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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 and host–mutualist associations by critically reviewing the literature. We show that 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 associations. 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.

The associations between pathogens and their hosts are complex and can result from a variety of evolutionary processes including codivergence, lateral transfer, or duplication. Papillomaviruses (PVs) are double-stranded DNA viruses ubiquitously present in mammals and are a suitable target for rigorous statistical tests of potential virus–host codivergence. We analyze the evolutionary dynamics of PV diversification by comparing robust phylogenies of PVs and their respective hosts using different statistical approaches to assess topological and branch-length congruence. Mammalian PVs segregated into four diverse major clades that overlapped to varying degrees in terms of their mammalian host lineages. The hypothesis that PVs and hosts evolved independently was globally rejected (P = 0.0001), although only 90 of 207 virus–host associations (43%) were significant in individual tests. Virus–host codivergence accounted roughly for one-third of the evolutionary events required to reconcile PV–host evolutionary histories. When virus–host associations were analyzed locally within each of the four viral clades, numerous independent topological congruencies were identified that were incompatible with respect to the global trees. These results support an evolutionary scenario in which early PV radiation was followed by independent codivergence between viruses within each of the major clades and their hosts. Moreover, heterogeneous groups of closely related PVs infecting non-related hosts suggest several interspecies transmission events. Our results argue thus for the importance of alternative events in PV evolution, in contrast to the prevailing opinion that these viruses show a high degree of host specificity and codivergence.

We used phylogenetic analyses of cytochrome b sequences of malaria parasites and their avian hosts to assess the coevolutionary relationships between host and parasite lineages. Many lineages of avian malaria parasites have broad host distributions, which tend to obscure cospeciation events. The hosts of a single parasite or of closely related parasites were nonetheless most frequently recovered from members of the same host taxonomic family, more so than expected by chance. However, global assessments of the relationship between parasite and host phylogenetic trees, using Component and ParaFit, failed to detect significant cospeciation. The event-based approach employed by TreeFitter revealed significant cospeciation and duplication with certain cost assignments for these events, but host switching was consistently more prominent in matching the parasite tree to the host tree. The absence of a global cospeciation signal despite conservative host distribution most likely reflects relatively frequent acquisition of new hosts by individual parasite lineages. Understanding these processes will require a more refined species concept for malaria parasites and more extensive sampling of parasite distributions across hosts. If parasites can disperse between allopatric host populations through alternative hosts, cospeciation may not have a strong influence on the architecture of host–parasite relationships. Rather, parasite speciation may happen more often in conjunction with the acquisition of new hosts followed by divergent selection between host lineages in sympatry. Detailed studies of the phylogeographic distributions of hosts and parasites are needed to characterize these events.

Lice in the genus Pectinopygus parasitize a single order of birds (Pelecaniformes). To examine the degree of congruence between the phylogenies of 17 Pectinopygus species and their pelecaniform hosts, sequences from mitochondrial 12S rRNA, 16S rRNA, COI, and nuclear wingless and EF1-α genes (2290 nucleotides) and from mitochondrial 12S rRNA, COI, and ATPases 8 and 6 genes (1755 nucleotides) were obtained for the lice and the birds, respectively. Louse data partitions were analyzed for evidence of incongruence and evidence of long-branch attraction prior to cophylogenetic analyses. Host-parasite coevolution was studied by different methods: TreeFitter, TreeMap, ParaFit, likelihood-ratio test, data-based parsimony method, and correlation of coalescence times. All methods agree that there has been extensive cospeciation in this host-parasite system, but the results are sensitive to the selection of different phylogenetic hypotheses and analytical methods for evaluating cospeciation. Perfect congruence between phylogenies is not found in this association, probably as a result of occasional host switching by the lice. Errors due to phylogenetic reconstruction methods, incorrect or incomplete taxon sampling, or to different loci undergoing different evolutionary histories cannot be rejected, thus emphasizing the need for improved cophylogenetic methodologies.