Parasites have the power to impose significant regulatory pressures on host populations, making evolutionary patterns of host switching by parasites salient to a range of contemporary ecological issues. However, relatively little is known about the colonization of new hosts by parasitic, commensal and mutualistic eukaryotes of metazoans. As ubiquitous symbionts of coelomate animals, Blastocystis spp. represent excellent candidate organisms for the study of evolutionary patterns of host switching by protists. Here, we apply a big-data phylogenetic approach using archival sequence data to assess the relative roles of several host-associated traits in shaping the evolutionary history of the Blastocystis species-complex within an ecological framework. Patterns of host usage were principally determined by geographic location and shared environments of hosts, suggesting that weight of exposure (i.e. propagule pressure) represents the primary force for colonization of new hosts within the Blastocystis species-complex. While Blastocystis lineages showed a propensity to recolonize the same host taxa, these taxa were often evolutionarily unrelated, suggesting that historical contingency and retention of previous adaptions by the parasite were more important to host switching than host phylogeny. Ultimately, our findings highlight the ability of ecological theory (i.e. ‘ecological fitting’) to explain host switching and host specificity within the Blastocystis species-complex.

Even the most generalist parasites usually occur in only a subset of potential host species, a tendency which reflects overriding environmental constraints on their distributions in nature. The periodic shifting of these limitations represented by host-switches may have been an important process in the evolution of many host-parasite assemblages. To study such events, however, it must first be established where and when they have occurred. Past host-switches within a group of parasites are usually inferred from a comparison of the parasite phylogeny with that of the hosts. Congruence between the phylogenies is often attributed to a history of association by descent with cospeciation, and incongruence to host-switching or extinction in ‘duplicated’ parasite lineages (which diverged without a corresponding branching of the host tree). The inference of host-switching from incongrucnt patterns is discussed. Difficulties arise because incongruence can frequently be explained by different combinations of biologically distinct events whose relative probabilities are uncertain. Also, the models of host parasite relationships implicit in historical reconstructions may often not allow for plausible sources of incongruence other than host-switching or duplication/extinction, or for the possibility that colonization could, in some circumstances, be disguised by ‘false’ congruence.