Abstract
Pathogens are a major force affecting the evolution of mammals. In primates, strong interspecies differences in disease susceptibility, progression, and survival after exposure to particular pathogens such as immunodeficiency viruses, Plasmodium, Trypanosoma, herpesvirus suggests the existence of species-specific pathogen-associated selective pressures in the past. Despite increasing recognition that the immune systems of particular primates have evolved to respond to unique challenges, we have a fairly superficial understanding of differences in primate immune function, primate–pathogen molecular interaction, and pathogen–primate coevolution. Research in this field is hindered by a lack of interdisciplinary and cross-field integration, a focus on a limited number of pathogens, and the separation of research on primate molecular evolution and primate immune function. To better understand human and nonhuman primate evolution, immune function, and susceptibility to infectious disease, a synthesis of research on the pathogen-related evolution and biochemical mechanisms of primate interaction with a broad range of microorganisms is required. A comprehensive model of how primates and pathogens have coevolved is crucial, as interspecies differences in primate–pathogen molecular interaction play a role in the emergence of pandemic human pathogens (HIV–1/HIV-2, malaria/Plasmodium, and lice) and affect the sustainability of primate populations (Toxoplasma and Mycobacterium), the utility of primate biomedical models, and the evolution of primate genomes.
This volume was assembled to address these needs. Here, we discuss the importance of understanding primate–pathogen interaction in the context of primate evolution, conservation, and medicine, as well as highlighting current obstacles to developing a holistic picture of evolutionary interaction between primates and pathogens.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abi-Rached L, Moesta AK, Rajalingam R, Guethlein LA, Parham P (2010) Human-specific evolution and adaptation led to major qualitative differences in the variable receptors of human and chimpanzee natural killer cells. PLoS Genet 6(11):e1001192
Allison AC (1956) The sickle-cell and haemoglobin C genes in some African populations. Ann Hum Genet 21(1):67–89
Arnaud F, Caporale M, Varela M, Biek R, Chessa B, Alberti A, Golder M, Mura M, Zhang YP, Yu L et al (2007) A paradigm for virus–host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses. PLoS Pathog 3(11):e170
Artenstein AW, Hicks CB, Goodwin BS Jr, Hilliard JK (1991) Human infection with B virus following a needlestick injury. Rev Infect Dis 13(2):288–291
Bannert N, Kurth R (2006) The evolutionary dynamics of human endogenous retroviral families. Annu Rev Genomics Hum Genet 7:149–173
Berdoy M, Webster JP, Macdonald DW (2000) Fatal attraction in rats infected with Toxoplasma gondii. Proc Biol Sci 267(1452):1591–1594
Brown KA, Brain SD, Pearson JD, Edgeworth JD, Lewis SM, Treacher DF (2006) Neutrophils in development of multiple organ failure in sepsis. Lancet 368(9530):157–169
Carp HJ, Selmi C, Shoenfeld Y (2012) The autoimmune bases of infertility and pregnancy loss. J Autoimmun 38(2–3):J266–J274
Catão-Dias JL, Epiphanio S, Martins Kierulff MC (2013) Neotropical primates and their susceptibility to Toxoplasma gondii: new insights for an old problem. In: Brinkworth JF, Pechenkina E (eds) Primates, pathogens, and evolution. Springer, Heidelberg
Chapman CA, Gillespie TR, Goldberg TL (2005) Primates and the ecology of their infectious diseases: How will anthropogenic change affect host-parasite interactions? Evolut Anthropol 14:134–144
Chellman GJ, Lukas VS, Eugui EM, Altera KP, Almquist SJ, Hilliard JK (1992) Activation of B virus (Herpesvirus simiae) in chronically immunosuppressed cynomolgus monkeys. Lab Anim Sci 42(2):146–151
Cheney DL, Seyfarth RM, Andelman SJ, Lee PC (1988) Reproductive success in vervet monkeys. In: Clutton-Brock TH (ed) Reproductive success. Chicago University Press, Chicago, IL, pp 384–402
