Genetic diversity at the edge: comparative assessment of Y-chromosome and autosomal diversity in eastern chimpanzees (Pan troglodytes schweinfurthii) of Ugalla, Tanzania

Abstract

One of the three categories of biodiversity for conservation priority recommended by the International Union for the Conservation of Nature is genetic diversity. In this study, we estimate the genetic diversity of eastern chimpanzees in the Ugalla region of western Tanzania, which represents the easternmost distribution of the subspecies Pan troglodytes schweinfurthii. We collected 237 fecal samples from a 624 km2 area of the Ugalla region, analyzed the DNA at 12 autosomal loci and identified 113 individuals (69 males and 44 females). We also analyzed 13 Y-chromosome loci in the Ugalla males. While autosomal genetic diversity is within the range of other eastern populations, at 0.27 the gene diversity of the Y-chromosome haplotypes present among 61 Ugalla males is extremely low as compared to other eastern chimpanzee populations. In addition, the most prevalent haplotype, found in 52 of the males, is distributed across the entire surveyed area of 624 km2. This low level of paternally-transmitted genetic diversity among the Ugalla males may be the result of a small or highly related, recent founder population (i.e., genetic drift), exacerbated by the male philopatric structure of chimpanzee communities and by male reproductive skew.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Ancrenaz M, Gimenez O, Ambu L, Ancrenaz K, Andau P, Goossens B, Payne J, Sawang A, Tuuga A, Lackman-Ancrenaz I (2005) Aerial surveys give new estimates for Orangutans in Sabah, Malaysia. PLoS Biol 3(1):e3

    PubMed Central  PubMed  Article  Google Scholar 

  2. Arandjelovic M, Guschanski K, Schubert G, Harris TR, Thalmann O, Siedel H, Vigilant L (2009) Two-step multiplex PCR improves the speed and accuracy of genotyping using DNA from noninvansive and museum samples. Mol Ecol Res 9:28–36

    CAS  Article  Google Scholar 

  3. Arandjelovic M, Head J, Kühl H, Boesch C, Robbins MM, Maisels F, Vigilant L (2010) Effective non-invasive genetic monitoring of multiple wild western gorilla groups. Biol Conserv 143(7):1780–1791

    Google Scholar 

  4. Arnaud-Haond S, Teixeira S, Massa SI, Billot C, Saenger P, Coupland G, Duarte CM, Serrão A (2006) Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennie marina) populations. Mol Ecol 15:3515–3525

    CAS  PubMed  Article  Google Scholar 

  5. Becquet C, Patterson N, Stone AC, Przeworski M, Reich D (2007) Genetic structure of chimpanzee populations. PLoS Genet 3(4):0617–0626

    CAS  Article  Google Scholar 

  6. Bjork A, Liu W, Wertheim JO, Hahn BH, Worobey M (2011) Evolutionary history of chimpanzees inferred from complete mitochondrial genomes. Mol Biol Evol 28(1):615–623. doi:10.1093/molbev/msq227

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  7. Boesch C, Boesch-Achermann H (2000) The chimpanzees of the Taï forest. Oxford University Press, Oxford

    Google Scholar 

  8. Boesch C, Kohou G, Néné H, Vigilant L (2006) Male competition and paternity in wild chimpanzees of the Taï forest. Am J Phys Anthropol 130(1):103–115

    PubMed  Article  Google Scholar 

  9. Boesch C, Crockford C, Herbinger I, Wittig R, Moebius Y, Normand E (2008) Intergroup conflicts among chimpanzees in Taï National Park: lethal violence and the female perspective. Am J Primatol 70:1–14

    Google Scholar 

  10. Böhme MU, Schneeweiß N, Fritz U, Schlegel M, Berendonk TU (2007) Small edge populations at risk: genetic diversity of the green lizard (Lacerta viridis viridis) in Germany and implications for conservation management. Conserv Genet 8:555–563

    Article  Google Scholar 

  11. Bradley BJ, Boesch C, Vigilant L (2000) Identification and redesign of human microsatellite markers for genotyping wild chimpanzee (Pan troglodytes verus) and gorilla (Gorilla gorilla gorilla) DNA from faeces. Conserv Genet 1:289–292

