Abstract
The spectacular progress in genomics increasingly highlights the importance of comparative biology in biomedical research. In particular, nonhuman primates, as model systems, provide a crucial intermediate between humans and mice. The close similarities between humans and other primates are stimulating primate studies in virtually every area of biomedical research, including development, anatomy, physiology, immunology, and behavior. The vervet monkey (Chlorocebus aethiops sabaeus) is an important model for studying human diseases and complex traits, especially behavior. We have developed a vervet genetic linkage map to enable mapping complex traits in this model organism and facilitate comparative genomic analysis between vervet and other primates. Here we report construction of an initial genetic map built with about 360 human orthologous short tandem repeats (STRs) that were genotyped in 434 members of an extended vervet pedigree. The map includes 226 markers mapped in a unique order with a resolution of 9.8 Kosambi centimorgans (cM) in the vervet monkey genome, and with a total length (including all 360 markers) of 2726 cM. At least one complex and 11 simple rearrangements in marker order distinguish vervet chromosomes from human homologs. While inversions and insertions can explain a similar number of changes in marker order between vervet and rhesus homologs, mostly inversions are observed when vervet chromosome organization is compared to that in human and chimpanzee. Our results support the notion that large inversions played a less prominent role in the evolution within the group of the Old World monkeys compared to the human and chimpanzee lineages.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bailey JN, Breidenthal SE, Jorgensen MJ, McCracken JT, Fairbanks LA (2007) The association of DRD4 and novelty seeking is found in a nonhuman primate model. Psychiatr Genet 17(1):23–27
Boles JW, Pitt ML, LeClaire RD, Gibbs PH, Torres E, et al. (2003) Generation of protective immunity by inactivated recombinant staphylococcal enterotoxin B vaccine in nonhuman primates and identification of correlates of immunity. Clin Immunol 108(1):51–59
Boehnke M (1991) Allele frequency estimation from data on relatives. Am J Hum Genet 48(1):22–25
Broman KW, Murray JC, Sheffield VC, White RL, Weber JL (1998) Comprehensive human genetic maps: individual and sex-specific variation in recombination. Am J Hum Genet 63(3):861–869
Broussard SR, Staprans SI, White R, Whitehead EM, Feinberg MB, et al. (2001) Simian immunodeficiency virus replicates to high levels in naturally infected African green monkeys without inducing immunologic or neurologic disease. J Virol 75(5):2262–2275
Cox LA, Mahaney MC, Vandeberg JL, Rogers J (2006) A second-generation genetic linkage map of the baboon (Papio hamadryas) genome. Genomics 88(3):274–281
Dutrillaux B (1979) Chromosomal evolution in primates: tentative phylogeny from Microcebus murinus (Prosimian) to man. Hum Genet 48:251–314
Ellegren H, Primmer CR, Sheldon BC (1995) Microsatellite ‘evolution’: directionality or bias? Nat Genet 11(4):360–362
Elsworth JD, Deutch AY, Redmond DE Jr, Taylor JR, Sladek JR Jr, et al. (1989) Symptomatic and asymptomatic 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated primates: biochemical changes in striatal regions. Neuroscience 33(2):323–331
Fairbanks LA (2001) Individual differences in response to a stranger: social impulsivity as a dimension of temperament in vervet monkeys (Cercopithecus aethiops sabaeus). J Comp Psychol 115(1):22–28
Fairbanks LA, McGuire MT (1988) Long-term effects of early mothering behavior on responsiveness to the environment in vervet monkeys. Dev Psychobiol 21(7):711–724
Fairbanks LA, Fontenot MB, Phillips-Conroy JE, Jolly CJ, Kaplan JR, et al. (1999) CSF monoamines, age and impulsivity in wild grivet monkeys (Cercopithecus aethiops aethiops). Brain Behav Evol 53(5–6):305–312
