Potential drivers of samango monkey (Cercopithecus albogularis) population subdivision in a highly fragmented mountain landscape in northern South Africa.
Gene flow
Habitat fragmentation
Microsatellites
Population structure
Soutpansberg mountain range
Journal
Primates; journal of primatology
ISSN: 1610-7365
Titre abrégé: Primates
Pays: Japan
ID NLM: 0401152
Informations de publication
Date de publication:
May 2022
May 2022
Historique:
received:
27
07
2021
accepted:
07
02
2022
pubmed:
1
3
2022
medline:
6
5
2022
entrez:
28
2
2022
Statut:
ppublish
Résumé
Forests affected by fragmentation are at risk of losing their primate populations over the long term. The impact of fragmentation on primate populations has been studied in several places in Africa, Asia and South America; however, there has been no discernible pattern of how primates react to forest disturbance and fragmentation. In fragmented habitats, the local extinction probability of a species increases due to a decrease in patch area and an increase in genetic isolation. Here we used microsatellite markers and mitochondrial DNA sequences to investigate how habitat fragmentation impacts on the genetic diversity and structure of a samango monkey population inhabiting forest patches in the Soutpansberg mountain range of northern South Africa. We sampled four local populations across the length of the mountain range and an additional outlying population from the Great Escarpment to the south. Our results indicate that local populations along the mountain range were historically more connected and less distinct than at present. In more recent times, a lack of contemporary gene flow is leading to a more pronounced genetic structure, causing population subdivision across the mountain and likely isolating the Soutpansberg population from the escarpment population to the south. Based on our results, we suggest that natural and anthropogenic fragmentation are driving population genetic differentiation, and that the matrix surrounding forests and their suitability for samango monkey utilisation play a role at the local scale. The degree of genetic isolation found for samango monkey populations in our study raises concerns about the long-term viability of populations across the mountain range.
Identifiants
pubmed: 35226214
doi: 10.1007/s10329-022-00981-7
pii: 10.1007/s10329-022-00981-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
245-260Informations de copyright
© 2022. The Author(s), under exclusive licence to Japan Monkey Centre.
Références
Ang A, Roesma DI, Nijman V, Meier R, Srivathsan A (2020) Faecal DNA to the rescue: Shotgun sequencing of non-invasive samples reveals two subspecies of Southeast Asian primates to be Critically Endangered species. Sci Rep 10(1):1–16
doi: 10.1038/s41598-019-56847-4
Bennun L, Dranzoa C, Pomeroy D (1996) The forest birds of Kenya and Uganda. J East Afr Nat Hist 85:23–48
doi: 10.2982/0012-8317(1996)85[23:TFBOKA]2.0.CO;2
Berliner BB (2005) Systematic conservation planning for the forest biome of South Africa. Approach, methods and results of the selection of the priority forests for conservation action. Technical report prepared for the Water and Forestry Support Programme and the Department of Water Affairs and Forestry (DWAF), South Africa
Brookfield J (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5(3):453–455. https://doi.org/10.1046/j.1365-294X.1996.00098.x
doi: 10.1046/j.1365-294X.1996.00098.x
pubmed: 8688964
