes,C

aprimulgifor

mes,C

harad

riifor

mes

andColumbif

orm

es)

Inconruen

tphylogen

ies

Brueeliaparasiticlice

considered

tobe

highlyhost-specific,

infectingbirds

15speciesof

Brueeliacol

lected

from

21

hostspecies

TREEMAP

7cospeciation

even

tsnotbeyondthat

expectedbychan

ce

Fortheparasite:

nuclea

rEF

-1a

and

mitochondrial

COI.Fo

rthe

host:

phylogen

ies

alread

ypublished

based

ontheDNA-

DNA

hyb

ridization

studies

Nottested

Johnsonetal.

(2002)

4Figtree

s(M

alvanthera)an

dfigwasps(Pleisto-

dontes,

Sycoscapter)

Partialcodiver-

gen

ce;H

ost

plant

switchingless

constrained

inparasites

than

inpollinators

Figs,obligated

mutualistic

pollinating

Pleistodonteswasps

and

parasiticnonpolli

natingSycoscapter

wasps.Ea

chFicus

speciesistypically

hostto

one

pollinatingan

dman

ydifferentnon

pollinatingwaspspe-

cies

20speciesof

Pleistodontes

and16species

ofSycoscapter

associated

with

Ficusspeciesin

thesection

Malvanthera

TREEMAP,SH

tests,ILD

Theleve

lof

cospeciationis

significantlygreater

than

that

expected

bychan

ce.

However,the

max

imum

leve

lof

cospeciationwas

only50–6

4%

of

nodes

Forthe

mutualisticwasp

Pleistodontes:

cytb,2

8S,

and

ITS2

.Fo

rthe

parasitic

Sycoscapter:cyt

ban

d28S

Thegreater

gen

etic

distancesbetween

Sycoscapterspecies

than

betweentheir

associated

pollina-

torssuggestthat

Sycoscaptermay

hav

ethehigherrate

ofmolecularev

olu-

tion.A

nother

possi

bility

isthat

Sycoscapterspecies

areolder

Lopez-

Vaa

monde

etal.(2001)





Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

4Lichen

s(Trebouxia):

algae

andfungi

Switchingof

algal

gen

otypes

occurred

repea

tedly

amongthese

symbiotic

lichen

associations

Long-term

mutualism

betwee

nof

photosyntheticalgae

orcyan

obacteria

andheterotrophic

fungi.Lo

walgal

specificity

33naturallichen

associations:46

fungalspecies

areassociated

withonly36

gen

otypes,

representing

fourorfewer

speciesofalgae

TREEMAP

10–11

cospeciations.

However,this

required

7–9

duplications,3–5

switches

and65–8

1sortingev

ents

Forboth

symbionts:ITS

Nottested

Piercey-

Norm

ore

&DeP

riest

(2001)

4Primates

and

Oxy

uridae

nem

atodes

Host-

switching

and

codivergen

ce

Enterobiinae

oxy

urid,

nem

atodes

parasites

ofprimates.Inmost

of

thecases,one

parasite

speciesper

host

species

48speciesof

Enterobiinae

analysed

(46

speciesofthe

subfamily

and2

outgroup

species)an

dtheirhosts

TREEMAP

6–8

cospeciation

even

ts,1

duplication,1–3

hostsw

itching,1–4

sortingev

ents

Fortheparasite:

45

morphological

charactersfrom

variousorgan

system

s.Fo

rthe

host,modified

from

apreviously

published

phylogen

y

Nottested

Hugot(1999)

4Puccinia

rustfungi

andBrassicacea

eplants

Hostshifts

more

common

than

codivergen

ce

Crucifersan

dtheir

flower-m

imicking

fungalpathogen

s

17Brassicacea

especiesan

d3

rustspecies

(multiple

individualsof

each)

Partition

homogen

eity

test

Incongruen

tphylogen

ies

Forthehost:cp

trnL-Fan

dITS;

forthefungi:ITS

and5.8S

Nottested

Roy(2001)