    CAS  Article  Google Scholar 

  12. Bradley BJ, Chambers KE, Vigilant L (2001) Accurate DNA-based sex identification of apes using non-invasive samples. Conserv Genet 2:179–181

    CAS  Article  Google Scholar 

  13. Caldecott J, Miles L (2005) World atlas of great apes and their conservation. University of California Press/UNEP World Conservation Monitoring Centre, Berkeley

    Google Scholar 

  14. Campbell G, Kuehl H, N’Goran Kouame P, Boesch C (2008) Alarming decline of West African chimpanzees in Cote d’Ivoire. Curr Biol 18(19):R903–R904

    CAS  PubMed  Article  Google Scholar 

  15. Chancellor RL, Langergraber K, Ramirez S, Rundus AS, Vigilant L (2012) Genetic sampling of unhabituated chimpanzees (Pan troglodytes schweinfurthii) in Gishwati forest reserve, an isolated forest fragment in Western Rwanda. Int J Primatol 33:479–488

    Article  Google Scholar 

  16. Conklin-Brittain NL, Wrangham RW, Hunt KD (1998) Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance II. Macronutrients. Int J Primatol 19(6):971–998

    Article  Google Scholar 

  17. Constable JL, Ashley MV, Goodall J, Pusey AE (2001) Noninvasive paternity assignment in Gombe chimpanzees. Mol Ecol 10(5):1279–1300. doi:10.1046/j.1365-294X.2001.01262.x

    CAS  PubMed  Article  Google Scholar 

  18. Devos C, Sanz C, Morgan D, Onononga JR, Laporte N, Huynen MC (2008) Comparing ape densities and habitats in northern Congo: surveys of sympatric gorillas and chimpanzees in the Odzala and Ndoki regions. Am J Primatol 70(5):439–451

    PubMed  Article  Google Scholar 

  19. Diekmann OE, Serrão EA (2012) Range-edge genetic diversity: locally poor extant southern patches maintain a regionally diverse hotspot in the seagrass Zostera marina. Mol Ecol 21:1647–1657

    PubMed  Article  Google Scholar 

  20. Emery Thompson M, Newton-Fisher N, Reynolds V (2006) Probable community transfer of parous adult female chimpanzees in the Budongo Forest Uganda. Int J Primatol 27(6):1601–1617

    Article  Google Scholar 

  21. Eriksson J, Siedel H, Lukas D, Kayser M, Erler A, Hashimoto C, Hohmann G, Boesch C, Vigilant L (2006) Y-chromosome analysis confirms highly sex-biased dispersal and suggests a low male effective population size in bonobos (Pan paniscus). Mol Ecol 15(4):939–949. doi:10.1111/j.1365-294X.2006.02845.x

    CAS  PubMed  Article  Google Scholar 

  22. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  PubMed Central  Google Scholar 

  23. Fischer A, Pollack J, Thalmann O, Nickel B, Pääbo S (2006) Demographic history and genetic differentiation in apes. Curr Biol 16(11):1133–1138. doi:10.1016/j.cub.2006.04.033

    CAS  PubMed  Article  Google Scholar 

  24. Freeland JR (2005) Molecular ecology. Wiley, West Sussex

    Google Scholar 

  25. Gagneux P, Wills C, Gerloff U, Tautz D, Morin PA, Boesch C, Fruth B, Hohmann G, Ryder O, Woodruff DS (1999) Mitochondrial sequences show diverse evolutionary histories of African hominoids. PNAS 96:5077–5082

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  26. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    CAS  PubMed  Article  Google Scholar 

  27. GeoComm International Corp (2011) GIS data depot. <www.geocomm.com>. Downloaded on February 14, 2011

  28. Goldberg TL, Ruvolo M (1997) The geographic apportionment of mitochondrial genetic diversity in east African chimpanzees, Pan troglodytes schweinfurthii. Mol Biol Evol 14(9):976–984

