Multiple host-switching of Haemosporidia parasites in bats

Duval, Linda; Robert, Vincent; Csorba, Gábor; Hassanin, Alexandre; Randrianarivelojosia, Milijaona; Walston, Joe; Nhim, Thy; Goodman, Steve; Ariey, Frédéric

doi:10.1186/1475-2875-6-157

Cited by 59 publications

(88 citation statements)

References 29 publications

(35 reference statements)

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“…The two major subgroups are clearly associated with vertebrate host: mammalian Plasmodium and Hepatocystis versus avian/reptilian Plasmodium and avian Leucocytozoon, Haemoproteus, and Parahaemoproteus. The chiropteran (bat) parasites Polychromophilus evidently were derived from parasites of birds or reptiles (3,20). Increasing the taxon sampling in the ingroup and in the putative outgroup (i.e., Leucocytozoon) for the mitochondrial cyt b gene (for which large samples are available) and using the same outgroup-free rooting approach also places Leucocytozoon inside the hemosporidian phylogeny, in this case as sister to Haemoproteus, which together are sister to Parahaemoproteus (Figs.…”

Section: Resultsmentioning

confidence: 99%

“…Recent surveys of blood parasites in vertebrate wildlife populations, using PCR to screen hosts for infections and DNA sequencing to identify parasite lineages, have revealed a rich diversity of hemosporidian parasites (3)(4)(5)(6), possibly comparable to the number of hosts surveyed (7,8). It is important to reevaluate our interpretation of hemosporidian evolution as we expand sampling, to provide insight into shifts among hosts and vectors-often implicated in emerging infectious diseases-and to interpret the evolution of malaria parasite life cycles.…”

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Rerooting the evolutionary tree of malaria parasites

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Ricklefs

2011

Proc. Natl. Acad. Sci. U.S.A.

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Malaria parasites (Plasmodium spp.) have plagued humans for millennia. Less well known are related parasites (Haemosporida), with diverse life cycles and dipteran vectors that infect other vertebrates. Understanding the evolution of parasite life histories, including switches between hosts and vectors, depends on knowledge of evolutionary relationships among parasite lineages. In particular, inferences concerning time of origin and trait evolution require correct placement of the root of the evolutionary tree. Phylogenetic reconstructions of the diversification of malaria parasites from DNA sequences have suffered from uncertainty concerning outgroup taxa, limited taxon sampling, and selection on genes used to assess relationships. As a result, inferred relationships among the Haemosporida have been unstable, and questions concerning evolutionary diversification and host switching remain unanswered. A recent phylogeny placed mammalian malaria parasites, as well as avian/reptilian Plasmodium, in a derived position relative to the avian parasite genera Leucocytozoon and Haemoproteus, implying that the ancestral forms lacked merogony in the blood and that their vectors were non-mosquito dipterans. Bayesian, outgroup-free phylogenetic reconstruction using relaxed molecular clocks with uncorrelated rates instead suggested that mammalian and avian/reptilian Plasmodium parasites, spread by mosquito vectors, are ancestral sister taxa, from which a variety of specialized parasite lineages with modified life histories have evolved.Bayes factors | parasite diversification | Plasmodiidae M alaria parasites [broadly Apicomplexa: Haemosporida (1, 2)] have been well sampled in primates and songbirds, but are poorly known in other vertebrate groups. Recent surveys of blood parasites in vertebrate wildlife populations, using PCR to screen hosts for infections and DNA sequencing to identify parasite lineages, have revealed a rich diversity of hemosporidian parasites (3-6), possibly comparable to the number of hosts surveyed (7,8). It is important to reevaluate our interpretation of hemosporidian evolution as we expand sampling, to provide insight into shifts among hosts and vectors-often implicated in emerging infectious diseases-and to interpret the evolution of malaria parasite life cycles. Because choice of outgroup taxa critically influences the reconstruction of evolutionary relationships (9), it is also important to reassess assumptions about ancestral relationships and the monophyly of taxa. Premolecular reconstructions based on morphology and life history traits presumed that a monophyletic clade of Plasmodium parasites exhibited the most derived traits [e.g., asexual reproduction (merogony) in the circulating blood of the vertebrate host, production of hemozoin pigment from the metabolism of hemoglobin] (10, 11); accordingly, Leucocytozoon, a parasite of birds that lacks these traits, was placed in a basal position (Fig. 1A). Such a position for Leucocytozoon was indeed suggested in early molecular analyses based on the ...

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Section: Resultsmentioning

confidence: 99%

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confidence: 99%

Rerooting the evolutionary tree of malaria parasites

Outlaw

Ricklefs

2011

Proc. Natl. Acad. Sci. U.S.A.