4Ascomycete

mycan

gial

(Ophiostom-

ataceae)

fungiand

Dendroctonusbark

bee

tles

Nowidespread

codivergen

ceMutualistan

dspecific

relationship:bee

tles

carrymycan

gia,

tegumen

tinva

ginationfor

fungal

dissemination

11fungalspecies

and6bee

tle

species

TREEMAP

4cospeciations,3

duplications,4

sortingev

entsan

d1

hostshift;more

cospeciationsthan

expectedbychan

ce

Isoen

zymes

Nottested

Six&Paine

(1999)




Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

4(8 cases)

and5

7 cases)

15Plant–fungal

symbioses

Acontinuum

ofcophylo-

gen

etic

patterns

rangingfrom

mostly

codivergen

ceto

mostly

switching

Differentplant-fungal

associations,ranging

from

parasitism

tomutualism

Symbiosesfrom

5Ordersan

d10

families

POptan

dTREEMAP

Sevenassociations

showed

significant

congruen

cewhile

eightwere

incongruen

t.Ev

entheassociation

inferred

assignificantly

congruen

tex

hibited

anumber

oflosses

orduplicationan

d/

orhostshifts

Phylogen

ies

alread

ypublished

and

bases

on

different

molecules

dep

endingon

thesymbiosis.In

gen

eral,forthe

fungal

symbiont:ITSor

nuclearrRNA.

Different

moleculesused

forthehost

phylogen

y

Nottested

Jackson

(2004)

5Fu

ngal

Pneumocystis

andmam

mals

Codivergen

ceParasiticfungus

19speciesof

mam

mals

TREEMAP

14cospeciationout

of18ev

ents

(number

ofother

even

tsinferred

not

indicated

)

Fortheparasite:

mtLSU

rDNA,

mtSSU

rDNA

andDHPS.

Phylogen

yof

themam

mals

previously

published

Nottested

Chab

� eetal.

(2012)

5Spinturnixmites

and

bats(Rhinolophus,

Myotis,Nyctalus,

Plecotus,

Miniopterusand

Barbastellus)

Cospeciation

andhost

shifts

Europea

nbatsan

dtheir

ectoparasiticmites

78Spinturnix

mites

(11mor

phospecies)

from

20Eu

ropeanbat

species

PARAFIT,M

ESQUITE

Significant

cophylogen

etic

structure,butat

leastfive

host

switch

even

ts

Formites:tw

omitochondrial

gen

es(16S–

COI).Fo

rbats,

published

phylogen

iesplus

cytb

Nottested

Bruyn

donckx

etal.(2009)

5a-Proteobacteria

and

Ishikawaellastink

bugs

Mainly

codivergen

ceVertically

tran

smitted

gutmutualistic

bacteriaofstinkb

ugs

14hostspecies

andtheir

symbiotic

bacteria

TREEMAPan

dTREEFITTER

10–1

1codivergen

ceev

ents,2–3

host

shifts,2–3

duplications,2–3

sortingev

ents

Forthebacteria:

16SrRNAan

dgroEL

t.Fo

rthe

host,COI

Nottested

Kikuchietal.

(2009)





Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

5Fu

ngal

Pneumocystis

andPrimates

Cospeciation

Highlyspecificfungal

parasites

20primate

species

TREEMAP

61–7

7%

ofthe

nodes

interpretedas

resultingfrom

codivergen

ceev

ents,butthe

numbersofother

even

tsthen

required

arenot

reported

Fortheparasite:

DHPS,

mtSSU

-rRNA,an

dmtLSU

-rRNA.

Forthehost:

phylogen

ies

alread

ypublished

based

onseveral

mitochondrial

andnuclea

rsequen

cesan

dmorphological

characters

Nottested

Hugotetal.