    CAS  PubMed  Article  Google Scholar 

  29. Gonder MK, Locatelli S, Ghobrial L, Mitchell MW, Kujawski JT, Lankester FJ, Stewart C-B, Tishkoff SA (2011) Evidence from Cameroon reveals differences in the genetic structure and histories of chimpanzee populations. Proc Natl Acad Sci 108(12):4766–4771. doi:10.1073/pnas.1015422108

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  30. Goodall J (1986) The chimpanzees of Gombe. Harvard University Press, Cambridge

    Google Scholar 

  31. Hammond RL, Lawson Handley LJ, Winney BJ, Bruford MW, Perrin N (2006) Genetic evidence for female-biased dispersal and gene flow in a polygynous primate. Proc Royal Soc B 273(1585):479–484

    CAS  Article  Google Scholar 

  32. Hernandez-Aguilar RA (2006) Ecology and nesting patterns of chimpanzees (Pan troglodytes) in Issa (Ph.D. Thesis). University of Southern California. 219 pp

  33. Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans Royal Soc B 359:183–195

    CAS  Article  Google Scholar 

  34. Hey J (2010) The Divergence of chimpanzee species and subspecies as revealed in multipopulation isolation-with-migration analyses. Mol Biol Evol 27(4):921–933. doi:10.1093/molbev/msp298

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  35. Inoue E, Tashiro Y, Ogawa H, Inoue-Murayama M, Nishida T, Takenaka O (2013) Gene flow and genetic diversity of chimpanzees in Tanzanian habitats. Primate Conserv 26:67–74

    Article  Google Scholar 

  36. Isbell LA (1991) Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behav Ecol 2(2):143–155

    Article  Google Scholar 

  37. IUCN (2012) Red list of threatened species. Version 1012.2

  38. Johnson AE, Knott CD, Pamungkas B, Pasaribu M, Marshall AJ (2005) A survey of the orangutan (Pongo pygmaeus wurmbii) population in and around Gunung Palung National Park, West Kalimantan, Indonesia based on nest counts. Biol Conserv 121(4):495–507

    Article  Google Scholar 

  39. Junker J, Blake S, Boesch C, Campbell G, Du Toit L, Duvall C, Ekobo A, Etoga G, Galat-Luong A, Gamys J, Ganas-Swaray J, Gatti S, Ghiurghi A, Granier N, Hart J, Head J, Herbinger I, Hicks TC, Huijbregts B, Imong IS, Kuempel N, Lahm S, Lindsell J, Maisels F, McLennan M, Martinez L, Morgan B, Morgan D, Mulindahabi F, Mundry R, N’Goran KP, Normand E, Ntongho A, Okon DT, Petre C-A, Plumptre A, Rainey H, Regnaut S, Sanz C, Stokes E, Tondossama A, Tranquilli S, Sunderland-Groves J, Walsh P, Warren Y, Williamson EA, Kuehl HS (2012) Recent decline in suitable environmental conditions for African great apes. Divers Distrib 18(11):1077–1091. doi:10.1111/ddi.12005

    Article  Google Scholar 

  40. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Mol Ecol 16(5):1099–1106

    Google Scholar 

  41. Kano T (1972) Distribution and adaptation of the chimpanzees on the eastern shore of Lake Tanganyika. Kyoto Univ Afr Stud 7:37–129

    Google Scholar 

  42. Kormos R, Boesch C, Bakarr MI, Butynski TM (2003) Status survey and conservation action plan. IUCN/SSC Primate Specialist Group. IUCN, Cambridge

    Google Scholar 

  43. Langergraber KE, Siedel H, Mitani JC, Wrangham RW, Reynolds V, Hunt K, Vigilant L (2007) The genetic signature of sex-biased migration in patrilocal chimpanzees and humans. PLoS One 2:e973

    PubMed Central  PubMed  Article  Google Scholar 

  44. Langergraber KE, Boesch C, Inoue E, Inoue-Murayama M, Mitani JC, Nishida T, Pusey A, Reynolds V, Schubert G, Wrangham RW, Wroblewski E, Vigilant L (2011) Genetic and ‘cultural' similarity in wild chimpanzees. Proc Royal Soc B Biol Sci 278(1704):408–416

