Abstract
BackgroundHaemoproteus parasites (Haemosporida, Haemoproteidae) are cosmopolitan in birds and recent molecular studies indicate enormous genetic diversity of these pathogens, which cause diseases in non-adapted avian hosts. However, life-cycles remain unknown for the majority of Haemoproteus species. Information on their exoerythrocytic development is particularly fragmental and controversial. This study aimed to gain new knowledge on life-cycle of the widespread blood parasite Haemoproteus majoris.MethodsTurdus pilaris and Parus major naturally infected with lineages hPHYBOR04 and hPARUS1 of H. majoris, respectively, were wild-caught and the parasites were identified using microscopic examination of gametocytes and PCR-based testing. Bayesian phylogeny was used to determine relationships between H. majoris lineages. Exoerythrocytic stages (megalomeronts) were reported using histological examination and laser microdissection was applied to isolate single megalomeronts for genetic analysis. Culicoides impunctatus biting midges were experimentally exposed in order to follow sporogonic development of the lineage hPHYBOR04.ResultsGametocytes of the lineage hPHYBOR04 are indistinguishable from those of the widespread lineage hPARUS1 of H. majoris, indicating that both of these lineages belong to the H. majoris group. Phylogenetic analysis supported this conclusion. Sporogony of the lineage hPHYBOR04 was completed in C. impunctatus biting midges. Morphologically similar megalomeronts were reported in internal organs of both avian hosts. These were big roundish bodies (up to 360 μm in diameter) surrounded by a thick capsule-like wall and containing irregularly shaped cytomeres, in which numerous merozoites developed. DNA sequences obtained from single isolated megalomeronts confirmed the identification of H. majoris.ConclusionsPhylogenetic analysis identified a group of closely related H. majoris lineages, two of which are characterized not only by morphologically identical blood stages, but also complete sporogonic development in C. impunctatus and development of morphologically similar megalomeronts. It is probable that other lineages belonging to the same group would bear the same characters and phylogenies based on partial cytb gene could be used to predict life-cycle features in avian haemoproteids including vector identity and patterns of exoerythrocytic merogony. This study reports morphologically unique megalomeronts in naturally infected birds and calls for research on exoerythrocytic development of haemoproteids to better understand pathologies caused in avian hosts.
Highlights
Haemoproteus parasites (Haemosporida, Haemoproteidae) are cosmopolitan in birds and recent molecular studies indicate enormous genetic diversity of these pathogens, which cause diseases in non-adapted avian hosts
This finding was in accordance with blood film microscopic examination, which allowed detecting the presence of single Haemoproteus infections of morphologically distinct gametocytes in these birds as well
The present study shows that megalomeronts are a normal part of exoerythrocytic development in common avian haemoproteids because the lineages hPHYBOR04 and hPARUS1 of H. majoris are widespread and their gametocytes have been often reported during natural infections (Fig. 3) [5], indicating a complete life-cycle in avian hosts
Summary
Haemoproteus parasites (Haemosporida, Haemoproteidae) are cosmopolitan in birds and recent molecular studies indicate enormous genetic diversity of these pathogens, which cause diseases in non-adapted avian hosts. Despite the cosmopolitan distribution and great species diversity, information about complete life-cycles of the vast majority of Haemoproteus parasites is lacking This is true for exoerythrocytic and sporogonic development of these pathogens [8, 9]. Such studies were designed mainly by analysing the blood stages (gametocytes), which are present in the circulation and are relatively easy to sample This provided opportunities to gain new knowledge on the molecular biology and ecology of these parasites, their molecular diagnostics, contributing scarce information about exoerythrocytic development in avian hosts and sporogonic development in vectors. Sporogonic stages (ookinetes) of avian Haemoproteus parasites can markedly damage the midguts of blood-sucking insects (both vectors and non-vectors) and even kill them after blood meals with heavy gametocytaemia, but this issue and its biological significance remains insufficiently understood in wildlife [25]
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