(2003)

5Cryptocercuscock

roaches

andtheir

bacteria

Blattab

acterium

cuenoti

Cospeciation

Cryptocercussubso-

cial,

xylophag

ouscock

roaches

andtheir

endosymbiotic

andverticallytran

s-mitted

bacteria

Blattabacterium

cuenoti

Sixoutofthe

seven

Cryptocercus

speciesan

dtheir

endosymbionts

COMPONEN

TLite

Significantsimilarity

betwee

nphylogen

ies

Forthebacteria:

16SrRNAan

d23SrRNA.Fo

rthehost:

portionsofthe

28SrRNAan

d5.8SrRNA

gen

esan

dthe

entire

ITS2

Nottested

Clark

etal.

(2001)

5Uroleuconap

hids

anden

dosymbiotic

Buchnera

bacteria

Cospeciation

Aphidsan

dtheir

mutualistic

vertically

tran

smitted

endobacteria,

required

forhost

reproduction

14representative

speciesof

Uroleuconan

dtheirbacteria

TREEMAP,

Kishino

–Haseg

awa

test,

likelihood-

ratiotest

Highlysignificant

leve

lsofsimilarity

betwee

nthetrees:

8–9

cospeciation

outof14possible

Forthemutualist:

partial

sequen

cesof

trpB.Fo

rthe

host:tree

based

on

mitochondrial

andnuclea

rsequen

ces

alread

ypublished

Nottested

Clark

etal.

(2000)

4an

d2

Viruses

(Partitiviridae),

plants

(Viridiplantae)

and

fungi

(Ascomycetes

and

Basidiomycetes)

Twovirus

families

with

codivergen

ceinferred

and

twofamilies

without

codivergen

ce


Vertically

and

horizontally

tran

smittedRNA

virus

175viral

gen

omes

PARAFITas

implemen

ted

inAXPARAFIT,

TREEFITTER,

TREEMAP

Man

yduplication

andsw

itching

even

tsinferred

even

forthefamilies

where

codivergen

ceissuggested

Complete

gen

omes

for

viruses

Nottested

G€ oke

retal.

(2011)




Tab

le2(Continued

)

Typ

e1Sy

stem

Inferred

conclusionby

authors:

cospeciationvs

hostshifts

Typ

eofsymbiont

Number

oftaxa

Methodsfor

testing

codivergen

ce%

cospeciation

even

tsinferred

Markersfor

phylogen

ies

Congruen

cein

time

ofdivergen

ceReferen

ces

4an

d5

Dove

s(Ave

s:Columbiform

es)

andlice

(Columbicola

and

Physconelloides)

Cospeciation

inbodylice

butnotin

winglice

Dove

bodylice

(Physconelloides)

and

dove

winglice

(Columbicola)para-

sitiz

ingpigeo

nsan

ddove

s,dove

bodylicebeing

more

host-specific

than

dove

winglice

13speciesof

dove

san

dtheir

associated

wing

andbodylice

TREEMAP

Ford

ove

winglice:4/

12cospeciation

even

ts,w

hichisnot

more

than

expected

bychan

ce.Forb

ody

lice:

8/12

cospeciation

even

ts,

congruen

cebeing

inferred

assignificant,butthe

numbersofother

even

tsassumed

are

notreported

Fortheparasite:

mitochondrial

COIan

d12S

rRNAan

dthe

nuclea

rEF

-1a

Forthehost:

mitochondrial

cytban

dthe

nuclea

rFIB7

Nottested

Clayton&

Johnson

(2003)

4an

d5

Figtree

s(Sycomorus)

andfigwasps

(Ceratosolenan

dApocryp

tophagus)

Cospeciation

formutualists

andhostshift

forparasites

Differenttypes

of

symbiontsoffigs:

Mutualistpollinator

Ceratosolenwasps

andparasite

Apocryp

tophagus

wasps

19speciesof

Sycomorusfigs.

19Ceratosolen

speciesan

d18

speciesof

Apocryp

-tophagus

TREEMAP

9–1

0cospeciation

(significant)for

mutualistsan

d7–8

fortheparasites

(notsignificant)

Forthesymbiotic

wasps:

mitochondrial

COI.