    Google Scholar 

  45. Langergraber K, Mitani J, Watts D, Vigilant L (2013) Male–female socio-spatial relationships and reproduction in wild chimpanzees. Behav Ecol Sociobiol 67(6):861–873. doi:10.1007/s00265-013-1509-6

    Article  Google Scholar 

  46. Lehmann J, Boesch C (2004) To fission or to fusion: effects of community size on wild chimpanzee (Pan troglodytes verus) social organisation. Behav Ecol Sociobiol 56(3):207–216

    Article  Google Scholar 

  47. Lesica P, Allendorf FW (1995) When are peripheral populations valuable for conservation? Soc Conserv Biol 9(4):753–760

    Article  Google Scholar 

  48. Lukas D, Reynolds V, Boesch C, Vigilant L (2005) To what extent does living in a group mean living with kin? Mol Ecol 14:2181–2196

    CAS  PubMed  Article  Google Scholar 

  49. Mann HB, Whitney DR (1947) On a test of whether one or two random variables is stochastically larger than the other. Ann Math Statist 18(1):50–60

    Article  Google Scholar 

  50. Matsumoto-Oda A (1999) Mahale chimpanzees: grouping patterns and cycling females. Am J Primatol 47:197–207

    CAS  PubMed  Article  Google Scholar 

  51. Moore JJ (1985) Chimpanzee survey in Mali, West Africa. Primate Conserv 6:59–63

    Google Scholar 

  52. Moore JJ (1994) Plants of the tongwe east reserve (Ugalla), Tanzania. Tropics 3:333–340

    Article  Google Scholar 

  53. Moore DL, Vigilant L (in press) A population estimate of chimpanzees (Pan troglodytes schweinfurthii) in the Ugalla region using standard and spatially explicit genetic capture-recapture methods. Am J Primatol

  54. Moyer D, Plumptre AJ, Pintea L, Hernandez-Aguilar A, Moore J, Stewart F, Davenport TRB, Piel A, Kamenya S, Mugabe H, Pmunga N, Mwangoka M (2006) Surveys of chimpanzees and other biodiversity in Western Tanzania. Unpublished Report to United States Fish and Wildlife Service

  55. Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70(12):3321–3323

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  56. Nei M (1977) F-statistics and analysis of gene diversity in subdivided populations. Ann Hum Genet 41:225–233

    CAS  PubMed  Article  Google Scholar 

  57. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed Central  PubMed  Google Scholar 

  58. Newton-Fisher NE, Emery Thompson M, Reynolds V, Boesch C, Vigilant L (2010) Paternity and social rank in wild chimpanzees (Pan troglodytes) from the Budongo Forest, Uganda. Am J Phys Anthropol 142:417–428

    PubMed  Article  Google Scholar 

  59. Nishida T (1968) The social group of wild chimpanzees in the Mahali Mountains. Primates 9(3):167–224

    Article  Google Scholar 

  60. Nishida T (1985) Group extinction and female transfer in wild chimpanzees in the Mahale National Park, Tanzania. Zeitschrift fur Teirpsychologie 67:284–301

    Article  Google Scholar 

  61. Nsubuga AM, Robbins MM, Roeder AD, Morin PA, Boesch C, Vigilant L (2004) Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method. Mol Ecol 13(7):2089–2094. doi:10.1111/j.1365-294X.2004.02207.x

    CAS  PubMed  Article  Google Scholar 

  62. Oates JF, Groves CP, Jenkins PD (2009) The type locality of Pan troglodytes vellerosus (Gray, 1862), and implications for the nomenclature of West African chimpanzees. Primates 50(1):78–80

    PubMed  Article  Google Scholar 

  63. Ogawa H, Idani G, Moore JJ, Pintea L, Hernandez A (2007) Sleeping parties and bed distribution of chimpanzees in the savanna woodland, Ugalla, Tanzania. Int J Primatol 28:1397–1412

    Article  Google Scholar 

  64. Piel AK, Stewart FA, Pintea L, Li Y, Ramirez MA, Loy DE, Crystal PA, Learn GH, Knapp LA, Sharp PM, Hahn BH (2013) The Malagarasi river does not form an absolute barrier to chimpanzee movement in Western Tanzania. PLoS One 8(3):e58965

