Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-848d4c4894-5nwft Total loading time: 0 Render date: 2024-06-02T21:13:39.663Z Has data issue: false hasContentIssue false

18 - The Use of Microsatellites in the Management of Captive Gibbons

Published online by Cambridge University Press:  13 April 2023

By
Lauren Lansdowne ,
Matyas Liptovszky ,
Kristiana Brink ,
Katie Dripps ,
Vivienne Li ,
Edward J. Hollox  and
Richard M. Badge
Edited by
Susan M. Cheyne ,
Carolyn Thompson ,
Peng-Fei Fan  and
Helen J. Chatterjee
Susan M. Cheyne
Affiliation:
Borneo Nature Foundation
Carolyn Thompson
Affiliation:
University College London
Peng-Fei Fan
Affiliation:
Sun Yat-Sen University, China
Helen J. Chatterjee
Affiliation:
University College London
Get access

Summary

Genetic profiling can validate pedigrees and reveal genetic diversity/inbreeding within populations. We have developed 12 autosomal microsatellite markers that can be used to DNA profile gibbon species. The panel generated full profiles for 39 individuals currently or previously housed at Twycross Zoo, UK, representing five species across three genera. The study is extending to a further approximate 100 samples, including three additional species, from captive populations across Europe. The panel’s cross-species utility allows for a single protocol to be used for all DNA profiling, avoiding the need for species-specific testing. In addition, the panel resolved an issue of uncertain paternity in a breeding group, with direct implications for group management and welfare. The loci reported here yielded profiles from blood, tissue and non-invasive hair samples. Positive impact on the viability and sustainability of captive breeding programmes is anticipated, by clarifying cryptic relatedness and informing future pairings. Potential exists for field application in investigating population dynamics, mating behaviours, relatedness and dispersal patterns, as well as assessing the impact of anthropogenic disturbances on the genetic architecture of populations. This established panel, effective across multiple gibbon species and genera, presents an affordable and expedient tool for research and captive management.

Keywords

gibbonsmicrosatellitescaptive breedinggenetic diversitypaternity testing
Type
Chapter
Information
Gibbon Conservation in the Anthropocene , pp. 302 - 318
Publisher: Cambridge University Press
Print publication year: 2023

