期刊论文详细信息
Annals of Occupational and Environmental Medicine
Fine-scale genetic structure analyses suggest further male than female dispersal in mountain gorillas
Justin Roy1  Maryke Gray3  Tara Stoinski2  Martha M Robbins1  Linda Vigilant1 
[1] Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103, Leipzig, Germany
[2] The Dian Fossey Gorilla Fund International and Zoo Atlanta, Atlanta, Georgia 30315, USA
[3] International Gorilla Conservation Program, P.O. Box 931, Kigali, Rwanda
关键词: Spatial genetic structure;    Social mammal;    Philopatry;    Mountain gorilla;    Microsatellite;    Inbreeding avoidance;    Dispersal;   
Others  :  870176
DOI  :  10.1186/1472-6785-14-21
 received in 2013-12-17, accepted in 2014-06-27,  发布年份 2014
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2014 Roy et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Clutton-Brock TH: Female transfer and inbreeding avoidance in social mammals. Nature 1989, 337:70-72.
  • [2]Storz JF: Genetic consequences of mammalian social structure. J Mammal 1999, 80:553-569.
  • [3]Clutton-Brock TH, Lukas D: The evolution of social philopatry and dispersal in female mammals. Mol Ecol 2012, 21:472-492.
  • [4]Clutton-Brock TH: Mammalian mating systems. Proc R Soc London Ser B Biol Sci 1989, 236:339-372.
  • [5]Hamilton WD: The genetical evolution of social behaviour. I. J Theor Biol 1964, 7:1-16.
  • [6]Lawson Handley LJ, Perrin N: Advances in our understanding of mammalian sex-biased dispersal. Mol Ecol 2007, 16:1559-1578.
  • [7]Keller LF, Waller DM: Inbreeding effects in wild populations. Trends Ecol Evol 2002, 17:230-241.
  • [8]Stockley P, Searle JB, MacDonald DW, Jones CS: Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding. Proc R Soc London Ser B Biol Sci 1993, 254:173-179.
  • [9]Jiménez JA, Hughes KA, Alaks G, Graham L, Lacy RC: An experimental study of inbreeding depression in a natural habitat. Science 1994, 266:271-273.
  • [10]Coltman DW, Pilkington JG, Smith JA, Josephine M: Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 1999, 53:1259-1267.
  • [11]Slate J, Kruuk LE, Marshall TC, Pemberton JM, Clutton-Brock TH: Inbreeding depression influences lifetime breeding success in a wild population of red deer (Cervus elaphus). Proc R Soc London Ser B Biol Sci 2000, 267:1657-1662.
  • [12]Packer C: Inter-troop transfer and inbreeding avoidance in Papio anubis. Anim Behav 1979, 27:1-36.
  • [13]Alberts SC, Altmann J: Balancing costs and opportunities: dispersal in male baboons. Am Sci 1995, 145:279-306.
  • [14]Bowler DE, Benton TG: Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 2005, 80:205-225.
  • [15]Greenwood PJ: Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 1980, 28:1140-1162.
  • [16]Sutherland GD, Harestad AS, Price K, Lertzman KP: Scaling of natal dispersal distances in terrestrial birds and mammals. Conserv Ecol 2000, 4:1-36.
  • [17]Koenig WD, Van Vuren D, Hooge PN: Detectability, philopatry, and the distribution of dispersal distances in vertebrates. Trends Ecol Evol 1996, 11:514-517.
  • [18]Wright S: Isolation by distance. Genetics 1943, 28:114-138.
  • [19]Smouse PE, Peakall R: Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 1999, 82:561-573.
  • [20]Peakall R, Ruibal M, Lindenmayer DB: Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 2003, 57:1182-1195.
  • [21]Hazlitt SL, Eldridge MDB, Goldizen AW: Fine-scale spatial genetic correlation analyses reveal strong female philopatry within a brush-tailed rock-wallaby colony in southeast Queensland. Mol Ecol 2004, 13:3621-3632.
  • [22]Bonnot N, Gaillard J-M, Coulon A, Galan M, Cosson J-F, Delorme D, Klein F, Hewison AJM: No difference between the sexes in fine-scale spatial genetic structure of roe deer. PloS One 2010, 5:e14436.
  • [23]Busch JD, Waser PM, DeWoody JA: The influence of density and sex on patterns of fine-scale genetic structure. Evolution 2009, 63:2302-2314.
