Population structure and phylogenetic analysis of laboratory rabbits in Taiwan based on microsatellite markers

Authors

  • Fang-Yu Lai National Taiwan University
  • Shih-Torng Ding National Taiwan University
  • Po-An Tu National Taiwan University
  • R.S. Chen Council of Agriculture, Executive Yuan
  • Der-Yuh Lin Council of Agriculture, Executive Yuan
  • En-Cheng Lin National Taiwan University
  • Pei-Hwa Wang National Taiwan University

DOI:

https://doi.org/10.4995/wrs.2018.7362

Keywords:

genetic monitoring, laboratory rabbit, microsatellite markers, phylogenetic analysis

Abstract

Laboratory rabbits used in Taiwan are primarily supplied by the Livestock Research Institute (LRI) and the Animal Drugs Inspection Branch (ADIB) of the Animal Health Research Institute. An analysis of the genetic characteristics and structure of these populations would thus be a fundamental step in building a long-term management programme for maintaining stable animal quality and preserving the genetic variation among the populations. In this study, DNA samples were isolated from founders of 5 populations: New Zealand White rabbits (NZW) and Japanese White rabbits (JPN) from the ADIB, NZW and Rex rabbits (REX) from the LRI, and NZW from a private rabbit breeding farm in Ban Ciao (BC). A set of microsatellite markers, 18 in total, was designed for genetic analysis. The average values for the allele number (Na), effective number of alleles (Ne), observed heterozygosity (Ho), expected heterozygosity (HE), and Wright’s fixation index (FIS) were 5.50, 2.437, 0.442, 0.568 and 0.232, respectively. These results revealed that this set of microsatellite markers has high diversity and that the major local populations have a tendency toward inbreeding. At the same time, analysis of molecular variance results showed that the laboratory rabbits used in Taiwan have maintained a high level of within-population genetic differentiation (83%). The genetic differentiation among clusters was moderate (FST=0.18), and Bayesian cluster analysis showed that the most likely number of groups was 4 (K=4). Principal component analysis (PCA) also showed 4 divergent clusters. The LRI and BC NZW populations were not separated when K=4 was used in a Structure software analysis and were also hard to split until principal component 3 in PCA. The individual unrooted phylogenetic tree showed that the 5 populations were separated, except that some individuals from the LRI NZW population overlapped with the ADIB NZW and BC NZW populations. As such, in order to counteract the reduced FIS (0.232) and maximise heterozygosity, the 3 NZW populations could be interbred or have new genes introduced into them. The set of microsatellite markers used herein was useful for studying the relationships and genetic diversities among these rabbit populations of Taiwan. Based on the resulting data, rabbit farms in Taiwan could select parental stocks for planned mating in the future as part of strategies to preserve and restore the rational breeding of laboratory rabbits.

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Author Biographies

Fang-Yu Lai, National Taiwan University

Department of Animal Science and Technology, College of Bioresources and Agriculture

Shih-Torng Ding, National Taiwan University

Department of Animal Science and Technology, College of Bioresources and Agriculture

Po-An Tu, National Taiwan University

Department of Animal Science and Technology, College of Bioresources and Agriculture, National Taiwan University

-------

Hsinchu Branch, Livestock Research Institute, Council of Agriculture, Executive Yuan

R.S. Chen, Council of Agriculture, Executive Yuan

Animal Drugs Inspection Branch, Animal Health Research Institute

Der-Yuh Lin, Council of Agriculture, Executive Yuan

Division of Animal Breeding and Genetics Division, Livestock Research Institute

En-Cheng Lin, National Taiwan University

Department of Animal Science and Technology, College of Bioresources and Agriculture

Pei-Hwa Wang, National Taiwan University

Department of Animal Science and Technology, College of Bioresources and Agriculture

References

Alves J.M., Carneiro M., Afonso S., Lopes S., Garreau H., Boucher S., Allain D., Queney G., Esteves P.J., Bolet G., Ferrand N. 2015. Levels and patterns of genetic diversity and population structure in domestic rabbits. PLoS ONE, 10: e0144687. https://doi.org/10.1371/journal.pone.0144687

Barker J.S.F. 1994. A global protocol for determining genetic distances among domestic livestock breeds. In Proc.: 5th World Congress Genet. Appl Livest. Prod., Guelph, Canada, 21: 501-508.