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barelli, C., Matsudaira, K., Wolf, T., et al. (2013). Extra-pair paternity confirmed in wild white-handed gibbons. American Journal of Primatology, 75(12): 1185–1195.Google Scholar
Beauclerc, K.B., Johnson, B. and White, B.N. (2010). Genetic rescue of an inbred captive population of the critically endangered Puerto Rican crested toad (Peltophryne lemur) by mixing lineage. Conservation Genetics, 11(1): 21–32.Google Scholar
Blouin, M.S. (2003). DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends in Ecology and Evolution, 18(10): 503–511.Google Scholar
Brinkmann, B., Klintschar, M., Neuhuber, F., Hu, J. and Rolf, B. (1998). Mutation rate in human microsatellites: influence of the structure and length of the tandem repeat. American Journal of Human Genetics, 62: 1408–1415.Google Scholar
Bryant, J.V., Gottelli, D., Zeng, X., et al. (2016). Assessing current genetic status of the Hainan gibbon using historical and demographic baselines: implications for conservation management of species of extreme rarity. Molecular Ecology, 25: 3540–3556.Google Scholar
Carbone, L., Harris, R.A., Gnerre, S., et al. (2014). Gibbon genome and the fast karyotype evolution of small apes. Nature, 513(7517): 195–201.CrossRefGoogle ScholarPubMed
Coltman, D.W., Bancroft, D.R., Robertson, A., et al. (1999). Male reproductive success in a promiscuous mammal: behavioural estimates compared with genetic paternity. Molecular Ecology, 8: 1199–1209.Google Scholar
Constable, J.L., Ashley, M.V., Goodall, J. and Pusey, A.E. (2001). Noninvasive paternity assignment in Gombe chimpanzees. Molecular Ecology, 10(5): 1279–1300.Google Scholar
Crawford, D.C., Akey, D.T. and Nickerson, D.A. (2005). The patterns of natural variation in human genes. Annual Review of Genomics and Human Genetics, 6(1): 287–312.Google Scholar
Daniels, S., Priddy, J. and Walters, J. (2000). Inbreeding in small populations of red-cockaded woodpeckers: insights from a spatially explicit individual-based model. In Young, A. and Clarke, G. (eds.), Genetics, Demography and Viability of Fragmented Populations. Cambridge University Press, Cambridge: 129–148.Google Scholar
Dietz, J., Baker, A. and Ballou, J. (2000). Demographic evidence of inbreeding depression in wild golden lion tamarins. In Young, A. and Clarke, G. (eds.), Genetics, Demography and Viability of Fragmented Populations. Cambridge University Press, Cambridge: 203–212.Google Scholar
Draheim, H.M., Miller, M.P., Baird, P. and Haig, S.M. (2010). Subspecific status and population genetic structure of least terns (Sternula antillarum) inferred by mitochondrial DNA control-region sequences and microsatellite DNA. The Auk, 127(4): 807–819.CrossRefGoogle Scholar
EAZA (European Association for Zoos and Aquaria). (2019). EAZA Population Management Manual: Standards, Procedures and Guidelines for Population Management within EAZA. EAZA, Amsterdam. Available at www.eaza.net/assets/Uploads/Governing-documents/EAZA-Population-Management-Manual-V2.1-FINAL.pdfGoogle Scholar
Ellegren, H. (2004). Microsatellites: simple sequences with complex evolution. Nature Reviews Genetics, 5(6): 435–445.Google Scholar
Field, D. (1998). Paternity determination in captive lowland gorillas and orangutans and wild mountain gorillas by microsatellite analysis. Primates, 39(2): 199–209.Google Scholar
Frankel, O., Brown, A. and Burdon, J. (1981). Conservation and Evolution. Cambridge University Press, Cambridge.Google Scholar
Frankham, R. (1996). Relationship of genetic variation to population size in wildlife. Conservation Biology, 10(6): 1500–1508.CrossRefGoogle Scholar
Frankham, R. (2005). Genetics and extinction. Biological Conservation, 126: 131–140.Google Scholar
Frankham, R., Ballou, J.D. and Briscoe, D.A. (2010). Introduction to Conservation Genetics, 2nd ed. Cambridge University Press, Cambridge.Google Scholar
Geissmann, T. (1991). Reassessment of the age of sexual maturity in gibbons. American Journal of Primatology, 22: 11–22.Google Scholar
Griffith, S.C., Owens, I.P.F. and Thuman, K.A. (2002). Extra pair paternity in birds: a review of interspecific variation and adaptive function. Molecular Ecology, 11: 2195–2212.Google Scholar
Grueber, C.E., Laws, R.J., Nakagawa, S. and Jamieson, I.G. (2010). Inbreeding depression accumulation across life-history stages of the endangered takahe. Conservation Biology, 24(6): 1617–1625.Google Scholar
Gutiérrez-Espeleta, G., Kalinowski, S. and Hedrick, P. (2000). Genetic population structure in desert bighorn sheep: implications for conservation in Arizona. In Young, A. and Clarke, G. (eds.), Genetics, Demography and Viability of Fragmented Populations. Cambridge University Press, Cambridge: 227–236.Google Scholar
