The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs
Liu, W. et al. African origin of the malaria parasite Plasmodium vivax. Nat. Commun. 5, 3346 (2014).PubMedÂ
Google ScholarÂ
Liu, W. et al. Multigenomic delineation of Plasmodium species of the Laverania subgenus infecting wild-living chimpanzees and gorillas. Genome Biol. Evolution 8, 1929â1939 (2016).CASÂ
Google ScholarÂ
Liu, W. et al. Single genome amplification and direct amplicon sequencing of Plasmodium spp. DNA from ape fecal specimens. Protocol Exchange 1â14 (2010).Liu, W. et al. Wild bonobos host geographically restricted malaria parasites including a putative new Laverania species. Nat. Commun. 8, 1635 (2017).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Prugnolle, F. et al. African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proc. Natl Acad. Sci. USA 107, 1458â1463 (2010).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Sharp, P. M., Plenderleith, L. J. & Hahn, B. H. Ape origins of human malaria. Annu. Rev. Microbiol. 74, 39â63 (2020).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Liu, W. et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467, 420â425 (2010).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Otto, T. D. et al. Genomes of all known members of a Plasmodium subgenus reveal paths to virulent human malaria. Nat. Microbiol. 3, 687â697 (2018).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Boundenga, L. et al. Diversity of malaria parasites in great apes in Gabon. Malar. J. 14, 1â8 (2015).CASÂ
Google ScholarÂ
DĂ©licat-Loembet, L. et al. No evidence for ape Plasmodium infections in humans in gabon. Plos One 10, e0126933 (2015).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Sundararaman, S. A. 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. USA 110, 7020â7025 (2013).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Junker, J. et al. Recent decline in suitable environmental conditions for African great apes. Diversity Distrib. 18, 1077â1091 (2012).
Google ScholarÂ
de Nys, H. M. et al. Age-related effects on malaria parasite infection in wild chimpanzees. Biol. Lett. 9, 20121160 (2013).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
de Nys, H. M. et al. Malaria parasite detection increases during pregnancy in wild chimpanzees. Malar. J. 13, 413 (2014).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Kaiser, M. et al. Wild chimpanzees infected with 5 Plasmodium species. Emerg. Infect. Dis. 16, 1956â1959 (2010).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Paupy, C. et al. Anopheles moucheti and Anopheles vinckei are candidate vectors of ape Plasmodium parasites, including Plasmodium praefalciparum in Gabon. PLoS ONE 8, e57294 (2013).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Makanga, B. et al. Ape malaria transmission and potential for ape-to-human transfers in Africa. Proc. Natl Acad. Sci. USA 113, 5329â5334 (2016).Loy, D. E. et al. Investigating zoonotic infection barriers to ape Plasmodium parasites using faecal DNA analysis. Int. J. Parasitol. 48, 531â542 (2018).Martin, M., Rayner, J., Gagneux, P., Barnwell, J. & Varki, A. Evolution of humanâchimpanzee differences in malaria susceptibility: Relationship to human genetic loss of N-glycolylneuraminic acid. Proc. Natl Acad. Sci. USA 102, 12819â12824 (2005).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Scully, E. J., Kanjee, U. & Duraisingh, M. T. Molecular interactions governing host-specificity of blood stage malaria parasites. Curr. Opin. Microbiol. 40, 21â31 (2017).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Sundararaman, S. A. et al. Genomes of cryptic chimpanzee Plasmodium species reveal key evolutionary events leading to human malaria. Nat. Commun. 7, 11078 (2016).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Wanaguru, M., Liu, W., Hahn, B. H., Rayner, J. C. & Wright, G. J. RH5-Basigin interaction plays a major role in the host tropism of Plasmodium falciparum. Proc. Natl Acad. Sci. USA 110, 20735â20740 (2013).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Ngoubangoye, B. et al. The host specificity of ape malaria parasites can be broken in confined environments. Int. J. Parasitol. 46, 737â744 (2016).PubMedÂ
Google ScholarÂ
Mapua, M. I. et al. A comparative molecular survey of malaria prevalence among Eastern chimpanzee populations in Issa Valley (Tanzania) and Kalinzu (Uganda). Malar. J. 15, 423 (2016).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Wu, D. F. et al. Seasonal and inter-annual variation of malaria parasite detection in wild chimpanzees. Malar. J. 17, 1â5 (2018).CASÂ
Google ScholarÂ
Craig, M., le Sueur, D. & Snow, B. A climate-based distribution model of malaria transmission in sub-Saharan Africa. Parasitol. Today 15, 105â111 (1999).CASÂ
PubMedÂ
Google ScholarÂ
Mordecai, E. A. et al. Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecol. Lett. 16, 22â30 (2013).PubMedÂ
Google ScholarÂ
Paaijmans, K. P. et al. Influence of climate on malaria transmission depends on daily temperature variation. Proc. Natl Acad. Sci. USA 107, 15135â15139 (2010).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Parham, P. E. & Michael, E. Modeling the effects of weather and climate change on malaria transmission. Environ. Health Perspect. 118, 620â626 (2010).PubMedÂ
Google ScholarÂ
LaPointe, D. A., Goff, M. L. & Atkinson, C. T. Thermal constraints to the sporogonic development and altitudinal distribution of avian malaria Plasmodium relictum in Hawaiâi. J. Parasitol. 96, 318â324 (2010).PubMedÂ
Google ScholarÂ
Vanderberg, J. P. & Yoeli, M. Effects of temperature on sporogonic development of Plasmodium berghei. J. Parasitol. 52, 559â564 (1966).Macdonald, G. The Epidemiology and Control of Malaria (Oxford University Press, 1957).Ryan, S. J. et al. Mapping physiological suitability limits for malaria in Africa under climate change. Vector-Borne Zoonotic Dis. 15, 718â725 (2015).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Gemperli, A. et al. Mapping malaria transmission in West and Central Africa. Tropical Med. Int. Health 11, 1032â1046 (2006).
