Haemoprotozoa: Making biological sense of molecular phylogenies

Abstract

A range of protistan parasites occur in the blood of vertebrates and are transmitted by haematophagous invertebrate vectors. Some 48 genera are recognized in bood primarily on the basis of parasite morphology and host specificity; including extracellular kinetoplastids (trypanosomatids) and intracellular apicomplexa (haemogregarines, haemococcidia, haemosporidia and piroplasms). Gene sequences are available for a growing number of species and molecular phylogenies often link parasite and host or vector evolution. This review endeavours to reconcile molecular clades with biological characters. Four major trypanosomatid clades have been associated with site of development in the vector: salivarian or stercorarian for Trypanosoma, and supra- or peri-pylorian for Leishmania. Four haemogregarine clades have been associated with acarine vectors (Hepatozoon A and B, Karyolysus, Hemolivia) and another two with leeches (Dactylosoma, Haemogregarina sensu stricto). Two haemococcidian clades (Lankesterella, Schellackia) using leeches and mosquitoes (as paratenic hosts!) were paraphyletic with monoxenous enteric coccidia. Two major haemosporidian clades have been associated with mosquito vectors (Plasmodium from mammals, Plasmodium from birds and lizards), two with midges (Hepatocystis from bats, Parahaemoproteus from birds) and two with louse-flies and black-flies (Haemoproteus and Leucocytozoon from birds). Three major piroplasm clades were recognized: one associated with transovarian transmission in ticks (Babesia sensu stricto); one with pre-erythrocytic schizogony in vertebrates (Theileria/Cytauxzoon); and one with neither (Babesia sensu lato). Broad comparative studies with allied groups suggest that trypanosomatids and haemogregarines evolved first in aquatic and then terrestrial environments, as evidenced by extant lineages in invertebrates and their radiation in vertebrates. In contrast, haemosporidia and haemococcidia are thought to have evolved first in vertebrates from proto-coccidia and then incorporated invertebrate vectors. Piroplasms are thought to have evolved in ticks and diversified into mammals. More molecular studies are required on more parasite taxa to refine current thought, but ultimately transmission studies are mandated to determine the vectors for many haemoprotozoa.

Hemogregarine and Rickettsial infection in ticks of toads from northeastern Colombia

“…( Guglielmone and Nava, 2010 ; Nava et al, 2017 ); therefore, it is possible that H. stellata is also associated with these ticks. However, many authors agree that the identification and phylogenetic positions of these hemogregarines, especially with respect to the genus Hepatozoon , are very imprecise given the lack of biogeographic, morphological, and especially molecular information ( Barta et al, 2012 ; Kvičerová et al, 2014 ; Karadjian et al, 2015 ; Maia et al, 2016 ; O'Donoghue, 2017 ). Sequences other than those for the 18S gene are necessary, given that 18S sequences are insufficient to resolve the relationship between these groups; in our study, the differences were evidenced by obtaining different topologies with the Maximum Likelihood and Bayesian Inference methods.…”

The distribution and host-association of a haemoparasite of damselfishes (Pomacentridae) from the eastern Caribbean based on a combination of morphology and 18S rDNA sequences

“…Also, merozoite stages of species of the genus Isospora (formerly regarded as a species of Atoxoplasma ) have been recorded infecting blood cells. Therefore, a second route of transmission may be ingestion by blood-feeding invertebrates that in turn act as paratenic transport hosts, infecting new vertebrate hosts upon being eaten ( O'Donoghue, 2017 ). In the Caribbean, the blood-feeding gnathiid isopod Gnathia marleyi is commonly found to infest over 20 different species of bony fishes, including species of Stegastes ( Farquharson et al, 2012 ; Coile and Sikkel, 2013 ; Jenkins et al, 2017 ).…”

“…species of Hepatozoon ). Haemococcidia, however, such as species of Lankesterella and Schellackia , complete their development in their vertebrate host, invertebrates acting only as paratenic or mechanical hosts when ingested by the vertebrate ( O'Donoghue, 2017 ). The vast majority of work on the phylum Apicomplexa has focused on Plasmodium and other genera of socioeconomic importance ( Wozniak et al, 1994 ; Bejon et al, 2006 ; Sant’Anna et al, 2008 ; Ogedengbe et al, 2013 ; Heddergott et al, 2012 ) in terrestrial systems.…”

“…In a subsequent study, Renoux et al (2017) developed an apicomplexan DNA barcoding system, targeting the 18S rDNA gene, to detect infections of the Haemohormidium -like parasites in Stegastes spp. Phylogenetic analysis of this parasite by Renoux et al (2017) placed it at the base of a major monophyletic clade containing species of coccidia, suggesting it to be more closely related to this group than to the pirosplasms, the group to which the Haemohormidiidae have been assigned pending molecular support (see O'Donoghue, 2017 ). As a follow-up to the work of Cook et al (2015) and Renoux et al (2017) , the aim of the current study was to determine the geographic distribution and host-association of this parasite in damselfishes in the eastern Caribbean.…”

Infecção por Cytauxzoon spp. em felinos domésticos

“…pertence à ordem Piroplasmida e família Theileriidae (Criado-Fornelio et al, 2003;Schreeg et al, 2016). Após o repasto sanguíneo de um carrapato infectado, os esporozoítos de Cytauxzoon felis adentram diretamente em monócitos e macrófagos de um felídeo, onde sofrem esquizogonia e dão origem à formação de esquizontes maduros que rompem os macrófagos infectados e liberam merozoítos (Tarigo et al, 2013;Reichard et al, 2010;O'Donoghue, 2017). Os merozoítos, por sua vez, entram em eritrócitos e se replicam induzindo à morte celular, resultando em liberação de novos merozoítos na circulação sanguínea, que por sua vez adentram em outros eritrócitos (Tarigo et al, 2013).…”