doi: 10.1111/j.1420-9101.2007.01340.x
When can host shifts produce congruent host and parasite
phylogenies? A simulation approach
D. M. DE VIENNE, T. GIRAUD & J. A. SHYKOFF
Ecologie, Systématique et Evolution, UMR 8079 CNRS-Université Paris Sud, Université Paris Sud, Orsay Cedex, France
Keywords:
Abstract
coevolution;
COMPONENT;
cophylogenetic analysis;
host shift;
reconciliation;
TREEFITTER;
TREEMAP.
Congruence between host and parasite phylogenies is often taken as evidence
for cospeciation. However, ‘pseudocospeciation’, resulting from host-switches
followed by parasite speciation, may also generate congruent trees. To
investigate this process and the conditions favouring its appearance, we here
simulated the adaptive radiation of a parasite onto a new range of hosts.
A very high congruence between the host tree and the resulting parasite trees
was obtained when parasites switched between closely related hosts. Setting a
shorter time lag for speciation after switches between distantly related hosts
further increased the degree of congruence. The shape of the host tree,
however, had a strong impact, as no congruence could be obtained when
starting with highly unbalanced host trees. The strong congruences obtained
were erroneously interpreted as the result of cospeciations by commonly used
phylogenetic software packages despite the fact that all speciations resulted
from host-switches in our model. These results highlight the importance of
estimating the age of nodes in host and parasite phylogenies when testing for
cospeciation and also demonstrate that the results obtained with software
packages simulating evolutionary events must be interpreted with caution.
Introduction
Host–parasite interactions now occupy a central place in
studies of evolutionary ecology, thanks to, among others,
the seminal work of Price (1980) and the ground
breaking papers of Hamilton (1980) and Hamilton &
Zuk (1982). With the development of molecular biology,
and hence molecular phylogenies, these interactions
have been studied in a new way: the joint analysis of
host and parasite phylogenies, or cophylogenetic analysis. These analyses of molecular data revealed that
phylogenies of interacting taxa sometimes have very
similar and even identical topologies (for a review, see
Page, 2003), referred to as congruence. This congruence
is considered to be generated by multiple cospeciation
events of host and parasite.
Cospeciation as the process generating congruence has
received much attention (Hafner et al., 1994; Page, 1994;
Peek et al., 1998; Dimcheff et al., 2000; Nuismer et al.,
Correspondence: Damien de Vienne Laboratoire Ecologie, Systématique et
Evolution Département Génétique et Ecologie Evolutives Université Paris
Sud, Bâtiment 360, 91405 Orsay Cedex, France. Tel.: +33 1 69 15 56 64;
fax: +33 169 154697; e-mail: [email protected]
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2003; Downie & Gullan, 2005). Its underlying premise is
that parasite speciation follows in a stepwise manner that
of its hosts or that hosts and parasites speciate simultaneously. This generates similar phylogenies of these two
sets of species as is found in the well-known association
between pocket gophers and their chewing lice (Hafner &
Nadler, 1988; Hafner et al., 1994). Although complete
congruence between host and parasite phylogenies is
rare, examples of phylogenies that are more congruent
than expected by chance are pervasive. These include
interactions as diverse as plants and insects (Itino et al.,
2001; Lopez-Vaamonde et al., 2001; Ronquist & Liljeblad,
2001), penguins and their lice (Banks et al., 2006), plants
and fungi (Holst-Jensen et al., 1997; Jackson, 2004),
animals and viruses (Dimcheff et al., 2000), fish and
Monogenes (Desdevises et al., 2002) or lizards and
malaria (Charleston & Perkins, 2003). Because congruence is assumed to arise from cospeciation, various
processes, such as host-switch, extinction, duplication
(i.e. intrahost speciation) and failure to speciate in
response to speciation in the other lineage (i.e. ‘missing
the boat’ or sorting events), are proposed to account for
these incomplete congruences (for a review, see Page,
2003, chapter I). Moreover, the hypothesis of cospeciation
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Conditions favouring pseudocospeciation
implies a temporal congruence between the two phylogenies (i.e. similar ages of the nodes, Page, 1996), which is
rarely tested (but see Hafner & Nadler, 1988).
We explore here an alternative mechanism that can
give rise to topological congruence between host and
parasite phylogenies: an adaptive radiation of a parasite
on a range of host species, by multiple host-switches at
the tip of the host phylogeny followed by speciation. This
idea has been proposed by some authors (Hafner &
Nadler, 1988; Hafner et al., 1994; Page, 1996; Roy, 2001)
and clearly explained by Paterson & Banks (2001):
‘Congruence, in itself, means little, as congruence may
be generated by parasites undergoing a series of hostswitches that mirror the host phylogeny[…]’. This
mechanism, called ‘pseudocospeciation’ (Hafner &
Nadler, 1988), is, however, rarely taken into account in
cophylogenetic studies and many authors still consider
congruence to result from cospeciation and incongruence
to result from host-switches (Brooks & McLennan, 1991).
