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Nuclear and Mitochondrial DNA Suggest That Nature Reserve Maintains Novel Haplotypes and Genetic Diversity of Honeybees (Apis cerana)

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Abstract

Declining wild honeybee (Apis) resources could cause the extinction of symbiotic relationships between plants and honeybees, reducing food production. Therefore, the protection of genetic resources and the diversity of wild honeybees are crucial. This study examined the honeybees in a plant nature reserve (Leigongshan) to better understand their genetic status in a purely natural state and explored the potential role of this plant nature reserve on pollinators. Nuclear (15 microsatellites) and mitochondrial markers (tRNAleu ~ COII and COI) were used to investigate the genetic resources and diversity of eastern honeybees (Apis cerana). Here, 31 new honeybee haplotypes were discovered from the inside and outside regions of the reserve. The honeybees showed a high genetic diversity level (He: 0.6564 ± 0.1594, Na: 3–18, PIC: 0.6191 ± 0.1718, Hd in tRNAleu ~ COII: 0.6797, Hd in COI: 0.8103), and no apparent genetic differentiation was observed between the two regions. Thus, we speculate that Leigongshan Nature Reserve protects honeybees from human disturbance and prevents a decline in their population size, preserving the honeybee genetic resources and high genetic diversity level. Furthermore, our results have revealed the practical function of the plant nature reserve on honeybee genetic resources, which explains the decreasing honeybee resources.

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REFERENCES

  1. Klein, A.-M., Vaissière, B.E., Cane, J.H., et al., Importance of pollinators in changing landscapes for world crops, Proc. R. Soc. London, Ser. B, 2006, vol. 274, no. 1608, pp. 303—313. https://doi.org/10.1098/rspb.2006.3721

    Article  Google Scholar 

  2. Kasina, J.M., Mburu, J., Kraemer, M. and Holm-Mueller, K., Economic benefit of crop pollination by bees: a case of Kakamega small-holder farming in Western Kenya, J. Econ. Entomol., 2009, vol. 102, no. 2, pp. 467—473. https://doi.org/10.1603/029.102.0201

    Article  CAS  Google Scholar 

  3. Roubik, D.W., The value of bees to the coffee harvest, Nature, 2002, vol. 417, no. 6890, p. 708. https://doi.org/10.1038/417708a

    Article  CAS  Google Scholar 

  4. Ollerton, J., Winfree, R. and Tarrant, S., How many flowering plants are pollinated by animals?, Oikos, 2011, vol. 120, no. 3, pp. 321—326. https://doi.org/10.1111/j.1600-0706.2010.18644.x

    Article  Google Scholar 

  5. Ilyasov, R.A., Lee, M.L., Yunusbaev, U., et al., Estimation of C-derived introgression into A. m. mellifera colonies in the Russian Urals using microsatellite genotyping, Genes Genomics, 2020, vol. 42, no. 9, pp. 987—996. https://doi.org/10.1007/s13258-020-00966-0

    Article  CAS  Google Scholar 

  6. Ilyasov, R.A., Poskryakov, A.V., Petukhov, A.V. and Nikolenko, A.G., Molecular genetic analysis of five extant reserves of black honeybee Apis melifera melifera in the Urals and the Volga region, Genetika, 2016, vol. 52, no. 8, pp. 828—839. https://doi.org/10.1134/s1022795416060053

    Article  CAS  Google Scholar 

  7. De la Rúa, P., Jaffé, R., Dall’Olio, R., et al., Biodiversity, conservation and current threats to European honeybees, Apidologie, 2009, vol. 40, no. 3, pp. 263—284. https://doi.org/10.1051/apido/2009027

    Article  Google Scholar 

  8. Neumann, P. and Carreck, N.L., Honey bee colony losses, J. Apic. Res., 2010, vol. 49, no. 1, pp. 1—6. https://doi.org/10.3896/IBRA.1.49.1.01

    Article  Google Scholar 

  9. Oldroyd, B.P. and Nanork, P., Conservation of Asian honey bees, Apidologie, 2009, vol. 40, no. 3, pp. 296—312. https://doi.org/10.1051/apido/2009021

    Article  Google Scholar 

  10. Xie, Z.G., Li, L., Pan, H.Y. and Zhang, Y.L., The biodiversity of Leigongshan National Nature Reserve and its protection measures, Mod. Agric. Sci., 2009, vol. 16, no. 5, pp. 167—167. https://doi.org/CNKI:SUN:NCSY.0.2009-05-073

  11. Carvalheiro, L.G., Seymour, C.L., Veldtman, R., and Nicolson, S.W., Pollination services decline with distance from natural habitat even in biodiversity-rich areas, J. Appl. Ecol., 2010, vol. 47, no. 4, pp. 810—820. https://doi.org/10.1111/j.1365-2664.2010.01829.x