Google ScholarÂ
Gething, P. W. et al. Modelling the global constraints of temperature on transmission of Plasmodium falciparum and P. vivax. Parasites Vectors 4, 92 (2011).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Weiss, D. J. et al. Air temperature suitability for Plasmodium falciparum malaria transmission in Africa 2000â2012: a high-resolution spatiotemporal prediction. Malar. J. 13, 171 (2014).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Lyons, C. L., Coetzee, M. & Chown, S. L. Stable and fluctuating temperature effects on the development rate and survival of two malaria vectors, Anopheles arabiensis and Anopheles funestus. Parasites Vectors 6, 104 (2013).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Paaijmans, K. P., Wandago, M. O., Githeko, A. K. & Takken, W. Unexpected high losses of Anopheles gambiae larvae due to rainfall. PLoS One 2, e1146 (2007).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Faust, C. & Dobson, A. P. Primate malarias: diversity, distribution and insights for zoonotic Plasmodium. One Health 1, 66â75 (2015).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Tucker Lima, J. M., Vittor, A., Rifai, S. & Valle, D. Does deforestation promote or inhibit malaria transmission in the Amazon? A systematic literature review and critical appraisal of current evidence. Philos. Trans. R. Soc. Lond. Ser. B, Biol. Sci. 372, 20160125 (2017).
Google ScholarÂ
Borner, J. et al. Phylogeny of haemosporidian blood parasites revealed by a multi-gene approach. Mol. Phylogenetics Evolution 94, 221â231 (2016).CASÂ
Google ScholarÂ
Emery Thompson, M., Muller, M. N., Machanda, Z. P., Otali, E. & Wrangham, R. W. The Kibale Chimpanzee Project: over thirty years of research, conservation, and change. Biol. Conserv. 252, 108857 (2020).
Google ScholarÂ
Langergraber, K. E., Mitani, J. C. & Vigilant, L. The limited impact of kinship on cooperation in wild chimpanzees. Proc. Natl Acad. Sci. USA 104, 7786â7790 (2007).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Arandjelovic, M. et al. Two-step multiplex polymerase chain reaction improves the speed and accuracy of genotyping using DNA from noninvasive and museum samples. Mol. Ecol. Resour. 9, 28â36 (2009).CASÂ
PubMedÂ
Google ScholarÂ
Herbert, A. et al. Malaria-like symptoms associated with a natural Plasmodium reichenowi infection in a chimpanzee. Malar. J. 14, 220 (2015).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Torres, J. R. Therapy of Infectious Diseases 597â613 (2003).Trampuz, A., Jereb, M., Muzlovic, I. & Prabhu, R. M. Clinical review: severe malaria. Crit. Care 7, 315 (2003).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Akim, N. I. et al. Dynamics of P. falciparum gametocytemia in symptomatic patients in an area of intense perennial transmission in Tanzania. Am. J. Tropical Med. Hyg. 63, 199â203 (2000).CASÂ
Google ScholarÂ
Mackinnon, M. J. & Read, A. F. Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53, 689â703 (1999).PubMedÂ
Google ScholarÂ
Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754â755 (2001).CASÂ
PubMedÂ
Google ScholarÂ
Prugnolle, F. et al. African monkeys are infected by Plasmodium falciparum nonhuman primate-specific strains. Proc. Natl Acad. Sci. USA 108, 11948â11953 (2011).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Ayouba, A. et al. Ubiquitous Hepatocystis infections, but no evidence of Plasmodium falciparum-like malaria parasites in wild greater spot-nosed monkeys (Cercopithecus nictitans). Int. J. Parasitol. 42, 709â713 (2012).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Martinsen, E. S., Perkins, S. L. & Schall, J. J. A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): Evolution of life-history traits and host switches. Mol. Phylogenetics Evolution 47, 261â273 (2008).CASÂ
Google ScholarÂ
Thurber, M. I. et al. Co-infection and cross-species transmission of divergent Hepatocystis lineages in a wild African primate community. Int. J. Parasitol. 43, 613â619 (2013).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Baayen, R. H. Analyzing Linguistic Data: A Practical Introduction to Statistics (Cambridge University Press, 2008).Stanisic, D. I. et al. Acquisition of antibodies against Plasmodium falciparum merozoites and malaria immunity in young children and the influence of age, force of infection, and magnitude of response. Infect. Immun. 83, 646â660 (2015).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Taylor, R. R., Allen, S. J., Greenwood, B. M. & Riley, E. M. IgG3 antibodies to Plasmodium falciparum merozoite surface protein 2 (MSP2): increasing prevalence with age and association with clinical immunity to malaria. Am. J. Tropical Med. Hyg. 58, 406â413 (1998).CASÂ
Google ScholarÂ
World Malaria Report (World Health Organization, 2015).Shaman, J. Letter to the Editor: Caution needed when using gridded meteorological data products for analyses in Africa. Eur. Surveill. 19, 20930 (2014).