Fairbanks LA, Melega WP, Jorgensen MJ, Kaplan JR, McGuire MT (2001) Social impulsivity inversely associated with CSF 5-HIAA and fluoxetine exposure in vervet monkeys. Neuropsychopharmacology 24(4):370–378
Fairbanks LA, Jorgensen MJ, Huff A, Blau K, Hung YY, et al. (2004) Adolescent impulsivity predicts adult dominance attainment in male vervet monkeys. Am J Primatol 64(1):1–17
Falk CT (1989) A simple scheme for preliminary ordering of multiple loci: application to 45 CF families. Prog Clin Biol Res 329:17–22
Finelli P, Stanyon R, Plesker R, Ferguson-Smith MA, O’Brien PC, et al. (1999) Reciprocal chromosome painting shows that the great difference in diploid number between human and African green monkey is mostly due to non-Robertsonian fissions. Mamm Genome 10(7):713–718
Goldstein S, Ourmanov I, Brown CR, Beer BE, Elkins WR, et al. (2000) Wide range of viral load in healthy African green monkeys naturally infected with simian immunodeficiency virus. J Virol 74(24):11744–11753
Goldstein S, Brown CR, Ourmanov I, Pandrea I, Buckler-White A, et al. (2006) Comparison of simian immunodeficiency virus SIVagmVer replication and CD4+ T-cell dynamics in vervet and sabaeus African green monkeys. J Virol 80(10):4868–4877
Gray WL, Mullis L, Soike KF (2002) Viral gene expression during acute simian varicella virus infection. J Gen Virol 83(Pt 4):841–846
Harvey DC, Lacan G, Melegan WP (2000) Regional heterogeneity of dopaminergic deficits in vervet monkey striatum and substantia nigra after methamphetamine exposure. Exp Brain Res 133(3):349–358
Hinrichs AS, Karolchik D, Baertsch R, Barber GP, Bejerano G, et al. (2006) The UCSC Genome Browser Database: update 2006. Nucleic Acids Res 34(Database issue):D590–D598
Hirsch VM, Dapolito G, Johnson PR, Elkins WR, London WT, et al. (1995) Induction of AIDS by simian immunodeficiency virus from an African green monkey: species-specific variation in pathogenicity correlates with the extent of in vivo replication. J Virol 69(2):955–967
Jentsch JD, Taylor JR, Elsworth JD, Redmond DE Jr, Roth RH (1999) Altered frontal cortical dopaminergic transmission in monkeys after subchronic phencyclidine exposure: involvement in frontostriatal cognitive deficits. Neuroscience 90(3):823–832
Joy A, Vogelnest L, Middleton DJ, Dale CJ, Campagna D, et al. (2001) Simian immunodeficiency virus infections in vervet monkeys (Clorocebus aethiops) at an Australian zoo. Aust Vet J 79(6):406–408
Kavanagh K, Fairbanks L, Bailey JN, Wilson M, et al. (2007) Characterization and heritability of obesity and associated risk factors in vervet monkeys. Obesity Res (in press)
Kehrer-Sawatzki H, Sandig C, Chuzhanova N, Goidts V, Szamalek JM, et al. (2005) Breakpoint analysis of the pericentric inversion distinguishing human chromosome 4 from the homologous chromosome in the chimpanzee (Pan troglodytes). Hum Mutat 25(1):45–55
Kong X, Murphy K, Raj T, He C, White PS, et al. (2004) A combined linkage-physical map of the human genome. Am J Hum Genet 75(6):1143–1148
Lange K, Cantor R, Horvath S, Perola M, Sabatti C, et al. (2001) Mendel version 4.0: A complete package for the exact genetic analysis of discrete traits in pedigree and population data sets. Am J Hum Genet 69:A1886
Lemere CA, Beierschmitt A, Iglesias M, Spooner ET, Bloom JK, et al. (2004) Alzheimer’s disease abeta vaccine reduces central nervous system abeta levels in a non-human primate, the Caribbean vervet. Am J Pathol 165(1):283–297
Marzella R, Viggiano L, Miolla V, Storlazzi CT, Ricco A, Gentile E, Roberto R, Surace C, Fratello A, Mancini M, Archidiacono N, Rocchi M (2000) Molecular cytogenetic resources for chromosome 4 and comparative analysis of phylogenetic chromosome IV in great apes. Genomics 63:307–313
Matise TC, Perlin M, Chakravarti A (1994) Automated construction of genetic linkage maps using an expert system (MultiMap): a human genome linkage map. Nat Genet 6(4):384–390