Forthehostfig:

ITS

Nottested

Weiblen&

Bush

(2002)

4an

d5

Chondracanthid

copep

odsan

dfishes

(Ophidiiform

es,

Pleuronectiform

es,

Scorpae

niform

es,

Zeiform

esan

dGad

iform

es)

Cospeciation

inonefish

order

butnot

inthesecond

Chondracanthid

copep

odsparasiticon

fish

considered

tobe

hostspecific

althoughthishas

beendeb

ated

26Chondr-

acanthusspp.

andtheirteleost

hostgen

era

from

five

orders

TREEMAP

Supportfor

cospeciationof

copep

odsan

dtheir

fish

hostsin

the

orders

Ophidiiform

es,

Pleuronectiform

es,

Scorpae

niform

esan

dZeiform

es,but

nosupportfor

cospeciationin

the

Gad

iform

es

Phylogen

ies

alread

ypublished

Not

tested

Paterson&

Poulin

(1999)

1Typ

e:1:convincingcasesofcospeciation(i.e.w

ithcomparisonofd

ivergen

cetimes):1a,mutualists,vertically

inherited

;1b,m

utualists;1c,en

doparasites;1d,parasites.2:cospeciationinferred

byau

thors,

buthostshiftspossiblymore

likelygiven

thehighnumber

ofother

even

tsinferred

(i.e.unlikelyhighnumber

ofintrah

ostspeciationan

dan

cestraln

umbersofparasites);ab

solute

timecongruen

cenot

tested

.3:cospeciationinferred

(i.e.significanttopologicalcongruen

ce,h

ighnumber

ofcospeciationev

ents)butcontrad

ictedbytimeinference

(either

absolute

orrelative);thisisindicativeofhostshifts

occurringpreferentiallybetweencloselyrelatedhosts(hostconservationism).4:frequen

thostshiftsinferred

byau

thorsbecau

seoflack

ofphylogen

eticcongruen

ce.5

:unclea

r(e.g.congruen

cewithout

absolute

timeinferred

orother

number

ofev

entsthan

cospeciationnotprovided

).ITS,

internaltran

scribed

spacer.





Clayton et al., 2003). Other ecological factors that may influencethe probability of codivergence include the abundance of the mainhost, the community of parasites, the degree of specialization, thepopulation sizes and generation times of hosts and symbionts(Whiteman et al., 2007; Gibson et al., 2010; Nieberding et al.,2010).

Notwithstanding the exemplary nature of the case of pocketgophers and their chewing lice, analyses of their association haveassumed multiple host shifts and intrahost speciation events toreconcile phylogenies, even with the great costs assumed forthese events (Light & Hafner, 2007). Lice species other thanthose of the pocket gopher have been investigated for codiver-gence. The heteromyid gophers, which are more social thanpocket gophers, display lower levels of tree congruence with theirsucking lice (Light & Hafner, 2008). Furthermore, the interceptof the regression line between the gopher and lice divergencetimes was significantly < 0, indicating that lice divergenceoccurred after host divergence (Light & Hafner, 2008).Similarly, the estimated dates of divergence between lice andprimates shows that the nodes in the host and parasite trees didnot coincide temporally (Reed et al., 2007). Nevertheless, event-based methods analyses misleadingly inferred ‘significant cospe-ciation’ (Page, 1996).

The most convincing examples of cospeciation appear toconcern mutualist associations in which the symbiont is transmit-ted vertically (Table 2, Fig. 5), as could be expected (Nieberding&Olivieri, 2007). A few host shifts have, nevertheless, been detectedin associations of mutualists with vertical transmission (Table 2,cases Fig. 1b).

Important conclusions from this literature review and theoreticalconsiderations are that symbiont speciation by host shift appears tobe more common than cospeciation – even more than is currentlyrecognized (Fig. 5, convincing examples of cospeciation representonly 7% of the cases) – and that the results of cophylogenetic testsare often overinterpreted to suggest cospeciation. A key questionthus concerns the short-term ecological and genetic mecha-nisms promoting host-shift speciation rather than cospeciation.Nieberding et al. (2010) put forward a list of ecological traits thatmight influence the degree of cospeciation. In the next section, weconsider the evolutionary mechanisms affecting the likelihood ofsymbiont specialization and speciation in relation to short-termcoevolution with hosts.