    Article  Google Scholar 

  12. Fründ, J., Dormann, C.F., Holzschuh, A., and Tscharntke, T., Bee diversity effects on pollination depend on functional complementarity and niche shifts, Ecology, 2013, vol. 94, no. 9, pp. 2042—2054. https://doi.org/10.1890/12-1620.1

    Article  Google Scholar 

  13. Gaines, S.D., White, C., Carr, M.H., and Palumbi, S.R., Designing marine reserve networks for both conservation and fisheries management, Proc. Natl. Acad. Sci. U. S. A., 2010, vol. 107, no. 43, pp. 18286—18293. https://doi.org/10.1073/pnas.0906473107

    Article  Google Scholar 

  14. Schoville, S.D., Dalongeville, A., Viennois, G., et al., Preserving genetic connectivity in the European Alps protected area network, Biol. Conserv., 2018, vol. 218, no. 1, pp. 99—109. https://doi.org/10.1016/j.biocon.2017.12.017

    Article  Google Scholar 

  15. Yang, J.D., Zhang, Z.H., Shen, F.J., et al., Microsatellite variability reveals high genetic diversity and low genetic differentiation in a critical giant panda population, Curr. Zool., 2011, vol. 57, no. 6, pp. 717—724. https://doi.org/10.1093/czoolo/57.6.717

    Article  Google Scholar 

  16. Garnery, L., Cornuet, J.M., and Solignac, M., Evolutionary history of the honey bee Apis mellifera inferred from mitochondrial DNA analysis, Mol. Ecol., 1992, vol. 1, no. 3, pp. 145—154. https://doi.org/10.1111/j.1365-294X.1992.tb00170.x

    Article  CAS  Google Scholar 

  17. Zhao, W.Z., Tan, K., Zhou, D.Y., et al., Phylogeographic analysis of Apis cerana populations on Hainan Island and southern mainland China, based on mitochondrial DNA sequences, Apidologie, 2014, vol. 45, pp. 21—33. https://doi.org/10.1007/s13592-013-0223-8

  18. Yu, Y., Zhou, S., Zhu, X., et al., Genetic differentiation of eastern honey bee (Apis cerana) populations across Qinghai—Tibet Plateau-Valley landforms, Front. Genet., 2019, vol. 10, no. 483, pp. 1—11. https://doi.org/10.3389/fgene.2019.00483

    Article  CAS  Google Scholar 

  19. Larkin, M.A., Blackshields, G., Brown, N.P., et al., Clustal W and Clustal X version 2.0, Bioinformatics, 2007, vol. 23, no. 21, pp. 2947—2948. https://doi.org/10.1093/bioinformatics/btm404

    Article  CAS  Google Scholar 

  20. Librado, P. and Rozas, J., DnaSP v5: a software for comprehensive analysis of DNA polymorphism data, Bioinformatics, 2009, vol. 25, no. 11, pp. 1451—1452. https://doi.org/10.1093/bioinformatics/btp187

    Article  CAS  Google Scholar 

  21. Fu, Y.X., Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection, Genetics, 1997, vol. 147, no. 2, pp. 915—925. https://doi.org/10.1017/S0016672397002966

    Article  CAS  Google Scholar 

  22. Tajima, F., Statistical method for testing the neutral mutation hypothesis by DNA polymorphism, Genetics, 1989, vol. 123, no. 3, pp. 585—595. https://doi.org/10.1101/gad.3.11.1801

    Article  CAS  Google Scholar 

  23. Excoffier, L. and Lischer, H.E., Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows, Mol. Ecol. Resour., 2010, vol. 10, no. 3, pp. 564—567. https://doi.org/10.1111/j.1755-0998.2010.02847.x

    Article  Google Scholar 

  24. Kumar, S., Stecher, G., and Tamura, K., MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets, Mol. Biol. Evol., 2016, vol. 33, no. 7, pp. 1870—1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  Google Scholar 

  25. Li, B., Lai, K., Xian, F.H., et al., Genetic diversity of Apis cerana cerana based on mitochondrial DNA in Tangjiahe National Nature Reserve, Sichuan, China, J. Sichuan Agric. Univ., 2018, vol. 36, no. 3, pp. 386—391. https://doi.org/10.16036/j.issn.1000-2650.2018.03.017

    Article  Google Scholar 

  26. Peakall, R. and Smouse, P.E., GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update, Bioinformatics, 2012, vol. 28, no. 19, pp. 2537—2539. https://doi.org/10.1093/bioinformatics/bts460

    Article  CAS  Google Scholar 

  27. Park, S., Trypanotolerance in West African Cattle and the Population Genetic Effects of Selection, Dublin: University of Dublin. 2001.

