Open Access

Diversity of malaria parasites in great apes in Gabon

  • Larson Boundenga1, 3Email author,
  • Benjamin Ollomo1,
  • Virginie Rougeron1, 2,
  • Lauriane Yacka Mouele1,
  • Bertrand Mve-Ondo1,
  • Lucrèce M Delicat-Loembet1,
  • Nancy Diamella Moukodoum1,
  • Alain Prince Okouga1,
  • Céline Arnathau2,
  • Eric Elguero2,
  • Patrick Durand2,
  • Florian Liégeois1, 4,
  • Vanina Boué1,
  • Peggy Motsch1,
  • Guillaume Le Flohic1,
  • Alphonse Ndoungouet1,
  • Christophe Paupy1, 2,
  • Cheikh Tidiane Ba3,
  • Francois Renaud2 and
  • Franck Prugnolle1, 2
Contributed equally
Malaria Journal201514:111

https://doi.org/10.1186/s12936-015-0622-6

Received: 20 November 2014

Accepted: 22 February 2015

Published: 14 March 2015

Abstract

Background

Until 2009, the Laverania subgenus counted only two representatives: Plasmodium falciparum and Plasmodium reichenowi. The recent development of non-invasive methods allowed re-exploration of plasmodial diversity in African apes. Although a large number of great ape populations have now been studied regarding Plasmodium infections in Africa, there are still vast areas of their distribution that remained unexplored. Gabon constitutes an important part of the range of western central African great ape subspecies (Pan troglodytes troglodytes and Gorilla gorilla gorilla), but has not been studied so far. In the present study, the diversity of Plasmodium species circulating in great apes in Gabon was analysed.

Methods

The analysis of 1,261 faecal samples from 791 chimpanzees and 470 gorillas collected from 24 sites all over Gabon was performed. Plasmodium infections were characterized by amplification and sequencing of a portion of the Plasmodium cytochrome b gene.

Results

The analysis of the 1,261 samples revealed that at least six Plasmodium species circulate in great apes in Gabon (Plasmodium praefalciparum, Plasmodium gorA (syn Plasmodium adleri), Plasmodium gorB (syn Plasmodium blacklocki) in gorillas and Plasmodium gaboni, P. reichenowi and Plasmodium billcollinsi in chimpanzees). No new phylogenetic lineages were discovered. The average infection rate was 21.3% for gorillas and 15.4% for chimpanzees. A logistic regression showed that the probability of infection was significantly dependent on the freshness of the droppings but not of the host species or of the average pluviometry of the months of collection.

Keywords

Plasmodial diversity Laverania clade Great apes Cytochrome-b Gabon

Background

Plasmodium falciparum is a protozoan parasite responsible for malaria in humans. Among the five parasites infecting humans (Plasmodium falciparum, Plasmodium malariae, Plasmodium ovale, Plasmodium vivax and Plasmodium knowlesi), P. falciparum is by far the most virulent, responsible every year for approximately 207 million clinical cases and 627,000 deaths in the world [1], of which 98% are in sub-Saharan Africa [2-5]. Malaria is proving to be an obstacle that can slow down economic prosperity in many tropical countries, particularly in Africa [3].

Plasmodium falciparum belongs to the subgenus Laverania, which up to 2009 included only two known representatives: P. falciparum and Plasmodium reichenowi, a parasite from chimpanzees. Since 2009, thanks to the use of molecular tools for species identification and the development of non-invasive methods, several studies re-explored the diversity of Plasmodium species circulating in non-human primates in Africa, especially great apes (gorillas and chimpanzees) [6-8]. These studies revealed the existence of several lineages/species related to P. falciparum, deeply modifying the comprehension of the evolution of this parasite and of Laverania more generally. Four Laverania species are now recognized to infect chimpanzees: P. reichenowi, Plasmodium billcollinsi, Plasmodium gaboni and Plasmodium billbrayi [9-11]. For gorillas, there are three species: Plasmodium praefalciparum (the closest relative of P. falciparum), Plasmodium gorB (syn-Plasmodium blacklocki) and Plasmodium gorA (syn-Plasmodium adleri) [2,12]. Great apes have also been shown to be infected with species of the subgenus Plasmodium (non-Laverania): P. malariae-like, P. ovale-like and P. vivax-like parasites [8,13,14].