V. Relationship between host–symbiont coevolutionand symbiont speciation

We aim here to review the processes by which coevolutionarymechanisms can promote symbiont diversification. For this tooccur, coevolution must first foster the specialization of symbi-onts, which could then lead to speciation. We thus review studies(1) showing how coevolution can promote symbiont specializa-tion and (2) providing experimental and theoretical evidence forsymbiont specialization leading to speciation. We argue thatdivergence as a result of specialization may occur, but that itoccurs more frequently through host-shift speciation thancospeciation.

1. Coevolution: short-term host–parasite interaction

Host–parasite coevolution is a process of prolonged reciprocalselection, for better recognition of the parasite by its host, and forgreater infectious ability of the parasites and the prevision ofparasitism by the host. In the simplest systems, this selectioninvolves a single locus in each partner. Two outcomes for thedynamics of host and pathogen allele frequencies are commonlydistinguished under frequency-dependent selection (Holub, 2001;Woolhouse et al., 2002). The ‘arms race’ model describes allelefrequency dynamics where advantageous new variants go tofixation. By contrast, the ‘trench warfare’ model depicts allelefrequencies in oscillating dynamically over time or converging toequilibrium frequencies, resulting in the maintenance of severalhost and pathogen alleles (Brown & Tellier, 2011).

Another classification considers the dynamics of phenotypeshifts caused by selection. When the phenotype values always shiftin the same direction, as in predator–prey systems with density-dependent selection, the interaction has been termed ‘phenotypedifference’ (Dawkins & Krebs, 1979), whereas when the systemoscillates depending on the phenotypic value of the interactingspecies, as in most self/nonself recognition systems with frequency-dependent selection, the interaction has been called ‘phenotypematching’ (Lahti, 2005).

Such dynamical systems led Van Valen (1973) to refer to thecoevolutionary processes between hosts and parasites as ‘RedQueen’ dynamics, in reference to Lewis Carroll’s tale Through theLooking Glass (the RedQueen character explains to Alice that in herworld that ‘it takes all the running you can do, to keep in the sameplace’). His paper was the first to connect short-term coevolution-ary dynamics with macroevolution, including the long-termpersistence of species in particular. The question here is whethercoevolution, regardless of the prevailing mechanism (arms race,trench warfare, etc.), can actually directly promote parasitespecialization.

2. From coevolution to specialization, models andobservations

A priori, we might expect all species to be selected for theexploitation of broad ecological niches. Becoming a generalistdecreases the spatial and temporal risks and efforts required for foodcollection and ensures survival in conditions in which theavailability of particular resources may reveal unreliable. General-ism is common in plant viruses (Garcia-Arenal et al., 2003) and inanimal viruses (Pedersen et al., 2005). However, specializationseems to be far more common than generalism in various parasitespecies ranging from phytophagous insects (Dres &Mallet, 2002;Nyman, 2010) to fungi (Giraud et al., 2008) and avian parasites(Proctor & Owens, 2000).

The relative paucity of generalist parasitesmay result from trade-offs between the ability to infect a broad range of host species andoptimized rates of exploitation for any particular host type. Suchtrade-offshavebeenobserved in serial passage experiments, inwhichpropagating a microorganism on a host species different from itsoriginal host species consistently leads to a decrease in fitness on the




original host (Ebert, 1998). By contrast, the instability of hostabundance proposed as a factor explaining the evolution ofgeneralists in natural systems (Jaenike, 1990; Norton&Carpenter,1998) has received some experimental support (Soler et al., 2009).A combination of these selection pressures may occur, as bothspecialists and generalists have emerged in several experimentalevolution studies (Little et al., 2006; Poullain et al., 2008).