The idea that congruence between host and parasite
trees can arise following preferential host-switching has
been verified by Charleston & Robertson (2002) in a
particular case. They observed that the phylogenies of
primates and their lentiviruses were more congruent
than expected by chance. Simulations of parasites
switching hosts at the tips of the primate phylogeny
generated similar levels of congruence between host and
parasite phylogeny when parasites were more likely to
switch between close relatives. However, the conditions
favouring pseudocospeciation have not been examined
in a systematic and general way to date. To fill this large
gap in our understanding of host–parasite evolutionary
interactions, we used a simulation approach of the
adaptive radiation of a parasite on a set of pre-existing
host species to determine what conditions other than
cospeciation could generate congruent host and parasite
phylogenies.
We modelled the arrival of a new parasite onto a
speciose host clade whose phylogeny was known. This
parasite then colonizes new hosts by switching between
terminal lineages with a probability that depends on the
relatedness between hosts and speciates either immediately or after a time lag. Once all hosts are parasitized, we
construct the phylogenetic tree of the parasites and
examine its shape and its congruence with the host tree.
We performed simulations with three host trees having
different topologies, from completely unbalanced to
highly balanced. We examined the effect of different
parameters concerning host and parasite behaviours and
evolution on the congruence between host and parasite
trees, such as host-switch probabilities, first host parasitized, shape of the host tree and time lag between a
switch and the speciation following this switch. Note that
here we did not simulate coevolution, the hosts neither
evolving nor speciating during the adaptive radiation of
their parasites. This situation can arise during biological
invasions or shifts of a parasite onto a new clade of pre-
1429
existing hosts. Clearly, such a process does not preclude
that the hosts can also speciate during the adaptive
radiation of their parasites.
Obviously, some simplifying assumptions and rules
had to be imposed: (1) we did not allow parasites to
sequentially replace each other on a particular host
species; (2) we did not allow more than one parasite
species to parasitize the same host; (3) parasites speciated
much more rapidly than did hosts (the phylogeny of the
host remained unchanged during the adaptive radiation
of the parasites); (4) no parasites went extinct; and (5)
speciation always followed a host-switch, although more
or less rapidly.
Our study thus differs from the one carried out by
Charleston & Robertson (2002) by the wider range of
hypotheses tested concerning host tree shape, first host
parasitized, ‘preferential’ host-switches performed by
parasites and time lag between switch and speciation,
as well as by precluding the replacement of parasites on a
given host.
Here, we address the following questions: (i) What
conditions of host-switch probabilities, time lag before
speciation, first host parasitized and topology of the host
tree generate the most congruence? (ii) Can the comparison between host and parasite phylogenies give us
any information about the evolutionary history of the
two interacting species? (iii) Can the model we propose
here contribute to a better understanding of the genetic
basis of host–parasite interactions?
Congruence between host and parasite trees was
assessed using cophylogenetic analysis software including
the event-based parsimony method implemented in
TREEFITTER (Ronquist, 1995). This software estimates,
for two given phylogenies, the most parsimonious evolutionary history of the two lineages by assigning to
cospeciation, duplication, sorting and switching events
different costs, without requiring knowledge of branch
lengths. We also used TREEMAP and COMPONENT in
one particular case where our model generated high
congruence to render our results comparable with
previous experimental work. Using these analytical
methods also allowed us to explore their limits because
the only type of evolutionary event that was simulated
here was host-switch, so all cospeciation, sorting and
duplication events inferred by TREEFITTER and TREEMAP were artefacts.
The model
General description
We simulated the colonization of a set of hosts with
known phylogenetic relationships by a new parasite,
through the following steps: (1) arrival of the parasite on
one host; (2) sequential switches from one tip of the host
phylogeny to another (host range expansion followed by
speciation after a certain time lag), each switch thus
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D. M. DE VIENNE ET AL.
giving rise to two parasite species specialized on two
different hosts; we considered that a given host could not
be parasitized by more than one parasite species; (3) once
all the hosts were parasitized, the phylogeny of the
parasites was constructed based on the order of the
switches and the timing of the speciations; and (4)
the topological congruence between this tree and the
host tree was estimated.
Simulations were performed under varying values for
the following parameters: (1) the topology of the host
tree; (2) the identity of the host that the parasite initially
infects (e.g. its degree of isolation); (3) how the probability of switch between two hosts depended on their
phylogenetic distance (e.g. switches more likely between
closely related hosts or switches more likely between
distantly related hosts); and (iv) the time lag before
speciation after a host-switch, depending on the phylogenetic distance between the hosts.