Coleman BT, Hill RA (2014) Living in a landscape of fear: the impact of predation, resource availability and habitat structure on primate range use. Anim Behav 88:165–173. https://doi.org/10.1016/j.anbehav.2013.11.027
doi: 10.1016/j.anbehav.2013.11.027
Cooper KH (1985) The conservation status of indigenous forests in Transvaal, Natal and O.F.S., South Africa. Report, Wildlife Society of Southern Africa, Durban
Cords M (2001) Friendship among adult female blue monkeys (Cercopithecus mitis). Behaviour 139:291–314
doi: 10.1163/156853902760102681
Cords M (2012) The 30-year blues: what we know and don’t know about life history, group size and group fission of blue monkeys in the Kakamega Forest, Kenya. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer, Berlin, pp 289–312
doi: 10.1007/978-3-642-22514-7_13
Cords M, Rowell TE (1986) Group fission in blue monkeys of the Kakamega Forest. Kenya Folia Primatol 46(2):70–82
doi: 10.1159/000156239
Cornuet J-M, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
doi: 10.1093/genetics/144.4.2001
Dalton DL, Linden B, Wimberger K, Nupen L, Tordiffe ASW, Taylor PJ, Madisha MT, Kotze A (2015) New insights into samango monkey speciation in South Africa. PLoS ONE 10(3):e0117003. https://doi.org/10.1371/journal.pone.0117003
doi: 10.1371/journal.pone.0117003
pubmed: 25798604
pmcid: 4370472
Deacon HJ (1983) Another look at the Pleistocene climates of South Africa. S Afr J Sci 79:325–328
Droomer EAP (1985) Volume and value loss owing to samango monkey damage to pine stands in the Northern Transvaal. South Afr for J 134(1):47–51. https://doi.org/10.1080/00382167.1985.9629594
doi: 10.1080/00382167.1985.9629594
Dudash MR, Fenster CB (2000) Inbreeding and outbreeding depression in fragmented populations. In: Young AG, Clarke GM (eds) Genetics, demography, and viability of fragmented populations. Cambridge University Press, Cambridge, pp 35–53
doi: 10.1017/CBO9780511623448.005
Earl DA (2012) BM vonHoldt. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Res 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
doi: 10.1007/s12686-011-9548-7
Eastwood E, Eastwood C (2006) Capturing the Spoor. An exploration of southern African rock art. David Philip, New Africa Books (Pty) Ltd, Claremont
Eeley HAC, Lawes MJ, Piper SE (1999) The influence of climate change on the distribution of indigenous forest in KwaZulu-Natal. South Africa J Biogeogr 26(3):595–617. https://doi.org/10.1046/j.1365-2699.1999.00307.x
doi: 10.1046/j.1365-2699.1999.00307.x
Eggert LS, Patterson G, Malsonado JE (2008) The Knysna elephants: a population study conducted using faecal DNA. Afr J Ecol 46:19–23. https://doi.org/10.1111/j.1365-2028.2007.00794.x
doi: 10.1111/j.1365-2028.2007.00794.x
Ekernas LS, Cords M (2007) Social and environmental factors influencing natal dispersal in blue monkeys, Cercopithecus mitis stuhlmanni. Anim Behav 73:1009–1020. https://doi.org/10.1016/j.anbehav.2006.11.007
doi: 10.1016/j.anbehav.2006.11.007
Estrada A, Garber PA, Rylands AB et al (2017) Impending extinction crisis of the world’s primates: why primates matter. Sci Adv 3(1):e1600946. https://doi.org/10.1126/sciadv.1600946
doi: 10.1126/sciadv.1600946
pubmed: 28116351
pmcid: 5242557
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. https://doi.org/10.1111/j.1365-294X.2005.02553.x
doi: 10.1111/j.1365-294X.2005.02553.x
pubmed: 15969739
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. https://doi.org/10.1111/j.1755-0998.2010.02847.x
doi: 10.1111/j.1755-0998.2010.02847.x
pubmed: 21565059
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131(2):479–491
doi: 10.1093/genetics/131.2.479