Was the entire diversity of Plasmodium species circulating in great apes in Africa discovered? Although a large number of great ape populations in Africa have now been studied regarding Plasmodium infections, there are still vast areas of their geographic distribution that remain unexplored. This is the case, for instance, for the western, central African populations of chimpanzees and gorillas (Pan troglodytes troglodytes and Gorilla gorilla gorilla). Although the range of both species covers all Gabon, half the surface of the Republic of the Congo, the south of Cameroon (south of the Sanaga river) and south of the Central African Republic, Plasmodium infections were almost only studied in populations from Cameroon, making about two-thirds of their range still unexplored [2,3,12].

In this study, using the second largest bank of faecal samples studied so far (more than 1,200 faecal samples), the diversity of Plasmodium species circulating in the great ape populations of Gabon was analysed. An investigation of the ecological factors susceptible to influence the detection of Plasmodium from these non-invasive samples was also performed.

Methods

Origin of faecal samples

Faecal samples of chimpanzees and gorillas were collected in 24 sites in Gabon from 2010 to 2014 (Figure 1a and Table 1). In the field, the origin of the faeces (chimpanzee or gorilla) was deduced according to cues such as the type of nest near which they were found, footprints, texture, and odours. Freshness of the faeces (>24or <24 hours post excretion) was also estimated based on the freshness of surrounding nests (when present), texture, colours, humidity, and level of degradation. All samples were preserved in RNAlater® (Life technologies, USA) and conserved at the CIRMF at -80°C. Their origin (chimpanzee or gorilla) was confirmed by mitochondrial DNA analysis as previously described [15,16]. This investigation was approved by the Government of the Republic of Gabon and with the authorization of the Agence Nationale des Parcs Nationaux (ANPN). In total, 791 faecal samples of chimpanzees and 470 of gorillas were collected and analysed.
Figure 1

Sampling sites and variations of Plasmodium prevalences in Gabon. (a) Distribution of the sampling sites and amount of gorilla and chimpanzee samples collected and analysed in each site. Figure also shows the variations of prevalence (frequency of PCR-positives) and relative frequencies among positives of the different parasite species within the various populations of gorillas (b) and chimpanzees (c) sampled.

Table 1

List of collection sites, abbreviations and geographical coordinates in Gabon

Sites

Abbreviations

Coordinates

(Degree, minute, second)