Note that the trees in this study have no branch
lengths sensu stricto. The term ‘phylogenetic distance’ will
be used to describe the number of evolutionary units
separating two given species in the trees. An evolutionary unit is the minimal time between two cladogenesis
events, i.e. the shortest distance between two nodes (see
Fig. 1a; for example, the phylogenetic distance between
hosts 2 and 3 is four units).
Simulations were run with each of the 12 hosts being
parasitized first.
Host-switch probabilities
The probability for a switch from an host X (parasitized)
to an host Y (not yet parasitized) was determined by: (1)
the phylogenetic distance between hosts X and Y, dXY;
and (2) by the isolation of host X in the tree, which
depends on the distances between each nonparasitized
host (Hj) with all other hosts (H) in the tree, dHHj. Three
assumptions on host-switch probabilities were considered, depending on host phylogenetic distances.
(1) Higher probability for switches between phylogenetically
close hosts. The probability p for a parasite to switch from
the host X to the host Y was computed as:
edXY
PX!Y ¼ P dHHj
e
j
Note that in this case, on host tree A, when host 12 is
the first host parasitized, any host-switch is highly
improbable because host 12 is highly isolated, but if a
switch does occur each of the possible hosts is equally
likely to be colonized.
(2) Lower probability for switches between phylogenetically
close hosts. The probability P for a switch from host X to
host Y was computed as:
Host trees used for the simulations
Three rooted host trees with 12 species each and
particular topologies were chosen. The first one was
completely unbalanced, the second one was intermediate
and the last one was the most balanced possible (Fig. 1A–
C respectively).
The first host parasitized
We assessed the effect of the degree of isolation in the
phylogeny of the first host parasitized on the congruence
between the host tree and the parasite tree resulting from
simulations. The degree of isolation of a given host
species in the phylogeny was estimated as its mean
phylogenetic distance to the other hosts divided by the
mean of the distances between all pairs of hosts.
12
11
10
9
8
7
6
5
4
3
2
1
A
edXY
PX!Y ¼ P dHHj
e
ð2Þ
j
The use of exponential functions as well as the fact that
we took into account the isolation of the host in these
two formulae allowed us to maximize the effect of the
between-host phylogenetic distance on the behaviour of
the parasites. The denominator allows one to have a
complete system of events (PH fi Hj).
(3) Equiprobability for all switches. The probability p for a
switch from host X to host Y was computed as:
PX!Y ¼
1
NHj NHi
ð3Þ
where NHi and NHj are the number of already parasitized
hosts and not yet parasitized hosts respectively.
9
10
11
12
1
2
3
4
5
6
7
8
9
10
11
12
8
7
6
5
1
2
3
4
0.1
B
ð1Þ
C
Fig. 1 The three host trees used for simulations. The black dots represent the roots of
the trees. The evolutionary units used as a
measure of ‘phylogenetic distance’ are represented at the bottom of tree A.
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Conditions favouring pseudocospeciation
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1
0.9
Fig. 2 Probabilities for a parasite colonizing
host 1 of the host tree A to switch to each of
the other hosts with increasing phylogenetic
distances from host 1, for the three different
functions of host-switch probability: the
dashed line represents the equiprobability for
all switches, the plain line a high probability
for switches to phylogenetically close hosts
and the dotted line a high probability for
switches to phylogenetically distant hosts.
Host-switch probability
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
2
4
Time lag between host range expansion and
speciation
Initial simulations considered that speciation immediately followed host range expansion. We subsequently
included the ability for the parasite to remain generalist
for a certain time. Two types of time lag between host
range expansion and speciation were considered.
(1) Shorter time lag for switches between phylogenetically
closer hosts. The time lag between the switch of the
parasite on the host X to the host Y and speciation
between the parasites on hosts X and Y (tXY) was then
computed as:
ð4Þ
with k being the ‘generalism coefficient’, a dimensionfree constant calibrating the global propensity of parasites
to remain generalist, and dXY the phylogenetic distance
between the hosts X and Y.
(2) Shorter time lag for switches between phylogenetically more
distant hosts. The time lag between the switch of the
parasite on the host X to the host Y and speciation
between the parasites on hosts X and Y (tXY) was then:
tXY ¼
k
dXY
8
10
12
14
16
18
20
22
Phylogenetic distance
To illustrate the above equations, we represented the
switch probabilities for a parasite that first colonized host
1 of host tree A to switch to each of the 11 other (not yet
parasitized) hosts as a function of the pairwise phylogenetic distances between host 1 and each other host
(Fig. 2). Note that these probabilities are perfectly symmetrical and very stringent.
tXY ¼ kdXY
6
ð5Þ
We ran simulations with k ranging from 10 to 300 with
steps of 10 units. We could find no studies that allowed
us to estimate this parameter but our aim was to
investigate whether a tendency to remain generalist
longer would influence the degree of congruence
between host and parasite phylogenies.