FAO (2018) The State of the World’s Forests 2018 - Forest pathways to sustainable development. Licence: CC BY-NC-SA 3.0 IGO, Rome
Faubet P, Gaggiotti OE (2008) A new Bayesian method to identify the environmental factors that influence recent migration. Genetics 178:1491–1504. https://doi.org/10.1534/genetics.107.082560
doi: 10.1534/genetics.107.082560
pubmed: 18245344
pmcid: 2278086
Gerloff U, Hartung B, Fruth B, Hohmann G, Tautz D (1999) Intracommunity relationships, dispersal pattern and paternity success in a wild living community of Bonobos (Pan paniscus) determined from DNA analysis of faecal samples. Proc Royal Soc B 266:1189–1195. https://doi.org/10.1098/rspb.1999.0762
doi: 10.1098/rspb.1999.0762
Gibbons MA, Harcourt AH (2009) Biological correlates of extinction and persistence of primates in small forest fragments: a global analysis. Trop Conserv Sci 2(4):388–403. https://doi.org/10.1177/194008290900200402
doi: 10.1177/194008290900200402
Goossens B, Anthony N, Jeffery K, Johnson-Bawe M, Bruford MW (2003) Collection, storage and analysis of non-invasive genetic material in primate biology. In: Setchell JM, Curtis DC (eds) Field and laboratory methods in primatology. Cambridge University Press, Cambridge, pp 295–308
doi: 10.1017/CBO9781139165105.022
Gründler W (1897) Geschichte der Bawenda Mission in Nord-Transvaal. Berlin no. 43, Buchhandlung der Berliner evangelischen Missionsgesellschaft
Hahn N (2017a) Endemic flora of the Soutpansberg, Blouberg and Makgabeng. S Afr J Bot 113:324–335. https://doi.org/10.1016/j.sajb.2017.09.006
doi: 10.1016/j.sajb.2017.09.006
Hahn N (2017b) An historic account of the extinct high rainfall grasslands of the Soutpansberg, South Africa. Trans R Soc South Africa 73(1):20–32. https://doi.org/10.1080/0035919X.2017.1346528
doi: 10.1080/0035919X.2017.1346528
Hartl D, Clark AG (1987) Principles of Population Genetics, 2nd edn. Sinauer Associates, Sunderland, Massachusetts
Henzi SP, Lawes M (1987) Breeding season influxes and the behaviour of adult male samango monkeys (Cercopithecus mitis albogularis). Folia Primatol 48:125–136. https://doi.org/10.1159/000156290
doi: 10.1159/000156290
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
doi: 10.1093/bioinformatics/btn129
pubmed: 18397895
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. https://doi.org/10.1186/1471-2156-11-94
doi: 10.1186/1471-2156-11-94
pubmed: 20950446
pmcid: 2973851
Kalinowski ST (2005) hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5(1):187–189. https://doi.org/10.1111/j.1471-8286.2004.00845.x
doi: 10.1111/j.1471-8286.2004.00845.x
Lacy RC (1997) Importance of genetic variation to the viability of mammalian populations. J Mammal 78:320–335. https://doi.org/10.2307/1382885
doi: 10.2307/1382885
Lacy RC (2000) Structure of the VORTEX simulation model for population viability analysis. Ecol Bull 48:191–203. https://doi.org/10.2307/20113257
doi: 10.2307/20113257
Lawes MJ (1990) The distribution of the Samango Monkey (Cercopithecus mitis erythrarchus Peters, 1852 and Cercopithecus mitis labiatus I. Geoffroy, 1843) and Forest History in Southern Africa. J Biogeogr 17(6):669–680. https://doi.org/10.2307/2845148
doi: 10.2307/2845148
Lawes MJ (1992) Estimates of population density and correlates of the status of the samango monkey Cercopithecus mitis in Natal, South Africa. Biol Conserv 60:197–210. https://doi.org/10.1016/0006-3207(92)91252-N
doi: 10.1016/0006-3207(92)91252-N
