The sampling scheme matters: Pan troglodytes troglodytes and P. t schweinfurthii are characterized by clinal genetic variation rather than a strong subspecies break

American Journal of Physical Anthropology

Volumn 156, Issue 2, 2015, Pages 181-191

  Fünfstück, Tillmann ^a   Arandjelovic, Mimi ^a   Morgan, David B ^b   Sanz, Crickette ^c   Reed, Patricia ^b   Olson, Sarah H ^b   Cameron, Ken ^b   Ondzie, Alain ^d   Peeters, Martine ^e   Vigilant, Linda ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b WILDLIFE CONSERVATION SOCIETY   (United States)

^c WASHINGTON UNIVERSITY   (United States)

^d WILDLIFE CONSERVATION SOCIETY   (Congo)

^e UNIVERSITÉ DE MONTPELLIER   (France)

Author keywords

Genetic differentiation; Genotyping; Isolation by distance; Microsatellites; Structure

Indexed keywords

AFRICA; ARTICLE; CHIMPANZEE; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHIC DISTRIBUTION; NONHUMAN; PAN TROGLODYTES; POPULATION STRUCTURE; SPECIES IDENTIFICATION; TAXONOMY; ANIMALS; ANTHROPOLOGY, PHYSICAL; CLASSIFICATION; EVOLUTION, MOLECULAR; FEMALE; GENETIC VARIATION; GENETICS; GENETICS, POPULATION; GENOTYPING TECHNIQUES; MALE; SPECIES SPECIFICITY;

MICROSATELLITE REPEATS;

ANIMALS; ANTHROPOLOGY, PHYSICAL; EVOLUTION, MOLECULAR; FEMALE; GENETIC VARIATION; GENETICS, POPULATION; GENOTYPE; GENOTYPING TECHNIQUES; MALE; MICROSATELLITE REPEATS; PAN TROGLODYTES; SPECIES SPECIFICITY;

EID: 84920774331     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.22638     Document Type: Article

References (66)