Ben Larbi M., San-Cristobal M., Chantry-Darmon C., Bolet G. 2014. Population structure in Tunisian indigenous rabbit ascertained using molecular information. World Rabbit Sci., 22: 223-230. https://doi.org/10.4995/wrs.2014.1468

Benavides F., Glasscock E, Coghlan L.G., Stern M.C., Weiss D.A., Conti C,J. PCR-based microsatellite analysis for differentiation and genetic monitoringof nine inbred SENCAR mouse strains. Lab. Anim., 35: 157-162. https://doi.org/10.1258/0023677011911534

Bowcock A.M., Ruiz-Linares A., Tomfohrde J., Minch E., Kidd J.R., Cavalli-Sforza L.L. 1994. High resolution of human evolutionary trees with polymeric microsatellites. Nature, 268: 455-457. https://doi.org/10.1038/368455a0

Chang H.L., Huang C.T., Wu M.C. 1998. Rabbit breed genotype glucose phosphate isomerase 6-phosphogluconate dehydrogenase. J. Taiwan Livest. Res., 31: 43-51.

Chantry-Darmon C., Urien C., Hayes H., Bertaud M., Chadi-Taourit S., Chardon P., Vaiman D., Rogel-Gaillard C. 2005. Construction of a cytogenetically anchored microsatellite map in rabbit. Mamm. Genome., 16: 442-459. https://doi.org/10.1007/s00335-005-2471-z

Chia R., Achilli F., Festing M.F.W., Fisher E.M.C. 2005. The origins and uses of mouse outbred stocks. Nat. Genet., 37: 1181-1186. https://doi.org/10.1038/ng1665

Dieringer D., Schlotterer C. 2003. Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol. Ecol., 3: 167-169. https://doi.org/10.1046/j.1471-8286.2003.00351.x

Druml T., Curik I., Baumung R., Aberle K., Distl O., Sölkner J. 2007. Individual-based assessment of population structure and admixture in Austrian, Croatian and German draught horses. Heredity, 98: 114-122. https://doi.org/10.1038/sj.hdy.6800910

Duchesne P., Turgeon J. 2012. FLOCK provides reliable solution to the “number of population” problem. J. Hered., 103: 734-743. https://doi.org/10.1093/jhered/ess038

Emam A., Azoz A., Mehaisen G., Ferrand N., Ahmed N. 2017. Diversity assessment among native Middle Egypt rabbit populations in North Upper-Egypt province by microsatellite polymorphism. World Rabbit Sci., 25: 9-16. https://doi.org/10.4995/wrs.2017.5298

Evanno G.G., Regnaut S.S., Goudet J.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

Excoffier L., Lischer H.E.L. 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

Fahey J.R., Katos H., Malcolm R., Perez A.V. 2013. The case for genetic monitoring of mice and rats used on biomedical research. Mamm. Genome, 24: 89-94. https://doi.org/10.1007/s00335-012-9444-9

Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39:783-791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x

Felsenstein, J. 2002. Phylogeny Inference Package (PHYLIP). Genomes scuences, Department of Genetics, Washington Univ., Seattle, WA. Software available http://evolution.gs.washington.edu/phylip.html

Fukuta K., Nagura Y., Harada M., Goto N. 1996. Analysis of Mandible of newly developing strain of Japanese White rabbit (Nlb:JWNS). Exp. Anim., 45: 361-368. https://doi.org/10.1538/expanim.45.361

Goldstein D., Schlötterer C. 1999. Microsatellites: evolution and applications. Oxford Univ. Press Oxford.

Grimal A., Safaa H.M., Saenz-de-Juano M.D., Viudes-de-Castro M.P., Mehaisen G.M.K., Elsayed D.A.A., Lavara R., Marco-Jimenez F., Vicente J.S. 2012. Phytogenetic relationship among 4 Egyptian and one Spanish rabbit populations based on microsatellite markers. In Proc.:10th World Rabbit Cong., 3-6 September, 2012, Sharm El- Sheikh, Egypt, 177-181.