  • [24]Van Horn RC, Engh AL, Scribner KT, Funk SM, Holekamp KE: Behavioural structuring of relatedness in the spotted hyena (Crocuta crocuta) suggests direct fitness benefits of clan-level cooperation. Mol Ecol 2004, 13:449-458.
  • [25]Liu XH, Yue LF, Wang DW, Li N, Cong L: Inbreeding avoidance drives consistent variation of fine-scale genetic structure caused by dispersal in the seasonal mating system of Brandt’s voles. PloS One 2013, 8:e58101.
  • [26]Kalpers J, Williamson EA, Robbins MM, McNeilage A, Nzamurambaho A, Lola N, Mugiri G: Gorillas in the crossfire: population dynamics of the Virunga mountain gorillas over the past three decades. Oryx 2003, 37:326-337.
  • [27]Robbins MM, Gray M, Fawcett KA, Nutter FB, Uwingeli P, Mburanumwe I, Kagoda E, Basabose A, Stoinski TS, Cranfield MR, Byamukama J, Spelman LH, Robbins AM: Extreme conservation leads to recovery of the Virunga mountain gorillas. PloS One 2011, 6:e19788.
  • [28]Groves CP: A History of Gorilla Taxonomy. In Gorilla biology: A multidisciplinary perspective. Edited by Taylor AB, Goldsmith ML. Cambridge: Cambridge University Press; 2003:15-34.
  • [29]Robbins MM: Gorillas: Diversity in ecology and behavior. In Primates in Perspective. 2nd edition. Edited by Campbell C, Fuentes A, MacKinnon K, Bearder S, Stumpf R. Oxford, UK: Oxford University Press; 2010:326-339.
  • [30]Robbins AM, Stoinski TS, Fawcett KA, Robbins MM: Leave or conceive: natal dispersal and philopatry of female mountain gorillas in the Virunga volcano region. Anim Behav 2009, 77:831-838.
  • [31]Robbins MM, Bermejo M, Cipolletta C, Magliocca F, Parnell RJ, Stokes E: Social structure and life-history patterns in western gorillas (Gorilla gorilla gorilla). Am J Primatol 2004, 64:145-159.
  • [32]Stoinski TS, Vecellio V, Ngaboyamahina T, Ndagijimana F, Rosenbaum S, Fawcett KA: Proximate factors influencing dispersal decisions in male mountain gorillas, Gorilla beringei beringei. Anim Behav 2009, 77:1155-1164.
  • [33]Bradley BJ, Robbins MM, Williamson EA, Steklis HD, Steklis NG, Eckhardt N, Boesch C, Vigilant L: Mountain gorilla tug-of-war: silverbacks have limited control over reproduction in multimale groups. Proc Natl Acad Sci U S A 2005, 102:9418-9423.
  • [34]Nsubuga AM, Robbins MM, Boesch C, Vigilant L: Patterns of paternity and group fission in wild multimale mountain gorilla groups. Am J Phys Anthropol 2008, 135:263-274.
  • [35]Stoinski TS, Rosenbaum S, Ngaboyamahina T, Vecellio V: Patterns of male reproductive behaviour in multi-male groups of mountain gorillas: examining theories of reproductive skew. Behaviour 2009, 146:1193-1215.
  • [36]Bradley BJ, Doran-Sheehy DM, Vigilant L: Potential for female kin associations in wild western gorillas despite female dispersal. Proc R Soc London Ser B Biol Sci 2007, 274:2179-2185.
  • [37]Guschanski K, Caillaud D, Robbins MM, Vigilant L: Females shape the genetic structure of a gorilla population. Curr Biol 2008, 18:1809-1814.
  • [38]Bradley BJ, Doran-sheehy DM, Lukas D, Boesch C, Vigilant L: Dispersed male networks in western gorillas. Curr Biol 2004, 14:510-513.
  • [39]Inoue E, Akomo-Okoue EF, Ando C, Iwata Y, Judai M, Fujita S, Hongo S, Nze-Nkogue C, Inoue-Murayama M, Yamagiwa J: Male genetic structure and paternity in western lowland gorillas (Gorilla gorilla gorilla). Am J Phys Anthropol 2013, 151:583-588.
  • [40]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
  • [41]Harcourt AH, Stewart KS, Fossey D: Male emigration and female transfer in wild mountain gorilla. Nature 1976, 263:226-227.