Cormier LA (2010) The historical ecology of human and wild primate malarias in the new world. Diversity 2(2):256–280
Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife–threats to biodiversity and human health. Science 287(5452):443–449
de Groot NG, Otting N, Doxiadis GG, Balla-Jhagjhoorsingh SS, Heeney JL, van Rood JJ, Gagneux P, Bontrop RE (2002) Evidence for an ancient selective sweep in the MHC class I gene repertoire of chimpanzees. Proc Natl Acad Sci USA 99(18):11748–11753
Dunlap KA, Palmarini M, Varela M, Burghardt RC, Hayashi K, Farmer JL, Spencer TE (2006) Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proc Natl Acad Sci USA 103(39):14390–14395
Duval L, Ariey F (2012) Ape Plasmodium parasites as a source of human outbreaks. Clin Microbiol Infect 18(6):528–532
Elde NC, Child SJ, Geballe AP, Malik HS (2009) Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457(7228):485–489
Elde NC, Child SJ, Eickbush MT, Kitzman JO, Rogers KS, Shendure J, Geballe AP, Malik HS (2012) Poxviruses deploy genomic accordions to adapt rapidly against host antiviral defenses. Cell 150(4):831–841
Epiphanio S, Sinhorini IL, Catao-Dias JL (2003) Pathology of toxoplasmosis in captive new world primates. J Comp Pathol 129(2–3):196–204
Estep RD, Messaoudi I, Wong SW (2010) Simian herpesviruses and their risk to humans. Vaccine 28(Suppl 2):B78–B84
Farah I, Borjesson A, Kariuki T, Yole D, Suleman M, Hau J, Carlsson HE (2003) Morbidity and immune response to natural schistosomiasis in baboons (Papio anubis). Parasitol Res 91(4):344–348
Filip LC, Mundy NI (2004) Rapid evolution by positive Darwinian selection in the extracellular domain of the abundant lymphocyte protein CD45 in primates. Mol Biol Evol 21(8): 1504–1511
Gao, F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, Cummins LB, Arthur LO, Peeters M, Shaw GM, Sharp PM, Hahn, BH (1999) Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397:436–441
Genovese G, Friedman DJ, Ross MD, Lecordier L, Uzureau P, Freedman BI, Bowden DW, Langefeld CD, Oleksyk TK, Uscinski Knob AL et al (2010) Association of trypanolytic ApoL1 variants with kidney disease in African Americans. Science 329(5993):841–845
Gogvadze E, Stukacheva E, Buzdin A, Sverdlov E (2009) Human-specific modulation of transcriptional activity provided by endogenous retroviral insertions. J Virol 83(12):6098–6105
Greenwood EJD, Schmidt F, Heeney JL (2013) The evolution of SIV in primates and the emergence of the pathogen of AIDS. In: Brinkworth JF, Pechenkina E (eds) Primates, pathogens, and evolution. Springer, Heidelberg
Haldane JBS (1949) The rate of mutation of human genes. Heredita 35(suppl):267–273
Hamblin MT, Di Rienzo A (2000) Detection of the signature of natural selection in humans: evidence from the Duffy blood group locus. Am J Hum Genet 66(5):1669–1679
Hedrick P (2004) Estimation of relative fitnesses from relative risk data and the predicted future of haemoglobin alleles S and C. J Evol Biol 17(1):221–224
Horie M, Honda T, Suzuki Y, Kobayashi Y, Daito T, Oshida T, Ikuta K, Jern P, Gojobori T, Coffin JM et al (2010) Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463(7277):84–87
Hraber P, Kuiken C, Yusim K (2007) Evidence for human leukocyte antigen heterozygote advantage against hepatitis C virus infection. Hepatology 46(6):1713–1721
Huang ES, Kilpatrick B, Lakeman A, Alford CA (1978) Genetic analysis of a cytomegalovirus-like agent isolated from human brain. J Virol 26(3):718–723
Hunter P (2010) The missing link. Viruses revise evolutionary theory. EMBO Rep 11(1):28–31
Izutsu Y (2009) The immune system is involved in Xenopus metamorphosis. Front Biosci 14:141–149
Jackson JA, Tinsley RC (2002) Effects of environmental temperature on the susceptibility of Xenopus laevis and X. wittei (Anura) to Protopolystoma xenopodis(Monogenea). Parasitol Res 88(7):632–638
Jia B, Serra-Moreno R, Neidermyer W, Rahmberg A, Mackey J, Fofana IB, Johnson WE, Westmoreland S, Evans DT (2009) Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog 5(5):e1000429