Kalinowski S.T. 2005. HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol. Ecol. Notes, 5: 187-189. https://doi.org/10.1111/j.1471-8286.2004.00845.x

Korstanje R., Gillissen G.F., Versteeg S.A., van Oost B.A., Bosma A.A., Rogel-Gaillard C., van Zutphen L.F.M., van Lith H.A. 2003. Mapping of rabbit microsatellite markers using chromosome-specific libraries. J. Hered., 94: 161-169. https://doi.org/10.1093/jhered/esg016

Lacy R.C. 1995. Clarification of genetic terms and their use in the management of captive populations. Zoo Biol. 14: 565-577. https://doi.org/10.1002/zoo.1430140609

Mougel C., Mounolou J.-C., Monnerot M. 1997. Nine polymorphic microsatellite loci in the rabbit, Ocryctolagus cuniculus. Amin. Genet., 28: 58-59. https://doi.org/10.1111/j.1365-2052.1997.00047.x

Moreno V.R., Grisolia A.B., Campagnari F., Milazzotto M., Adania C.H., Garcia J.F., de Souza E.B. 2006. Genetic variability of Herpailurus yagouaroundi, Puma concolor and Panthera onca (Mammalia, Felidae) studied using Felis catus microsatellites. Genet. Mol. Biol., 29: 290-293. https://doi.org/10.1590/S1415-47572006000200017

O’Connell M.M., Dillon C., Wright J.M. 1998. Development of primers for polymorphic microsatellite loci in the Pacific herring. Mol. Ecol., 7: 357-363.

Olsen J.B., Bentzen P., Seeb J.E. 1998. Characterization of seven microsatellite loci derived from pink salmon. Mol. Ecol., 7: 1083-1090.

O’Reilly P., Wright J.M. 1995. The evolving technology fingerprinting and its application to fisheries an aquaculture. J. Fish Biol., 47: 29-55. https://doi.org/10.1111/j.1095-8649.1995.tb06042.x

Park, S.D.E. 2001. Trypanotolerance in West African cattle and the population genetic effects of selection. Ph. D. Thesis. Trinity College, Dublin Univ., Ireland.

Parker H.G., Kim L.V., Sutter N.B., Carlson S., Lorentzen T.D., Malek T.B., Johnson G.S., DeFrance H.B., Ostrander E.A., Kruglyak L. 2004. Genetic structure of the purebred domestic dog. Science, 304: 1160-1164. https://doi.org/10.1126/science.1097406

Peakall R.R., Smouse P.E.P. 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research - an update. 28: 2537-2549.

Pritchard J.K., Stephens M., Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics, 155 945-959.

Raymond M., Rousset F. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered., 86: 248-249. https://doi.org/10.1093/oxfordjournals.jhered.a111573

Rosenberg N.A., Pritchard J.K., Weber J.L., Cann H.M., Kidd K.K., Zhivotovsky L.A., Feldman M.W. 2002. Genetic structure of human populations. Science, 298: 2381-2385. https://doi.org/10.1126/science.1078311

Rosenberg N.A. 2004. DISTRUCT: a program for the graphical display of population structure. Mol. Ecol. Notes, 4: 137-138. https://doi.org/10.1046/j.1471-8286.2003.00566.x

Saitou N., Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol., 4: 406-425. https://doi.org/10.1093/oxfordjournals.molbev.a040454

Sambrook J., Russell D.W. 2001. Molecular cloning: A Laboratory Manual. 3rd ed. New York: Cold Spring Harbor Laboratory Press. Pp. 6.4-6.12.

Schuelke M. 2000. An economic method for the fluorescent labeling of PCR fragments. Nat. Biotech., 18: 233-234. https://doi.org/10.1038/72708

Surridge A.K., Bell D., Rico J.C., Hewitt G.M. 1997. Polymorphic microsatellite loci in the European rabbit (Oryctolagus cuniculus) are also amplified in other lagomorph species. Amin. Genet., 28: 302-305. https://doi.org/10.1111/j.1365-2052.1997.00137.x

Takezaki N., Nei M. 1996. Genetic distances and reconstruction of phylogenetic tree from microsatellite DNA. Genetics, 144: 389-399.

Toro M.A., Fernández J., Caballero A. 2009. Molecular characterization of breeds and its use in conservation. Liv. Sci., 120: 174-195. https://doi.org/10.1016/j.livsci.2008.07.003

Weir B.S., Cockerham C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38: 1358-1370. https://doi.org/10.1111/j.1558-5646.1984.tb05657.x

Wu T.W., Xu G.J., Pan Y.L., Xie X.P., Li B.C., Wu X.S. 2010. Study on genetic diversity of 7 rabbit population evidenced by microsatellite markers. J. Anim. Vet. Adv., 9: 359-365. https://doi.org/10.1016/j.livsci.2008.07.003

Yeh, S.H., Huang F.F., Liu-Tai J.J., Chang H.L. 1993. The polymorphism of PHI, PGD and Hb in the native breed of domestic animals. J. Chin. Soc. Anim. Sci., 22(Suppl.): 138.

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Published

2018-03-28

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Genetics