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- The model
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.
- Top of page
- The model
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., 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 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 host-switches 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-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.