Jones JL, Kruszon-Moran D, Sanders-Lewis K, Wilson M (2007) Toxoplasma gondii infection in the United States, 1999 2004, decline from the prior decade. Am J Trop Med Hyg 77(3):405–410
Kageruka P, Mangus E, Bajyana Songa E, Nantulya V, Jochems M, Hamers R, Mortelmans J (1991) Infectivity of Trypanosoma (Trypanozoon) brucei gambiense for baboons (Papio hamadryas, Papio papio). Ann Soc Belg Med Trop 71(1):39–46
Keet DF, Kriek NP, Bengis RG, Grobler DG, Michel A (2000) The rise and fall of tuberculosis in a free-ranging chacma baboon troop in the Kruger National Park. Onderstepoort J Vet Res 67(2):115–122
Kim N, Dabrowska A, Jenner RG, Aldovini A (2007) Human and simian immunodeficiency virus-mediated upregulation of the apoptotic factor TRAIL occurs in antigen-presenting cells from AIDS-susceptible but not from AIDS-resistant species. J Virol 81(14):7584–7597
Kim HS, Kim DS, Huh JW, Ahn K, Yi JM, Lee JR, Hirai H (2008) Molecular characterization of the HERV-W env gene in humans and primates: expression, FISH, phylogeny, and evolution. Mol Cells 26(1):53–60
Klimovich VB (2002) Actual problems of evolutional immunology. Zh Evol Biokhim Fiziol 38(5):442–451
Kondgen S, Kuhl H, N'Goran PK, Walsh PD, Schenk S, Ernst N, Biek R, Formenty P, Matz-Rensing K, Schweiger B et al (2008) Pandemic human viruses cause decline of endangered great apes. Curr Biol 18(4):260–264
Koppensteiner H, Brack-Werner R, Schindler M (2012) Macrophages and their relevance in human immunodeficiency virus type I infection. Retrovirology 9:82
Koyanagi M, Kerns JA, Chung L, Zhang Y, Brown S, Moldoveanu T, Malik HS, Bix M (2010) Diversifying selection and functional analysis of interleukin-4 suggests antagonism-driven evolution at receptor-binding interfaces. BMC Evol Biol 10:223
Kwiatkowski DP (2005) How malaria has affected the human genome and what human genetics can teach us about malaria. Am J Hum Genet 77(2):171–192
Lambrecht FL (1985) Trypanosomes and Hominid evolution. Bioscience 35(10):640–646
Lapoumeroulie C, Dunda O, Ducrocq R, Trabuchet G, Mony-Lobe M, Bodo JM, Carnevale P, Labie D, Elion J, Krishnamoorthy R (1992) A novel sickle cell mutation of yet another origin in Africa: the Cameroon type. Hum Genet 89(3):333–337
Lee YK, Mazmanian SK (2010) Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330(6012):1768–1773
Leffler EM, Gao Z, Pfeifer S, Segurel L, Auton A, Venn O, Bowden R, Bontrop R, Wall JD, Sella G et al (2013) Multiple instances of ancient balancing selection shared between humans and chimpanzees. Science 339(6127):1578–1582
Levin JL, Hilliard JK, Lipper SL, Butler TM, Goodwin WJ (1988) A naturally occurring epizootic of simian agent 8 in the baboon. Lab Anim Sci 38(4):394–397
Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, Ndjango JB, Sanz CM, Morgan DB, Locatelli S et al (2010) Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467(7314):420–425
Loisel DA, Rockman MV, Wray GA, Altmann J, Alberts SC (2006) Ancient polymorphism and functional variation in the primate MHC-DQA1 5′ cis-regulatory region. Proc Natl Acad Sci USA 103(44):16331–16336
Maier AG, Duraisingh MT, Reeder JC, Patel SS, Kazura JW, Zimmerman PA, Cowman AF (2003) Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations. Nat Med 9(1):87–92
Mandl JN, Barry AP, Vanderford TH, Kozyr N, Chavan R, Klucking S, Barrat FJ, Coffman RL, Staprans SI, Feinberg MB (2008) Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections. Nat Med 14(10):1077–1087
Mandl JN, Akondy R, Lawson B, Kozyr N, Staprans SI, Ahmed R, Feinberg MB (2011) Distinctive TLR7 signaling, type I IFN production, and attenuated innate and adaptive immune responses to yellow fever virus in a primate reservoir host. J Immunol 186(11):6406–6416
Marmor M, Sheppard HW, Donnell D, Bozeman S, Celum C, Buchbinder S, Koblin B, Seage GR 3rd (2001) Homozygous and heterozygous CCR5-Delta32 genotypes are associated with resistance to HIV infection. J Acquir Immune Defic Syndr 27(5):472–481
Matzinger P (1994) Tolerance, danger, and the extended family. Annu Rev Immunol 12: 991–1045
