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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
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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
� 2013 The Authors
New Phytologist� 2013 New Phytologist TrustNew Phytologist (2013) 198: 347–385
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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)
Cospeciationconsidered
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
Cospeciationconsidered
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
Cospeciationconsidered
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
Cospeciationconsidered
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
Cospeciationconsidered
themost
parsimonioushyp
othesis
Cospeciationscannotbemore
costlythan
host-shift
speciations
Possibletimingincompatibilities
lead
ingto
potentiallyerroneo
us
conclusions
Ronquist(1995)
http://sourceforge.
net/projects/
treefitter/
New Phytologist (2013) 198: 347–385 � 2013 The Authors
New Phytologist� 2013 New Phytologist Trustwww.newphytologist.com
Review Tansley reviewNewPhytologist350
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
Cospeciationconsidered
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
� 2013 The Authors
New Phytologist� 2013 New Phytologist TrustNew Phytologist (2013) 198: 347–385
www.newphytologist.com
NewPhytologist Tansley review Review 351
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.
New Phytologist (2013) 198: 347–385 � 2013 The Authors
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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.
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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.
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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.
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NewPhytologist Tansley review Review 355
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)
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Review Tansley reviewNewPhytologist356
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)
� 2013 The Authors
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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)
New Phytologist (2013) 198: 347–385 � 2013 The Authors
New Phytologist� 2013 New Phytologist Trustwww.newphytologist.com
Review Tansley reviewNewPhytologist358
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
gophers
Codivergen
ceChew
ingparasite
licean
dtheir
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)
� 2013 The Authors
New Phytologist� 2013 New Phytologist TrustNew Phytologist (2013) 198: 347–385
www.newphytologist.com
NewPhytologist Tansley review Review 359
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)
New Phytologist (2013) 198: 347–385 � 2013 The Authors
New Phytologist� 2013 New Phytologist Trustwww.newphytologist.com
Review Tansley reviewNewPhytologist360
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)
� 2013 The Authors
New Phytologist� 2013 New Phytologist TrustNew Phytologist (2013) 198: 347–385
www.newphytologist.com
NewPhytologist Tansley review Review 361
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
gophers
Preva
lent
cospeciation
Highlyhost-specific
parasiticchew
ing
liceonpocket
gophersoccurring
onasingle
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)
New Phytologist (2013) 198: 347–385 � 2013 The Authors
New Phytologist� 2013 New Phytologist Trustwww.newphytologist.com
Review Tansley reviewNewPhytologist362
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)
� 2013 The Authors
New Phytologist� 2013 New Phytologist TrustNew Phytologist (2013) 198: 347–385
www.newphytologist.com
NewPhytologist Tansley review Review 363
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)
New Phytologist (2013) 198: 347–385 � 2013 The Authors
New Phytologist� 2013 New Phytologist Trustwww.newphytologist.com
Review Tansley reviewNewPhytologist364
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)
� 2013 The Authors
New Phytologist� 2013 New Phytologist TrustNew Phytologist (2013) 198: 347–385
www.newphytologist.com
NewPhytologist Tansley review Review 365
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)
New Phytologist (2013) 198: 347–385 � 2013 The Authors
New Phytologist� 2013 New Phytologist Trustwww.newphytologist.com
Review Tansley reviewNewPhytologist366
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
Parasiticrelationship:
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)
� 2013 The Authors
New Phytologist� 2013 New Phytologist TrustNew Phytologist (2013) 198: 347–385
www.newphytologist.com
NewPhytologist Tansley review Review 367
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)
New Phytologist (2013) 198: 347–385 � 2013 The Authors
New Phytologist� 2013 New Phytologist Trustwww.newphytologist.com
Review Tansley reviewNewPhytologist368
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)
� 2013 The Authors
New Phytologist� 2013 New Phytologist TrustNew Phytologist (2013) 198: 347–385
www.newphytologist.com
NewPhytologist Tansley review Review 369
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)
New Phytologist (2013) 198: 347–385 � 2013 The Authors
New Phytologist� 2013 New Phytologist Trustwww.newphytologist.com
Review Tansley reviewNewPhytologist370
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)
� 2013 The Authors
New Phytologist� 2013 New Phytologist TrustNew Phytologist (2013) 198: 347–385
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NewPhytologist Tansley review Review 371
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)
New Phytologist (2013) 198: 347–385 � 2013 The Authors
New Phytologist� 2013 New Phytologist Trustwww.newphytologist.com
Review Tansley reviewNewPhytologist372
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)
� 2013 The Authors
New Phytologist� 2013 New Phytologist TrustNew Phytologist (2013) 198: 347–385
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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)
New Phytologist (2013) 198: 347–385 � 2013 The Authors
New Phytologist� 2013 New Phytologist Trustwww.newphytologist.com
Review Tansley reviewNewPhytologist374
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)
� 2013 The Authors
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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
Parasiticrelationship:
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)
New Phytologist (2013) 198: 347–385 � 2013 The Authors
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Review Tansley reviewNewPhytologist376
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.
� 2013 The Authors
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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
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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.
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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
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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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