Host associations and evolutionary relationships of avian blood parasites from West Africa

Abstract

The host specificity of blood parasites recovered from a survey of 527 birds in Cameroon and Gabon was examined at several levels within an evolutionary framework. Unique mitochondrial lineages of Haemoproteus were recovered from an average of 1.3 host species (maximum=3) and 1.2 host families (maximum=3) while lineages of Plasmodium were recovered from an average of 2.5 species (maximum=27) and 1.6 families (maximum=9). Averaged within genera, lineages of both Plasmodium and Haemoproteus were constrained in their host distribution relative to random expectations. However, while several individual lineages within both genera exhibited significant host constraint, host breadth varied widely among related lineages, particularly within the genus Plasmodium. Several lineages of Plasmodium exhibited extreme generalist host-parasitism strategies while other lineages appeared to have been constrained to certain host families over recent evolutionary history. Sequence data from two nuclear genes recovered from a limited sample of Plasmodium parasites indicated that, at the resolution of this study, inferences regarding host breadth were unlikely to be grossly affected by the use of parasite mitochondrial lineages as a proxy for biological species. The use of divergent host-parasitism strategies among closely related parasite lineages suggests that host range is a relatively labile character. Since host specificity may also influence parasite virulence, these results argue for considering the impact of haematozoa on avian hosts on a lineage-specific basis.

Fig. 1

Map indicating sampling locations within West Africa.

Fig. 2

Evolutionary relationships among Plasmodium mitochondrial lineages estimated using maximum likelihood. Branches with bootstrap support > 70% are highlighted in red. Squares to the right of lineage names indicate unique host species in which a particular lineage was recovered and are color coded to indicate the family to which the host species belongs. Numbers within squares indicate the number of host individuals infected. Parasite lineages exhibiting significantly higher specificity at the host species or host family level than expected by chance are indicated by bold or underlined type, respectively.

Fig. 3

Evolutionary relationships among Haemoproteus mitochondrial lineages estimated using maximum likelihood. Branches with bootstrap support > 70% are highlighted in red. Squares to the right of lineage names indicate unique host species in which a particular lineage was recovered and are color coded to indicate the family to which the host species belongs. Numbers within squares indicate the number of host individuals infected. Parasite lineages exhibiting significantly higher specificity at the host species or host family level than expected by chance are indicated by bold or underlined type, respectively.

Fig. 4

Linkage plot. Shaded squares indicate sharing of nuclear haplotypes dihydrofolate reductase-thymidylate synthase (DHFR-TS) below the diagonal; transferase above the diagonal) between individual parasite mitochondrial lineages (identified at left and depicted with corresponding alternate shading in the same order across top). Boxes outlined along the diagonal indicate the squares that would be shaded if each mitochondrial lineage were associated with a unique nuclear signature. Hashed squares indicate sharing of nuclear haplotypes among different mitochondrial lineages. In some cases, identification of shared nuclear haplotypes was not possible (N) due to unsuccessful amplifications of one locus or the other in certain samples.

Fig. 5

Logistic regression curves modeling the probability that two parasite lineages exhibit the same host range at different levels of genetic divergence. For both Haemoproteus and Plasmodium, separate trend lines were calculated using data from the entire genus (black line), a well-supported group of parasites within each genus (HA or PA, dotted line; see Figs. 2 and 3) and the entire genus excluding HA or PA (dashed line). Trend lines that intersect the y-axis below 0.5 indicate that, on average, parasite lineages in the group being considered exhibited less than a 50% chance of being found in just a single host species (above) or family (below).