Lope

LP

S0°13′21.5″

E11°36′ 37.5″

Lope-Mikongo

LPM

S0°18′27.2″

E11°40′10.3″

Tsouba

TB

S1°09′54.2″

E14°26′46.8″

Makande

MD

S0°40′53.7″

E11°55′34.4″

Langoue

LG

N0°00′05.8″

E12°27′25.9″

Parc Ivindo-Langoue

PIL

S0°11′23.0″

E12°34′58.4″

Parc Ivindo-Iret-Kongou-Djidji

PIKD

N0°30′05.2″

E12°48′ 03.4″

Makatamangoye 1

MAK1

S0°08′39.3″

E13°36′47.6″

Monts De Cristal

MC

N0°40′15.4″

E10°24′54.2″

Parc Ivindo

PI

N0°23′24.8″

E12°41′33.1″

Djidji

DJ

N0°10′41.2″

E12°43′51.8″

Mwagna

MG

N0°38′53.5″

E13°52′08.2″

Boumango

BG

S1°43′36.0″

E14°03′10.0″

Malouma

ML

N0°39′01.6″

E13°52′17.2″

Lope 3

LP3

S0°19′32.4″

E11°37′23.6″

Gabonville

GV

N1°46′55.7″

E11°56′58.4″

Tomassi

TM

N1° 06′37.0″

E11°42′42.4″

Iyokomilieu

IYO

N0°02′54.1″

E13°36′05.6″

Boue

BE

S0°11′52. 7″

E12°02′01.8″

Parc de Loango

PL

S1°59′54.8″

E9°27′10.5″

Waka

WK

S1°07′57.3″

E11°08′30.8″

Bakoumba

BKB

S1°45′47.8″

E12°57′06.2″

Lope-Nord

LPN

N0°18′52.1″

E12°34′37.7″

Konossaville

KSV

N1°40′23.9″

E12°04′ 09.7″

Extraction of DNA and PCR

Faecal DNA was extracted using the QIAamp DNA Stool Mini Kit (Qiagen, Courteboeuf, France) as previously described [17] and Plasmodium infections were determined after amplification of a portion of Plasmodium mitochondrial genome (cytochrome b: cyt-b) as described in Prugnolle et al. [2]. All amplified products (10 μl) were run on 1.5% agarose gels in TAE buffer. The PCR-amplified products (956 bp) were used as templates for sequencing. DNA sequencing was performed by Eurofin MWG [18].

Species identification in mixed infections

When sequence chromatograms showed multiple peaks (heterozygous base calling), the program Mixed Sequences Reader (MSR) was used to determine if the isolates were mixed infected and by which species [19]. This program can directly analyse heterozygous base-calling fluorescence chromatograms and identify species in presence from a list of reference sequences (Table 2).
Table 2

Percentage of mixed infections detected from sequence chromatograms with multiple peaks using the program MSR (Mixed Sequences Reader)

Host

Percentage (%) of mixed infections

Associated species (n)

  

P. reichenowi + P. gaboni(6)

P. billcollinsi + P. gaboni(1)

Chimpanzees

20% (8/40)

P. reichenowi + P. billcollinsi(1)

Gorillas

28% (8/29)

P. adleri + P. praefalciparum(7)

P. adleri + P. blacklocky(1)

n: Number of mixed infection found.

Phylogenetic analyses

Phylogenetic analyses were performed using only cyt-b sequences derived from chromatograms with no ambiguous base calls. To examine the relationship of the cyt-b sequences obtained with the different Plasmodium species known so far, a phylogenetic tree was constructed using a set of reference sequences belonging to different Plasmodium species. Hosts and GenBank accession numbers for these reference sequences are given in Table 3. The multiple alignment of all partial cyt-b sequences (686 nucleotides) was done using ClustalW (v 1.8.1 in BioEdit v.7.0.9.0. software) [20]. Maximum likelihood (ML) tree construction was based on the cyt-b sequences. The best-fitting ML model under the Akaike Information Criterion was GTR (general time reversible) + ModelTest. [21] The highest-likelihood DNA tree and corresponding bootstrap support values were obtained by PhyML (freely available at the ATGC bioinformatics platform [22,23]) using NNI (nearest neighbour interchange) + SPR (sub-tree pruning regrafting) branch swapping and 100 bootstrap replicates [24].
Figure 2

Phylogenetic relationships between the Cytochrome b sequences obtained in the study and those of known Plasmodium species (represented by their accession number). The tree was built based on cytochrome b (cyt-b) sequences of 686 bp. Red indicates sequences obtained from chimpanzees and green from gorillas. Bootstrap values are given at each node. More details on the different reference sequences can be found in Table 3.

Table 3

Accession numbers of the sequences of reference used in the phylogenetic tree

Accession number

Isolates

Species

Host species

References

HM235178

C1 BBptt238

P. reichenowi

Chimpanzee

Liu et al. [12]

HM235317

C2 LBptt176

P. gaboni

Chimpanzee

Liu et al. [12]

HM234979

C2 BBptt93

P. gaboni

Chimpanzee

Liu et al. [12]

HM234980

C1 BBptt93

P. reichenowi

Chimpanzee

Liu et al. [12]

HM234976

C3 BApts1413

P. billcollinsi

Chimpanzee

Liu et al. [12]

KC203544

EC4014_SGA500.11

P. falciparum

Human

Sundararaman et al. [25]

FJ895308

Isolate B

P. gaboni

Chimpanzee

Ollomo et al. [11]

GU045315

BQ642

P. reichenowi

Chimpanzee

Prugnolle et al. [2]

GQ355486

DRCJ

P. malariae

Bonobo

Krief et al. [26]

FJ409564

CPZcam91

P. ovale

Chimpanzee

Duval et al. [27]

KF591814

MRL49_FD_SGA1k.