Lawes MJ, Henzi SP (1995) Inter-group encounters in blue monkeys: how territorial must a territorial species be? Anim Behav 49:240–243. https://doi.org/10.1016/0003-3472(95)80173-1
doi: 10.1016/0003-3472(95)80173-1
Lawes MJ, Henzi SP, Perrin MR (1990) Diet and feeding behaviour in Samango Monkeys (Cercopithecus mitis labiatus) in Ngoye Forest. South Africa Folia Primatol 54:57–69. https://doi.org/10.1159/000156426
doi: 10.1159/000156426
Leigh JW, Bryant D (2015) Popart: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410
doi: 10.1111/2041-210X.12410
Li CC, Weeks DE, Chakravarti A (1993) Similarity of DNA fingerprints due to chance and relatedness. Hum Hered 43:45–52
doi: 10.1159/000154113
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
doi: 10.1093/bioinformatics/btp187
pubmed: 19346325
Linden B, Linden JD, Fischer F, Linsenmair KE (2015) Seed dispersal by South Africa’s only forest-dwelling guenon, the samango monkey (Cercopithecus mitis). Afr J Wildl Res 45(1):88–99. https://doi.org/10.3957/056.045.0110
doi: 10.3957/056.045.0110
Linden B, Foord S, Horta-Lacueva QJB, Taylor PJ (2020) Bridging the gap: how to design canopy bridges for arboreal guenons to mitigate road collisions. Biol Conserv 246:108560. https://doi.org/10.1016/j.biocon.2020.108560
doi: 10.1016/j.biocon.2020.108560
Linden B, Wimberger K, Ehlers-Smith Y, Child MF (2016) A conservation assessment of Cercopithecus albogularis. In: Child MF, Roxburgh L, Do Linh San E, Raimondo D, Davies-Mostert HT (eds) The Red List of Mammals of South Africa, Swaziland and Lesotho. South African National Biodiversity Institute and Endangered Wildlife Trust, South Africa
Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766
doi: 10.1093/genetics/152.4.1753
Madisha MT, Dalton DL, Jasen R, Kotze A (2017) Genetic assessment of an isolated endemic samango monkey (Cercopithecus albogularis labiatus) population in the Amathole Mountains, Eastern Cape Province. South Africa Primates 59(2):197–207. https://doi.org/10.1007/s10329-017-0636-5
doi: 10.1007/s10329-017-0636-5
pubmed: 29080055
Marsh LK (2003) Primates in fragments. Ecology and conservation. Kluwer Academic/Plenum Publishers, New York
doi: 10.1007/978-1-4757-3770-7
Marsh LK (2013) Primates in fragments. Complexity and resilience. Springer, New York, USA
doi: 10.1007/978-1-4614-8839-2
Maseko MST, Ramesh T, Kalle R, Downs CT (2017) Response of crested Guinea-fowl (Guttera edouardi), a forest specialist, to spatial variation in land use in iSimangaliso Wetland Park, South Africa. J Ornithol 158:469–477
doi: 10.1007/s10336-016-1406-7
McAlpine CA, Rhodes JR, Callaghan JG, Bowen ME, Lunney D, Mitchell DL, Possingham HP (2006) The importance of forest area and configuration relative to local habitat factors for conserving forest mammals: a case study of koalas in Queensland. Australia Biol Conserv 132:153–165
doi: 10.1016/j.biocon.2006.03.021
Meyer D, Rinaldi ID, Ramlee H, Perwitasari-Farajallah D, Hodges JK, Roos C (2011) Mitochondrial phylogeny of leaf monkeys (genus Presbytis, Eschscholtz, 1821) with implications for taxonomy and conservation. Mol Phylogenet Evol 59(2):311–319. https://doi.org/10.1016/j.ympev.2011.02.015
doi: 10.1016/j.ympev.2011.02.015
pubmed: 21333742
Milligan BG (2003) Maximum-likelihood estimation of relatedness. Genetics 163:1153–1167
doi: 10.1093/genetics/163.3.1153
Moir M, Richards LR, Rambau RV, Cherry MI (2021) Functional diversity and trait filtering of insectivorous bats relate to forest biogeography and fragmentation in South Africa. J Biogeogr. https://doi.org/10.1111/jbi.14069
doi: 10.1111/jbi.14069