Factors favoring specialization even in the absence of fitnesstrade-offs and in the presence of stable host populations have beeninvestigated in theoretical studies. In particular, parasite

specializationmay also evolve because of themore rapid adaptationof specialists than generalists to each host species (Whitlock, 1996;Kawecki, 1998) as assumed in the ‘Red Queen dynamics’ theory(Whitlock, 1996). According to the model developed by Kawecki(1998), if recurrent selection for new alleles at the loci controllinginfectivity occurs because of coevolution, then specializationwill beselected for because specialist parasites adapt more rapidly thangeneralists. Indeed, selection for a greater ability to infect a givenhost operates at every generation in specialized parasites, but onlyoccasionally in generalists distributed between several host species.

Fig. 5 Illustration of the literature survey inTable 2, with number of cases representingeither convincing cases of cospeciation (inred), cases of host shifts inferred fromincongruent topologies, discordant times ofdivergence or likely given the high number ofduplication and extinction inferred (in blue), orfinally unclear cases (in green).

Box 1 Glossary

Codivergence Process whereby a symbiont population or species splits at the same time as that of its host population or species. This is a patternand does not assume causal relationships.

Coevolution (to bedistinguished fromcospeciation)

Process of never-ending reciprocal selection for improvements in parasite recognition in the host, and for improvements inrecognition escape mechanisms in the parasite.

Congruence Phylogenetic trees are said to be congruent when their topologies are highly similar; temporal congruence also implies that thecorresponding nodes are of similar ages in the two phylogenies.

Cospeciation Process whereby a symbiont speciates at the same time as another species (this may result from vicarious events or from narrowhost specificity). This is a pattern and does not assume causal relationships.

Generalist Symbiont able to take resources from different host species.Host Organism from which another smaller organism (the symbiont), from another species, takes resources; the symbiont may be

either a parasite or a mutualist. Mutualists also provide the host with resources.Host-shift speciation Speciation of the symbiont by specialization of a daughter species on a new host.Intrahost speciation(called ‘duplication’in some papers andcophylogenysoftware)

Speciation of the symbiont without speciation of the host or host shift: both daughter symbiont species continue to parasitize thesame host species. This may be because of vicarious events affecting only the symbiont or specialization on different organs ofthe host.

Mutualist Organism both taking and resources from and providing resources to another larger organism (the host), from another species,resulting in an overall increase in host fitness.

Parasite Organism taking resources from another larger organism (the host), from another species, decreasing host fitness.Specialist Symbiont able to take resources from a single host species.Symbiont Organism taking resources from another larger organism (the host) from another species. The symbiont is either a parasite or a

mutualist. Mutualists also provide the host with resources.





The chances of specialist parasites to persist are thus increased. Inaddition, once a species specializes in a narrow niche, the otherspecies suffer less competition in the alternative niches, indirectlypromoting specialization on these other niches (Whitlock, 1996).In summary, specialization (i.e. the formation of host races inparasites) can be promoted directly by coevolution because of theimprobability of success on several different hosts and/or a higherrate of adaptation of specialists, and indirectly through competitionwith other specialist species.

Theoretical models have shown that the type of interaction maydetermine whether coevolution promotes or hinders specializationin both hosts and parasites (Yoder &Nuismer, 2010). Interactionsmediated by phenotype matching promote specialization of thespecies experiencing a cost of phenotype matching, for example,pathogens being recognized by hosts and prevented from infecting.By contrast, they inhibit specialization of the interacting speciesthat benefit from phenotypicmatching, for example, the host beingable to detect a pathogen and thereby impair infection (Yoder &Nuismer, 2010).

Cospeciation or host-shift speciation thus requires host speci-ation by independent mechanisms, such as geographic isolation, orparasite specialization by the mechanisms described earlierfollowed by parasite speciation. In the next section, we presenttheoretical considerations concerning the effects of specializationon parasite speciation.

3. Specialization and parasite speciation, theoreticalconsiderations

The evolution of host-specific genotypes leads to the emergence ofspecialist parasite species only if reproductive isolation also occurs(Giraud et al., 2008). This corresponds to ecological speciation, inwhich parasite species occupying different niches (i.e. different hostspecies) become reproductively isolated one from another (Giraudet al., 2010). The possibility of ecological speciation has beensupported by many different studies on systems as diverse asherbivorous insects, vertebrates and plants (for reviews, see Hendryet al., 2007; Nyman, 2010).