  • [42]Harcourt AH: Strategies of emigration and transfer by primates, with particular reference to gorillas. Z Tierpsychol 1978, 48:401-420.
  • [43]Douadi MI, Gatti S, Levrero F, Duhamel G, Bermejo M, Vallet D, Menard N, Petit EJ: Sex-biased dispersal in western lowland gorillas (Gorilla gorilla gorilla). Mol Ecol 2007, 16:2247-2259.
  • [44]Caillaud D, Ndagijimana F, Giarrusso AJ, Vecellio V, Stoinski TS: Mountain gorilla ranging patterns: Influence of group size and group dynamics. Am J Primatol 2014, 76:1-17.
  • [45]Coltman DW, Pilkington JG, Pemberton JM: Fine-scale genetic structure in a free-living ungulate population. Mol Ecol 2003, 12:733-742.
  • [46]Frantz AC, Hamann J-L, Klein F: Fine-scale genetic structure of red deer (Cervus elaphus) in a French temperate forest. Eur J Wildl Res 2007, 54:44-52.
  • [47]Cullingham CI, Merrill EH, Pybus MJ, Bollinger TK, Wilson GA, Coltman DW: Broad and fine-scale genetic analysis of white-tailed deer populations: estimating the relative risk of chronic wasting disease spread. Evol Appl 2011, 4:116-131.
  • [48]Robbins AM, Gray M, Basabose A, Uwingeli P, Mburanumwe I, Kagoda E, Robbins MM: Impact of male infanticide on the social structure of mountain gorillas. PloS One 2013, 8:e78256.
  • [49]Harcourt AH, Stewart KS: Gorilla Society: Conflict, Compromise, and Cooperation Between the Sexes. Chicago: University of Chicago Press; 2007.
  • [50]Robbins AM, Stoinski TS, Fawcett KA, Robbins MM: Socioecological influences on the dispersal of female mountain gorillas—evidence of a second folivore paradox. Behav Ecol Sociobiol 2009, 63:477-489.
  • [51]Watts DP: Mountain gorilla reproduction and sexual behavior. Am J Primatol 1991, 24:211-225.
  • [52]Watts DP: Social relationships of immigrant and resident female mountain gorillas, II : relatedness, residence, and relationships between females. Am J Primatol 1994, 32:13-30.
  • [53]Crockett CM, Pope TR: Consequences of sex differences in dispersal for juvenile red howler monkeys. In Juvenile primates: life history, development, and behavior. Edited by Pereira ME, Fairbanks LA. New York: Oxford University Press; 1993:104-118.
  • [54]Fedigan LM, Carnegie SD, Jack KM: Predictors of reproductive success in female white-faced capuchins (Cebus capucinus). Am J Phys Anthropol 2008, 137:82-90.
  • [55]Dobson FS, Jacquot C, Baudoin C: An experimental test of kin association in the house mouse. Can J Zool 2000, 78:1806-1812.
  • [56]Gray M, Roy J, Vigilant L, Fawcett K, Basabose A, Cranfield M, Uwingeli P, Mburanumwe I, Kagoda E, Robbins MM: Genetic census reveals increased but uneven growth of a critically endangered mountain gorilla population. Biol Conserv 2013, 158:230-238.
  • [57]Robbins MM: A demographic analysis of male life history and social structure of mountain gorillas. Behaviour 1995, 132:21-47.
  • [58]Robbins AM, Robbins MM: Fitness consequences of dispersal decisions for male mountain gorillas (Gorilla beringei beringei). Behav Ecol Sociobiol 2005, 58:295-309.
  • [59]Robbins MM: Male mating patterns in wild multimale mountain gorilla groups. Anim Behav 1999, 57:1013-1020.
  • [60]Sillero-Zubiri C, Gottelli D, Macdonald DW: Male philopatry, extra-pack copulations and inbreeding avoidance in Ethiopian wolves (Canis simensis). Behav Ecol Sociobiol 1996, 38:331-340.
  • [61]Inoue E, Inoue-Murayama M, Vigilant L, Takenaka O, Nishida T: Relatedness in wild chimpanzees: influence of paternity, male philopatry, and demographic factors. Am J Phys Anthropol 2008, 137:256-262.
  • [62]Sigg H, Stolba A, Abegglen J, Dasser V: Life history of hamadryas baboons: physical development, infant mortality, reproductive parameters and family relationships. Primates 1982, 23:473-487.
  • [63]Pusey AE: Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol Evol 1987, 2:295-299.
