Extensive diversity of malaria parasites circulating in Central African bats and monkeys

Boundenga, Larson; Ngoubangoye, Barthélémy; Mombo, Illich Manfred; Tsoubmou, Thierry Audrey; Renaud, François; Rougeron, Virginie; Prugnolle, Franck

doi:10.1002/ece3.4539

Cited by 18 publications

(20 citation statements)

References 28 publications

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“…The prevalences (of 25 and 42%) are similar to previous reports from epauletted fruit bats in other West, Central and East African countries (e.g. Schaer et al ., 2013; Lutz et al ., 2016; Boundenga et al ., 2018) with the exceptions of the studies in South Sudan and Central Gabon (Schaer et al ., 2017; Rosskopf et al ., 2019). The study in South Sudan revealed Hepatocystis infections in over 80% of the investigated epauletted fruit bats and in contrast, the study in Central Gabon reported no haemosporidian infections in the epauletted fruit bats (Schaer et al ., 2017; Rosskopf et al ., 2019).…”

Section: Discussionmentioning

confidence: 97%

“…Apart from these three studies, which date back well over 50 years ago, no infections with haemosporidian parasites have been re-discovered in R. aegyptiacus (e.g. Schaer et al ., 2013; Lutz et al ., 2016; Boundenga et al ., 2018; Rosskopf et al ., 2019). Strikingly, here we detected Hepatocystis parasites, and not the previously reported Plasmodium species in this bat host.…”

Section: Discussionmentioning

confidence: 99%

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Survey of Hepatocystis parasites of fruit bats in the Amurum forest reserve, Nigeria, identifies first host record for Rousettus aegyptiacus

Atama

Manu²,

Ivande³

et al. 2019

Parasitology

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Parasites of the genus Hepatocystis are close relatives of Plasmodium that frequently infect epauletted fruit bats across West and East Africa. Our understanding of susceptible hosts and prevalence of infection of Hepatocystis remains fragmented. Non-invasive sampling of bat assemblages in representative habitats critically contribute to haemosporidian parasite distribution maps. Here, we report on a survey of Hepatocystis parasite infections in bats undertaken over two consecutive years in a protected area in Nigeria, where prevalence and diversity of bat-infecting haemosporidian parasites have not been studied. Microscopic examination of blood films in combination with PCR detection and sequencing revealed Hepatocystis infections with prevalences of 25% and 42% in the closely related epauletted fruit bats Epomophorus sp. and Micropteropus pusillus. For the first time, mature Hepatocystis gametocytes were identified in one Egyptian fruit bat (Rousettus aegyptiacus). This novel host record was confirmed by parasite and host genotyping and suggests that Hepatocystis parasites have a broader host distribution in African fruit bats than currently known.

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

Survey of Hepatocystis parasites of fruit bats in the Amurum forest reserve, Nigeria, identifies first host record for Rousettus aegyptiacus

Atama

Manu²,

Ivande³

et al. 2019

Parasitology

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show abstract

“…There is consensus that Hepatocystis spp. are nested within the Plasmodium genus (2,8,9), however their placement within the genus has not been robustly determined. Indeed, our cytochrome b phylogeny confirms that our assembled genome is that of Hepatocystis spp., but it provides little support for the placement of this genus in relation to Plasmodium spp.…”

Section: Phylogenetic Position Of Hepatocystis Sp Ex Piliocolobus Tmentioning

confidence: 99%

Genomic and transcriptomic evidence for descent from Plasmodium and loss of blood schizogony in Hepatocystis parasites from naturally infected red colobus monkeys

Aunin

Boehme

Sanderson

et al. 2019

Preprint

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Hepatocystis is a genus of single-celled parasites infecting monkeys, bats and squirrels. Although thought to descend from malaria parasites (Plasmodium spp.), Hepatocystis spp. are thought not to undergo replication in the bloodthe part of the Plasmodium life cycle which causes the symptoms of malaria. Furthermore, Hepatocystis is transmitted by midges, not mosquitoes. Comparative genomics of Hepatocystis and Plasmodium species therefore presents an opportunity to better understand some of the most important aspects of malaria parasite biology. We were able to generate a draft genome for Hepatocystis using DNA sequencing reads from the blood of a naturally infected red colobus monkey. We provide robust phylogenetic support for Hepatocystis as a sister group to Plasmodium parasites infecting rodents. We show transcriptomic support for a lack of replication in the blood and genomic support for a complete loss of a family of genes involved in red blood cell invasion. Our analyses highlight the rapid evolution of genes involved in parasite vector stages, revealing genes that may be critical for interactions between malaria parasites and mosquitoes.* including pseudogenes, duplications and partial genes, excluding non-coding RNA genes ** two small contigs have telomeric repeats (scaffold 2410 (5 telomeric repeats, scaffold 2364, 9 telomeric repeats))

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“…Probabilities of infections were high, and multiple infections were common in the study population, as observed in African great apes (Kaiser et al, 2010; Liu et al, 2010; Otto et al, 2018) but in contrast to captive mandrills living in Southern Gabon (Boundenga et al, 2018; Ngoubangoye et al, 2016). We found also slight evidence that the presence of one Plasmodium species facilitated the establishment of the second species.…”

Section: Discussionmentioning

confidence: 73%

A longitudinal molecular study of the ecology of malaria infections in free-ranging mandrills

Charpentier

Boundenga

Beaulieu

et al. 2019

International Journal for Parasitology: Parasites and Wildlife

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Unravelling the determinants of host variation in susceptibility and exposure to parasite infections, infection dynamics and the consequences of parasitism on host health is of paramount interest to understand the evolution of complex host-parasite interactions. In this study, we evaluated the determinants, temporal changes and physiological correlates of Plasmodium infections in a large natural population of mandrills (Mandrillus sphinx). Over six consecutive years, we obtained detailed parasitological and physiological data from 100 male and female mandrills of all ages. The probability of infection by Plasmodium gonderi and P. mandrilli was elevated (ca. 40%) but most infections were chronical and dynamic, with several cases of parasite switching and clearance. Positive co-infections also occurred between both parasites. Individual age and sex influenced the probability of infections with some differences between parasites: while P. mandrilli appeared to infect its hosts rather randomly, P. gonderi particularly infected middle-aged mandrills. Males were also more susceptible to P. gonderi than females and were more likely to be infected by this parasite at the beginning of an infection by the simian immunodeficiency virus. P. gonderi, and to a lesser extent P. mandrilli, influenced mandrills’ physiology: skin temperatures and neutrophil/lymphocyte ratio were both impacted, generally depending on individual age and sex. These results highlight the ecological complexity of Plasmodium infections in nonhuman primates and the efforts that need to be done to decipher the epidemiology of such parasites.

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Extensive diversity of malaria parasites circulating in Central African bats and monkeys

Cited by 18 publications

References 28 publications

Survey of Hepatocystis parasites of fruit bats in the Amurum forest reserve, Nigeria, identifies first host record for Rousettus aegyptiacus

Survey of Hepatocystis parasites of fruit bats in the Amurum forest reserve, Nigeria, identifies first host record for Rousettus aegyptiacus

Genomic and transcriptomic evidence for descent from Plasmodium and loss of blood schizogony in Hepatocystis parasites from naturally infected red colobus monkeys

A longitudinal molecular study of the ecology of malaria infections in free-ranging mandrills

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