The genetic population structure of wild western lowland gorillas (Gorilla gorilla gorilla) living in continuous rain forest

American Journal of Primatology

Volumn 76, Issue 9, 2014, Pages 868-878

  Fünfstück, Tillmann ^a   Arandjelovic, Mimi ^a   Morgan, David B ^b   Sanz, Crickette ^c   Breuer, Thomas ^b   Stokes, Emma J ^b   Reed, Patricia ^b   Olson, Sarah H ^b   Cameron, Ken ^b   Ondzie, Alain ^d   Peeters, Martine ^e   Kühl, Hjalmar S ^a   Cipolletta, Chloe ^f   Todd, Angelique ^f   Masi, Shelly ^g   Doran Sheehy, Diane M ^h   Bradley, Brenda J ⁱ   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)

^f WWF CAR ^*  (Central African Republic)

^g MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^h STONY BROOK UNIVERSITY   (United States)

ⁱ YALE UNIVERSITY   (United States)

Author keywords

Gorilla gorilla gorilla; Philopatry; Population structure; Sex specific dispersal

Indexed keywords

EVOLUTIONARY BIOLOGY; GENE FLOW; GEOGRAPHICAL VARIATION; LANDSCAPE CHANGE; PHILOPATRY; POPULATION STRUCTURE; PRIMATE; RAINFOREST; SEX-RELATED DIFFERENCE; SPECIES CONSERVATION; WILD POPULATION;

CAMEROON; CENTRAL AFRICAN REPUBLIC; CONGO;

ANIMALIA; GORILLA GORILLA GORILLA;

MICROSATELLITE DNA;

ANIMAL; CENTRAL AFRICA; CLUSTER ANALYSIS; EVOLUTION; FEMALE; FOREST; GENE FLOW; GENETIC VARIATION; GENETICS; GENOTYPE; GEOGRAPHY; GORILLA; MALE; PHYLOGEOGRAPHY; POPULATION GENETICS; SEX DIFFERENCE;

AFRICA, CENTRAL; ANIMALS; BIOLOGICAL EVOLUTION; CLUSTER ANALYSIS; FEMALE; FORESTS; GENE FLOW; GENETIC VARIATION; GENETICS, POPULATION; GENOTYPE; GEOGRAPHY; GORILLA GORILLA; MALE; MICROSATELLITE REPEATS; PHYLOGEOGRAPHY; SEX FACTORS;

EID: 84906317076     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.22274     Document Type: Article

References (74)