Two factors promote the evolution of reproductive isolation inpopulations adapted to different ecological niches. First, thereshould be low levels of dispersal among populations (Hendry et al.,2007). Second, mating should occur only among individualsspecialized for the niche (Rice, 1984), by means of adaptedbehavior (Funk, 1998), specific life-history traits, such as themating of microbial parasites within hosts after infection (Giraudet al., 2006, 2010), or physical linkage between the loci controllingniche choice and mate choice (Slatkin, 1996). For example, peaaphids harbor tightly linked loci controlling host preference andmating preference, potentially facilitating the observed divergencebetween species (Hawthorne & Via, 2001). Phytophagous insectsexperience selection against mating with congeners feeding on adifferent plant species, potentially contributing to future diver-gence (Johnson et al., 1996; Nosil et al., 2002; Egan et al., 2008).Fungal ascomycete plant parasites thatmatewithin their host plantsdisplay high rates of divergence without selection for strongintersterility, possibly because the genes responsible for adaptation

to the host pleiotropically cause reproductive isolation (Peever,2007; Le Gac & Giraud, 2008; Giraud et al., 2010). As a result,parasite specialization seems to contribute to diversificationthrough speciation in various systems. The speed at which thisspeciation occurs depends on many factors, including parasite andhost generation time, dispersal rates and effective population size(Huyse et al., 2005).

Coevolution thus clearly fosters parasite speciation by special-ization to particular hosts (for a review, see Summers et al., 2003)such that specialization of two parasite lineages on sister hostspecies may result in a cospeciation event. However, is cospeciationthe most likely outcome in the long term, as is often implicitlyassumed? The reasons for disruption of a host–parasite associationare numerous, and such disruption may interfere with long-termparallel evolution between hosts and parasites, even in highlyspecialized lineages. Parasites may go extinct or may have a lowincidence in host populations or small population sizes, such that ahost speciation event may be missed. This becomes highlyprobable if, for example, a new host species originates by foundinga population in allopatry from only a few individuals that are freeof parasites. Many examples are known of biological invasions inwhich a population of hosts invading a new continent haveundergone ‘enemy release’ (Keane & Crawley, 2002; Gentonet al., 2005). Extinctions are also quite frequent in parasites owingto, for example, the evolution of resistance in host, decreasingniche size (Thrall et al., 1993; Ricklefs, 2010), or to a decline inhost population size (de Castro & Bolker, 2005). Indeed,endangered plant and animal species, with their smaller and morefragmented population structures, have been shown to harbor alower diversity of parasites than hosts with larger population sizes(Altizer et al., 2007; Gibson et al., 2010). Small host populationsizes may not be compatible with the persistence of specialistpathogens (de Castro & Bolker, 2005), and this may be anotherreason for which coevolution does not promote cospeciation:incipient host species often have small populations and thereforecannot sustain specialist parasites evolving with them. If coevo-lution hinders the persistence of generalist parasites, as arguedearlier, it would even decrease the probability of cospeciation incases in which the new host species is initially present as smallpopulations. In the few cases in which the dates of divergenceevents have been estimated, plant speciation has been shown to befollowed by rapid host shifts of parasites, as reported for Eiosmothson Piper plants (Wilson et al., 2012).

The converse question of whether parasites can trigger hostspeciation has been less explored. Cophylogenetic analyses showthat speciation occurs at a higher rate in primate lineages harboringlarger numbers of parasites (Nunn et al., 2004), so theremaywell bereciprocal influences on speciation of hosts and parasites (but seealso Pedersen & Davies, 2009). By contrast, some experimentalstudies have suggested that coevolution with parasites may hinderhost diversification (Buckling & Rainey, 2002).