Note that host-switches continued to take place during
the period where a particular parasite remains generalist
and even for generalist parasites that occupy more than
one host.
Generation, comparison and imbalance of the trees
The program was written using the software R, version
2.0.1 (Ihaka & Gentleman, 1996), with the package
‘ape’ (Analyses of Phylogenetics and Evolution, Paradis
et al., 2004). The code of the program is available on
request.
Random trees were generated to: (1) compare
observed vs. expected congruence between host and
parasite trees; and (2) explore the impact of the
imbalance of the host trees on the expected degree of
congruence among random trees to control for this
parameter in our comparisons. These random trees were
generated using COMPONENT 2.0 (Page, 1993) whose
seed for the random number generator is taken from
the system clock and whose algorithm for generating
rooted labelled trees is the one described by Furnas
(1984).
We ran 1000 simulations of adaptive radiations for
each of the different combinations of host tree shape,
initially parasitized host, assumption on host-switch
probability and assumption on time lag between host
range expansion and speciation. Using the software
TREEFITTER version 1.0 (Ronquist, 1995, 1997), the
host trees were compared with: (1) the 1000 parasite
trees resulting from our simulation for each combination of parameters; and (2) 1000 randomly generated
trees, to compare the congruence observed in (1) to the
level of congruence expected by chance. Note that
TREEFITTER can generate random trees for each comparison of one host tree to one parasite tree, but we
chose not to use this function because the time needed
to do the tests was too long given the large number of
comparisons. We used the default values of the parameters, suggested in the software, giving costs for
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D. M. DE VIENNE ET AL.
codivergence, duplication, sorting and switching events
were set to 0, 0, 1 and 2, as respectively. TREEFITTER
estimates the minimum and maximum numbers of each
of these four types of events for each pair of host and
parasite trees, representing the range over all equally
optimal reconstructions (i.e. same cost). We chose the
minimum number of cospeciation events estimated to
give us a conservative estimate of congruence. Clearly,
the maximum number of cospeciation events yielded an
even higher degree of congruence. For each comparison
of one host tree to the 1000 corresponding parasite trees
generated by our model, as well as to the 1000
randomly generated ones, the mean proportion of
estimated cospeciation events among the total number
of events was calculated and taken as the degree of
congruence between the host and parasite trees. Indeed,
if the trees are highly congruent, TREEFITTER estimates
a high number of cospeciation events (the maximum
number of cospeciation events being the number of
nodes in the phylogenies) and few, if any, duplication,
switching or sorting events. In this case, the proportion
of cospeciation events among the total number of
events will be close to or equal to one. If the trees are
not topologically more similar than expected by chance
alone, the number of cospeciation events estimated by
TREEFITTER will be low and the number of duplication,
switching and sorting events will be high. The mean
proportion of estimated cospeciation events among the
total number of events will then be close to what is
obtained when comparing one host tree with 1000
randomly generated trees.
TREEFITTER was preferred to other available similar
software packages, such as TREEMAP (Page, 1994),
because it allows fitting any number of parasite trees to
a given host tree and can execute commands from
external files, allowing us to perform a high number of
comparisons. We used two additional software packages
for the set of parameters that generated the most
completely congruent host and parasite phylogenies:
(1) COMPONENT 2.0 (Page, 1993) assessed the plain
topological congruence between trees without inferring
evolutionary events by counting the number of species
that had to be removed in the host and the parasites
phylogenies to obtain identical trees (Kubicka et al.,
1995); the smaller this number, the more congruent
the phylogenies. (2) TREEMAP v1.0a (Page, 1994) was
used because it is one of the most frequently used
software packages for cophylogenetic analyses.
The imbalance of the three host trees was calculated
using the modification to Fusco & Cronk’s (1995) method
proposed by Purvis et al. (2002) and programmed with R,
version 2.0.1 (Ihaka & Gentleman, 1996).
Because our study was based on simulations, we did
not perform statistical tests, as the significance of a test
depends upon the number of runs. We therefore decided
to analyse and present the results in a qualitative instead
of a quantitative manner.