Mucina L, Geldenhuys CJ (2006) Afromontane, subtropical and azonal forests, Chapter 12. In: Mucina L, Rutherford MC (eds) The vegetation of South Africa, Lesotho and Swaziland. South African National Biodiversity Institute, Strelitzia 19, Pretoria, pp 584–615
Mucina L, Rutherford MC (Eds) (2006) The vegetation of South Africa, Lesotho and Swaziland. South African Biodiversity Institute, Pretoria
Munyati C, Kabanda TA (2009) Using multitemporal Landsat TM imagery to establish land use pressure induced trends in forest and woodland cover in sections of the Soutpansberg Mountains of Venda region, Limpopo Province. South Africa Reg Environ Change 9:41–56. https://doi.org/10.1007/s10113-008-0066-4
doi: 10.1007/s10113-008-0066-4
Nievergelt CM, Digby LJ, Ramakrishnan U, Woodruff DS (2000) Genetic analysis of group composition and breeding system in a wild common marmoset (Callithrix jacchus) population. Int J Primatol 21:1–20
doi: 10.1023/A:1005411227810
Novak K, le Roux A, Richards SA, Scheijen CPJ, Hill RA (2014) Human observers impact habituated samango monkeys’ perceived landscape of fear. Behav Ecol 25(5):1199–1204. https://doi.org/10.1093/beheco/aru110
doi: 10.1093/beheco/aru110
Oklander LI, Miño CI, Fernândez G, Caputo M, Corach D (2017) Genetic structure in the southernmost populations of black-and-gold howler monkeys (Alouatta caraya) and its conservation implications. PLoS ONE 12(10):e0185867. https://doi.org/10.1371/journal.pone.0185867
doi: 10.1371/journal.pone.0185867
pubmed: 28968440
pmcid: 5624639
Olivier TJ, Ober C, Buettner–Janusch J, Sade DS (1981) Genetic differentiation among matrilines in social groups of rhesus monkeys. Behav Ecol Sociobiol 8:279–285
doi: 10.1007/BF00299527
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research - an update. Bioinformatics 28:2537–2539. https://doi.org/10.1093/bioinformatics/bts460
doi: 10.1093/bioinformatics/bts460
pubmed: 22820204
pmcid: 3463245
Pew J, Muir PH, Wang J, Frasier TR (2015) related: An R package for analysing pairwise relatedness from codominant molecular markers. Mol Ecol Resour 15:557–561. https://doi.org/10.1111/1755-0998.12323
doi: 10.1111/1755-0998.12323
pubmed: 25186958
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1111/j.1471-8286.2007.01758.x
doi: 10.1111/j.1471-8286.2007.01758.x
pubmed: 10835412
pmcid: 1461096
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275. https://doi.org/10.2307/2409206
doi: 10.2307/2409206
pubmed: 28568555
Robin VV, Gupta P, Thatte P, Ramakrishnan U (2015) Islands within islands: two montane palaeo-endemic birds impacted by recent anthropogenic fragmentation. Mol Ecol 24(14):3572–3584. https://doi.org/10.1111/mec.13266
doi: 10.1111/mec.13266
pubmed: 26133900
Scheepers JC (1978) The vegetation of Westfalia-Estate on the north-eastern Transvaal escarpment. Mem Bot Surv South Africa 42:1–230
Scholes RJ, Berns J, Everard DA, Scott D, Van Thienhoven M, Viljoen P (1995) The costs and benefits of forestry, case studies from Mpumalanga. Report FOR-DEA 939, Environmentek, CSIR, Pretoria
Scott L (1987) Late quaternary forest history in Venda, southern Africa. Rev Palaeobot Palynol 53:1–10. https://doi.org/10.1016/0034-6667(87)90008-X
doi: 10.1016/0034-6667(87)90008-X
Seufert V, Linden B, Fischer F (2009) Revealing secondary seed removers: results from camera trapping. Afr J Ecol 48:914–922. https://doi.org/10.1111/j.1365-2028.2009.01192.x
doi: 10.1111/j.1365-2028.2009.01192.x
Silk JB, Kappeler PM (2017) Sociality in primates. In: Rubenstein DR, Abbot P (eds) Comparative social evolution. Cambridge University Press, Cambridge, pp 253–383
