Genetic diversity of the critically endangered Blue-crowned laughingthrush (Garrulax courtoisi)

Abstract

To evaluate the genetic quality and provide available management strategies for Blue-crowned laughingthrush (BCLT), fifteen polymorphic microsatellite loci were developed and applied. The genetic diversity of wild individuals was indicated to be higher than the two captive populations. The average number of alleles (5.50 ± 0.317), the number of effective alleles (3.417 ± 0.222), observed heterozygosity (0.828 ± 0.04), and genetic differentiation index (0.028 ± 0.007) of 64 wild individuals showed high genetic diversity despite drastic bottleneck and low genetic differentiation. The number of effective migrants (22.737 ± 8.318) indicated the intriguing wintering grounds may be surrounded by the breeding sites where the syncheimadia occurred in Wuyuan. Efficient conservation, winter flocking, and cooperative breeding may facilitate gene exchange and inclusive fitness. We recommend that monitoring concentrated distribution areas for BCLT should be strengthened, and geographical barriers, interference types, and the inner mechanism of distribution patterns should be further explored.

Keywords

critically endangered / Garrulax courtoisi / genetic diversity / isolation / microsatellite

References

[1] Balloux, F. & Lugon-Moulin, N. (2002) The estimation of population differentiation with microsatellite markers. Molecular Ecology, 11, 155–165. Available from:

[2] BirdLife International. (2018) “Garrulax courtoisi. The IUCN Red List of Threatened Species,” e.T22732350A131890764. Available from: https://www.iucnredlist.org/species/22732350/131890764 [Accessed 7th August 2023]

[3] Botstein, D., White, R.L., Skolnick, M. & Davis, R.W. (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. American Journal of Human Genetics, 32(3), 314–331.

[4] 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 polymorphic microsatellites. Nature, 368(6470), 455–457. Available from:

[5] Chen, G., Zheng, C., Wan, N., Liu, D., Fu, V.W.K., Yang, X. et al. (2019) Low genetic diversity in captive populations of the critically endangered Blue-crowned Laughingthrush (Garrulax courtoisi) revealed by a panel of novel microsatellites. PeerJ, 7, e6643. Available from:

[6] Chen, H., Huang, M., Liu, D., Tang, H., Zheng, S., Ouyang, J. et al. (2022) Genomic signatures and evolutionary history of the endangered blue-crowned laughingthrush and other Garrulax species. BMC Biology, 20, 188. Available from:

[7] Van Dyke, F. (Ed.). (2008) Genetic diversity-understanding conservation at genetic levels. In: Conservation biology: foundations, concepts, applications. Dordrecht: Springer, pp. 153–184.

[8] Earl, D.A. & VonHoldt, B.M. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4(2), 359–361. Available from:

[9] Fu, Y.M., Li, S.P. & Wu, Y.F. (2008) Research technology and advances in Avian conservation genetics. Journal of Hebei Normal University (Natural Science Edition), 32(03), 397–403.

[10] Gao, J.W. (2012) Parentage and genetic diversity studies in Yanbian Captive Black Bear using Microsatellite DNA markers. Yanbian: Yanbian University.

[11] Goudet, J., Raymond, M., Meeüs, T. & Rousset, F. (1996) Testing differentiation in diploid populations. Genetics, 139, 463–471. Available from:

[12] Gu, L., Liu, Y., Wang, N. & ZHANG, Z. (2012) A panel of polymorphic microsatellites in the Blue Eared Pheasant (Crossoptilon auritum) developed by cross-species amplification. Chinese Birds, 3(2), 103–107.

[13] Hartl, D.L. & Clark, A.G. (1997) Principles of population genetics, vol. 116. Sunderland: Sinauer associates.

[14] He, C.H., Zhou, Y., Wang, L.F. & Zhang, L. (2015) Estimating population size and genetic diversity of Asian elephant in the Shangyong Nature Reserve. Biodiversity, 23(2), 202–209. Available from:

[15] He, F.Q., Lin, J.S. & Wen, C. (2017) Prelim of biology of the Blue-crowned Laughingthrush Garrulax courtoisi in Wuyuan of NE Jiangxi, SE China. Chinese Journal of Zoology, 52(01), 167–175.

[16] Hou, X., Zaks, T., Langer, R. & Dong, Y. (2021) Lipid nanoparticles for mRNA delivery. Nature Reviews Materials, 6(12), 1078–1094.

[17] Huang, H.Q. (2016) Study on habitat selection and influence factors of the Blue-crowned Laughingthrush (Garrulax courtoisi). Harbin: Northeast Forestry University.

[18] Huang, J., Li, Y.Z., Li, P., Yue, H., Zhang, X.Y., Li, X.-X. et al. (2013) Genetic quality of the Miyaluo captive forest musk deer (Moschus berezovskii) population as assessed by microsatellite loci. Biochemical Systematics & Ecology, 47, 25–30. Available from:

[19] Kalinowski, S.T., Taper, M.L. & Marshall, T.C. (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology, 16(5), 1099–1106. Available from:

[20] Kong, J., Jiang, X.H., Zhou, Z., Zhang, Z., Zhou, L. & Li, D. (2016) Development of microsatellite in Cranoglanis bouderius by magnetic beads. Guizhou Agricultural Sciences, 44(07), 14–17.

[21] Liao, W.M., Hong, Y.H., Yu, X.X., Ouyang, X.Z. & He, G.X. (2007) A study on the propagation habitat of Garrulax galbanus courtoisi and the relationship of the birds with village forests in Wuyuan, Jiangxi Province. Journal of Jiangxi Agricultural University, 29(05), 837–841.