P. vivax

Human

Liu et al. [14]

JQ345521

KN013

P. knowlesi

Human

Neoh Wan Fen et al. [28]

GU045317

BQ668

P. blacklocki

Gorilla

Prugnolle et al. [2]

GU045322

BQ638

P. adleri

Gorilla

Prugnolle et al. [2]

HM235386

G1 DDgor27

P. praefalciparum

Gorilla

Liu et al. [12]

HM235295

G3 DSgor24

P. blacklocki

Gorilla

Liu et al. [12]

HM235203

G1 DSgor86

P. praefalciparum

Gorilla

Liu et al. [12]

HM235059

G2 KKgor2638

P. adleri

Gorilla

Liu et al. [12]

JF923762

MO454

P. praefalciparum

C. nictitans

Prugnolle et al. [2]

GU815512

Louise

P. billcollinsi

Chimpanzee

Kaiser et al. [8]

GQ355478

UGF

P. billcollinsi

Chimpanzee

Krief et al. [26]

GQ355477

UGD

P. billcollinsi

Chimpanzee

Krief et al. [26]

AJ251941

-

P. reichenowi

Chimpanzee

Conway et al. [29]

JX893151

Clone39C

P. gaboni

Chimpanzee

Pacheco et al. [30]

JX893154

Clone20A

P. reichnowi

Chimpanzee

Pacheco et al. [30]

Statistical analyses

All statistical analyses were performed using R [31]. A logistic regression was used to analyse the variations among individuals in the infection status. In these models, the variable to be predicted was the presence/absence of a Plasmodium infection. The predictive variables were: (i) the site of collection (random effect); (ii) freshness of the faeces; (iii) host species; and, (iv) average pluviometry during months of collection (fixed effects). For the second predictive variable, faeces were subdivided into two groups: the faecal samples deposited less than 24 hours before collection and those collected after 24 hours. The host species corresponded to gorilla and chimpanzee. Finally, for each month of collection, the average Gabonese pluviometry (estimated from data collected from1960 to 1990) was retrieved from [32], which data were produced by the Climatic Research Unit (CRU) of University of East Anglia (UEA). Pluviometry was considered as a possible predictive variable because it is known to influence levels of infection in human foci [33,34].

GeneBank accession numbers published in this study

The sequences reported in this study were deposited in GenBank under the following accession numbers KP875428 to KP875480

Results

Plasmodium species infecting great apes in Gabon

Some 1,261 faecal samples from wild chimpanzees (n = 791) and gorillas (n = 470) from 24 sites were analysed (Figure 1a). Among them, 122 samples of chimpanzees (15.42%) and 100 of gorillas (21.28%) were detected positive to a Plasmodium infection by Cyt-b PCR. Sequences of quality (of sufficient size (>600 bp) and with a clear chromatogram) were obtained for 31% (n = 69) of the Cyt-b amplicons. Among them, sixteen showed multiple peaks and were identify as clear mixed infections by the program MSR. The frequency of mixed infections observed in chimpanzees and gorillas as estimated by the analysis of the chromatograms is given in Table 2. Phylogenetic analyses (Figure 2) revealed the presence of three Plasmodium species in chimpanzees (P. gaboni, P. reichenowi and P. billcollinsi) and three in gorillas (P. praefalciparum, P. gorA and P. gorB). Neither species of the subgenus Plasmodium (P. vivax-like, P. malariae-like and P. ovale-like) nor new phylogenetic lineages were found in these samples. Relative frequencies of each Plasmodium species in each site among positives are given in Figure 1a-c.

Over the entire dataset, logistic regressions revealed that the probability of infection was only significantly dependent on the variable ‘freshness of the stool’. Pluviometry as well as host species did not significantly explain the probability of infection (Table 4). As shown in Table 4, the probability of infection was higher in stools collected less than 24 hours after dropping than in the older ones. Overall, freshness of the stools did not significantly differ between chimpanzees and gorillas (p-value = 0.07).
Table 4

Results of the logistic regression

Variable

P-value

Odds ratio [CI 95% ]

Host species

0.051390

0.67 [0.503 to 0. 905]

Freshness of the faeces

0.006684

2.038[1.458 to 2. 849]

Pluviometry

0.581011

0.576 [0.429 to 0. 775]

The presence or absence of infection by Plasmodium was the variable to be predicted. Predictive variables were: host species, freshness of faeces (<24 or >24 hr) and pluviometry. CI95%: 95% Confidence Interval.