doi: 10.1017/9781107338319.010
Snyder-Mackler N, Majoros WH, Yuan ML, Shaver AO, Gordon JB, Kopp GH, Schlebusch SA, Wall JD, Alberts SC, Mukherjee S, Zhou X (2016) Efficient genome-wide sequencing and low-coverage pedigree analysis from noninvasively collected samples. Genetics 203:699–714. https://doi.org/10.1534/genetics.116.187492
doi: 10.1534/genetics.116.187492
pubmed: 27098910
pmcid: 4896188
Swart J, Lawes MJ (1996) The effect of habitat patch connectivity on samango monkey (Cercopithecus mitis) metapopulation persistence. Ecol Model 93:57–74. https://doi.org/10.1016/0304-3800(95)00211-1
doi: 10.1016/0304-3800(95)00211-1
Swart J, Lawes MJ, Perrin MR (1993) A mathematical model to investigate the demographic viability of low-density samango monkey (Cercopithecus mitis) populations in Natal, South Africa. Ecol Model 70:289–303. https://doi.org/10.1016/0304-3800(93)90062-W
doi: 10.1016/0304-3800(93)90062-W
Taberlet P, Waits LP, Luikart G (1999) Noninvasive genetic sampling: look before you leap. Trends Ecol Evol 14:323–327. https://doi.org/10.1016/S0169-5347(99)01637-7
doi: 10.1016/S0169-5347(99)01637-7
pubmed: 10407432
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121
doi: 10.1093/molbev/msr121
pubmed: 21546353
pmcid: 3203626
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 60. Mol Biol Evol 30(12):2725–2729. https://doi.org/10.1093/molbev/mst197
doi: 10.1093/molbev/mst197
pubmed: 24132122
pmcid: 3840312
Tempelhoff JWN (1999) Townspeople of the Soutpansberg. A centenary history (1899–1999). Greater Louis Trichardt Transitional Council, Louis Trichardt
Van Horn RC, Buchan JC, Altmann J, Alberts SC (2007) Divided destinies: group choice by female savannah baboons during social group fission. Behav Ecol Sociobiol 61(12):1823–1837. https://doi.org/10.1007/s00265-007-0415-1
doi: 10.1007/s00265-007-0415-1
Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4(3):535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
doi: 10.1111/j.1471-8286.2004.00684.x
von dem Bussche GH, Van der Zee D (1985) Damage by Samango monkeys, Cercopithecus (mitis) albogularis, to pine trees in the Northern Transvaal. South Afr for J 134:47–51. https://doi.org/10.1080/00382167.1985.9629573
doi: 10.1080/00382167.1985.9629573
Wahlund S (1928) Zusammensetzung von Populationen und Korelationserscheinungen vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas 11:175–195
Wang J (2002) An estimator for pairwise relatedness using molecular markers. Genetics 160:1203–1215
doi: 10.1093/genetics/160.3.1203
Wang J (2007) Triadic IBD coefficients and applications to estimating pairwise relatedness. Genet Res 89:135–153. https://doi.org/10.1017/S0016672307008798
doi: 10.1017/S0016672307008798
pubmed: 17894908
Waples RS, Gaggiotti O (2006) Invited review: What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439
doi: 10.1111/j.1365-294X.2006.02890.x
Wasser S, Houston C, Koehler G, Cadd G, Fain S (1997) Techniques for application of fecal DNA methods to field studies of Ursids. Mol Ecol 6:1091–1097. https://doi.org/10.1046/j.1365-294x.1997.00281.x
doi: 10.1046/j.1365-294x.1997.00281.x
pubmed: 9394465
Wimberger K, Novak K, Hill RA (2017) Reliance on exotic plants by two groups of threatened samango monkeys, Cercopithecus albogularis labiatus, at their southern range limit. Int J Primatol 38(2):151–171. https://doi.org/10.1007/s10764-016-9949-2
doi: 10.1007/s10764-016-9949-2
Wright S (1943) Isolation by distance. Genetics 28(2):114–138
doi: 10.1093/genetics/28.2.114