Within-host speciation of malaria parasites

Abstract

Background: Sympatric speciation-the divergence of populations into new species in absence of geographic barriers to hybridization-is the most debated mode of diversification of life forms. Parasitic organisms are prominent models for sympatric speciation, because they may colonise new hosts within the same geographic area and diverge through host specialization. However, it has been argued that this mode of parasite divergence is not strict sympatric speciation, because host shifts likely cause the sudden effective isolation of parasites, particularly if these are transmitted by vectors and therefore cannot select their hosts. Strict sympatric speciation would involve parasite lineages diverging within a single host species, without any population subdivision.

Methodology/principal findings: Here we report a case of extraordinary divergence of sympatric, ecologically distinct, and reproductively isolated malaria parasites within a single avian host species, which apparently occurred without historical or extant subdivision of parasite or host populations.

Conclusions/significance: This discovery of within-host speciation changes our current view on the diversification potential of malaria parasites, because neither geographic isolation of host populations nor colonization of new host species are any longer necessary conditions to the formation of new parasite species.

Figure 1

Variation in richness of malaria parasites among different bird host species. The curves represent parasite cumulative richness in 15 passerine species with more than 25 scored parasite infections, belonging to 10 bird genera (represented in different colours, see details in Table 1). The curves provide a standard estimate of parasite richness (R₂₅) for each species, given by the number of parasites accumulated after analysing 25 infected individuals. The small graph shows the curves of parasite accumulation including all infections scored in each species (n = 26-353), crossed by a dotted line at R₂₅. Blackcaps show the highest richness of malaria parasites in both graphs.

Figure 2

The blackcap parasite flock placed in a phylogenetic context. The tree A shows the phylogenetic position of parasites found in blackcaps (red), garden warblers (blue) and African hill babblers (purple), among 143 parasite lineages found in 48 bird species. Monophyletic parasite groups apparently exclusive to some species are encircled in orange (species names are mentioned and the number of parasites in each group is shown in brackets). The tree B shows the parasite flock (represented by a triangle in the tree A). Numbers represent >75% support to internal branches, based on bootstrap replicates (above) or posterior probabilities (below). For six parasites in this cluster, the figure shows the match between phylogenies based on mitochondrial cytochrome b and nuclear DHFR-TS genes (the number of cases with each association of haplotypes is indicated, and bootstrap support is reported if >75%).

Figure 3

The geographic distribution of the parasite flock. The map shows the location of our sampling sites within the range of blackcaps, garden warblers and African hill babblers, which are shadowed in different colours according to the key below the map. Blackcaps and garden warblers are sympatric (S) in wide areas of Europe and Africa, during the breeding season and in winter, respectively. African hill babblers are year-round residents. Many blackcaps and garden warblers from Europe spend the winter in the range of African hill babblers, where the three species occur in the same habitat. For each sampling site, the squares indicate the number of parasite lineages from the flock that were found in each species (blackcap parasites in red, garden warbler parasites in blue, and hill babbler parasites in purple).

Figure 4

Co-occurrence of sister blackcap parasites (see tree in Fig. 2B) in mixed infections of individual hosts. Numbers indicate the frequency of occurrence of each parasite combination. Combinations in red involve parasites for which frequent hybridisation is unlikely, according to linkage between mitochondrial and nuclear haplotypes.