Abstract
Western lowland gorillas (Gorilla gorilla gorilla) were imported from across their geographical range to North American zoos from the late 1800s through 1974. The majority of these gorillas were imported with little or no information regarding their original provenance and no information on their genetic relatedness. Here, we analyze 32 microsatellite loci in 144 individuals using a Bayesian clustering method to delineate clusters of individuals among a sample of founders of the captive North American zoo gorilla collection. We infer that the majority of North American zoo founders sampled are distributed into two distinct clusters, and that some individuals are of admixed ancestry. This new information regarding the existence of ancestral genetic population structure in the North American zoo population lays the groundwork for enhanced efforts to conserve the evolutionary units of the western lowland gorilla gene pool. Our data also show that the genetic diversity estimates in the founder population were comparable to those in wild gorilla populations (Mondika and Cross River), and that pairwise relatedness among the founders is no different from that expected for a random mating population. However, the relatively high level of relatedness (R = 0.54) we discovered in a pair of known breeding pairs reveals the need for incorporating genetic relatedness estimates in the captive management of western lowland gorillas.
Similar content being viewed by others
References
Anthony NM, Johnson-Bawe M, Jeffery K, Clifford SL, Abernethy KA, Tutin CE, Lahm SA, White LJT, Utley JF, Wickings EJ, Bruford MW (2007) The role of Pleistocene refugia and rivers in shaping gorilla genetic diversity in central Africa. Proc Natl Acad Sci 104:20432–20436
Archie JW (1985) Statistical analysis of heterozygosity data: independent sample comparisons. Evolution 39:623–637
Ballou J, Foose T (1996) Demographic and genetic management of captive populations. In: Kleiman D, Allen M, Thompson K, Lumpkin S, Harris H (eds) Wild mammals in captivity. University of Chicago Press, Chicago, pp 263–283
Ballou J, Gilpin M, Foose T (eds) (1995) Population management for survival and recovery. Columbia University Press, New York
Ballou JD, Lacy RC (1995) Identifying genetically important individuals for management of genetic diversity in pedigreed populations. In: Ballou JD, Gilpin M, Foose TJ (eds) Population management for survival recovery. Columbia Press, New York
Basset P, Yannic G, Hausser J (2006) Genetic and karyotypic structure in the shrews of the (Sorex araneus) group: are they independent? Mol Ecol 15:1577–1587
Bayes MK, Smith KL, Alberts SC, Altmann J, Bruford MW (2000) Testing the reliability of microsatellite typing from faecal DNA in the Savannah baboon. Conserv Genet 1:173–176
Beaumont M, Barratt EM, Gottelli D, Kitchener AC, Daniels MJ, Pritchards JK, Bruford MW (2001) Genetic diversity and introgression in the Scottish wildcat. Mol Ecol 10:319
Beck BB (1982) Fertility in North American male lowland gorillas. Am J Primatol 3:7–11
Beck BB, Power ML (1988) Correlates of sexual and maternal competence in captive gorillas. Zoo Biol 7:339–350
Becquet C, Patterson N, Stone AC, Przeworski M, Reich D (2007) Genetic structure of chimpanzee populations. PLoS Genet 3:617–626
Bergl RA, Vigilant L (2007) Genetic analysis reveals population structure and recent migration within the highly fragmented range of the Cross River gorilla (Gorilla gorilla diehli). Mol Ecol 16:501–516
Bergl RA, Bradley BJ, Nsubuga AM, Vigilant L (2008) Effects of habitat fragmentation, population size and demographic history on genetic diversity: the cross river gorilla in a comparative context. Am J Primatol 70:848–859
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 feces. Conserv Genet 1:289–292
Bradley BJ, Chambers KE, Vigilant L (2001) Accurate DNA-based sex identification of apes using non-invasive samples. Conserv Genet 2:179–181
Bradley BJ, Doran-Sheehy DM, Lukas D, Boesch C, Vigilant L (2004) Dispersed male networks in western gorillas. Curr Biol 14:510–513
Bradley BJ, Robbins MM, Williamson EA, Steklis DH, Steklis NG, Eckhardt N, Boesch C, Vigilant L (2005) Mountain gorilla tug-of-war: silverbacks have limited control over reproduction in multimale groups. Proc Natl Acad Sci USA 102:9418–9423
Bradley BJ, Doran-Sheehy DM, Vigilant L (2007) Potential for female kin associations in wild western gorillas despite female dispersal. Proc R Soc B: Biol Sci 274:2179–2185