Results
Congruence with random trees
Congruence with random trees, estimated as the mean
proportion of estimated cospeciation events when comparing one host tree with 1000 randomly generated trees,
differed for the three host trees used in this study: these
values were 0.266, 0.298 and 0.307 for host trees A, B
and C respectively. This discrepancy is probably due to
the fact that the three host trees do not have the same
probability of being obtained by chance. Indeed, over
10 000 randomly generated trees with 12 species, when
the range of the imbalance values of these trees was
divided into 20 classes, the imbalance values for the trees
A, B and C fell within classes containing 6.86%, 4.08%
and 0.05% of the total number of trees respectively (data
not shown). Because two completely congruent trees
necessarily have the same level of imbalance, different
probabilities of generating trees with particular degrees of
imbalance can explain the difference between the three
host trees we used on their level of congruence with
random trees.
Speciation immediately following host range
expansion
Effects of the topology of the host tree and of the hostswitch probabilities
We first investigated the effects of the topology of the
host tree and of the three different host-switch probabilities on the congruence between the host tree and the
parasite trees when parasites speciate immediately after
host shift. For the host trees B and C, and for the host tree
A with high probability of distant switches or equiprobability for all switches, each tree was compared with
12 000 parasite trees generated by our program (1000
simulations for each of the 12 hosts initially parasitized).
For the host tree A and a high probability for close
switches, the parasite had too low a probability to
perform the first switch when initially on hosts 9, 10,
11 or 12, so the host tree A was compared with only 8000
parasite trees (hosts 1–8 and 1000 parasite trees generated for each host parasitized first).
Most combinations of host tree topology and relatedness-dependent probabilities of host-switches yielded
parasite trees that were not different from random trees
in terms of the mean proportion of estimated cospeciation events (Fig. 3). This was always true for host tree A.
However, for host trees B and C, when switches were
more likely towards phylogenetically close hosts, parasite
adaptive radiation yielded trees that were more congruent to host trees than were random trees (Fig. 3, cases 2),
leading TREEFITTER to estimate a higher mean proportion of estimated cospeciation events than for random
trees. This effect was most pronounced for the highly
balanced host tree C. However, congruence was never
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Mean proportion of estimated cospeciation events
Conditions favouring pseudocospeciation
1
HOST B
HOST A
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HOST C
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
(1)
(2)
(3)
(1)
(2)
(3)
(1)
(2)
(3)
0
Fig. 3 Mean proportion of cospeciation events estimated by TREEFITTER when comparing the three host trees (A, B and C) and 1000 parasite
trees generated under three different hypotheses: (1) equiprobability for all host-switches, (2) high probability for switches to phylogenetically
close hosts, (3) high probability for switches to phylogenetically distant hosts. For each host tree and each type of most probable switch, the
different points represent the cases of each particular host being parasitized first (host 1 to host 12 from left to right). The grey dots represent the
mean number of species pruned when comparing each one of the three host trees with 1000 randomly generated trees. For all points, the
standard errors are smaller than the size of the dots themselves.
very high, the mean proportion of estimated cospeciation
events never approaching 1. For host trees B and C,
when the probability for shifts to phylogenetically distant
hosts was high, the mean proportion of estimated
cospeciation events was slightly lower than for random
parasite trees (Fig. 3, cases 3).
Effect of the first host parasitized
The first host parasitized further influenced the congruence, but mainly when the switches were not equiprobable and when the host tree was not completely
balanced. For the unbalanced host tree A, when the first
host parasitized was not very isolated (hosts 1, 2, 3 and
4), the resulting parasite trees were less congruent with
the host tree than were random trees. From hosts 5 to 9,
as isolation increased, congruence became closer to the
congruence obtained with random trees. For the very
isolated hosts (hosts 10, 11 and 12) parasitized first, when
testing was possible (i.e. when the probability for
switches to distant hosts was high; see above), congruence slightly decreased. For the host tree C, no effect of
the first host parasitized was detectable. Finally, for the
host tree B, the congruence appeared to improve with
increasing isolation of the first host parasitized (the mean
proportion of estimated cospeciation events was higher
for hosts 5–8 than for hosts 9–12 parasitized first, and
higher for hosts 9–12 than for hosts 1–4 parasitized first;
Fig. 3).
To summarize, the host tree topology, the host-switch
probabilities and the degree of isolation of the first host
parasitized influenced the congruence between the host
and the parasite trees following a parasite adaptive
radiation onto an existing set of hosts. In some particular
cases, the congruence could be higher than with random
trees, although it was never very high and never total.
Time lag between switch and speciation
A time lag between a host-switch and subsequent
speciation that was a function of: (1) the phylogenetic
distance between the hosts from which and to which the
parasite was switching and (2) the coefficient k (see eqns
4 and 5) further influenced tree congruence. For clarity,
for each host tree topology, we only represented congruence with parasite trees resulting from a first colonization event to a small subset of hosts. We chose first
hosts colonized that had different levels of isolation
within the host tree: hosts 1, 8 and 12 for the intermediate host tree B and only hosts 1 and 12 for the balanced
host tree C. For the host tree A, the pectinate comb, the
chosen hosts depended on the host-switch probability
that was tested: hosts 1, 6 and 12 when the probability
for switches to phylogenetically distant hosts was high or
for equiprobability for all switches, and hosts 1, 5 and 8
when this probability was small. This was because, in the
latter case, if the first host parasitized was very isolated,
the first switch seldom occurred and adaptive radiation
did not take place.