  28. Do, C., Waples, R.S., Peel, D., et al., NEESTIMATOR v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data, Mol. Ecol. Resour., 2014, vol. 14, no. 1, pp. 209—214. https://doi.org/10.1111/1755-0998.12157

    Article  CAS  Google Scholar 

  29. Cornuet, J.M. and Luikart, G., Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data, Genetics, 1996, vol. 144, no. 4, pp. 2001—2014. https://doi.org/10.3892/ijo_00000551

    Article  CAS  Google Scholar 

  30. R-Core-Team, R: A Language and Environment for Statistical Computing, Vienna: R Foundation for Statistical Computing. 2016.

  31. Jakobsson, M. and Rosenberg, N.A., CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure, Bioinformatics, 2007, vol. 23, no. 14, pp. 1801—1806. https://doi.org/10.1093/bioinformatics/btm233

    Article  CAS  Google Scholar 

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

  33. Oleksa, A., Chybicki, I., Tofilski, A. and Burczyk, J., Nuclear and mitochondrial patterns of introgression into native dark bees (Apis mellifera mellifera) in Poland, J. Apic. Res., 2011, vol. 50, no. 2, pp. 116—129. https://doi.org/10.3896/ibra.1.50.2.03

    Article  Google Scholar 

  34. Pentek-Zakar, E., Oleksa, A., Borowik, T., and Kusza, S., Population structure of honey bees in the Carpathian Basin (Hungary) confirms introgression from surrounding subspecies, Ecol. Evol., 2015, vol. 5, no. 23, pp. 5456—5467. https://doi.org/10.1002/ece3.1781

    Article  Google Scholar 

  35. De la Rúa, P., Simon, U., Tilde, A., et al., MtDNA variation in Apis cerana populations from the Philippines, Heredity (Edinburg), 2000, vol. 84, no. 1, pp. 124—130. https://doi.org/10.1046/j.1365-2540.2000.00646.x

    Article  Google Scholar 

  36. Smith, D.R. and Hagen, R.H., The biogeography of Apis cerana as reveal by mitochondrial DNA sequence data, J. Kansas Entomol. Soc., 1996, vol. 69, no. 4, pp. 294—310. https://doi.org/10.1016/S0022-474X(96)00026-4

    Article  Google Scholar 

  37. Takahashi, J.I., Yoshida, T., Takagi, T., et al., Geographic variation in the Japanese islands of Apis cerana japonica and in A. cerana populations bordering its geographic range, Apidologie, 2007, vol. 38, no. 4, pp. 335—340. https://doi.org/10.1051/apido:2007018

    Article  CAS  Google Scholar 

  38. Gong, X.Y., Zhao, W.Z., Zhou, D.Y., et al., Genetic variation and population structure of Apis cerana in northern, central and southern mainland China, based on COXI gene sequences, J. Apic. Res., 2018, vol. 57, no. 3, pp. 364—373. https://doi.org/10.1080/00218839.2018.1454036

    Article  Google Scholar 

  39. Ren, Q., Cao, L.F., Zhao, H.X., et al., Analysis of genetic diversity of main Apis cerana populations in China, J. Henan Agric. Univ., 2018, vol. 52, no. 1, pp. 91—95. https://doi.org/CNKI:SUN:NNXB.0.2018-01-015.

    Google Scholar 

  40. Zhou, S.J., Xu, X.J., Zhu, X.J., et al., Genetic diversity of Apis cerana cerana in Hainan based on mitochondrial DNA., J. Fujian Agric. For. Univ., 2012, vol. 41, no. 2, pp. 170—175. https://doi.org/10.3969/j.issn.1671-5470.2012.02.013

    Article  Google Scholar 

  41. Cao, L.F., Su, X.L., Zhao, D.X., et al., Genetic diversity of microsatellite DNA for Apis cerana cerana in Zhejiang, Apic. China, 2013, vol. 64, no. 2, pp. 10—11. https://doi.org/10.3969/j.issn.0412-4367.2013.02.002

    Article  Google Scholar 

  42. Chen, Y., Zong, C., Yu, L.S., and Ji, T., Study on microsatellite DNA genetic diversity of Apis cerana cerana in Wannan Mountain area and Wangxi Da Bie Mountain area., Apic. China, 2011, vol. 62, no. 10, pp. 8—11. https://doi.org/CNKI:SUN:ZGYF.0.2011-Z4-005