[22] Liu, T., Wu, Z.Y., Liu, B., Zhang, W.W. & Shi, J.Z. (2017) Study on the activity rhythm and time budget of captive Garrulax courtoisi. Sichuan Journal of Animal Science, 36(06), 674–679. Available from:

[23] Liu, T., Xu, Y., Mo, B., Shi, J., Cheng, Y., Zhang, W. et al. (2020) Home range size and habitat use of the blue-crowned laughingthrush during the breeding season. PeerJ, 8, e8785. Available from:

[24] Liu, T., Xu, Y.T., Xia, C.W., Edwards, D., Hu, X.L., Su, Y.Y. et al. (2022) Multiple lines of evidence confirm that the critically endangered Blue-crowned Laughingthrush (Garrulax courtoisi) is an independent species. Avian Research, 13(3), 9. Available from:

[25] Liu, X.H. (2014) ISSR Analysis of the Syrmaticus humiae genetic diversity and genetic relationship. Nanning: Guangxi Normal University.

[26] Luikart, G. & Cornuet, J.M. (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conservation Biology, 12(1), 228–237. http://www.jstor.org/stable/2387479

[27] Maia, A.K.S., Terto, J., Oliveira, I.F., Nascimento, W.F., Almeida, C. & Silva, E.F. (2022) Genetic diversity and structure of Hancornia speciosa gomes populations characterized by microsatellites markers. Crop Breeding and Applied Biotechnology, 22, e38012228. Available from:

[28] Mohr, F., Betson, M. & Quintard, B. (2017) Investigation of the presence of atoxoplasma spp. in Blue-crowned laughingthrush (Dryonastes courtoisi) adults and neonates. Journal of Zoo and Wildlife Medicine, 48(1), 1–6. Available from:

[29] Piry, S., Luikart, G. & Cornuet, J.M. (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. Journal of Heredity, 90(4), 502–503.

[30] Di Rienzo, A., Peterson, A.C., Garza, J.C., Valdes, A.M., Slatkin, M. & Freimer, N.B. (1994) Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Sciences, 91(8), 3166–3170.

[31] Rosenberg, N.A. (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes, 4(1), 137–138. Available from:

[32] Shi, J.Z., Wu, Z.Y., Liu, T., Weiwei, Z. & Dechang, N. (2017) Feeding habits of captive Blue-crowned laughingthrush (Garrulax courtoisi). Chinese Journal of Wildlife, 38(04), 617–621. Available from:

[33] Su, Y., Long, R., Chen, G., Wu, X., Xie, K. & Wan, J. (2007) Genetic analysis of six endangered local duck populations in China based on microsatellite markers. Journal of Genetics and Genomics, 34(11), 1010–1018. Available from:

[34] Wan, Q.H., Wu, H., Fujihara, T. & Fang, S.G. (2004) Which genetic marker for which conservation genetics issue. Electrophoresis, 25, 2165–2176. Available from:

[35] Wang, C., Li, J., Cheng, Y., Tang, H., Xiong, Y., Wu, Y. et al. (2022) Investigation on the characteristics of gut microbiota in critically endangered blue-crowned laughingthrush (Garrulax courtoisi). Molecular Genetics and Genomics: MGG, 297, 655–670. Available from:

[36] Wang, L.Y. (2011) Mining and application of molecular markers from EST database and transcriptome sequencing in Tea plant (Camellia sinensis). Chinese Academy of Agricultural Sciences.

[37] Wilkinson, R., He, F.Q., Gardner, L. & Wirth, R. (2004) A highly threatened bird-Chinese Yellow-throated Laughing thrushes in China and in zoos. International Zoo News, 51, 456–469.

[38] Willoughby, J.R., Fernandez, N.B., Lamb, M.C., Ivy, J.A., Lacy, R.C. & DeWoody, J.A. (2015) The impacts of inbreeding, drift and selection on genetic diversity in captive breeding populations. Molecular Ecology, 24(1), 98–110.

[39] Xu, Y., Hu, Z., Li, W., Zeng, T., Zhang, X., Li, J. et al. (2019) Isolation and strategies of novel tetranucleotide microsatellites with polymorphisms from different chromosomes of the rhesus monkey (Macaca mulatta). Molecular Biology Reports, 46(4), 3955–3966.

[40] Xu, Y., Hu, Z., Wang, C., Zhang, X., Li, J. & Yue, B. (2016) Characterization of perfect microsatellite based on genome-wide and chromosome level in Rhesus monkey (Macaca mulatta). Gene, 592(2), 269–275. Available from:

[41] Xu, Y., Li, W., Hu, Z., Zeng, T., Shen, Y., Liu, S. et al. (2018) Genome-wide mining of perfect microsatellites and tetranucleotide orthologous microsatellites estimates in six primate species. Gene, 643, 124–132. Available from:

[42] Yan, Q.L., Zhai, H.J. & Liu, C. (2009) Development and application of EST-SSR markers in the research of animal. China animal husbandry and veterinary medicine, 36(07), 102–105.

[43] Zhang, Y.D. (2004) Study on DNA polymorphism in artificially reared Nipponia nippon. Northwest Agriculture & Forestry University.

[44] Zhao, Y.H., Ou, Y.J., Wen, J.F., Li, J. & Zhou, H. (2019) Development of SSR markers in Bahaba flavolabiata by transcriptome sequencing. Journal of Southern Agriculture, 50(09), 2078–2087.

[45] Zhu, J.K. (2000) Genetic analysis of plant salt tolerance using arabidopsis. Plant Physiology, 124(3), 941–948.

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2024 The Author(s). Wildlife Letters published by Northeast Forestry University and John Wiley & Sons Australia, Ltd.