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Genomic Tools for Evolution and Conservation in the Chimpanzee: Is a Genetically Distinct Population


In spite of its evolutionary significance and conservation importance, the population structure of the common chimpanzee, Pan troglodytes, is still poorly understood. An issue of particular controversy is whether the proposed fourth subspecies of chimpanzee, Pan troglodytes ellioti, from parts of Nigeria and Cameroon, is genetically distinct. Although modern high-throughput SNP genotyping has had a major impact on our understanding of human population structure and demographic history, its application to ecological, demographic, or conservation questions in non-human species has been extremely limited. Here we apply these tools to chimpanzee population structure, using ∼700 autosomal SNPs derived from chimpanzee genomic data and a further ∼100 SNPs from targeted re-sequencing. We demonstrate conclusively the existence of P. t. ellioti as a genetically distinct subgroup. We show that there is clear differentiation between the verus, troglodytes, and ellioti populations at the SNP and haplotype level, on a scale that is greater than that separating continental human populations. Further, we show that only a small set of SNPs (10–20) is needed to successfully assign individuals to these populations. Tellingly, use of only mitochondrial DNA variation to classify individuals is erroneous in 4 of 54 cases, reinforcing the dangers of basing demographic inference on a single locus and implying that the demographic history of the species is more complicated than that suggested analyses based solely on mtDNA. In this study we demonstrate the feasibility of developing economical and robust tests of individual chimpanzee origin as well as in-depth studies of population structure. These findings have important implications for conservation strategies and our understanding of the evolution of chimpanzees. They also act as a proof-of-principle for the use of cheap high-throughput genomic methods for ecological questions.


Vyšlo v časopise: Genomic Tools for Evolution and Conservation in the Chimpanzee: Is a Genetically Distinct Population. PLoS Genet 8(3): e32767. doi:10.1371/journal.pgen.1002504
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002504

Souhrn

In spite of its evolutionary significance and conservation importance, the population structure of the common chimpanzee, Pan troglodytes, is still poorly understood. An issue of particular controversy is whether the proposed fourth subspecies of chimpanzee, Pan troglodytes ellioti, from parts of Nigeria and Cameroon, is genetically distinct. Although modern high-throughput SNP genotyping has had a major impact on our understanding of human population structure and demographic history, its application to ecological, demographic, or conservation questions in non-human species has been extremely limited. Here we apply these tools to chimpanzee population structure, using ∼700 autosomal SNPs derived from chimpanzee genomic data and a further ∼100 SNPs from targeted re-sequencing. We demonstrate conclusively the existence of P. t. ellioti as a genetically distinct subgroup. We show that there is clear differentiation between the verus, troglodytes, and ellioti populations at the SNP and haplotype level, on a scale that is greater than that separating continental human populations. Further, we show that only a small set of SNPs (10–20) is needed to successfully assign individuals to these populations. Tellingly, use of only mitochondrial DNA variation to classify individuals is erroneous in 4 of 54 cases, reinforcing the dangers of basing demographic inference on a single locus and implying that the demographic history of the species is more complicated than that suggested analyses based solely on mtDNA. In this study we demonstrate the feasibility of developing economical and robust tests of individual chimpanzee origin as well as in-depth studies of population structure. These findings have important implications for conservation strategies and our understanding of the evolution of chimpanzees. They also act as a proof-of-principle for the use of cheap high-throughput genomic methods for ecological questions.


Zdroje

1. OatesJFGrovesCPJenkinsPD 2009 The type locality of Pan troglodytes vellerosus (Gray, 1862), and implications for the nomenclature of West African chimpanzees. Primates 50 78 80

2. GonderMKOatesJFDisotellTRForstnerMRMoralesJC 1997 A new west African chimpanzee subspecies? Nature 388 337

3. GonderMKDisotellTROatesJF 2006 New genetic evidence on the evolution of chimpanzee populations and implications for taxonomy. Int J Primatol 27 1103 1127

4. GrovesCP 2001 Primate Taxonomy Washington DC Smithsonian Institution Press 350

5. GrubbPButynskiTOatesJFBearderSDisotellT 2003 Assessment of the diversity of African primates. Int J Primatol 24 1301 1357

6. GonderMKDisotellTR 2006 Contrasting phylogeographic histories of chimpanzees in Nigeria and Cameroon: A multilocus analysis. LehmanSFleagleJ Primate Biogeography New York Springer 129 161

7. BecquetCPattersonNStoneACPrzeworskiMReichD 2007 Genetic structure of chimpanzee populations. PLoS Genet 3 e66 doi:10.1371/journal.pgen.0030066

8. GonderMKLocatelliSGhobrialLMitchellMWKujawskiJT 2011 Evidence from Cameroon reveals differences in the genetic structure and histories of chimpanzee populations. Proc Natl Acad Sci U S A 108 4766 4771