    Google Scholar 

  43. Xu, X.J., Zhou, S.J., Zhu, X.J., and Zhou, B.F., Microsatellite DNA analysis of genetic diversity of Apis cerana cerana in Hainan Island, southern China, Acta Entomol. Sin., 2013, vol. 56, no. 5, pp. 554—560. https://doi.org/10.16380/j.kcxb.2013.05.012

    Article  CAS  Google Scholar 

  44. Xu, X.J., Zhou, S.J., Zhu, X.J., and Zhou, B.F., Microsatellite DNA genetic diversity of Apis cerana cerana from the Loess Plateau, Northwest China, J. Fujian Agric. For. Univ., 2013, vol. 42, no. 6, pp. 638—642. https://doi.org/10.13323/j.cnki.j.fafu(nat.sci.).2013.06.020

    Article  Google Scholar 

  45. Ji, T., Yin, L., and Chen, G.H., Genetic diversity and population structure of Chinese honeybees (Apis cerana) under microsatellite markers, Afr. J. Biotechnol., 2011, vol. 10, no. 9, pp. 1712—1720. https://doi.org/10.5897/AJB10.753

    Article  Google Scholar 

  46. Xie, Z.G., Lan, K.M., and Yang, C.D., Analysis on seed plants in Guizhou Leigongshan National Nature Reserve, For. Resour. Manag., 2010, vol. 1, no. 1, pp. 84—88. https://doi.org/10.3969/j.issn.1002-6622.2010.01.016

    Article  Google Scholar 

  47. Myburgh, A.M. and Daniels, S.R., Exploring the impact of habitat size on phylogeographic patterning in the overberg velvet worm Peripatopsis overbergiensis (Onychophora: Peripatopsidae), J. Hered., 2015, vol. 106, no. 3, pp. 296—305. https://doi.org/10.1093/jhered/esv014

    Article  CAS  Google Scholar 

  48. Nunziata, S.O., Wallenhorst, P., Barrett, M.A., et al., Population and conservation genetics in an endangered lemur, Indri indri, across three forest reserves in Madagascar, Int. J. Primatol., 2016, vol. 37, pp. 688—702. https://doi.org/10.1007/s10764-016-9932-y

    Article  Google Scholar 

  49. Masuda, M., Fukagawa, T., and Nishimura, F., Genetic diversity and genetic structure of an endangered species, Eriocaulon nudicuspe, growing in artifical disturbing habitats, Int. J. Geomate, 2017, vol. 13, no. 35, pp. 136—143. https://doi.org/10.21660/2017.35.6626

    Article  Google Scholar 

  50. Zong, M., Liu, H.L., Qiu, Y.X., et al., Genetic diversity and geographic differentiation in the threatened species Dysosma pleiantha in China as revealed by ISSR analysis, Biochem. Genet., 2008, vol. 46, nos. 3—4, pp. 180—196. https://doi.org/10.1007/s10528-007-9141-7

    Article  CAS  Google Scholar 

  51. Feng, H., Feng, C.L., Wang, L., and Huang, Y., Genetic diversity of golden takin (Budorcas taxicolor bedfordi) population from Qinling Mountains in China revealed by sequence analysis of mitochondrial DNA control region, Biochem. Syst. Ecol., 2017, vol. 70, pp. 1—6. https://doi.org/10.1016/j.bse.2016.10.014

    Article  CAS  Google Scholar 

  52. Laura, T., Groom, R.J., Khuzwayo, J., and Jansen Van Vuuren, B., The genetic tale of a recovering lion population (Panthera leo) in the Savé Valley region (Zimbabwe): a better understanding of the history and managing the future, PLoS One, 2018, vol. 13, no. 2. e0190369. https://doi.org/10.1371/journal.pone.0190369

    Article  CAS  Google Scholar 

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ACKNOWLEDGMENTS

We are grateful to Leigongshan National Nature Reserve Administration and the beekeepers who allowed and helped us during sample collection.

Funding

This research was supported by Guizhou Provincial Science and Technology Project ([2019]1453, ZK[2021]112), Guizhou Academy of Agricultural Sciences (no. 202008, 202109, 202216), and the China Agriculture Research System of MOF and MARA (no. CARS-44-SYZ 22).

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  1. Guizhou Institute of Integrated Agriculture Development, Guizhou Academy of Agricultural Sciences, 1 Jinxin Community, 550006, Guiyang, People’s Republic of China

    Y. Yu, W. Zhou, Y. Li, W. Wan, D. Yao & X. Wei

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Yu, Y., Zhou, W., Li, Y. et al. Nuclear and Mitochondrial DNA Suggest That Nature Reserve Maintains Novel Haplotypes and Genetic Diversity of Honeybees (Apis cerana). Russ J Genet 58, 1513–1523 (2022). https://doi.org/10.1134/S1022795422120146

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