Matzinger P (2002) The danger model: a renewed sense of self. Science 296(5566):301–305
Maynard CL, Elson CO, Hatton RD, Weaver CT (2012) Reciprocal interactions of the intestinal microbiota and immune system. Nature 489(7415):231–241
Moesta AK, Abi-Rached L, Norman PJ, Parham P (2009) Chimpanzees use more varied receptors and ligands than humans for inhibitory killer cell Ig-like receptor recognition of the MHC-C1 and MHC-C2 epitopes. J Immunol 182(6):3628–3637
Murdoch C, Finn A (2003) The role of chemokines in sepsis and septic shock. Contrib Microbiol 10:38–57
Murray S, Stem C, Boudreau B, Goodall J (2000) Intestinal parasites of baboons (Papio cynocephalus anubis) and chimpanzees (Pan troglodytes) in Gombe National Park. J Zoo Wildl Med 31(2):176–178
Mutombo M, Arita I, Jezek Z (1983) Human monkeypox transmitted by a chimpanzee in a tropical rain-forest area of Zaire. Lancet 1(8327):735–737
Nakajima T, Ohtani H, Satta Y, Uno Y, Akari H, Ishida T, Kimura A (2008) Natural selection in the TLR-related genes in the course of primate evolution. Immunogenetics 60(12):727–735
Nunn CL (2012) Primate disease ecology in comparative and theoretical perspective. Am J Primatol 74(6):497–509
Nunn C, Thrall P, Stewart K, Harcourt A (2008) Emerging infectious diseases and animal social systems. Evolut Ecol 22(4):519–543
Oner C, Dimovski AJ, Olivieri NF, Schiliro G, Codrington JF, Fattoum S, Adekile AD, Oner R, Yuregir GT, Altay C et al (1992) Beta S haplotypes in various world populations. Hum Genet 89(1):99–104
Ortiz M, Bleiber G, Martinez R, Kaessmann H, Telenti A (2006) Patterns of evolution of host proteins involved in retroviral pathogenesis. Retrovirology 3:11
Oyston PC, Dorrell N, Williams K, Li SR, Green M, Titball RW, Wren BW (2000) The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect Immun 68(6):3419–3425
Palacios G, Lowenstine LJ, Cranfield MR, Gilardi KV, Spelman L, Lukasik-Braum M, Kinani JF, Mudakikwa A, Nyirakaragire E, Bussetti AV et al (2011) Human metapneumovirus infection in wild mountain gorillas, Rwanda. Emerg Infect Dis 17(4):711–713
Pandrea I, Apetrei C (2010) Where the wild things are: pathogenesis of SIV infection in African nonhuman primate hosts. Curr HIV/AIDS Rep 7(1):28–36
Pandrea I, Apetrei C, Gordon S, Barbercheck J, Dufour J, Bohm R, Sumpter B, Roques P, Marx PA, Hirsch VM et al (2007) Paucity of CD4+CCR5+ T cells is a typical feature of natural SIV hosts. Blood 109(3):1069–1076
Puissant B, Abbal M, Blancher A (2003) Polymorphism of human and primate RANTES, CX3CR1, CCR2 and CXCR4 genes with regard to HIV/SIV infection. Immunogenetics 55(5):275–283
Pujol C, Bliska JB (2003) The ability to replicate in macrophages is conserved between Yersinia pestis and Yersinia pseudotuberculosis. Infect Immun 71(10):5892–5899
Redford PS, Murray PJ, O’Garra A (2011) The role of IL-10 in immune regulation during M. tuberculosis infection. Mucosal Immunol 4(3):261–270
Reynolds MG, Carroll DS, Karem KL (2012) Factors affecting the likelihood of monkeypox’s emergence and spread in the post-smallpox era. Curr Opin Virol 2(3):335–343
Rockman MV, Hahn MW, Soranzo N, Goldstein DB, Wray GA (2003) Positive selection on a human-specific transcription factor binding site regulating IL4 expression. Curr Biol 13(23):2118–2123
Santiago ML, Rodenburg CM, Kamenya S, Bibollet-Ruche F, Gao F, Bailes E, Meleth S, Soong SJ, Kilby JM, Moldoveanu Z et al (2002) SIVcpz in wild chimpanzees. Science 295(5554):465
Sawyer SL, Emerman M, Malik HS (2004) Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2(9):E275
Sawyer SL, Wu LI, Emerman M, Malik HS (2005) Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci USA 102(8):2832–2837
Song B, Javanbakht H, Perron M, Park DH, Stremlau M, Sodroski J (2005) Retrovirus restriction by TRIM5alpha variants from old world and new world primates. J Virol 79(7):3930–3937
Soto PC, Stein LL, Hurtado-Ziola N, Hedrick SM, Varki A (2010) Relative over-reactivity of human versus chimpanzee lymphocytes: implications for the human diseases associated with immune activation. J Immunol 184(8):4185–4195