Discussion

In the last few years, several new Plasmodium species were discovered in African non-human primates, especially great apes [2,3,6,10,26]. These discoveries were made possible by the development of a non-invasive method allowing detection of Plasmodium infections from faecal samples [2,6], despite inherent problems of DNA degradation with this type of biological material. This issue was overcome by the use of mitochondrial sequences to amplify the parasite, which presents several advantages: 1) Mitochondrial DNA is in multiple copy inside parasites (unlike nuclear DNA) and 2) if properly chosen, small portions of the mitochondrial genome (as small as 200 bp), can contain enough phylogenetic information to identify the different Plasmodium species. This method is now one of the main methods used to analyse Plasmodium from wild non-human primates [2,7,12,25].

In the present study, analyses were performed on a set of 1,261 faecal samples collected all over Gabon from chimpanzees and gorillas. All Plasmodium species found belonged to the subgenus Laverania and were all previously identified in Pan troglodytes troglodytes and Gorilla gorilla gorilla, respectively [2,12]. No new phylogenetic lineage or species were identified. Surprisingly, no species of the subgenus Plasmodium (non-Laverania) were identified either. This is at odds with recent observations made from ape blood samples or infected sylvatic anopheline mosquitoes collected in Gabon showing the circulation of P. vivax-like parasites in the area. [13] These results are nevertheless congruent with those from Liu et al. [12]. Although they analysed 3,000 ape faecal samples from west and central Africa, they only obtained seven sequences of Plasmodium belonging to the subgenus Plasmodium (non-Laverania).

One main factor could explain why parasites of the subgenus Plasmodium were not detected and this is most likely linked to the nature of the primers used to perform PCRs. Indeed, as in the study of Liu et al. [12], the primers used were specifically designed to amplify sequences of Laverania parasites. As a consequence, several nucleotides of differences separated them from the homologous sequences in P. vivax, P. malariae and P. ovale, thus very likely reducing the sensitivity of this PCR to detect non-Laverania species. In addition, such problem might have been amplified by the presence of co-infections with Laverania species. Indeed, it has been demonstrated that in case of co-infection, the PCR tends to favour the amplification of the parasite with the best matching sequence to the primers [35,36]. Recently, Liu et al. [14] solved this problem by designing primers specific to P. vivax. Out of the 3,000 samples previously analysed and re-analysed with other samples, they finally detected more than 87 P. vivax infections.

In this study, no Laverania species were found to infect both hosts (gorillas and chimpanzees). This reinforces the hypothesis that Laverania lineages infect specific hosts [10], a specificity that could be associated to specific ligand/receptor interactions occurring in the vertebrate host, as suggested by several studies [37], or by ecological factors such as the trophic preferences of the vectors [38] or the fact that gorillas’ and chimpanzees’ home ranges might not overlap in space and time. Additional studies would be needed to disentangle these different possibilities.

No human Plasmodium species were found. This result is congruent with other studies performed so far on wild populations of apes [8,12,39] thus confirming that, contrarily to what some authors have feared [7,40], great apes do not (and will certainly never) constitute reservoirs of Plasmodium, in particular P. falciparum, for humans. The fact that their populations are rapidly declining [41,42] is unfortunately another element in support of this prediction. Finally, no evidence of ape-to-human transfers of Laverania species was ever recorded despite efforts to find them [37]. The only documented record of this kind of transfer, in a natural context, was for a P. vivax-like (non-Laverania) parasite [13].