1. Arandjelovic M, Guschanski K, Schubert G., Harris TR, Thalmann O, Siedel H, Vigilant L. 2009. Two-step multiplex polymerase chain reaction improves the speed and accuracy of genotyping using DNA from noninvasive and museum samples. Mol Ecol Resour 9:28-36.
2. 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 Con-serv 143:1780-1791.
3. Arandjelovic M, Head J, Rabanal L.I., Schubert G., Mettke E, Boesch C, Robbins M.M., Vigilant L. 2011. Non-invasive genetic monitoring of wild central chimpanzees. PLoS ONE 6: e14761.
4. Avise JC. 1996. Introduction: the scope of conservation genetics. In: Avise JC, Hamrick J, editors. Conservation genetics: case histories from nature. New York: Chapman & Hall. p 1-9.
5. Balcomb SR, Chapman CA. 2003. Bridging the gap: influence of seed deposition on seedling recruitment in a primate-tree interaction. Ecol Monogr 73:625-642.
6. Becquet C, Patterson N, Stone A.C., Przeworski M., Reich D. 2007. Genetic structure of chimpanzee populations. PLoS Genet 3:e66.
7. Bjork A, Liu W, Wertheim J.O., Hahn BH, Worobey M. 2010. Evolutionary history of chimpanzees inferred from complete mitochondrial genomes. Mol Biol Evol 28:615-623.
8. Boesch C, Head J, Tagg N., Arandjelovic M, Vigilant L, Robbins MM. 2007. Fatal chimpanzee attack in Loango National Park, Gabon. Int J Primatol 28:1025-1034.
9. Bowden R, MacFie TS, Myers S, Hellenthal G., Nerrienet E, Bontrop RE, Freeman C, Donnelly P., Mundy NI. 2012. Genomic tools for evolution and conservation in the chimpanzee: Pan troglodytes ellioti is a genetically distinct population. PLoS Genet 8:e1002504.
10. Bradley BJ, Chambers KE, Vigilant L. 2001. Accurate DNA-based sex identification of apes using non-invasive samples. Conserv Genet 2:179-181.
11. Cavalli-Sforza LL, Menozzi P, Piazza A. 1994. The history and geography of human genes. Princeton, NJ: Princeton University Press.
12. Earl DA, vonHoldt BM. 2011. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359-361.
13. Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611-2620.
14. Excoffier L, Lischer HEL. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564-567.
15. Fischer A, Pollack J, Thalmann O., Nickel B, Paabo S. 2006. Demographic history and genetic differentiation in apes. Curr Biol 16:1133-1138.
16. Fischer A, Prufer K, Good J.M., Halbwax M., Wiebe V, André C, Atencia R, Mugisha L, Ptak SE, Paabo S. 2011. Bonobos fall within the genomic variation of chimpanzees. PloS One 6: e21605.
17. Frantz AC, Cellina S, Krier A., Schley L, Burke T 2009. Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? J Appl Ecol 46:493-505.
18. Funfstuck T, Arandjelovic M, Morgan D.B., Sanz C., Breuer T, Stokes EJ, Reed P, Olson S.H., Cameron K., Ondzie A, Peeters M, Kuhl HS, Cipolletta C, Todd A, Masi S, Doran-Sheehy DM, Bradley BJ, Vigilant L. 2014. The genetic population structure of wild western lowland gorillas (Gorilla gorilla gorilla) living in continuous rain forest. Am J Primatol 76: 868-878.
19. Gagneux P, Gonder MK, Goldberg T.L., Morin PA. 2001. Gene flow in wild chimpanzee populations: what genetic data tell us about chimpanzee movement over space and time. Philos Trans R Soc B Biol Sci 356:889-897.
20. Gagneux P, Wills C, Gerloff U., Tautz D, Morin PA, Boesch C, Fruth B., Hohmann G, Ryder OA, Woodruff DS. 1999. Mitochondrial sequences show diverse evolutionary histories of African hominoids. Proc Natl Acad Sci 96:5077-5082.
21. Gonder MK, Disotell TR, Oates JF. 2006. New genetic evidence on the evolution of chimpanzee populations and implications for taxonomy. Int J Primatol 27:1103-1127.
22. Gonder MK, Locatelli S, Ghobrial L., Mitchell MW, Kujawski JT, Lankester FJ, Stewart C-B, Tishkoff SA. 2011. From the Cover: evidence from Cameroon reveals differences in the genetic structure and histories of chimpanzee populations. Proc Natl Acad Sci 108:4766-4771.
23. Gonder MK, Oates JF, Disotell T.R., Forstner MR., Morales JC, Melnick DJ. 1997. A new West African chimpanzee subspecies? Nature 388:337.
24. Groves C. 2001. Primate taxonomy. Washington, DC: Smithsonian Institution Press.