Google ScholarÂ
Tatem, A. J., Goetz, S. J. & Hay, S. I. Terra and Aqua: new data for epidemiology and public health. Int. J. Appl. Earth Observation Geoinf. 6, 33â46 (2004).
Google ScholarÂ
Adler, R. F. et al. The version-2 global precipitation climatology project (GPCP) monthly precipitation analysis (1979âpresent). J. Hydrometeorol. 4, 1147â1167 (2003).
Google ScholarÂ
Hansen, M. C. et al. High-resolution global maps of 21st-century forest cover change. Science 342, 850â853 (2013).CASÂ
PubMedÂ
Google ScholarÂ
Carter, R. & Mendis, K. N. Evolutionary and historical aspects of the burden of malaria. Clin. Microbiol. Rev. 15, 564â594 (2002).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Kwiatkowski, D. P. How malaria has affected the human genome and what human genetics can teach us about malaria. Am. J. Hum. Genet. 77, 171â192 (2005).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Tarello, W. A fatal Plasmodium reichenowi infection in a chimpanzee? Rev. de. Med. Veterinaire 156, 503â505 (2005).
Google ScholarÂ
Taylor, D. W. et al. Parasitologic and immunologic studies of experimental Plasmodium falciparum infection in nonsplenectomized chimpanzees (Pan troglodytes). Am. J. Tropical Med. Hyg. 34, 36â44 (1985).CASÂ
Google ScholarÂ
Krief, S., Martin, M., Grellier, P., Kasenene, J. & Sevenet, T. Novel antimalarial compounds isolated in a survey of self-medicative behavior of wild chimpanzees in Uganda. Antimicrobial Agents Chemother. 48, 3196â3199 (2004).CASÂ
Google ScholarÂ
Cox-Singh, J. et al. Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Clin. Infect. Dis. 46, 165â171 (2008).CASÂ
PubMedÂ
Google ScholarÂ
Singh, B. & Daneshvar, C. Human infections and detection of Plasmodium knowlesi. Clin. Microbiol. Rev. 26, 165â184 (2013).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Brasil, P. et al. Outbreak of human malaria caused by Plasmodium simium in the Atlantic Forest in Rio de Janeiro: a molecular epidemiological investigation. Lancet Global Health 5, e1038âe1046 (2017).Krief, S. et al. On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from bonobos. PLoS Pathog. 6, e1000765 (2010).Pacheco, M. A., Cranfield, M., Cameron, K. & Escalante, A. A. Malarial parasite diversity in chimpanzees: the value of comparative approaches to ascertain the evolution of Plasmodium falciparum antigens. Malar. J. 12, 328 (2013).PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Etienne, L. et al. Noninvasive follow-up of simian immunodeficiency virus infection in wild-living nonhabituated western lowland gorillas in Cameroon. J. Virol. 86, 9760â9772 (2012).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Keele, B. F. et al. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313, 523â526 (2006).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Keele, B. F. et al. Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature 460, 515â519 (2009).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Li, Y. et al. Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir. J. Virol. 86, 10776â10791 (2012).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Neel, C. et al. Molecular epidemiology of simian immunodeficiency virus infection in wild-living gorillas. J. Virol. 84, 1464â1476 (2010).CASÂ
PubMedÂ
Google ScholarÂ
Rudicell, R. S. et al. Impact of simian immunodeficiency virus infection on chimpanzee population dynamics. PLoS Pathog. 6, 1â17 (2010).
Google ScholarÂ
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772 (2012).CASÂ
PubMedÂ
PubMed CentralÂ
Google ScholarÂ
Bates, D. & Maechler, M. Lme4: linear mixed-effects models using s4 classes. Cran R Project Website (2010). More