Unexpected absence of exo-erythrocytic merogony during high gametocytaemia in two species of Haemoproteus (Haemosporida: Haemoproteidae), including description of Haemoproteus angustus n. sp. (lineage hCWT7) and a report of previously unknown residual bodies during in vitro gametogenesis

Gediminas Valkiūnas; Tatjana Iezhova; Mikas Ilgūnas; Mélanie Tchoumbou; Mélanie Duc; Dovilė Bukauskaitė; Tanja Himmel; Josef Harl; Herbert Weissenböck

doi:10.1016/j.ijppaw.2024.100905

Unexpected absence of exo-erythrocytic merogony during high gametocytaemia in two species of Haemoproteus (Haemosporida: Haemoproteidae), including description of Haemoproteus angustus n. sp. (lineage hCWT7) and a report of previously unknown residual bodies during in vitro gametogenesis

Int J Parasitol Parasites Wildl. 2024 Jan 9:23:100905. doi: 10.1016/j.ijppaw.2024.100905. eCollection 2024 Apr.

Authors

Gediminas Valkiūnas¹, Tatjana Iezhova¹, Mikas Ilgūnas¹, Mélanie Tchoumbou¹, Mélanie Duc¹, Dovilė Bukauskaitė¹, Tanja Himmel², Josef Harl², Herbert Weissenböck²

Affiliations

¹ Nature Research Centre, Akademijos 2, 08412, Vilnius, Lithuania.
² Institute of Pathology, Department for Biological Sciences and Pathobiology, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210, Vienna, Austria.

Abstract

Neglected avian blood parasites of the genus Haemoproteus (Haemoproteidae) have recently attracted attention due to the application of molecular diagnostic tools, which unravelled remarkable diversity of their exo-erythrocytic (or tissue) stages both regarding morphology and organ tropism levels. The development of haemoproteids might result in pathologies of internal organs, however the exo-erythrocytic development (EED) of most Haemoproteus species remains unknown. Seven individual birds - Curruca communis (1) and Phylloscopus trochilus (6) - with high gametocytaemia (between 1% and 24%) of Haemoproteus angustus n. sp. (hCWT7) and Haemoproteus palloris (lineage hWW1) were sampled in Lithuania, and their internal organs were examined extensively by parallel application of histology and chromogenic in situ hybridization methods. Tissue stages were apparently absent, suggesting that the parasitaemia was not accompanied by detectable tissue merogony. Haemoproteus angustus n. sp. was described and characterized morphologically and molecularly. Sexual process and ookinete development of the new species readily occurred in vitro, and a unique character for Haemoproteus parasites was discovered - the obligatory development of several tiny residual bodies, which were associated with intracellular transformation of both macrogametocytes and microgametocytes before their escape from the host cells and formation of gametes. A DNA haplotype network was constructed with lineages that cluster in one clade with the lineage hCWT7. This clade consists of lineages mostly found in Curruca birds, indicating specificity for birds of this genus. The lineage hCWT7 is mainly a parasite of C. communis. Most reports of this lineage came from Turkey, with only a few records in Europe, mostly in birds wintering in Africa where transmission probably occurs. This study highlights unexpected difficulties in the research of EED even when using sensitive molecular diagnostic tools and extends information about transformation in early stages of gametogenesis in haemosporidian parasites.

Keywords: Avian haemosporidian parasites; Chromogenic in situ hybridization; DNA haplotype network; In vitro gametogenesis; New species; Tissue merogony.