25. Guo SW, Thompson EA. 1992. Performing exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361-372.
26. Guy F, Brunet M, Schmittbuhl M., Viriot L. 2003. New approaches in hominoid taxonomy: morphometrics. Am J Phys Anthropol 121:198-218.
27. Hicks TC, Darby L, Hart J., Swinkels J, January N, Menken S. 2010. Trade in orphans and bushmeat threatens one of the Democratic Republic of the Congo's most important populations of eastern chimpanzees (Pan troglodytes schweinfurthii). Afr Primates 7:1-18.
28. Hicks TC, Tranquilli S, Kuehl H., Campbell G, Swinkels J, Darby L., Boesch C, Hart J, Menken SBJ. 2014. Absence of evidence is not evidence of absence: discovery of a large, continuous population of Pan troglodytes schweinfurthii in the Central Uele region of northern DRC. Biol Conserv 171:107-113.
29. Hill WCO. 1969. The nomenclature, taxonomy, and distribution of chimpanzees. In: Bourne GH, editor. The chimpanzee, Vol. 1. Basel: Karger. p 22-49.
30. Hvilsom C, Frandsen P, Børsting C, Carlsen F, Salle B, Simonsen BT, Siegismund HR. 2013. Understanding geographic origins and history of admixture among chimpanzees in European zoos, with implications for future breeding programmes. Heredity 110:586-593.
31. Junker J, Blake S, Boesch C., Campbell G, Toit L du, 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 18:1077-1091.
32. Kalinowski ST, Taper ML, Marshall TC. 2007. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099-1106.
33. Langergraber K, Mitani J, Vigilant L. 2009. Kinship and social bonds in female chimpanzees (Pan troglodytes). Am J Primatol 71:840-851.
34. Langergraber K, Schubert G, Rowney C., Wrangham R, Zommers Z, Vigilant L. 2011. Genetic differentiation and the evolution of cooperation in chimpanzees and humans. Proc R Soc B Biol Sci 278:2546-2552.
35. Lao O, Lu TT, Nothnagel M, Junge O., Freitag-Wolf S, Caliebe A, Balascakova M., Bertranpetit J, Bindoff LA, Comas D, Holmlund G, Kouvatsi A, Macek M, Mollet I, Parson W, Palo J, Ploski R, Sajantila A, Tagliabracci A, Gether U, Werge T, Rivadeneira F, Hofman A, Uitterlinden AG, Gieger C, Wichmann H-E, Ruther A, Schreiber S, Becker C, Nurnberg P Nelson MR, Krawczak M, Kayser M. 2008. Correlation between genetic and geographic structure in Europe. Curr Biol 18:1241-1248.
36. Laporte NT, Stabach JA, Grosch R, Lin T.S., Goetz SJ. 2007. Expansion of industrial logging in Central Africa. Science 316:1451-1451.
37. McBrearty S, Jablonski NG. 2005. First fossil chimpanzee. Nature 437:105-108.
38. Mitani JC, Watts DP, Amsler SJ. 2010. Lethal intergroup aggression leads to territorial expansion in wild chimpanzees. Curr Biol 20: R507-R508.
39. Morgan D, Sanz C. 2003. Naïve encounters with chimpanzees in the Goualougo Triangle, Republic of Congo. Int J Primatol 24:369-381.
40. Morin PA, Chambers KE, Boesch C, Vigilant L. 2001. Quantitative polymerase chain reaction analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzees (Pan troglodytes verus). Mol Ecol 10:1835-1844.
41. Morin PA, Moore JJ, Chakraborty R, Jin L., Goodall J, Woodruff DS. 1994. Kin selection, social structure, gene flow, and the evolution of chimpanzees. Science 265:1193-1201.
42. Newton-Fisher NE. 2003. The home range of the Sonso community of chimpanzees from the Budongo Forest, Uganda. Afr J Ecol 41:150-156.
43. Nsubuga AM, Robbins MM, Roeder A.D., 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 13:2089-2094.
44. 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: 78-80.
45. Pilbrow V 2006. Population systematics of chimpanzees using molar morphometrics. J Hum Evol 51:646-662.
46. Plumptre A, Rose R, Nangendo G., Williamson EA, Didier K, Hart F, Mulindahabi F., Hicks C, Griffin B, Ogawa H, Nixon S, Pintea L, Vosper A, McLennan M, 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, Tranquilli S, Beyers R, Hashimoto C, Furuichi T, Bennett E. 2010. Status survey and conservation action plan for the Eastern chimpanzee (Pan troglodytes schweinfurthii), 2010-2020. Gland, Switzerland: IUCN. p 48.