Cegelski CC, Waits LP, Anderson NJ (2003) Assessing population structure and gene flow in Montana wolverines (Gulo gulo) using assignment-based approaches. Mol Ecol 12:2907
Clifford SL, Jeffrey K, Bruford MW, Wickings EJ (1999) Identification of polymorphic microsatellite loci in the gorilla (Gorilla gorilla gorilla) using human primers: application to noninvasively collected samples. Mol Ecol 8:1556–1558
Clifford SL, Anthony NM, Bawe-Johnson M, Abernethy KA, Tutin CEG, White LJT, Bermejo M, Goldsmith ML, McFarland K, Jeffery KJ, Bruford MW, Wickings EJ (2004) Mitochondrial DNA phylogeography of western lowland gorillas (Gorilla gorilla gorilla). Mol Ecol 13:1551–1565
Coltman DW, Bancroft DR, Robertson A, Smith JA, Clutton-brock TH, Pemberton JM (1999) Male reproductive success in a promiscuous mammal: behavioural estimates compared with genetic paternity. Mol Ecol 8:1199–1209
Crandall L (1964) The management of wild mammals in captivity. University of Chicago Press, Chicago
Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295
Debruyne R (2005) A case study of apparent conflict between molecular phylogenies: the interrelationships of African elephants. Cladistics 21:31–50
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
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
Garnier-Gere P, Dillmann C (1992) A computer program for testing pairwise linkage disequilibria in subdivided populations. J Hered 83:239
Geyer CJ, Ryder OA, Chemnick LG, Thompson EA (1993) Analysis of relatedness in the California condors, from DNA fingerprints. Mol Biol Evol 10:571–589
Goodnight KF, Queller DC (1999) Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol Ecol 8:1231–1234
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). Department of Ecology and Evolution, Lausanne University, Switzerland. Available at http://www.unil.ch/izea/softwares/fstat.html
Groves C, Grubb P (2000) Do Loxodonta cyclotis and L. africana interbreed? Elephant. Elephant 2:4–7
Grubb P, Groves C, Dudley J, Shoshani J (2000) Living African elephants belong to two species: Loxodonta africana (Blumenbach, 1797) and Loxodonta cyclotis (Matschie, 1900). Elephant 2:1–4
Guo SW, Thomson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372
Guschanski K, Caillaud D, Robbins M, Vigilant L (2008) Females shape the genetic structure of a gorilla population. Curr Biol 18:1809–1814
Johnson M, Clifford S, Goossens B, Nyakaana S, Curran B, White L, Wickings EJ, Bruford M (2007) Complex phylogeographic history of central African forest elephants and its implications for taxonomy. BMC Evol Biol 7:244
Jones KL, Glenn TC, Lacy RC, Pierce JR, Unruh N, Mirande CM, Chavez-Ramirez F (2002) Refining the whooping crane studbook by incorporating microsatellite DNA and leg-banding analyses. Conserv Biol 16:789–799
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
Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738
Kumamoto A, Charter S, Houck M, Frahm M (1996) Chromosomes of Damaliscus (Artiodactyla, Bovidae): simple and complex centric fusion rearrangements. Chromosome Res 4:614–621
Lecis R, Pierpaoli M, BirÒ ZS, Szemethy L, Ragni B, Vercillo F, Randi E (2006) Bayesian analyses of admixture in wild and domestic cats (Felis silvestris) using linked microsatellite loci. Mol Ecol 15:119–131
Lei R, Brenneman RA, Louis EE Jr (2008) Genetic diversity in the North American captive African elephant collection. J Zool 275:252–267
Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends Ecol Evol 20:136–142
Marshall TC, Slate J, Kruuk LE, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655
Melnick D, Hoelzer G (1992) Differences in male and female macaque dispersal lead to contrasting distributions of nuclear and mitochondrial DNA variation. Int J Primatol 13:379–393
Mills LS, Citta JJ, Lair KP, Schwarz MK, Tallmon DA (2000) Estimating animal abundance using noninvasive DNA sampling: promise and pitfalls. Ecol Appl 10:283–294
Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Nsubuga AM, Robbins MM, Roeder AD, Morin AP, 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
Nsubuga AM, Robbins MM, Boesch C, Vigilant L (2008) Patterns of paternity and group fission in wild multimale mountain gorilla groups. Am J Phys Anthropol 135:263–274
Olson DJ (2003) North American region studbook for the African elephants (Loxodonta africana). Indianapolis Zoological Society, Indiana
Paetkau D, Strobeck C (1994) Microsatellite analysis of genetic-variation in black bear populations. Mol Ecol 3:489–495
Priest JH (1997) General cell culture principles and fibroblast culture. In: Barch MJ, Knutsen T, Spurbeck JL (eds) The AGT cytogenetics laboratory manual. Lippincott-Raven Publishers, Pennsylvania, pp 173–197