Hedrick, P.W. and Fredrickson, R. (2010). Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conservation Genetics, 11(2): 615–626.Google Scholar
Hof, A.E.V.T., Campagne, P., Rigden, D.J., et al. (2016). The industrial melanism mutation in British peppered moths is a transposable element. Nature, 534(7605): 102–105.Google Scholar
Hosey, G., Melfi, V. and Pankhurst, S. (2009). Zoo Animals. Oxford University Press, New York.Google Scholar
Hu, N., Joseph, O., Huang, B., He, K. and Jiang, X. (2014). Isolation and characterization of thirteen microsatellite loci for the western black crested gibbon (Nomascus concolor) by high-throughput sequencing. Conservation Genetics Resources, 6(1): 179–181.CrossRefGoogle Scholar
Hu, N., Guan, Z., Huang, B., et al. (2018). Dispersal and female philopatry in a long-term, stable, polygynous gibbon population: evidence from 16 years field observation and genetics. American Journal of Primatology, 80(9): 1–12.Google Scholar
Hynes, E.F., Rudd, C.D., Temple-Smith, P.D., et al. (2005) Mating sequence, dominance and paternity success in captive male tammar wallabies. Reproduction, 130(1): 123–130.CrossRefGoogle ScholarPubMed
IUCN (International Union for Conservation of Nature). (2020). The IUCN Red List of Threatened Species. Version 2020-2. Available at www.iucnredlist.orgGoogle Scholar
Janse, M., Kappe, A.L. and Van Kuijk, B.L.M. (2013). Paternity testing using the poisonous sting in captive white-spotted eagle rays Aetobatus narinari: a non-invasive tool for captive sustainability programmes. Journal of Fish Biology, 82(3): 1082–1085.CrossRefGoogle ScholarPubMed
Jobling, M.A. and Gill, P. (2004). Encoded evidence: DNA in forensic analysis. Nature Reviews Genetics, 5(10): 739–751.Google Scholar
Johnson, R.N. (2010). The use of DNA identification in prosecuting wildlife-traffickers in Australia: do the penalties fit the crimes? Forensic Science, Medicine and Pathology, 6(3): 211–216.Google Scholar
Kanthaswamy, S., von Dollen, A., Kurushima, J.D., et al. (2006). Microsatellite markers for standardized genetic management of captive colonies of rhesus macaques (Macaca mulatta). American Journal of Primatology, 68: 73–95.Google Scholar
Karolchik, D., Hinrichs, A.S., Furey, T.S., et al. (2004). The UCSC Table Browser data retrieval tool. Nucleic Acids Research, 32(Database issue): D493–D496.Google Scholar
Kent, W.J., Sugnet, C.W., Furey, T.S., et al. (2002). The human genome browser at UCSC. Genome Research, 12: 996–1006.CrossRefGoogle ScholarPubMed
Kettlewell, H. (1973). The Evolution of Melanism. Clarendon Press, Oxford.Google Scholar
Koljonen, M.-L., Tahtinen, J., Saisa, M. and Koskiniemi, J. (2002). Maintenance of genetic diversity of Atlantic salmon (Salmo salar) by captive breeding programmes and the geographic distribution of microsatellite variation. Aquaculture, 212: 69–92.Google Scholar
Lai, Y. and Sun, F. (2003). The relationship between microsatellite slippage mutation rate and the number of repeat units. Molecular Biology and Evolution, 20(12): 2123–2131.Google Scholar
McNeely, J., Miller, K., Reid, W.V., Mittermeier, R.A. and Werner, T.B. (1990). Conserving the World’s Biological Diversity. IUCN and World Resources Institute, Gland, Switzerland and Washington, DC.Google Scholar
Madsen, T., Stille, B. and Shine, R. (1996). Inbreeding depression in an isolated population of adders Vipera berus. Biological Conservation, 75(2): 113–118.CrossRefGoogle Scholar
Mittermeier, R., Rylands, A. and Wilson, D. (eds.) (2013) Handbook of the Mammals of the World, Vol. 3. Primates. Lynx Edicions, Barcelona.Google Scholar
Monckton, D.G. and Jeffreys, A.J. (1993). DNA profiling. Current Opinion in Biotechnology, 4: 660–664.Google Scholar
Montgomery, M.E., Ballou, J.D., Nurthen, R.K., et al. (1997). Minimizing kinship in captive breeding programs. Zoo Biology, 16: 377–389.3.0.CO;2-7>CrossRefGoogle Scholar
Moore, J.A., Nelson, N.J., Keall, S.N. and Daugherty, C.H. (2008). Implications of social dominance and multiple paternity for the genetic diversity of a captive-bred reptile population (tuatara). Conservation Genetics, 9(5): 1243–1251.Google Scholar
Mucci, N., Mengoni, C. and Randi, E. (2014). Wildlife DNA forensics against crime: resolution of a case of tortoise theft. Forensic Science International: Genetics, 8(1): 200–202.Google Scholar
Oka, T. and Takenaka, O. (2001). Wild gibbons’ parentage tested by non-invasive DNA sampling and PCR-amplified polymorphic microsatellites. Primates, 42(1): 67–73.Google Scholar
Queller, D.C., Strassmann, J.E. and Hughes, C.R. (1993). Microsatellites and kinship. Trends in Ecology and Evolution, 8(8): 285–288.Google Scholar