Regarding the prevalence of infections, more than 15% of the chimpanzee and 21% of the gorilla samples were positive to Plasmodium. Infections were detected in 17out of 23sites for chimpanzees and 16 out of 24 for gorillas. Global rates of infection found in this study are similar to those found by Prugnolle et al. [2], Kaiser et al. [8], and Liu et al. [12] in other areas. As previously discussed [2,12], it is very likely that the accurate rates of infection are higher, because the detection of Plasmodium in this kind of biological material (faecal) is expected to be less sensitive than in blood, as it is the case for urine and saliva [12,43,44], due to sample degradation or repeated sampling (faecal samples from the same individual may have been collected several times). The effect of sample degradation (and hence DNA degradation) is evident here when comparing the rates of infection detected in the faeces that were collected before and after 24 hours post excretion. The freshest (and so the less degraded) faecal samples significantly present more Plasmodium infections than the other ones (odds ratio = 2.038).

Notes

Declarations

Acknowledgements

Authors thank the three reviewers for their constructive comments. The study was funded by Centre International de Recherches Médicales de Franceville (CIRMF, Gabon), Centre National de la Recherche Scientifique (CNRS, France), Institut de Recherche pour le Développement (IRD, France) and Agence Nationale de la Recherche (ANR, France, grant ORIGIN JCJC 012). We thank all the persons that were involved in the sampling as well as the Gabonese national agency of the national parks (authorization of collection: N° AE13009/PR/ANPN/SE/CS/AEPN). We also thank Bouanga Miriame for her help.

Authors’ Affiliations

(1)
Centre International de Recherche Médicale de Franceville
(2)
MIVEGEC (Laboratoire Maladies Infectieuses et Vecteurs, Ecologie, Génétique, Evolution et Contrôle), UMR CNRS 5290 / IRD 224, Université Montpellier 1
(3)
Laboratoire d’Écologie et Biologie évolutive, Département de Biologie Animale, Faculté des Sciences et Techniques, Université Cheikh Anta Diop de Dakar
(4)
TransVIHMI (Recherche Translationnelle sur le VIH et les Maladies Infectieuses), UMI 233, Institut de Recherche pour le Développement (IRD) and Université Montpellier 1

