Wild bonobos host geographically restricted malaria parasites including a putative new Laverania species

Abstract

Malaria parasites, though widespread among wild chimpanzees and gorillas, have not been detected in bonobos. Here, we show that wild-living bonobos are endemically Plasmodium infected in the eastern-most part of their range. Testing 1556 faecal samples from 11 field sites, we identify high prevalence Laverania infections in the Tshuapa-Lomami-Lualaba (TL2) area, but not at other locations across the Congo. TL2 bonobos harbour P. gaboni, formerly only found in chimpanzees, as well as a potential new species, Plasmodium lomamiensis sp. nov. Rare co-infections with non-Laverania parasites were also observed. Phylogenetic relationships among Laverania species are consistent with co-divergence with their gorilla, chimpanzee and bonobo hosts, suggesting a timescale for their evolution. The absence of Plasmodium from most field sites could not be explained by parasite seasonality, nor by bonobo population structure, diet or gut microbiota. Thus, the geographic restriction of bonobo Plasmodium reflects still unidentified factors that likely influence parasite transmission.

Evolutionary history of humanPlasmodium vivaxrevealed by genome-wide analyses of related ape parasites

“…It has recently become apparent that wild-living African apes, including western and eastern gorillas as well as chimpanzees and bonobos, harbor malaria parasites that appear to be very closely related to P. vivax strains infecting humans in Asia and Central/South America ( 7 , 8 , 11 ). Since these results were based on a small number of mostly mitochondrial DNA fragments, we have now generated two nearly complete and several partial genome sequences from ape-infecting parasites.…”

“…However, the finding of closely related parasites in wild-living chimpanzees and gorillas suggested an African origin of P. vivax ( 7 ). Indeed, parasite sequences closely resembling P. vivax have been detected in western ( Pan troglodytes verus ), central ( Pan troglodytes troglodytes ), and eastern ( Pan troglodytes schweinfurthii ) chimpanzees, eastern ( Gorilla beringei graueri ) and western lowland ( Gorilla gorilla gorilla ) gorillas, and most recently in bonobos ( Pan paniscus ) ( 7 – 11 ). Phylogenetic analyses of available sequences revealed that ape and human parasites were nearly identical, with human P. vivax sequences forming a monophyletic lineage that usually fell within the radiation of the ape parasites ( 7 ).…”

Capture-based enrichment of Theileria parva DNA enables full genome assembly of first buffalo-derived strain and reveals exceptional intra-specific genetic diversity

“…These include the fact that tick transmission of buffalo-derived T. parva to other cattle has only been achieved on a few occasions and at low efficiency (Neitz 1957;Maritim et al 1992), and previously described immunological observations that differentiate the two parasites (Radley et al 1979;Radley 1981). The description of new Apicomplexa species based on genetic information alone is controversial (Krief et al 2010;Rayner et al 2011) but not unprecedented (Liu et al 2017), and it has been proposed that species identification based only on DNA characterization would be more efficient, even though inclusion of other data, such as host and geography, when available, is advisable (Cook et al 2010). Given the mounting evidence of genomic, immunological and epidemiological differences between cattle-and buffalo-derived T. parva, we posit that it is appropriate to return to the original classification of these two parasite populations as separate subspecies (Uilenberg 1981;Norval et al 1991), or perhaps even discuss their classification as separate species.…”

Origin of Two Most Virulent Agents of Human Malaria:Plasmodium falciparumandPlasmodium vivax

“…Among species classified into Laverania group, four species infect chimpanzees (P. gaboni, P. billcollinsi, P. billbrayi, and P. reichenowi), only three infect gorillas (P. adleri, P. blacklocki, and P. praefalciparum), and only one infect bonobo (P. lomamiensis) [8,9,12]. Therefore, P. billbrayi [10] is not accepted as a new species by some authors [6,13] who reported that these isolates did not seem to be sufficiently distinct from P. gaboni to warrant a separate species designation [6].…”