  • [64]Lukas D, Clutton-Brock TH: Group structure, kinship, inbreeding risk and habitual female dispersal in plural-breeding mammals. J Evol Biol 2011, 24:2624-2630.
  • [65]Robbins MM, Robbins AM, Gerald-Steklis N, Steklis HD: Socioecological influences on the reproductive success of female mountain gorillas (Gorilla beringei beringei). Behav Ecol Sociobiol 2007, 61:919-931.
  • [66]Sholley CR: Conserving Gorillas in the Midst of Guerrillas. American Association of Zoological Parks and Aquarium, Annual Conference Proceedings 1991, 30-37.
  • [67]McNeilage A, Robbins MM, Gray M, Olupot W, Babaasa D, Bitariho R, Kasangaki A, Rainer H, Asuma S, Mugiri G, Baker J: Census of the mountain gorilla Gorilla beringei beringei population in Bwindi Impenetrable National Park, Uganda. Oryx 2006, 40:419-427.
  • [68]Nsubuga AM, Robbins MM, Roeder AD, Morin PA, Boesch C, Vigilant L: Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method. Mol Ecol 2004, 13:2089-2094.
  • [69]Bradley BJ, Chambers KE, Vigilant L: Accurate DNA-based sex identification of apes using non-invasive samples. Conserv Genet 2001, 2:179-181.
  • [70]Arandjelovic M, Guschanski K, Schubert G, Harris TR, Thalmann O, Siedel H, Vigilant L: Two-step multiplex polymerase chain reaction improves the speed and accuracy of genotyping using DNA from noninvasive and museum samples. Mol Ecol Resour 2009, 9:28-36.
  • [71]Morin PA, Mahboubi P, Wedel S, Rogers J: Rapid screening and comparison of human microsatellite markers in baboons: allele size is conserved, but allele number is not. Genomics 1998, 53:12-20.
  • [72]Bradley BJ, Boesch C, Vigilant L: Identification and redesign of human microsatellite markers for genotyping wild chimpanzee (Pan troglodytes verus) and gorilla (Gorilla gorilla gorilla) DNA from faeces. Conserv Genet 2000, 1:289-292.
  • [73]Guschanski K, Vigilant L, McNeilage A, Gray M, Kagoda E, Robbins MM: Counting elusive animals: Comparing field and genetic census of the entire mountain gorilla population of Bwindi Impenetrable National Park, Uganda. Biol Conserv 2009, 142:290-300.
  • [74]Kalinowski ST, Taper ML, Marshall TC: Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 2007, 16:1099-1106.
  • [75]Raymond M, Rousset F: GENEPOP (Version 1.2): Population genetics software for exact tests and ecumenicism. J Hered 1995, 86:248-249.
  • [76]Weir BS, Cockerham CC: Estimating F-statistics for the analysis of population structure. Evolution 1984, 38:1358-1370.
  • [77]Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P: MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 2004, 4:535-538.
  • [78]Rousset F: Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 1997, 145:1219-1228.
  • [79]Hardy OJ, Vekemans X: SPAGEDI: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2002, 2:618-620.
  • [80]Queller DC, Goodnight KF: Estimating relatedness using genetic markers. Evolution 1989, 43:258-275.
  • [81]R Core Team: R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2013.
  • [82]Peakall R, Smouse PE: GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 2006, 6:288-295.
  • [83]Double MC, Peakall R, Beck NR, Cockburn A: Dispersal, philopatry, and infidelity: dissecting local genetic structure in superb fairy-wrens (Malurus cyaneus). Evolution 2005, 59:625-635.
  • [84]Banks SC, Peakall R: Genetic spatial autocorrelation can readily detect sex-biased dispersal. Mol Ecol 2012, 21:2092-2105.
  • [85]Wilson AG, Arcese P, Chan YL, Patten MA: Micro-spatial genetic structure in song sparrows (Melospiza melodia). Conserv Genet 2011, 12:213-222.
  • [86]Roy J, Yannic G, Côté SD, Bernatchez L: Negative density-dependent dispersal in the American black bear (Ursus americanus) revealed by noninvasive sampling and genotyping. Ecology and Evolution 2012, 2:525-537.
  • [87]Colson KE, Brinkman TJ, Person DK, Hundertmark KJ: Fine-scale social and spatial genetic structure in Sitka black-tailed deer. Conserv Genet 2013, 14:439-449.
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