The switching of parasitic organisms to novel hosts, in which they may cause the emergence of new diseases, is of great concern to human health and the management of wild and domesticated populations of animals. We used a phylogenetic approach to develop a better statistical assessment of host switching in a large sample of vector-borne malaria parasites of birds (Plasmodium and Haemoproteus) over their history of parasite-host relations. Even with sparse sampling, the number of parasite lineages was almost equal to the number of avian hosts. We found that strongly supported sister lineages of parasites, averaging 1.2% sequence divergence, exhibited highly significant host and geographical fidelity. Event-based matching of host and parasite phylogenetic trees revealed significant cospeciation. However, the accumulated effects of host switching and long distance dispersal cause these signals to disappear before 4% sequence divergence is achieved. Mitochondrial DNA nucleotide substitution appears to occur about three times faster in hosts than in parasites, contrary to findings on other parasite-host systems. Using this mutual calibration, the phylogenies of the parasites and their hosts appear to be similar in age, suggesting that avian malaria parasites diversified along with their modern avian hosts. Although host switching has been a prominent feature over the evolutionary history of avian malaria parasites, it is infrequent and unpredictable on time scales germane to public health and wildlife management.

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.

We studied the organization and temporal stability of an assemblage of malaria parasites (genera Plasmodium and Haemoproteus) and their passerine avian hosts in a forested study area in southern Missouri, USA, over four years. We detected parasite infections by polymerase chain reaction (PCR) of parasite DNA from host blood samples and identified parasite lineages by sequencing a part of the mitochondrial cytochrome b gene. We obtained 757 blood samples from 42 host species. Prevalence of malaria parasitism judged by PCR averaged 38.6% and varied in parallel in the three most abundant host species over the four years of the study. Parasite prevalence bore a U‐shaped relationship to host sample size. Prevalence was weakly positively associated with host body mass, but not with foraging stratum, nest height, nest type, plumage brightness, or sexual dichromatism. Over the sample as a whole, parasite prevalence did not vary between males and females or between hatch‐year and older individuals. We differentiated 34 parasite lineages. The number of host species per lineage varied from one to eight and increased with sample size. We recovered up to 14 lineages of parasite from a single host. Three relatively common lineages in the Ozarks were found nowhere else; four others were recovered from other sites in eastern North America; and six additional well‐sampled lineages were distributed in the Greater Antilles among resident island host species. Parasites that are endemic among native species of hosts on the tropical wintering grounds of Ozark birds were recovered from hatch‐year birds in the Ozarks, indicating that transmission takes place on the summer breeding grounds, and consequently, that suitable vectors are present in both the temperate and tropical portions of the parasite lineage distributions. We estimate that the number of parasite lineages within a local area will approximate the number of host species and that our perception of host breadth and parasite diversity will increase for most lineages and hosts with increased sampling. Thus, host–parasite relationships in a local area, including the role of parasites in sexual selection and the evolutionary maintenance of sex, are likely to be complex, with population and evolutionary dynamics involving many actors.