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  65. Pintea L, Bauer ME, Bolstad PV, Pusey A (2002). Matching multiscale remote sensing data to interdisciplinary conservation needs: the case of chimpanzees in western Tanzania. In: Morain S, Budge A (eds), Pecora 15/Land Satellite Information IV/ISPRS Commission I/FIEOS 2002 Conference Proceedings: Integrated Remote Sensing at the Global, Regional and Local Scale

  66. Plumptre AJ, Rose R, Nangendo G, Williamson EA, Didier K, Hart J, Mulindahabi F, Hicks C, Griffin B, Ogawa H, Nixon S, Pintea L, Vosper A, McLennan MR, Amsini F, McNeilage A, Makana JR, Kanamori M, Hernandez A, Piel A, Stewart F, Moore J, Zamma K, Nakamura M, Kamenya S, Idani G, Sakamaki T, Yoshikawa M, Greer D, Tranquili S, Beyers R, Hashimoto C, Furuichi T, Bennet EL (2010) Eastern chimpanzee (Pan troglodytes schweinfurthii): status survey and conservation action plan 2010–2020. IUCN, Switzerland

    Google Scholar 

  67. Pruetz JD, Marchant LF, Arno J, McGrew WC (2002) Survey of savanna chimpanzees (Pan troglodytes verus) in Southeastern Sénégal. Am J Primatol 58(1):35–43

    CAS  PubMed  Article  Google Scholar 

  68. Pruetz JD, Fulton SJ, Marchant LF, McGrew WC, Schiel M, Waller M (2007) Arboreal nesting as anti-predator adaptation by savanna chimpanzees (Pan troglodytes verus) in southeastern Senegal. Am J Primatol 70:1–9

    Google Scholar 

  69. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17(1):230–237. doi:10.1046/j.1523-1739.2003.01236.x

    Article  Google Scholar 

  70. Rowe G, Beebee TJC, Burke T (1999) Microsatellite heterozygosity, fitness and demography in natterjack toads Bufo calamita. Anim Conserv 2:85–92

    Article  Google Scholar 

  71. Rudicell RS, Piel AK, Stewart F, Moore DL, Learn GH, Li Y, Takehisa J, Pintea L, Shaw GM, Moore J, Sharp PM, Hahn BH (2011) High prevalence of simian immunodeficiency virus infection in a community of savanna chimpanzees. J Virol 85(19):9918–9928

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  72. Schubert G, Stoneking CJ, Arandjelovic M, Boesch C, Eckhardt N, Hohmann G, Langergraber K, Lukas D, Vigilant L (2011) Male-mediated gene flow in patrilocal primates. PLoS One 6(7):e21514. doi:10.1371/journal.pone.0021514

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  73. Schwarz E (1934) On the local races of the chimpanzee. Ann Mag Nat Hist 1:576–583

    Article  Google Scholar 

  74. Segurel L, Martinez-Cruz B, Quintana-Murci L, Balaresque P, Georges M, Hegay T, Aldashev A, Nasyrova F, Jobling MA, Heyer E, Vitalis R (2008) Sex-specific genetic structure and social organization in central asia: insights form a multi-locus study. PLoS Genet 4(9):e1000200

    PubMed Central  PubMed  Article  Google Scholar 

  75. Sterck EHM, Watts DP, Van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309

    Article  Google Scholar 

  76. Stewart FA, Pruetz JD (2013) Do chimpanzee nests serve an anti-predatory function? Am J Primatol 75(6):593–604

    PubMed  Article  Google Scholar 

  77. Stone AC, Battistuzzi FU, Kubatko LS, Perry GH, Trudeau E, Lin H, Kumar S (2010) More reliable estimates of divergence times in Pan using complete mtDNA sequences and accounting for population structure. Philos Trans Royal Soc B 365:3277–3288

    CAS  Article  Google Scholar 

  78. Tutin C, McGrew W, Baldwin P (1983) Social organization of savanna-dwelling chimpanzees, Pan troglodytes verus, at Mt. Assirik, Senegal. Primates 24(2):154–173