Equiprobability for all switches or preferential
switches to distant hosts
Adding a time lag between host-switch and speciation did
not influence the congruence between host and parasite
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Preferential switches to proximate hosts
In contrast to the above-described situation, when
switches occurred preferentially between phylogenetically close hosts and the lag-time was short for such
switches between phylogenetically close hosts, the congruence between the trees was closer to what was
obtained in random trees than the cases where no time
lag was allowed (k ¼ 0). This was true for all values of k
greater than 0.
However, when the time lag before speciation was
shorter for switches between phylogenetically distant
hosts (Fig. 4) the shapes of the curves were completely
different. For all host trees, increasing the coefficient k
increased the congruence, but the strength of this
increase depended on the shape of the host tree. For the
host tree A, the congruence was only slightly affected. For
the host trees B and C, this increase was sharper. Some
parasite trees were even completely congruent with their
host tree, leading to a mean proportion of estimated
cospeciation events estimated close to 1. For example, for
the host tree C, for k equal to 300 and for an initial
infection of host 12, 21.3% of the parasite trees were
totally congruent with the host tree, leading COMPONENT to estimate that a very small number of species had
to be pruned to obtain identical trees (Fig. 5) and
TREEMAP to estimate a mean number of cospeciation
events close to 10, the maximum possible being 11.
The effect of the first host parasitized was not consistent across the different cases of host tree topology. For
the host trees A and C, it appeared that the more isolated
the first host was, the more congruent were parasite
phylogenies resulting from adaptive radiation of parasites: the mean proportion of estimated cospeciation
events across all the values of k increased with increasing
isolation of the first host parasitized. This was not true for
800
700
Number of trees
trees when all switches were equiprobable or when
switches were more likely between phylogenetically
distant hosts.
600
500
400
300
200
100
0
0
1
2
3
4
5
6
7
Number of species pruned
8
9
Fig. 5 Particular frequency distribution of the number of species
that had to be pruned in 1000 parasite trees generated by hostswitches to make them congruent with the host tree (grey bars). The
particular assumptions were: host tree C, k ¼ 300, host 12
parasitized first, i.e. high host-switch probability for switches to
phylogenetically close hosts and shorter time lag before speciation
for switches between phylogenetically far than close hosts. The
striped bars represent the frequency distribution obtained when
comparing the same host tree with 1000 randomly generated
parasite trees.
host tree B, however, as the best congruence was
obtained with host 12 initially infected, whereas host 8
was more isolated (Fig. 4)
The results obtained under the different hypotheses are
recapitulated in Table 1. It appears clearly that substantial congruence is only obtainable when considering
preferential switches between closely related hosts, and
that a long time lag before speciation after this kind of
switch enormously increases this congruence. The shape
of the host tree also seems to have a strong impact, as the
simulations performed with the host tree A never gave a
noticeable congruence with the parasite trees, in contrast
to the ones preformed with the host trees B and C.
Finally, the influence of the first host parasitized was not
clear (Figs 3 and 4) and was therefore not represented in
Table 1.
1
Mean proportion of estimated
cospeciation events
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
0
20
40
60
80
100 120 140 160 180 200 220 240 260 280 300
k
Fig. 4 Effect of a time lag (k, Y-axis)
between a switch and the subsequent speciation on the congruence between host and
parasite trees, in the case of a high probability for close switches and a longer time-lag
after such switches than after distant ones.
Plain lines represent the results obtained
with host tree A, dashed lines with host tree
B and dotted lines with host tree C. The
Y-axis represents the mean proportion of
cospeciation events estimated by TREEFITTER.
ª 2007 THE AUTHORS 20 (2007) 1428–1438
JOURNAL COMPILATION ª 2007 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Conditions favouring pseudocospeciation
1435
Table 1 Recapitulation of the congruence between host and parasite trees under the nine hypotheses tested and the three host trees (A, B and
C; see Fig. 1).
No time lag
Shorter time lag before speciation
for switches between phylogenetically
close than distant hosts
Shorter time lag before speciation
for switches between phylogenetically
far than near hosts
Host tree
Equiprobability for
all switches
Close switches
Far switches
A
B
C
A
B
C
A
B
C
)
)
)
)
)
)
)
)
)
)
±
+
)
)
)
)
++
++
)
)
)
)
)
)
)
)
)
): no noticeable congruence between host and parasite trees; ±: congruence slightly higher than expected by chance, +: congruence clearly
higher than expected by chance; ++: clear congruence with at least 1% of trees completely identical to the host tree.