Stenger S, Hanson DA, Teitelbaum R, Dewan P, Niazi KR, Froelich CJ, Ganz T, Thoma-Uszynski S, Melián A, Bogdan C et al (1998) An antimicrobial activity of cytolytic T cells mediated by granulysin. Science (New York, NY) 282(5386):121–125
Stothard JR, Mugisha L, Standley CJ (2012) Stopping schistosomes from “monkeying-around” in chimpanzees. Trends Parasitol 28(8):320–326
Switzer WM, Parekh B, Shanmugam V, Bhullar V, Phillips S, Ely JJ, Heneine W (2005) The epidemiology of simian immunodeficiency virus infection in a large number of wild- and captive-born chimpanzees: evidence for a recent introduction following chimpanzee divergence. AIDS Res Hum Retroviruses 21(5):335–342
Thomson R, Molina-Portela P, Mott H, Carrington M, Raper J (2009) Hydrodynamic gene delivery of baboon trypanosome lytic factor eliminates both animal and human-infective African trypanosomes. Proc Natl Acad Sci USA 106(46):19509–19514
Tishkoff SA, Varkonyi R, Cahinhinan N, Abbes S, Argyropoulos G, Destro-Bisol G, Drousiotou A, Dangerfield B, Lefranc G, Loiselet J et al (2001) Haplotype diversity and linkage disequilibrium at human G6PD: recent origin of alleles that confer malarial resistance. Science 293(5529):455–462
Van Heuverswyn F, Li Y, Neel C, Bailes E, Keele BF, Liu W, Loul S, Butel C, Liegeois F, Bienvenue Y et al (2006) Human immunodeficiency viruses: SIV infection in wild gorillas. Nature 444(7116):164
Van Valen L (1973) A new evolutionary law. Evolut Theor 1:1–30
Vandamme AM, Salemi M, Desmyter J (1998) The simian origins of the pathogenic human T-cell lymphotropic virus type I. Trends Microbiol 6(12):477–483
Vizoso AD (1975) Recovery of herpes simiae (B virus) from both primary and latent infections in rhesus monkeys. Br J Exp Pathol 56(6):485–488
Wallis J, Lee DR (1999) Primate conservation: the prevention of disease transmission. Int J Primatol 20(6):803–826
Wang T, Zeng J, Lowe CB, Sellers RG, Salama SR, Yang M, Burgess SM, Brachmann RK, Haussler D (2007) Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc Natl Acad Sci USA 104(47):18613–18618
Welburn SC, Fevre EM, Coleman PG, Odiit M, Maudlin I (2001) Sleeping sickness: a tale of two diseases. Trends Parasitol 17(1):19–24
Wheatley B, Harya Putra DK (1994) Biting the hand that feeds you: Monkeys and tourists in Balinese monkey forests. Trop Biodivers 2:317–327
Wlasiuk G, Nachman MW (2010) Adaptation and constraint at Toll-like receptors in primates. Mol Biol Evol 27(9):2172–2186
Wooding S, Stone AC, Dunn DM, Mummidi S, Jorde LB, Weiss RK, Ahuja S, Bamshad MJ (2005) Contrasting effects of natural selection on human and chimpanzee CC chemokine receptor 5. Am J Hum Genet 76(2):291–301
Yim JJ, Adams AA, Kim JH, Holland SM (2006) Evolution of an intronic microsatellite polymorphism in Toll-like receptor 2 among primates. Immunogenetics 58(9):740–745
Yohn CT, Jiang Z, McGrath SD, Hayden KE, Khaitovich P, Johnson ME, Eichler MY, McPherson JD, Zhao S, Paabo S et al (2005) Lineage-specific expansions of retroviral insertions within the genomes of African great apes but not humans and orangutans. PLoS Biol 3(4):e110
Zemans RL, Colgan SP, Downey GP (2009) Transepithelial migration of neutrophils: mechanisms and implications for acute lung injury. Am J Respir Cell Mol Biol 40(5):519–535
Zhou D, Han Y, Yang R (2006) Molecular and physiological insights into plague transmission, virulence and etiology. Microbes Infect 8(1):273–284
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media New York
About this chapter
Cite this chapter
Brinkworth, J.F., Pechenkina, K. (2013). Primates, Pathogens and Evolution: An Introduction. In: Brinkworth, J., Pechenkina, K. (eds) Primates, Pathogens, and Evolution. Developments in Primatology: Progress and Prospects. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7181-3_1
Download citation
DOI: https://doi.org/10.1007/978-1-4614-7181-3_1
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-7180-6
Online ISBN: 978-1-4614-7181-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)