References

  1. WHO. World malaria report 2013. Geneva: World Health Organization; 2014. p. 178.Google Scholar
  2. Prugnolle F, Ollomo B, Durand P, Yalcindag E, Arnathau C, Elguero E, et al. African monkeys are infected by Plasmodium falciparum nonhuman primate-specific strains. Proc Natl Acad Sci U S A. 2011;108:11948–53.View ArticlePubMed CentralPubMedGoogle Scholar
  3. Rich SM, Leendertz FH, Xu G, LeBreton M, Djoko CF, Aminake MN, et al. The origin of malignant malaria. Proc Natl Acad Sci U S A. 2009;106:14902–7.View ArticlePubMed CentralPubMedGoogle Scholar
  4. Jeffares DC, Pain A, Berry A, Cox AV, Stalker J, Ingle CE, et al. Genome variation and evolution of the malaria parasite Plasmodium falciparum. Nat Genet. 2007;39:120–5.View ArticlePubMed CentralPubMedGoogle Scholar
  5. Rich SM, Ayala FJ. Population structure and recent evolution of Plasmodium falciparum. Proc Natl Acad Sci U S A. 2000;97:6994–7001.View ArticlePubMed CentralPubMedGoogle Scholar
  6. Prugnolle F, Ayala F, Ollomo B, Arnathau C, Durand P, Renaud F. Plasmodium falciparum is not as lonely as previously considered. Virulence. 2011;2:71–6.View ArticlePubMedGoogle Scholar
  7. Duval L, Fourment M, Nerrienet E, Rousset D, Sadeuh SA, Goodman SM, et al. African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus. Proc Natl Acad Sci U S A. 2010;107:10561–6.View ArticlePubMed CentralPubMedGoogle Scholar
  8. Kaiser M, Lowa A, Ulrich M, Ellerbrok H, Goffe AS, Blasse A, et al. Wild chimpanzees infected with 5 Plasmodium species. Emerg Infect Dis. 2010;16:1956–9.View ArticlePubMed CentralPubMedGoogle Scholar
  9. Snounou G, Escalante A, Kasenene J, Renia L, Gruner AC, Krief S. [Malaria in hominids](in French). Bull Acad Natl Med. 2011;195:1945–54.PubMedGoogle Scholar
  10. Rayner JC, Liu W, Peeters M, Sharp PM, Hahn BH. A plethora of Plasmodium species in wild apes: a source of human infection? Trends Parasitol. 2011;27:222–9.View ArticlePubMed CentralPubMedGoogle Scholar
  11. Ollomo B, Durand P, Prugnolle F, Douzery E, Arnathau C, Nkoghe D, et al. A new malaria agent in African hominids. PLoS Pathog. 2009;5:e1000446.View ArticlePubMed CentralPubMedGoogle Scholar
  12. Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature. 2010;467:420–5.View ArticlePubMed CentralPubMedGoogle Scholar
  13. Prugnolle F, Rougeron V, Becquart P, Berry A, Makanga B, Rahola N, et al. Diversity, host switching and evolution of Plasmodium vivax infecting African great apes. Proc Natl Acad Sci U S A. 2013;110:8123–8.View ArticlePubMed CentralPubMedGoogle Scholar
  14. Liu W, Li Y, Shaw KS, Learn GH, Plenderleith LJ, Malenke JA, et al. African origin of the malaria parasite Plasmodium vivax. Nat Commun. 2014;5:3346.PubMed CentralPubMedGoogle Scholar
  15. Santiago ML, Lukasik M, Kamenya S, Li Y, Bibollet-Ruche F, Bailes E, et al. Foci of endemic simian immunodeficiency virus infection in wild-living eastern chimpanzees (Pan troglodytes schweinfurthii). J Virol. 2003;77:7545–62.View ArticlePubMed CentralPubMedGoogle Scholar
  16. Santiago ML, Range F, Keele BF, Li Y, Bailes E, Bibollet-Ruche F, et al. Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Tai Forest, Cote d’Ivoire: implications for the origin of epidemic human immunodeficiency virus type 2. J Virol. 2005;79:12515–27.View ArticlePubMed CentralPubMedGoogle Scholar
  17. Keele BF, Van Heuverswyn F, Li Y, Bailes E, Takehisa J, Santiago ML, et al. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science. 2006;313:523–6.View ArticlePubMed CentralPubMedGoogle Scholar
  18. Eurofine ME. [www.eurofinsgenomics.com]
  19. Chang CT, Tsai CN, Tang CY, Chen CH, Lian JH, Hu CY, et al. Mixed sequence reader: a program for analyzing DNA sequences with heterozygous base calling. Sci World J. 2012;2012:365104.Google Scholar
  20. Hall T. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:45–98.Google Scholar
  21. Posada D, Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14:817–8.View ArticlePubMedGoogle Scholar
  22. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008;36:465–9.View ArticleGoogle Scholar
  23. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52:696–704.View ArticlePubMedGoogle Scholar
  24. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21.View ArticlePubMedGoogle Scholar
  25. Sundararaman SA, Liu W, Keele BF, Learn GH, Bittinger K, Mouacha F, et al. Plasmodium falciparum-like parasites infecting wild apes in southern Cameroon do not represent a recurrent source of human malaria. Proc Natl Acad Sci U S A. 2013;110:7020–5.View ArticlePubMed CentralPubMedGoogle Scholar