Overall, theoretical evidence and natural observations ofcomplexes of sibling species of parasites suggest that coevolutionmay promote parasite speciation via specialization on differenthosts. As a consequence of specialization, parasites may thus beexpected to form two different species as a host lineage splits, and




this is termed cospeciation. However, this leads to cospeciationpatterns only if parasites remain associated with the same hostlineages throughout host speciation events. This assumption ofcontinuity of host–parasite associations during speciation is rarelymade explicitly or tested directly. In addition, we argued earlier thatthere may be reasons why coevolution could impede cospeciation.By reviewing cophylogenetic analyses, we have shown that host-shift speciations seem to bemuchmore prevalent than cospeciationin host–parasite associations, even noting the predominant influ-ence of coevolution over short time-scales. In any case, the rareinstances of convincing codivergence relate to vertically inheritedmutualists, where host shifts can still be observed even in thesesystems (Table 2).

VI. Conclusion

Several important conclusions can be drawn fromour review on thetheoretical advances and available data concerning long-term hostand parasite coevolutionary dynamics:(1) Parasite speciation was long expected to follow the Fahrenholzrule of cospeciation (‘parasite phylogeny mirrors that of the host’),but we have seen that speciation following host shifts (host-shiftspeciation) is at least as likely as cospeciation. The early studiessuggesting a predominance of cospeciation are now subject to somedoubt with the use of larger samples and the advent ofmore reliableand powerful tools for comparing phylogenies. In many instances,parasites have been shown to divergemore recently than their hosts,mostly by host-shift speciation. In the rare cases where cospeciationseems to have occurred, the synchronous divergence of host andparasite lineages seems to result primarily from strict verticalinheritance, rather than the reciprocal selection pressures exerted bythe partners.(2) As the reciprocal selection pressures between hosts andparasites do not prevent speciation mechanisms other thancospeciation, coevolution does not imply widespread cospeciation.We argue that the term ‘coevolution’ should be used only to meanreciprocal selection pressure in host and parasite systems, as alreadyadvocated by other authors (Smith et al., 2008a), and that this termshould not refer simply to patterns of diversification.(3) The concept of cospeciation has fostered the development ofvery useful tools for comparing phylogenies, based on systems withinteresting ecological features (such as the pocket gophers and theirchewing lice). Although the basis of the cospeciation concept – thattight physiological interaction leads to parallel speciation – has nowlargely been invalidated, the methods developed so far have help usto understand the extent to which the partners in a host–symbiontsystem influence their own diversification. For example, do host-shift speciations occur more frequently between more closelyrelated hosts or between hosts with similar ecological traits? Weargue that the results obtained with any of cophylogenetic methodsshould be interpreted with caution because many of these methodsoverestimate the probability of cospeciation. Most importantly,evaluating the temporal coincidence of speciation events insymbionts and hosts, with calibrated phylogenies, is required todistinguish between cospeciation and host-shift speciations onclosely related host species.

(4) Further methodological developments would be also welcomein the field. For example, Nieberding et al. (2010) proposed amethod that could be used to identify ecological traits (e.g. numberof host species, abundance of main host, degree of specialization,dispersal ability, population sizes of hosts and symbionts, sex ratioand generation time) influencing the cophylogenetic pattern. Suchcophylogenetic analyses of ecological traits have revealed, forexample, that dispersal, rather than an ability to colonize new hosts,seems to be the main factor affecting codivergence in the louse–pocket gopher system (Reed&Hafner, 1997;Clayton et al., 2004).Further developments would also be welcome for the analysis ofbiological networks, the neutral theory of tree diversity andphylogenetic community structure models.

Acknowledgements

This work was funded by grants ANR 06-BLAN-0201 and ANR07-BDIV-003. A.T. thanks the Volkswagen Stiftung (grantI/82752) and DFG (grant HU1776/1 to S. Hutter) for financialsupport.M.E.H. received funding fromgrantNSF-DEB0747222.We thankNova Science Publishers, Inc. for permission to use someof the text from Tellier et al. (2010). We thank the anonymousreferees for their helpful comments and we apologize to all thosecolleagues whose work we have omitted to cite in this article.

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