A genetic linkage map of the vervet monkey (Chlorocebus aethiops sabaeus)

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.

[1]  P. Johnson,et al.  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 , 1995, Journal of virology.

[2]  L. Fairbanks,et al.  Long-term effects of early mothering behavior on responsiveness to the environment in vervet monkeys. , 1988, Developmental psychobiology.

[3]  J. Wienberg,et al.  Reciprocal chromosome painting shows that the great difference in diploid number between human and African green monkey is mostly due to non-Robertsonian fissions , 1999, Mammalian Genome.

[4]  S. Müller,et al.  The evolutionary history of human chromosome , 2004 .

[5]  J John Mann,et al.  Adolescent impulsivity predicts adult dominance attainment in male vervet monkeys , 2004, American journal of primatology.

[6]  J. McCracken,et al.  The association of DRD4 and novelty seeking is found in a nonhuman primate model , 2007, Psychiatric genetics.

[7]  C. Smuts,et al.  Effect of palm olein oil in a moderate-fat diet on plasma lipoprotein profile and aortic atherosclerosis in non-human primates. , 2002, Asia Pacific journal of clinical nutrition.

[8]  J. Mann,et al.  CSF Monoamines, Age and Impulsivity in Wild Grivet Monkeys (Cercopithecus aethiops aethiops) , 1999, Brain, Behavior and Evolution.

[9]  B. Dutrillaux Chromosomal evolution in Primates: Tentative phylogeny from Microcebus murinus (Prosimian) to man , 1979, Human Genetics.

[10]  J. Rogers,et al.  A genetic linkage map of the baboon (Papio hamadryas) genome based on human microsatellite polymorphisms. , 2000, Genomics.

[11]  S. Staprans,et al.  Simian Immunodeficiency Virus Replicates to High Levels in Naturally Infected African Green Monkeys without Inducing Immunologic or Neurologic Disease , 2001, Journal of Virology.

[12]  J C Murray,et al.  Pediatrics and , 1998 .

[13]  J. Rogers,et al.  A second-generation genetic linkage map of the baboon (Papio hamadryas) genome. , 2006, Genomics.

[14]  Jeffrey Rogers,et al.  An initial genetic linkage map of the rhesus macaque (Macaca mulatta) genome using human microsatellite loci. , 2006, Genomics.

[15]  J. Sawyer,et al.  Hepatic origin of cholesteryl oleate in coronary artery atherosclerosis in African green monkeys. Enrichment by dietary monounsaturated fat. , 1997, The Journal of clinical investigation.

[16]  J R O'Connell,et al.  PedCheck: a program for identification of genotype incompatibilities in linkage analysis. , 1998, American journal of human genetics.

[17]  N. Archidiacono,et al.  Molecular cytogenetic dissection of human chromosomes 3 and 21 evolution. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[18]  L. Fairbanks,et al.  Characterization and Heritability of Obesity and Associated Risk Factors in Vervet Monkeys , 2007, Obesity.

[19]  David Haussler,et al.  The UCSC genome browser database: update 2007 , 2006, Nucleic Acids Res..

[20]  T. Matise,et al.  A combined linkage-physical map of the human genome. , 2004, American journal of human genetics.

[21]  J. Yunis,et al.  The origin of man: a chromosomal pictorial legacy. , 1982, Science.

[22]  J. Olobo,et al.  The African Green Monkey model for cutaneous and visceral leishmaniasis. , 2001, Trends in parasitology.

[23]  William P. Melega,et al.  Social Impulsivity Inversely Associated with CSF 5-HIAA and Fluoxetine Exposure in Vervet Monkeys , 2001, Neuropsychopharmacology.

[24]  W. Melega,et al.  Regional heterogeneity of dopaminergic deficits in vervet monkey striatum and substantia nigra after methamphetamine exposure , 2000, Experimental Brain Research.

[25]  R. Roth,et al.  Altered frontal cortical dopaminergic transmission in monkeys after subchronic phencyclidine exposure: involvement in frontostriatal cognitive deficits , 1999, Neuroscience.

[26]  Aravinda Chakravarti,et al.  Automated construction of genetic linkage maps using an expert system (MultiMap): a human genome linkage map , 1994, Nature Genetics.

[27]  Daniel E. Weeks,et al.  Mega2: data-handling for facilitating genetic linkage and association analyses , 2005, Bioinform..