Mukhopadhyay N, Almasy L, Schroeder M, Mulvihill WP, Weeks DE (2005) Mega2: data-handling for facilitating genetic linkage and association analyses. Bioinformatics 21(10):2556–2557
Muller S, Stanyon R, Finelli P, Archidiacono N, Wienberg J (2000) Molecular cytogenetic dissection of human chromosomes 3 and 21 evolution. Proc Natl Acad Sci U S A 97(1):206–211
Muller S, Finelli P, Neusser M, Wienberg J (2004) The evolutionary history of human chromosome 7. Genomics 84(3):458–467
Murphy WJ, Agarwala R, Schaffer AA, Stephens R, Smith C Jr, et al. (2005) A rhesus macaque radiation hybrid map and comparative analysis with the human genome. Genomics 86(4):383–395
O’Connell JR, Weeks DE (1998) PedCheck: a program for identification of genotype incompatibilities in linkage analysis. Am J Hum Genet 63(1):259–266
Olobo JO, Gicheru MM, Anjili CO (2001) The African Green Monkey model for cutaneous and visceral leishmaniasis. Trends Parasitol 17(12):588–592
Palmour RM, Ervin FR, Baker GB, Young SN (1998) An amino acid mixture deficient in phenylalanine and tyrosine reduces cerebrospinal fluid catecholamine metabolites and alcohol consumption in vervet monkeys. Psychopharmacology (Berl) 136(1):1–7
Raz A, Frechter-Mazar V, Feingold A, Abeles M, Vaadia E, et al. (2001) Activity of pallidal and striatal tonically active neurons is correlated in mptp-treated monkeys but not in normal monkeys. J Neurosci 21(3):RC128
Rogers J, Mahaney MC, Witte SM, Nair S, Newman D, et al. (2000) A genetic linkage map of the baboon (Papio hamadryas) genome based on human microsatellite polymorphisms. Genomics 67(3):237–247
Rogers J, Garcia R, Shelledy W, Kaplan J, Arya A, et al. (2006) An initial genetic linkage map of the rhesus macaque (Macaca mulatta) genome using human microsatellite loci. Genomics 87(1):30–38
Rudel LL, Haines J, Sawyer JK, Shah R, Wilson MS, et al. (1997) Hepatic origin of cholesteryl oleate in coronary artery atherosclerosis in African green monkeys. Enrichment by dietary monounsaturated fat. J Clin Invest 100(1):74–83
Szamalek JM, Goidts V, Chuzhanova N, Hameister H, Cooper DN, et al. (2005) Molecular characterisation of the pericentric inversion that distinguishes human chromosome 5 from the homologous chimpanzee chromosome. Hum Genet 117(2–3):168–176
Taylor JR, Elsworth JD, Roth RH, Sladek JR Jr, Redmond DE Jr (1997) Severe long-term 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced parkinsonism in the vervet monkey (Cercopithecus aethiops sabaeus). Neuroscience 81(3):745–755
Traina-Dorge V, Blanchard J, Martin L, Murphey-Corb M (1992) Immunodeficiency and lymphoproliferative disease in an African green monkey dually infected with SIV and STLV-I. AIDS Res Hum Retroviruses 8(1):97–100
van Jaarsveld PJ, Smuts CM, Benade AS (2002) Effect of palm olein oil in a moderate-fat diet on plasma lipoprotein profile and aortic atherosclerosis in non-human primates. Asia Pac J Clin Nutr 11 Suppl 7:S424–S432
Ventura M, Weigl S, Carbone L, Cardone MF, Misceo D, et al. (2004) Recurrent sites for new centromere seeding. Genome Res 14(9):1696–1703
Yunis JJ, Prakash O (1982) The origin of man: a chromosomal pictorial legacy. Science 215(4539):1525–1530
Acknowledgments
The authors thank Dr. Stephen Sawcer (Genetic Analysis of Multiple Sclerosis in Europeans Initiative, Cambridge, UK) for providing fluorescently labeled human markers and Maricel Almonte and Harpreet Sandhu for their contribution in genotyping. This work was supported by NIH grant R01 RR016300 (NBF) and funding from Genome Canada and Genome Québec (KD). The Center for Primate Neuroethology, which supplied the pedigree samples, was supported by NIH grants MH061852 and RR019963 (LAF).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jasinska, A.J., Service, S., Levinson, M. et al. A genetic linkage map of the vervet monkey (Chlorocebus aethiops sabaeus). Mamm Genome 18, 347–360 (2007). https://doi.org/10.1007/s00335-007-9026-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00335-007-9026-4