Discussion
Congruence between host and parasite trees
following host shifts
Parasites that colonize and radiate on a new host phylum
can have phylogenies highly congruent to that of their
hosts even without cospeciation. Congruence was maximized: (1) when parasites were better at switching to
hosts phylogenetically closely related to the host they
were already parasitizing, as previously shown on a
specific host–parasite case (Charleston & Robertson,
2002); and (2) when speciation occurred more slowly,
with parasites remaining generalists for longer after
switching between closely related hosts than when they
switched between phylogenetically distantly related
ones. Under these conditions, TREEFITTER and TREEMAP estimated that most, if not all, of the evolutionary
events were cospeciations.
Assumptions on host and parasite behaviour and
evolution
Several of our assumptions on the behaviour and the
evolution of hosts and the parasites may influence our
results. First, in contrast to Charleston & Robertson’s
(2002) model, we did not allow parasites to replace each
other on a particular host species. It seems indeed
realistic to consider that unoccupied hosts were more
readily colonized than those already parasitized. Thus, in
our model, we considered the extreme case where the
probability for a parasite to infect an already parasitized
host was null.
Second, we did not allow for colonization of an already
parasitized host species by an additional parasite. Because
stable coexistence of distinct species having exactly the
same ecological niche is unlikely in theory, one can
assume that highly related species of parasites are
unlikely to be able to form distinct species parasitizing
the same host species, although such cases have been
reported (Desdevises et al., 2002; Percy et al., 2004; Le
Gac et al., 2007). These existing cases of infections of a
single host species by multiple related parasite species can
be due to the fact that the host represents various
ecological niches, because of its anatomy (e.g. different
parasites on different organs), its own life history (e.g.
existence of different classes of individuals, such as male
and female, old and young, susceptible and resistant,
etc.) or because of its habitat (Thomas et al., 2002).
However, we do not know if these parasites specialized
on the same organs, for example, are more closely related
to each other between host species than parasites on
different organs within a single host species.
Third, parasites had a higher rate of speciation than
hosts. Indeed, in our model, hosts did not speciate and
parasites radiated onto a pre-existing clade. Although
host–parasite coevolutionary history is likely to be
characterized by cospeciation events as well as parasite
speciation on pre-existing host species, we here address
an ecological context involving only the latter. In
particular, we consider cases of parasites with rapid
evolutionary rates compared with those of their hosts
colonizing new environments previously unoccupied by
such parasites (Ricklefs & Fallon, 2002).
Fourth, we did not consider parasite extinctions or
parasite speciation in the absence of a host-switch, i.e.
duplication. These events are generally considered as
factors increasing the discordance between host and
parasite phylogenies (for a review, see Page, 2003,
chapter I) and we expect that parasite extinctions and
speciation in situ would have similar effects in our study.
Probabilities of host-switches and time lag before
speciation
Host-switches have been inferred from incongruent
cophylogenies in many host–parasite systems. However,
details, such as the relative probability of switching to
ª 2007 THE AUTHORS 20 (2007) 1428–1438
JOURNAL COMPILATION ª 2007 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
1436
D. M. DE VIENNE ET AL.
phylogenetically more or less distant hosts or the probability of speciation following such a range expansion,
remain unclear. Host shifts occur more readily to phylogenetically more similar hosts in several systems (Reed
& Hafner, 1997; Janz & Nylin, 1998; Nishiguchi et al.,
1998; Ricklefs & Fallon, 2002), but there is no correlation
between the phylogenetic distance between host plants
and the switches of their leaf beetle parasites (Futuyma
et al. (1995). Both scenarios of host-switches are plausible: switches will occur preferentially between closely
related hosts if the mechanisms employed by a parasite to
attack its habitual host are more effective on a closely
related host or if closely related hosts have more similar
habitat requirements. This will be the case if there is a
phylogenetic signal in anti-parasite defence or habitat
use. On the other hand, switches will occur preferentially
between distantly related hosts if phylogenetically similar
hosts are geographically or ecologically separated as
would be the case during incipient allopatric speciation
or when there was strong character displacement
between newly diverged species.