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“…In total, we tested 130 DNA samples from great apes for Plasmodium infection, using primarily cytochrome b (cyt b) molecular tools (44); the apes included 105 chimpanzees from four subspecies (60 Pan t. troglodytes, 39 P. t. vellerosus, three P. t. schweinfurthii, and three P. t. verus), eight chimpanzees of undetermined subspecies, and 17 gorillas (Gorilla gorilla).…”

Section: Methodsmentioning

confidence: 99%

“…Under an agreement with the Institut Pasteur de Madagascar, the University Louis Pasteur of Strasbourg provided blood samples from these different lemurs to the Institut Pasteur de Madagascar, where they were frozen and stored. DNA was obtained from lemur blood samples using a phenol/chloroform extraction technique and then screened for Plasmodium infection using cyt b molecular tools (44).…”

Section: Methodsmentioning

confidence: 99%

“…Cytb gene fragments of 708 bp were amplified using published primers (44). The PCR and nested PCR reactions were carried out in a final volume of 25 μL under the following conditions: 2.5 μL of each primer, 2 mM of each dNTP, 2.5 U of Taq polymerase (Solis), 2 mM MgCl 2 , 5 min at 94°C, 30 s at 94°C, 30 s at 55°C, and 90 s at 72°C for 40 cycles, and a final 10-min extension at 72°C.…”

Section: Methodsmentioning

confidence: 99%

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African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus

Duval

Fourment

Nerrienet

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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We investigated two mitochondrial genes (cytb and cox1), one plastid gene (tufA), and one nuclear gene (ldh) in blood samples from 12 chimpanzees and two gorillas from Cameroon and one lemur from Madagascar. One gorilla sample is related to Plasmodium falciparum, thus confirming the recently reported presence in gorillas of this parasite. The second gorilla sample is more similar to the recently defined Plasmodium gaboni than to the P. falciparum-Plasmodium reichenowi clade, but distinct from both. Two chimpanzee samples are P. falciparum. A third sample is P. reichenowi and two others are P. gaboni. The other chimpanzee samples are different from those in the ape clade: two are Plasmodium ovale, and one is Plasmodium malariae. That is, we have found three human Plasmodium parasites in chimpanzees. Four chimpanzee samples were mixed: one species was P. reichenowi; the other species was P. gaboni in three samples and P. ovale in the fourth sample. The lemur sample, provisionally named Plasmodium malagasi, is a sister lineage to the large cluster of primate parasites that does not include P. falciparum or ape parasites, suggesting that the falciparum + ape parasite cluster (Laverania clade) may have evolved from a parasite present in hosts not ancestral to the primates. If malignant malaria were eradicated from human populations, chimpanzees, in addition to gorillas, might serve as a reservoir for P. falciparum.T here is a revolution afoot concerning our understanding of human malaria. It was shown in 1994/1995 that the closest relative of Plasmodium falciparum, the agent of malignant malaria was Plasmodium reichenowi, a chimpanzee parasite, the only ape malaria parasite that had been molecularly characterized (1-4). The close phylogenetic relationship between P. falciparum and Plasmodium reichenowi, their distinctness from the three other known human malaria parasites (Plasmodium vivax, Plasmodium ovale, and Plasmodium malariae), as well as from other primate parasites, and their remoteness from bird or lizard parasites, was soon confirmed by other studies (5-7). It was assumed, as a working hypothesis, that P. falciparum and P. reichenowi had evolved from a common ancestor parasite, independently in their respective hosts, humans and chimpanzees, as these two lineages gradually diverged from one another over the last 5-7 million years-the cospeciation hypothesis. Two alternative hypotheseseither (i) a human origin (P. reichenowi evolved from an introduction of P. falciparum into chimpanzee hosts) or (ii) a chimpanzee origin (P. falciparum evolved from the introduction of P. reichenowi into the human lineage)-could not be tested against each other or against the cospeciation hypothesis, because only one P. reichenowi isolate was available, which had been isolated from a captive chimpanzee.It was soon demonstrated by Rich et al. (8), Rich and Ayala (9), and Ayala and Rich (10) that P. falciparum has very low levels of neutral genetic polymorphism, a result that was subsequently confirmed by other investigators (11...

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Apicomplexans and Bats

2017

Bats and Human Health

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Multiple host-switching of Haemosporidia parasites in bats

Cited by 59 publications

References 29 publications

Rerooting the evolutionary tree of malaria parasites

Rerooting the evolutionary tree of malaria parasites

African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus

Apicomplexans and Bats

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