    Article  Google Scholar 

  79. van Oven M, Hämmerle JM, van Schoor M, Kushnick G, Pennekamp P, Zega I, Lao O, Brown L, Kennerknecht I, Kayser M (2011) Unexpected island effects at an extreme: reduced Y Chromosome and mitochondrial DNA diversity in Nias. Mol Biol Evol 28(4):1349–1361. doi:10.1093/molbev/msq300

    PubMed  Article  Google Scholar 

  80. Vigilant L, Hofreiter M, Siedel H, Boesch C (2001) Paternity and relatedness in wild chimpanzee communities. PNAS 98(23):12890–12895. doi:10.1073/pnas.231320498

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  81. Walsh PD, Abernethy KA, Bermejo M, Beyers R, De Wachter P, Akou ME, Huijbregts B, Mambounga DI, Toham AK, Kilbourn AM, Lahm SA, latour S, Maisels F, Mbina C, Mihindou Y, Obiang SN, Effa ES, Starkey MP, Telfer P, Thibault M, Tutin CEG, White LJT, Wilkie DS (2003) Catastrophic ape decline in western equatorial Africa. Nature 201:1264–1266

    Google Scholar 

  82. Wang J (2004) Application of the one-migrant-per-generation rule to conservation and management. Conserv Biol 18(2):332–343

    Article  Google Scholar 

  83. Wegmann D, Excoffier L (2010) Bayesian inference of the demographic history of chimpanzees. Mol Biol Evol 27(6):1425–1435. doi:10.1093/molbev/msq028

    CAS  PubMed  Article  Google Scholar 

  84. Weir BS (1990) Genetic data analysis. Methods for discrete population genetic data. Sinauer Associates Inc, Sunderland

    Google Scholar 

  85. Wrangham R (1979) On the evolution of ape social systems. Soc Sci Inform 13(3):336–368

    Article  Google Scholar 

  86. Wright S (1949) The genetical structure of populations. Ann Eugen 15(1):323–354. doi:10.1111/j.1469-1809.1949.tb02451.x

    Article  Google Scholar 

  87. Wroblewski EE, Murray CM, Keele BF, Schumacher-Stankey JC, Hahn BH, Pusey AE (2009) Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii. Animal Behaviour 77(4):873–885

    PubMed Central  PubMed  Article  Google Scholar 

  88. Yu N, Jensen-Seaman MI, Chemnick L, Kidd JR, Deinard AS, Ryder O, Kidd KK, Li W-H (2003) Low nucleotide diversity in chimpanzees and bonobos. Genetics 164(4):1511–1518

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the Tanzania Wildlife Research Institute (TAWIRI) and the Tanzania Commission for Science and Technology (COSTECH) for permission to conduct the fieldwork for this study. We are very grateful to Mimi Arandjelovic for her extensive support and assistance throughout the laboratory work and analyses. Comments from Kevin Langergraber substantially improved the manuscript. We thank Fiona Stewart and Alex Piel, and the field assistants at Camp Issa for their invaluable assistance. The samples analyzed for this study could not have been collected without the assistance of Abdallah Moshi and Halufani Mulalelwa; their collaboration is greatly appreciated. We would also like to thank the reviewers of this manuscript, whose thoughtful comments improved this final version. This research was supported through funding by The Margot Marsh Biodiversity Foundation, The Leakey Foundation, The Wenner-Gren Foundation, the Max Planck Institute for Evolutionary Anthropology, the Lambda Alpha Anthropology Honor Society, and the Department of Anthropology at the University of Texas at San Antonio.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Deborah L. Moore.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Moore, D.L., Vigilant, L. Genetic diversity at the edge: comparative assessment of Y-chromosome and autosomal diversity in eastern chimpanzees (Pan troglodytes schweinfurthii) of Ugalla, Tanzania. Conserv Genet 15, 495–507 (2014). https://doi.org/10.1007/s10592-013-0556-x

Download citation

Keywords

  • Genetic diversity
  • Y-chromosome
  • Chimpanzees
  • Heterozygosity
  • Male philopatry