Within-Host Speciation of Malaria Parasites

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

Diversity, Loss, and Gain of Malaria Parasites in a Globally Invasive Bird

Invasive species can displace natives, and thus identifying the traits that make aliens successful is crucial for predicting and preventing biodiversity loss. Pathogens may play an important role in the invasive process, facilitating colonization of their hosts in new continents and islands. According to the Novel Weapon Hypothesis, colonizers may out-compete local native species by bringing with them novel pathogens to which native species are not adapted. In contrast, the Enemy Release Hypothesis suggests that flourishing colonizers are successful because they have left their pathogens behind. To assess the role of avian malaria and related haemosporidian parasites in the global spread of a common invasive bird, we examined the prevalence and genetic diversity of haemosporidian parasites (order Haemosporida, genera Plasmodium and Haemoproteus) infecting house sparrows (Passer domesticus). We sampled house sparrows (N = 1820) from 58 locations on 6 continents. All the samples were tested using PCR-based methods; blood films from the PCR-positive birds were examined microscopically to identify parasite species. The results show that haemosporidian parasites in the house sparrows' native range are replaced by species from local host-generalist parasite fauna in the alien environments of North and South America. Furthermore, sparrows in colonized regions displayed a lower diversity and prevalence of parasite infections. Because the house sparrow lost its native parasites when colonizing the American continents, the release from these natural enemies may have facilitated its invasion in the last two centuries. Our findings therefore reject the Novel Weapon Hypothesis and are concordant with the Enemy Release Hypothesis

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How can we determine the molecular clock of malaria parasites?

The association of contemporary hosts and their parasites might reflect either cospeciation or more recent shifts among existing hosts. Cospeciation implies that lineages of hosts and parasites diverge in parallel at the same time, but testing this prediction requires time-calibrated phylogenies, which are particularly difficult to obtain in organisms that leave few fossils. It has successively become clear that host shifts have been frequent in the evolutionary history of malaria parasites, but dating these host shifts cannot be done without calibrated phylogenies. Hence, it remains unresolved how long contemporary hosts and vectors have been coevolving with their malaria parasites. This review addresses conflicting rate estimates of molecular evolution and suggests research directions to aid dating diversification events in malaria parasites

FIGURE 1 in Molecular characterization of Haemoproteus sacharovi (Haemosporida, Haemoproteidae), a common parasite of columbiform birds, with remarks on classification of haemoproteids of doves and pigeons

FIGURE 1. Mature gametocytes of haemoproteids of columbiform birds: Haemoproteus (Parahaemoproteus) turtur (A–C), Haemoproteus (Parahaemoproteus) sacharovi (D–F), Haemoproteus (Haemoproteus) columbae (G–I), Haemoproteus (Haemoproteus) multipigmentatus (J–L), and Haemoproteus (Haemoproteus) iwa (M–O). A, B, D, E, G, H, J, K, M, N—macrogametocytes; C, F, I, L, O—microgametocytes. Long arrows—nuclei of parasites; short arrows—unfilled spaces between gametocyte and nucleus of infected erythrocyte; triangle arrow heads—volutin granules; simple arrow head—vacuole. Giemsa-stained thin blood films. Bar = 10 µm.Published as part of <i>Križanauskienė, Asta, Iezhova, Tatjana A., Sehgal, Ravinder N. M., Carlson, Jenny S., Palinauskas, Vaidas, Bensch, Staffan & Valkiūnas, Gediminas, 2013, Molecular characterization of Haemoproteus sacharovi (Haemosporida, Haemoproteidae), a common parasite of columbiform birds, with remarks on classification of haemoproteids of doves and pigeons, pp. 85-94 in Zootaxa 3613 (1)</i> on page 88, DOI: 10.11646/zootaxa.3616.1.7, <a href="http://zenodo.org/record/10097290">http://zenodo.org/record/10097290</a&gt

Figure 4

<p>Co-occurrence of sister blackcap parasites (see tree in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0000235#pone-0000235-g002" target="_blank">Fig. 2B</a>) 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.</p

Sampling details of the 48 bird species included in this study (part one).

<p>For each bird species, the table shows the number of individuals screened and the number of infections scored. Parasite richness is given both as a raw value for all species, and also as R25 (± S.E.) for 15 species with more than 25 scored infections. The percentage of exclusive parasite lineages is only calculated for widely sampled bird species (with more than 25 scored infections). The blackcap entries have been boldfaced.</p

Figure 3

<p>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).</p