9. PattenMAUnittPSheldonF 2002 Diagnosability versus mean differences of sage sparrow subspecies. The Auk 119 26 35

10. International HapMap Consortium 2005 A haplotype map of the human genome. Nature 437 1299 1320

11. KeinanAMullikinJCPattersonNReichD 2007 Measurement of the human allele frequency spectrum demonstrates greater genetic drift in East Asians than in Europeans. Nat Genet 39 1251 1255

12. LiJZAbsherDMTangHSouthwickAMCastoAM 2008 Worldwide human relationships inferred from genome-wide patterns of variation. Science 319 1100 1104

13. HennBMGignouxCRJobinMGrankaJMMacphersonJM 2011 Hunter-gatherer genomic diversity suggests a southern African origin for modern humans. Proc Natl Acad Sci U S A 108 5154 5162

14. KarlssonEKBaranowskaIWadeCMSalmon HillbertzNHCZodyMC 2007 Efficient mapping of Mendelian traits in dogs through genome-wide association. Nat Genet 39 1321 1328

15. WillingEVABentzenPvan OosterhoutCHoffmannMCableJ 2010 Genome wide single nucleotide polymorphisms reveal population history and adaptive divergence in wild guppies. Mol Ecol 19 968 984

16. Chimpanzee Sequencing and Analysis Consortium 2005 Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437 69 87

17. MyersSBowdenRTumianABontropREFreemanC 2010 Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327 876 879

18. PritchardJKStephensMDonnellyP 2000 Inference of population structure using multilocus genotype data. Genetics 155 945 959

19. FalushDStephensMPritchardJK 2003 Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164 1567 1587

20. MacfieTSNerrienetEde GrootNGBontropREMundyNI 2009 Patterns of diversity in HIV-related loci among subspecies of chimpanzee: concordance at CCR5 and differences at CXCR4 and CX3CR1. Mol Biol Evol 26 719 727

21. FischerAPollackJThalmannONickelBPaaboS 2006 Demographic history and genetic differentiation in apes. Curr Biol 16 1133 1138

22. ConradDFJakobssonMCoopGWenXWallJD 2006 A worldwide survey of haplotype variation and linkage disequilibrium in the human genome. Nat Genet 38 1251 1260

23. HellenthalGAutonAFalushD 2008 Inferring human colonization history using a copying model. PLoS Genet 4 e1000078 doi:10.1371/journal.pgen.1000078

24. PinhoCHeyJ 2010 Divergence with gene flow: Models and data. Annu Rev Ecol Evol Syst 41 215 230

25. LiNStephensM 2003 Modeling linkage disequilibrium and identifying recombination hotspots using single-nucleotide polymorphism data. Genetics 165 2213 2233

26. LawsonDJHellenthalGMyersSFalushD 2012 Inference of population structure using dense haplotype data. PLoS Genet 8 e1002453 doi:10.1371/journal.pgen.1002453

27. AltshulerDMGibbsRAPeltonenLSchaffnerSFYuF 2010 Integrating common and rare genetic variation in diverse human populations. Nature 467 52 58

28. CaswellJLMallickSRichterDJNeubauerJSchirmerC 2008 Analysis of chimpanzee history based on genome sequence alignments. PLoS Genet 4 e1000057 doi:10.1371/journal.pgen.1000057

29. HeyJ 2010 The divergence of chimpanzee species and subspecies as revealed in multipopulation isolation-with-migration analyses. Mol Biol Evol 27 921 933

30. WegmannDExcoffierL 2010 Bayesian inference of the demographic history of chimpanzees. Mol Biol Evol 27 1425

31. BjorkALiuWWertheimJOHahnBHWorobeyM 2011 Evolutionary history of chimpanzees inferred from complete mitochondrial genomes. Mol Biol Evol 28 615 623

32. StoneACBattistuzziFUKubatkoLSPerryGHJrTrudeauE 2010 More reliable estimates of divergence times in Pan using complete mtDNA sequences and accounting for population structure. Philos Trans R Soc Lond B Biol Sci 365 3277 3288

33. KormosRBoeschC 2003 Regional action plan for the conservation of chimpanzees in West Africa Washington DC Conservation International

34. OatesJFTutinCEGHumleTWilsonMLBaillieJEM 2008 Pan troglodytes. IUCN 2008 2008 IUCN Red List of Threatened Species

35. ExcoffierLLavalGSchneiderS 2005 Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1 47 50

36. R Development Core Team 2007 R: A language and environment for statistical computing Vienna R Foundation for Statistical Computing, Vienna, Austria

37. StephensMSmithNJDonnellyP 2001 A new statistical method for haplotype reconstruction from population data. Am J Hu Genet 68 978 989

38. StephensMScheetP 2005 Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Hum Genet 76 449 462

39. CrawfordDCBhangaleTLiNHellenthalGRiederMJ 2004 Evidence for substantial fine-scale variation in recombination rates across the human genome. Nat Genet 36 700 706

40. HellenthalGAutonAFalushD 2008 Inferring human colonization history using a copying model. PLoS Genet 4 e1000078 doi:10.1371/journal.pgen.1000078

41. HudsonRRSlatkinMMaddisonWP 1992 Estimation of levels of gene flow from DNA sequence data. Genetics 132 583

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