47. Prado-Martinez J, Sudmant PH, Kidd J.M., Li H., Kelley JL, Lorente-Galdos B, Veeramah KR, Woerner A.E., O'Connor TD, Santpere G, Cagan A, Theunert C, Casals F, Laayouni H, Munch K, Hobolth A, Halager AE, Malig M, Hernandez-Rodriguez J, Hernando-Herraez I, Prufer K, Pybus M, Johnstone L, Lachmann M, Alkan C, Twigg D, Petit N, Baker C, Hormozdiari F, Fernandez-Callejo M, Dabad M, Wilson ML, Stevison L, Camprubí C, Carvalho T, Ruiz-Herrera A, Vives L, Mele M, Abello T, Kondova I, Bontrop RE, Pusey A, Lankester F, Kiyang JA, Bergl RA, Lonsdorf E, Myers S, Ventura M, Gagneux P, Comas D, Siegismund H, Blanc J, Agueda-Calpena L, Gut M, Fulton L, Tishkoff SA, Mullikin JC, Wilson RK, Gut IG, Gonder MK, Ryder OA, Hahn BH, Navarro A, Akey JM, Bertranpetit J, Reich D, Mailund T, Schierup MH, Hvilsom C, Andres AM, Wall JD, Bustamante CD, Hammer MF, Eichler EE, Marques-Bonet T 2013. Great ape genetic diversity and population history. Nature 499:471-475.
48. Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
49. Pritchard JK, Wen W, Falush D. 2003. Documentation for STRUCTURE software: version 2. Available at: http://seq.ege.fcen.uba.ar/materias/ecomolecular/Material/An%C3%A1lsis%20Bayesiano%20Metapoblaciones.%20STRUCTURE/Structure2.1/Help%20Files/readme.pdf. Accessed on July 13, 2004.
50. Raymond M, Rousset F. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248-249.
51. R Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
52. Rosenberg NA, Mahajan S, Ramachandran S., Zhao C, Pritchard JK, Feldman MW. 2005. Clines, clusters, and the effect of study design on the inference of human population structure. PLoS Genet 1:e70.
53. Rosenberg NA, Pritchard JK, Weber J.L., Cann, H. W., Kidd KK, Zhivotovsky L.A., Feldman MW. 2002. Genetic structure of human populations. Science 298:2381-2385.
54. Schonewald-Cox CM, Chambers SM, MacBryde B, Thomas WL. 1983. Genetics and conservation: a reference for managing wild animal and plant populations. Menlo Park, California: Benjamin/Cummings Publishing Company.
55. Schwartz MK, McKelvey KS. 2009. Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441-452.
56. Serre D, Pääbo, S. 2004. Evidence for gradients of human genetic diversity within and among continents. Genome Res 14:1679-1685.
57. Stone AC, Griffiths RC, Zegura S.L., Hammer MF. 2002. High levels of Y-chromosome nucleotide diversity in the genus Pan. Proc Natl Acad Sci 99:43-48.
58. Taberlet P, Griffin S, Goossens B., Questiau S, Manceau V, Escaravage N., Waits LP, Bouvet J. 1996. Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24:3189-3194.
59. Tishkoff SA, Reed FA, Friedlaender F.R., Ehret C., Ranciaro A, Froment A, Hirbo J.B., Awomoyi AA, Bodo J-M, Doumbo O, Ibrahim M, Juma AT, Kotze MJ, Lema G, Moore JH, Mortensen H, Nyambo TB, Omar SA, Powell K, Pretorius GS, Smith MW, Thera MA, Wambebe C, Weber JL, Williams SM. 2009. The genetic structure and history of Africans and African Americans. Science 324:1035-1044.
60. Waits LP, Luikart G, Taberlet P. 2001. Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249-256.
61. Walsh P, Abernathy K, Bermejo M., Beyers R, De Wachter P, Akou ME, Huijbregts B, Mambounga D.I., Toham AK, Kilbourn AM, Lahm SA, Latour S, Maisels F, Mbina C, Mihindou Y, Obiang SN, Effa EN, Starkey MP, Telfer P, Thibault M, Tutin CEG, White LJT, Wilkie DS. 2003. Catastrophic ape decline in western equatorial Africa. Nature 422: 611-614.
62. Weir BS. 1996. Genetic data analysis II. Sunderland, Massachusetts: Sinauer.
63. Wilson ML, Balmforth Z, Cox D., et al. 2009. Pan troglodytes ssp. schweinfurthii. 2009 IUCN red list of threatened species. Version 2009.1. Available at: www.iucnredlist.org. Accessed 17 March 2010.
64. Witzenberger KA, Hochkirch A. 2011. Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodivers Conserv 20:1843-1861.
65. Wrangham RW, Hagel G, Leighton M., Marshall AJ, Waldau P, Nishida T. 2008. The great ape world heritage species project. In: Stoinski TS, Steklis HD, Mehlman PT, editors. Conservation in the 21st century: gorillas as a case study. New York: Springer Science and Business Media, LLC. p 282-296.
66. Wright S. 1943. Isolation by distance. Genetics 28:114.