Reed, D.H. and Frankham, R. (2003). Correlation between fitness and genetic diversity. Conservation Biology, 17(1): 230–237.Google Scholar
Roelke, M.E., Martenson, J.S. and O’Brien, S.J. (1993). The consequences of demographic reduction and genetic depletion in the endangered Florida panther. Current Biology, 3(6): 340–350.Google Scholar
Roode, J. de (2007). The moths of war. New Scientist, 196(2633): 46–49.Google Scholar
Rooney, A.P., Merritt, D.B. and Derr, J.N. (1999). Microsatellite diversity in captive bottlenose dolphins (Tursiops truncatus). Journal of Heredity, 90(1): 228–231.Google Scholar
Rubidge, E.M., Patton, J.L., Lim, M., et al. (2012). Climate-induced range contraction drives genetic erosion in an alpine mammal. Nature Climate Change, 2(4): 285–288.Google Scholar
Sacchei, I., Kuussaari, M., Kankare, M., et al. (1998). Inbreeding and extinction in a butterfly metapopulation. Nature, 392: 491–494.Google Scholar
Saiki, R.K., Scharf, S., Faloona, F., et al. (1985). Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science, 230(4732): 1350–1354.Google Scholar
Sakaoka, K., Suzuki, I., Kasugai, N. and Fukumoto, Y. (2014). Paternity testing using microsatellite DNA markers in captive Adélie penguins (Pygoscelis adeliae). Zoo Biology, 33(5): 463–470.CrossRefGoogle ScholarPubMed
Sanger, F., Nicklen, S. and Couldson, A.R. (1977). DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences USA, 74(12): 5463–5467.Google Scholar
Selkoe, K.A. and Toonen, R.J. (2006). Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology Letters, 9(5): 615–629.Google Scholar
Shen, F., Zhang, Z., He, W., et al. (2009). Microsatellite variability reveals the necessity for genetic input from wild giant pandas (Ailuropoda melanoleuca) into the captive population. Molecular Ecology, 18: 1061–1070.Google Scholar
Sherwin, W. and Moritz, C. (2000). Managing and monitoring genetic erosion. In Young, A. and Clarke, G. (eds.), Genetics, Demography and Viability of Fragmented Populations. Cambridge University Press, Cambridge: 9–34.Google Scholar
Sinclair-Winters, C., Moler, P.E. and Berish, J.D. (2017). Microsatellite assessment of Gopherus polyphemus populations in the Florida Panhandle. Florida Scientist, 80(4): 151–158.Google Scholar
Smit, A., Hubley, R. and Green, P. (2013–2015). RepeatMasker Open-4.0. Available at www.repeatmasker.orgGoogle Scholar
Smith, L.M., Sanders, J.Z., Kaiser, R.J., et al. (1986). Fluorescence detection in automated DNA sequence analysis. Nature, 321(6071): 674–679.Google Scholar
Soule, M., Gilpin, M., Conway, W. and Foose, T. (1986). The Millenium Ark: how long a voyage, how many staterooms, how many passengers? Zoo Biology, 5: 101–113.Google Scholar
Srikwan, S. and Woodruff, D.S. (2000). Genetic erosion in isolated small-mammal populations following rainforest fragmentation. In Young, A. and Clarke, G. (eds.), Genetics, Demography and Viability of Fragmented Populations. Cambridge University Press, Cambridge: 149–172.Google Scholar
Takenaka, O., Kawamoto, S., Udono, T., et al. (1993). Chimpanzee microsatellite PCR primers applied to paternity testing in a captive colony. Primates, 34(3): 357–363.Google Scholar
Tautz, D. (1989). Hypervariability of simple sequences as a general source for polymorphic DNA markers. Nucleic Acids Research, 17(16): 6463–6471.Google Scholar
Tautz, D. and Renz, M. (1984). Simple sequences are ubiquitous repetitive components of eukaryotic genomes. Nucleic Acids Research, 12(10): 4127–4138.Google Scholar
Udupa, S.M. and Baum, M. (2001). High mutation rate and mutational bias at (TAA)n microsatellite loci in chickpea (Cicer arietinum L.). Molecular Genetics and Genomics, 265(6): 1097–1103.Google Scholar
Wang, X. and Wang, L. (2016). GMATA: an integrated software package for genome-scale SSR mining, marker development and viewing. Frontiers in Plant Science, 7: 1350.Google Scholar
Wasser, S.K., Shedlock, A.M., Comstock, K., et al. (2004). Assigning African elephant DNA to geographic region of origin: applications to the ivory trade. Proceedings of the National Academy of Sciences USA, 101(41): 14847–14852.Google Scholar
Webster, M.S. and Reichart, L. (2005). Use of microsatellites for parentage and kinship analyses in animals. Methods in Enzymology, 395: 222–238.Google Scholar
Witzenberger, K.A. and Hochkirch, A. (2011). Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodiversity and Conservation, 20(9): 1843–1861.Google Scholar
Zhang, Y.-P., Ryder, O., Zhao, Q.-G., et al. (1994). Non-invasive giant panda paternity exclusion. Zoo Biology, 13(6): 569–573.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×