  26. Krief S, Escalante AA, Pacheco MA, Mugisha L, Andre C, Halbwax M, et al. On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from Bonobos. PLoS Pathog. 2010;6:e1000765.View ArticlePubMed CentralPubMedGoogle Scholar
  27. Duval L, Nerrienet E, Rousset D, Sadeuh Mba SA, Houze S, Fourment M, et al. Chimpanzee malaria parasites related to Plasmodium ovale in Africa. PLoS One. 2009;4:e5520.View ArticlePubMed CentralPubMedGoogle Scholar
  28. Joveen-Neoh WF, Chong KL, Wong CM, Lau TY. Incidence of malaria in the interior division of sabah, malaysian borneo, based on nested PCR. J Parasitol Res. 2011;2011:104284.View ArticlePubMed CentralPubMedGoogle Scholar
  29. Conway DJ, Fanello C, Lloyd JM, Al-Joubori BM, Baloch AH, Somanath SD, et al. Origin of Plasmodium falciparum malaria is traced by mitochondrial DNA. Mol Biochem Parasitol. 2000;111:163–71.View ArticlePubMedGoogle Scholar
  30. Pacheco MA, Cranfield M, Cameron K, Escalante AA. Malarial parasite diversity in chimpanzees: the value of comparative approaches to ascertain the evolution of Plasmodium falciparum antigens. Malar J. 2013;12:328.View ArticlePubMed CentralPubMedGoogle Scholar
  31. R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2008. URL: http://www.R-project.org. ISBN 3-900051-07-0.Google Scholar
  32. Group WB. Climate change Knowledge Portal: Average Monthly Rainfall 1901 to 2009 of Gabon. [www.worldbank.org/contry/gabon]. 2014.
  33. Robert V, Dieng H, Lochouran L, Traore SF, Trape JF, Simondon F, et al. [Malaria transmission in the rural zone of Niakhar, Senegal](in French). Trop Med Int Health. 1998;3:667–77.View ArticlePubMedGoogle Scholar
  34. Ouldabdallahi M, Ouldbezeid M, Diop C, Dem E, Lassana K. [Epidemiology of human schistosomiasis in Mauritania. The right bank of the Senegal River as model](in French). Bull Soc Pathol Exot. 2010;103:317–22.View ArticlePubMedGoogle Scholar
  35. Valkiunas G, Palinauskas V, Ilgunas M, Bukauskaite D, Dimitrov D, Bernotiene R, et al. Molecular characterization of five widespread avian haemosporidian parasites (Haemosporida), with perspectives on the PCR-based detection of haemosporidians in wildlife. Parasitol Res. 2014;113:2251–63.View ArticlePubMedGoogle Scholar
  36. Zehtindjiev P, Krizanauskiene A, Bensch S, Palinauskas V, Asghar M, Dimitrov D, et al. A new morphologically distinct avian malaria parasite that fails detection by established polymerase chain reaction-based protocols for amplification of the cytochrome B gene. J Parasitol. 2012;98:657–65.View ArticlePubMedGoogle Scholar
  37. Wanaguru M, Liu W, Hahn BH, Rayner JC, Wright GJ. RH5-Basigin interaction plays a major role in the host tropism of Plasmodium falciparum. Proc Natl Acad Sci U S A. 2013;110:20735–40.View ArticlePubMed CentralPubMedGoogle Scholar
  38. Paupy C, Makanga B, Ollomo B, Rahola N, Durand P, Magnus J, et al. Anopheles moucheti and Anopheles vinckei are candidate vectors of ape Plasmodium parasites, including Plasmodium praefalciparum in Gabon. PLoS One. 2013;8:e57294.View ArticlePubMed CentralPubMedGoogle Scholar
  39. Prugnolle F, Durand P, Neel C, Ollomo B, Ayala FJ, Arnathau C, et al. African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proc Natl Acad Sci U S A. 2010;107:1458–63.View ArticlePubMed CentralPubMedGoogle Scholar
  40. Duval L, Ariey F. Ape Plasmodium parasites as a source of human outbreaks. Clin Microbiol Infect. 2012;18:528–32.View ArticlePubMedGoogle Scholar
  41. Prado-Martinez J, Sudmant PH, Kidd JM, Li H, Kelley JL, Lorente-Galdos B, et al. Great ape genetic diversity and population history. Nature. 2013;499:471–5.View ArticlePubMedGoogle Scholar
  42. Campbell G, Kuehl H, N’Goran Kouame P, Boesch C. Alarming decline of West African chimpanzees in Cote d’Ivoire. Curr Biol. 2008;18:R903–4.View ArticlePubMedGoogle Scholar
  43. Nwakanma DC, Gomez-Escobar N, Walther M, Crozier S, Dubovsky F, Malkin E, et al. Quantitative detection of Plasmodium falciparum DNA in saliva, blood, and urine. J Infect Dis. 2009;199:1567–74.View ArticlePubMedGoogle Scholar
  44. Mharakurwa S, Simoloka C, Thuma PE, Shiff CJ, Sullivan DJ. PCR detection of Plasmodium falciparum in human urine and saliva samples. Malar J. 2006;5:103.View ArticlePubMed CentralPubMedGoogle Scholar

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© Boundenga et al.; licensee BioMed Central. 2015

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