Speciation following host-switches has been observed
in several parasites (Zietara & Lumme, 2002; LopezVillavicencio et al., 2005), but the rapidity of speciation as
a function of phylogenetic distance between the hosts
has not, as far as we know, been assessed. Again, the two
hypotheses that we considered are plausible: when
closely related hosts are ecologically and/or geographically separated by character displacement or allopatry,
switches between these more closely related species will
be rare and thus lead to rapid parasite speciation in
isolation. On the other hand, when closely related hosts
overlap more in ecology and defence against parasites,
rare switches to distantly related hosts would lead to
rapid speciation in isolation facilitated by strong tradeoffs for infecting very different hosts (Timms & Read,
1999). Although we tested all combinations of preferential host-switches and time lag before speciation, the
cases where the highest and even perfect congruence was
obtained – preferential host-switch to closely related host
species but with relatively long lag time until speciation
after these switches – corresponded to the more probable
scenario we test. Indeed, it seems intuitive: (1) that
parasites can jump more easily between more closely
related hosts, those being more likely to share general
ecological, physiological and chemical properties; and (2)
that they will be able to remain generalists longer (i.e.
speciate slower) on such similar hosts where trade-offs in
performance are less strong and where repeated
exchange maintains selection for success on both hosts.
Our model thus shows that interpreting congruence as
evidence of cospeciation should be treated most cautiously for species groups where closely related species
share ecological and life-history traits.
Indeed, Charleston & Robertson (2002) observed that
the phylogenies of primates and their lentiviruses were
more congruent than expected by chance but that the
nodes in the viral phylogeny were much younger than
those in the host phylogeny. Similarly, Hirose et al.
(2005) found a high degree of congruence between the
phylogenies of maple powdery mildews (Sawadaea,
Erysiphaceae) and their maple tree hosts (Acer spp.)
despite the divergence of the different species of Acer
occurring many millions of years before that of Sawadaea.
In both cases, as in our model, congruent phylogenies
resulted from host shifts and not from cospeciation.
Hence, even though the choices of parameter values,
such as the generalism coefficient k or of the functions
governing the probabilities of host shifts for our model,
were not based on empirical studies, we generated
theoretical predictions consistent with real-world observations.
Adaptive radiation and coevolution
For simplicity, we decided to consider in our model
parasites undergoing an adaptive radiation on a set of
pre-existing and phylogenetically stable hosts. This way,
the model was simpler than if we incorporated coevolution with the hosts and the results were much easier to
interpret, avoiding having to tease out cospeciation and
pseudocospeciation for congruent nodes. Pseudocospeciation should also occur when the hosts and the parasites
are coevolving, as was initially proposed (Hafner &
Nadler, 1988). In the context of contemporaneous
speciations by both hosts and parasites the opportunity
for pseudocospeciation to occur and its relative importance compared with cospeciation will depend on the
proportion of empty niches (hosts free of parasites) left by
the cospeciation process. If many host speciations are
followed by lineage sorting of the parasite (i.e. missing
the boat) or if parasite extinctions are frequent, then
hosts scattered across the host phylogeny will be, from
time to time, free of parasites. This will provide the
opportunity for host shifts between more or less distant
hosts. Under such conditions, symmetrical trees, preferential host shifts to phylogenetically similar hosts and
longer time lag to speciation for these compared with the
rarer shifts to phylogenetically distant hosts should
artificially inflate congruence even if cospeciations also
occur contemporaneously.
Implications of this study
Our model confirmed that congruence between host and
parasite phylogenies could arise without cospeciation but
through a rapid adaptive radiation under some plausible
hypotheses about host-switches, time lag before speciation and host tree shape. This ‘pseudocospeciation’
mechanism was proposed a long time ago, but the
conditions favouring its appearance had never been
explored in a general way. Further, we hope that our
model will reinforce the idea that congruence does not
necessarily imply cospeciation and that the two following
ª 2007 THE AUTHORS 20 (2007) 1428–1438
JOURNAL COMPILATION ª 2007 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Conditions favouring pseudocospeciation
points will now be systematically taken into consideration:
(i) assessing temporal congruence between host and
parasite phylogenies is absolutely necessary, in addition
to topological congruence, for concluding that cospeciation occurred; it should not be considered only as optional
additional evidence; and (ii) results obtained with
softwares like TREEFITTER or TREEMAP, that infer a
coevolutionary scenario from the topologies of two given
phylogenies, have to be considered with great care, as a
high number of cospeciation events can be estimated in
some cases where none actually occurred.
Furthermore, applied to real phylogenies of recently
interacting hosts and parasites, this simulation approach
may bring insights into some aspects of the genetics of
resistance and infectivity. Indeed, if some recently interacting hosts and parasites have phylogenies with significant congruence, one can conclude that these parasites
more easily switch to hosts that are phylogenetically close
to their native host than more distant ones, and that the
rare distant switches are rapidly followed by speciation.
Acknowledgments
M. Blum and E. Paradis have been of invaluable help for
the programming of the model. We also thank R. Page, A.
Paterson, R. Cruickshank and two anonymous referees
for their interesting comments and suggestions on the
manuscript.
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Received 24 January 2007; accepted 9 February 2007
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