[28]  Terrence S. Furey,et al.  The UCSC Genome Browser Database: update 2006 , 2005, Nucleic Acids Res..

[29]  J. Schmitz,et al.  Comparison of Simian Immunodeficiency Virus SIVagmVer Replication and CD4+ T-Cell Dynamics in Vervet and Sabaeus African Green Monkeys , 2006, Journal of Virology.

[30]  Charles R. Brown,et al.  Wide Range of Viral Load in Healthy African Green Monkeys Naturally Infected with Simian Immunodeficiency Virus , 2000, Journal of Virology.

[31]  J. Blanchard,et al.  Immunodeficiency and lymphoproliferative disease in an African green monkey dually infected with SIV and STLV-I. , 1992, AIDS research and human retroviruses.

[32]  Richa Agarwala,et al.  A rhesus macaque radiation hybrid map and comparative analysis with the human genome. , 2005, Genomics.

[33]  Falk Ct,et al.  A simple scheme for preliminary ordering of multiple loci: application to 45 CF families. , 1989 .

[34]  K. Soike,et al.  Viral gene expression during acute simian varicella virus infection. , 2002, The Journal of general virology.

[35]  M. Mancini,et al.  Molecular cytogenetic resources for chromosome 4 and comparative analysis of phylogenetic chromosome IV in great apes. , 2000, Genomics.

[36]  S. Bavari,et al.  Generation of protective immunity by inactivated recombinant staphylococcal enterotoxin B vaccine in nonhuman primates and identification of correlates of immunity. , 2003, Clinical immunology.

[37]  E. Eichler,et al.  Recurrent sites for new centromere seeding. , 2004, Genome research.

[38]  D. Purcell,et al.  Simian immunodeficiency virus infections in vervet monkeys (Clorocebus aethiops) at an Australian zoo. , 2001, Australian veterinary journal.

[39]  Matthias Platzer,et al.  Breakpoint analysis of the pericentric inversion distinguishing human chromosome 4 from the homologous chromosome in the chimpanzee (Pan troglodytes) , 2005, Human mutation.

[40]  R. Palmour,et al.  An amino acid mixture deficient in phenylalanine and tyrosine reduces cerebrospinal fluid catecholamine metabolites and alcohol consumption in vervet monkeys , 1998, Psychopharmacology.

[41]  D. Cooper,et al.  Molecular characterisation of the pericentric inversion that distinguishes human chromosome 5 from the homologous chimpanzee chromosome , 2005, Human Genetics.

[42]  M. Boehnke,et al.  Allele frequency estimation from data on relatives. , 1991, American journal of human genetics.

[43]  R. Roth,et al.  Severe long-term 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced parkinsonism in the vervet monkey (Cercopithecus aethiops sabaeus) , 1997, Neuroscience.

[44]  R. Roth,et al.  Symptomatic and asymptomatic 1 -methyl-4-phenyl-1,2,3,6-tetrahydropyridinetreated primates: Biochemical changes in striatal regions , 1989, Neuroscience.

[45]  Frank R. Ervin,et al.  Alzheimer's Disease Aβ Vaccine Reduces Central Nervous System Aβ Levels in a Non-Human Primate, the Caribbean Vervet , 2004 .

[46]  D. Selkoe,et al.  Alzheimer's disease abeta vaccine reduces central nervous system abeta levels in a non-human primate, the Caribbean vervet. , 2004, The American journal of pathology.

[47]  J. Wienberg,et al.  The evolutionary history of human chromosome 7. , 2004, Genomics.

[48]  L. Fairbanks Individual differences in response to a stranger: social impulsivity as a dimension of temperament in vervet monkeys (Cercopithecus aethiops sabaeus). , 2001, Journal of comparative psychology.

[49]  C T Falk,et al.  A simple scheme for preliminary ordering of multiple loci: application to 45 CF families. , 1989, Progress in clinical and biological research.

[50]  M Abeles,et al.  Activity of Pallidal and Striatal Tonically Active Neurons Is Correlated in MPTP-Treated Monkeys But Not in Normal Monkeys , 2001, The Journal of Neuroscience.

[51]  H. Ellegren,et al.  Microsatellite ‘evolution’: directionality or bias? , 1995, Nature Genetics.