1. Anthony NM, Johnson-Bawe M, Jeffery K, et al. 2007. The role of Pleistocene refugia and rivers in shaping gorilla genetic diversity in central Africa. Proceedings of the National Academy Sciences of the United States of America 104:20432-20436.
2. Arandjelovic M, Guschanski K, Schubert G, et al. 2009. Two-step multiplex polymerase chain reaction improves the speed and accuracy of genotyping using DNA from noninvasive and museum samples. Molecular Ecology Resources 9:28-36.
3. Arandjelovic M, Head J, Kühl H, et al. 2010. Effective non-invasive genetic monitoring of multiple wild western gorilla groups. Biological Conservation 143:1780-1791.
4. Arora N, Nater A, van Schaik CP, et al. 2010. Effects of Pleistocene glaciations and rivers on the population structure of Bornean orangutans (Pongo pygmaeus). Proceedings of the National Academy Sciences of the United States of America 107:21376-21381.
5. Balarin JD. 1985. The status of fish farming in Zimbabwe and future prospects. Zimbabwe Agricultural Journal 83:3-9.
6. Beadle LC. 1981. The inland waters of tropical Africa. London, United Kingdom: Longman.
7. Blair C, Weigel DE, Balazik M, et al. 2012. A simulation-based evaluation of methods for inferring linear barriers to gene flow. Molecular Ecology Resources. Available online at: http://onlinelibrary.wiley.com/doi/10.1111/j1755-0998.2012.03151.x/full
8. Blanchong JA, Samuel MD, Scribner KT, et al. 2008. Landscape genetics and the spatial distribution of chronic wasting disease. Biology Letters 4:130-133.
9. Bradley BJ, Chambers KE, Vigilant L. 2001. Accurate DNA-based sex identification of apes using non-invasive samples. Conservation Genetics 2:179-181.
10. Bradley BJ, Doran-Sheehy DM, Lukas D, Boesch C, Vigilant L. 2004. Dispersed male networks in western gorillas. Current Biology 14:510-513.
11. Brandt AL, Ishida Y, Georgiadis NJ, Roca AL. 2012. Forest elephant mitochondrial genomes reveal that elephantid diversification in Africa tracked climate transitions. Molecular Ecology 21:1175-1189.
12. Breuer T, Hockemba MB-N, Olejniczak C, Parnell RJ, Stokes EJ. 2009. Physical maturation, life-history classes and age estimates of free-ranging western gorillas-insights from Mbeli Bai, Republic of Congo. American Journal of Primatology 71:106-119.
13. Breuer T, Robbins AM, Olejniczak C, et al. 2010. Variance in the male reproductive success of western gorillas: acquiring females is just the beginning. Behavioural Ecology and Sociobiology 64:515-528.
14. Burrows W, Ryder OA. 1997. Y-chromosome variation in great apes. Nature 385:125-126.
15. Collins A, Dubach J. 2000. Biogeographic and ecological forces responsible for speciation in Ateles. International Journal of Primatology 21:421-444.
16. Corander J, Marttinen P. 2006. Bayesian identification of admixture events using multilocus molecular markers. Molecular Ecology 15:2833-2843.
17. Corander J, Sirén J, Arjas E. 2007. Bayesian spatial modeling of genetic population structure. Computation Statistics 23:111-129.
18. Craul M, Radespiel U, Rasolofoson DW, et al. 2008. Large rivers do not always act as species barriers for Lepilemur sp. Primates 49:211-218.
19. De Thoisy B, da Silva A, Ruiz-García M, et al. 2010. Population history, phylogeography, and conservation genetics of the last Neotropical mega-herbivore, the lowland tapir (Tapirus terrestris). BMC Evolutionary Biology 10:278.
20. Douadi MI, Gatti S, Levrero F, et al. 2007. Sex-biased dispersal in western lowland gorillas (Gorilla gorilla gorilla). Molecular Ecology 16:2247-2259.
21. Earl DA, vonHoldt BM. 2011. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4:359-361.
22. Eriksson J, Hohmann G, Boesch C, Vigilant L. 2004. Rivers influence the population genetic structure of bonobos (Pan paniscus). Molecular Ecology 13:3425-3435.
23. Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14:2611-2620.
24. Falush D, Stephens M, Pritchard JK. 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567-1587.
25. Falush D, Stephens M, Pritchard JK. 2007. Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7:574-578.
26. Gatti S, Levréro F, Ménard N, Gautier-Hion A. 2004. Population and group structure of western lowland gorillas (Gorilla gorilla gorilla) at Lokoué, Republic of Congo. American Journal of Primatology 63:111-123.
27. Gonder MK, Oates JF, Disotell TR, et al. 1997. A new west African chimpanzee subspecies? Nature 388:337.
28. Gonder MK, Disotell TR, Oates JF. 2006. New genetic evidence on the evolution of chimpanzee populations and implications for taxonomy. International Journal of Primatology 27:1103-1127.
29. Greenwood PJ. 1980. Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour 28:1140-1162.
30. Guillot G. 2005. A spatial statistical model for landscape genetics. Genetics 170:1261-1280.
31. Guillot G. 2008. Inference of structure in subdivided populations at low levels of genetic differentiation-the correlated allele frequencies model revisited. Bioinformatics 24:2222-2228.
32. Guillot G, Mortier F, Estoup A. 2005. GENELAND: a computer package for landscape genetics. Molecular Ecology Notes 5:712-715.
33. Guillot G, Santos F, Estoup A. 2008. Analysing georeferenced population genetics data with Geneland: a new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics 24:1406-1407.
34. Guo SW, Thompson EA. 1992. Performing exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361-372.
35. Guschanski K, Caillaud D, Robbins MM, Vigilant L. 2008. Females shape the genetic structure of a gorilla population. Current Biology 18:1809-1814.
36. Haag T, Santos AS, Sana DA, et al. 2010. The effect of habitat fragmentation on the genetic structure of a top predator: loss of diversity and high differentiation among remnant populations of Atlantic Forest jaguars (Panthera onca). Molecular Ecology 19:4906-4921.
37. Haffer J. 1969. Speciation in Amazonian forest birds. Science 165:131-137.