Pritchard JK, Wen W (2004) Documentation for structure software: version 2. Department of Human Genetics, University of Chicago, Chicago
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275
Ralls K, Ballou JD (2004) Genetic status and management of California condors. Condor 106:215–228
Rassmann K, Tautz D, Trillmich F, Gliddon C (1997) The microevolution of the Galápagos marine iguana Amblyrhynchus cristatus assessed by nuclear and mitochondrial genetic analyses. Mol Ecol 6:437–452
Redmond I (2006) Presence of great apes in Bas-Congo. Gorilla J 33:10–12
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Robinson SJ, Waits LP, Martin ID (2007) Evaluating population structure of black bears on the Kenai peninsula using mitochondrial and nuclear analyses. J Mammal 88:1288–1299
Roca A, Georgiadis N, Pecon-Slattery J, O’Brien S (2001) Genetic evidence for two species of elephant in Africa. Science 293:1473–1477
Roca AL, Georgiadis N, O’Brien SJ (2004) Cytonuclear genomic dissociation in African elephant species. Nat Genet 37:96–100
Rosenberg NA, Burke T, Elo K, Feldman MW, Freidlin PJ, Groenen MAM, Hillel J, Maki-Tanila A, Tixier-Boichard M, Vignal A, Wimmers K, Weigend S (2001) Empirical evaluation of genetic clustering methods using multilocus genotypes from 20 chicken breeds. Genetics 159:699–713
Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106
Rudnick J, Lacy R (2008) The impact of assumptions about founder relationships on the effectiveness of captive breeding strategies. Conserv Genet 9:1439–1450
Slate J, Kruuk LEB, Marshall TC, Pemberton JM, Clutton-Brock TH (2000) Inbreeding depression influences lifetime breeding success in a wild population of red deer (Cervus elaphus). Proc R Soc Lond B Biol Sci 267:1657–1662
Stoinski TS, Lukas KE, Kuhar CW, Maple TL (2004) Factors influencing the formation and maintenance of all-male gorilla groups in captivity. Zoo Biol 23:189–203
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
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
Walsh PD, Tutin CEG, Oates JF, Baillie JEM, Maisels F, Stokes EJ, Gatti S, Bergl RA, Sunderland-Groves J, Dunn A (2008) Gorilla gorilla. In: IUCN 2009. IUCN Red List of Threatened Species. Version 2009.2. Available at http://www.iucnredlist.org
Wharton D (2000) Gorilla management for the 21st century. In: American Zoo and Aquarium Association annual conference proceedings. Disney’s Animal Kingdom, Orlando
Wharton D (2007) North American studbook for the western lowland gorilla (Gorilla gorilla gorilla). In: Regional studbook. Chicago Zoological Society, Chicago
Wharton D (2009) North American regional western lowland gorilla studbook. Chicago Zoological Society, Chicago
Yeh FC, Yang RC, Boyle TBJ, Ye ZH, Mao JX (1999) POPGENE, the user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Center, University of Alberta Edmonton, Alberta
Zhang Y-W, Morin P, Ryder O, Zhang Y-P (2001) A set of human tri- and tetra-nucleotide microsatellite loci useful for population analyses in gorillas (Gorilla gorilla gorilla) and orangutans (Pongo pygmaeus). Conserv Genet 2:391–395
Acknowledgments
We would like to thank the numerous zoos belonging to the Association of Zoos and Aquariums who have over the years contributed gorilla samples that made the basis of this study. We also are grateful to Drs. S. Burgess-Herbert and R. van Horn of San Diego Zoo’s Institute for Conservation Research, Dr. L. Vigilant of the Max Planck Institute for Evolutionary Anthropology, and two anonymous reviewers for their useful comments on the manuscript, and to all members of the Genetics lab at San Diego Zoo’s Institute for Conservation Research, especially H. Davis, C. Otten, J. Fronczek, and S. Charter, for their technical assistance. We thank Dr. William Karesh, Wildlife Conservation Society, for providing samples from Odzala National Park, Congo, and Dr. Bethan Morgan of San Diego Zoo’s Institute for Conservation Research for providing samples from Ebo Forest, Cameroon. The Zoological Society of San Diego, the James and Helen Copley Foundation, the Bud Heller Foundation, and Twila Schoettger funded this study.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nsubuga, A.M., Holzman, J., Chemnick, L.G. et al. The cryptic genetic structure of the North American captive gorilla population. Conserv Genet 11, 161–172 (2010). https://doi.org/10.1007/s10592-009-0015-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-009-0015-x