38. Hardy OJ, Vekemans X. 2002. SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2:618-620.
39. Hellborg L. 2003. Low levels of nucleotide diversity in mammalian y chromosomes. Molecular Biology and Evolution 21:158-163.
40. Hewitt GM. 1996. Some genetic consequences of ice ages and their role in divergence and speciation. Biological Journal of the Linnean Society 58:247-276.
41. Inoue E, Akomo-Okoue EF, Ando C, et al. 2013. Male genetic structure and paternity in western lowland gorillas (Gorilla gorilla gorilla). American Journal of Physical Anthropology 151:583-588.
42. Jalil M, Cable J, Inyor J, et al. 2008. Riverine effects on mitochondrial structure of Bornean orang-utans (Pongo pygmaeus) at two spatial scales. Molecular Ecology 17:2898-2909.
43. Kalinowski ST, Taper ML, Marshall TC. 2007. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 16:1099-1106.
44. Kawamoto Y, Takemoto H, Higuchi S, et al. 2013. Genetic structure of wild bonobo populations: diversity of mitochondrial DNA and geographical distribution. PLoS ONE 8:e59660.
45. Lawson Handley LJ, Perrin N, 2007. Advances in our understanding of mammalian sex-biased dispersal. Molecular Ecology 16:1559-1578.
46. Levréro F. 2005. Structure d'une population de gorilles (Gorilla gorilla gorilla) visitant une Clairière Forestière-nature et rôle des rencontres intergroupes dans sa dynamique [Ph.D. Thesis]. France: Université de Rennes 1.
47. Mabry KE, Shelley EL, Davis KE, Blumstein DT, Van Vuren DH. 2013. Social mating system and sex-biased dispersal in mammals and birds: a phylogenetic analysis. PLoS ONE 8:e57980.
48. Martínez-Cruz B, Godoy JA, Negro JJ. 2007. Population fragmentation leads to spatial and temporal genetic structure in the endangered Spanish imperial eagle. Molecular Ecology 16:477-486.
49. 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). Molecular Ecology 10:1835-1844.
50. Neaves LE, Zenger KR, Prince RIT, Eldridge MDB, Cooper DW. 2009. Landscape discontinuities influence gene flow and genetic structure in a large, vagile Australian mammal, Macropus fuliginosus. Molecular Ecology 18:3363-3378.
51. Nsubuga AM, Robbins MM, Roeder AD, et al. 2004. Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method. Molecular Ecology 13:2089-2094.
52. Osman-Hill WC. 1969. The nomenclature, taxonomy, and distribution of chimpanzees. In: Bourne GH. editors. The chimpanzee. Vol. 1. Basel, Switzerland: Karger. p 22-49.
53. Parnell RJ. 2002. Group size and structure in western lowland gorillas (Gorilla gorilla gorilla) at Mbeli Bai, Republic of Congo. American Journal of Primatology 56:193-206.
54. Peakall ROD, Smouse PE. 2006. GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Molecular Ecology Notes 6:288-295.
55. Peakall R, Smouse P. 2012. GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research-an update. Bioinformatics. Available online at: http://bioinformatics.oxfordjournals.org/content/early/2012/07/20/bioinformatics.bts460.short
56. Pérez-Espona S, Pérez-Barbería FJ, Mcleod JE, et al. 2008. Landscape features affect gene flow of Scottish Highland red deer (Cervus elaphus). Molecular Ecology 17:981-996.
57. Piertney SB, MacColl ADC, Bacon JP, Dallas JF. 1998. Local genetic structure in red grouse (Lagopus lagopus scoticus): evidence from microsatellite DNA markers. Molecular Ecology 7:1645-1654.
58. Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
59. Raymond M, Rousset F. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86:248-249.
60. Reding DM, Bronikowski AM, Johnson WE, Clark WR. 2012. Pleistocene and ecological effects on continental-scale genetic differentiation in the bobcat (Lynx rufus). Molecular Ecology 21:3078-3093.
61. Robbins MM, Bermejo M, Cipolletta C, et al. 2004. Social structure and life-history patterns in western gorillas (Gorilla gorilla gorilla). American Journal of Primatology 64:145-159.
62. Roca AL, Georgiadis N, Pecon-Slattery J, O'Brien SJ. 2001. Genetic evidence for two species of elephant in Africa. Science 293:1473-1477.
63. Ruell EW, Riley SPD, Douglas MR, et al. 2012. Urban habitat fragmentation and genetic population structure of bobcats in Coastal Southern California. American Midland Naturalist 168:265-280.
64. Ruiter JD, Geffen E. 1998. Relatedness of matrilines, dispersing males and social groups in long-tailed macaques (Macaca fascicularis). Proceedings of the Royal Society B: Biological Sciences 265:79-87.
65. Schwarz E. 1934. On the local races of chimpanzees. Annals and Magazine of Natural History, London 13:576-583.
66. Stauch A. 1963. Contribution a l'etude de la peche dans le Cuvette Congolaise. Bulletin de l' Institut des Recherches Scientifiques du Congo 2:49-85.
67. Stoinski TS, Vecellio V, Ngaboyamahina T, et al. 2009. Proximate factors influencing dispersal decisions in male mountain gorillas, Gorilla beringei beringei. Animal Behaviour 77:1155-1164.
68. Stokes EJ, Parnell RJ, Olejniczak C. 2003. Female dispersal and reproductive success in wild western lowland gorillas (Gorilla gorilla gorilla). Behavioral Ecology and Sociobiology 54:329-339.
69. Storfer A, Murphy MA, Spear SF, Holderegger R, Waits LP. 2010. Landscape genetics: where are we now? Molecular Ecology 19:3496-3514.
70. Taberlet P, Griffin S, Goossens B, et al. 1996. Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Research 24:3189-3194.
71. Tutin CEG, White LJT, Mackanga-Missandzou A. 1997. The use by rain forest mammals of natural forest fragments in an equatorial African savanna. Conservation Biology 11:1190-1203.
72. Tutin C, Stokes E, Boesch C, et al. 2005. Regional action plan for the conservation of chimpanzees and gorillas in western equatorial Africa. Washington, DC: IUCN/SSC Primate Specialist Group Conservation International.
73. Waits LP, Luikart G, Taberlet P. 2001. Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Molecular Ecology 10:249-256.
74. Weir BS. 1996. Genetic data analysis II. Sunderland, MA: Sinauer.