Defining honeybee subspecies in an evolutionary context warrants strategized conservation.

Lifei Qiu, Jiangxing Dong, Xingan Li, Sajad H Parey, Ken Tan, Michael Orr, Aquib Majeed, Xue Zhang, Shiqi Luo, Xuguo Zhou, Chaodong Zhu, Ting Ji, Qingsheng Niu, Shanlin Liu, Xin Zhou
Author Information
  1. Lifei Qiu: Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China.
  2. Jiangxing Dong: Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China.
  3. Xingan Li: Key Laboratory for Bee Genetics and Breeding, Jilin Provincial Institute of Apicultural Sciences, Jilin, Jilin 132108, China.
  4. Sajad H Parey: Department of Zoology, School of Biosciences and Biotechnology, Baba Ghulam Shah Badshah University, Rajouri (Jammu and Kashmir) 185234, India.
  5. Ken Tan: CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Xishuangbanna, Yunnan 650000, China.
  6. Michael Orr: Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
  7. Aquib Majeed: Department of Zoology, School of Biosciences and Biotechnology, Baba Ghulam Shah Badshah University, Rajouri (Jammu and Kashmir) 185234, India.
  8. Xue Zhang: Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China.
  9. Shiqi Luo: Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China.
  10. Xuguo Zhou: Department of Entomology, University of Kentucky, Lexington, KY 40546, USA.
  11. Chaodong Zhu: Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
  12. Ting Ji: Yangzhou University, Yangzhou, Jiangsu 225009, China.
  13. Qingsheng Niu: Key Laboratory for Bee Genetics and Breeding, Jilin Provincial Institute of Apicultural Sciences, Jilin, Jilin 132108, China.
  14. Shanlin Liu: Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China. E-mail: shanlin.liu@cau.edu.cn.
  15. Xin Zhou: Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China. E-mail: xinzhou@cau.edu.cn.

Abstract

Despite the urgent need for conservation consideration, strategic action plans for the preservation of the Asian honeybee, Fabricius, 1793, remain lacking. Both the convergent and divergent adaptations of this widespread insect have led to confusing phenotypical traits and inconsistent infraspecific taxonomy. Unclear subspecies boundaries pose a significant challenge to honeybee conservation efforts, as it is difficult to effectively prioritize conservation targets without a clear understanding of subspecies identities. Here, we investigated genome variations in 362 worker bees representing almost all populations of mainland to understand how evolution has shaped its population structure. Whole-genome single nucleotide polymorphisms (SNPs) based on nuclear sequences revealed eight putative subspecies, with all seven peripheral subspecies exhibiting mutually exclusive monophyly and distinct genetic divergence from the widespread central subspecies. Our results demonstrated that most classic morphological traits, including body size, were related to the climatic variables of the local habitats and did not reflect the true evolutionary history of the organism. Thus, such morphological traits were not suitable for subspecific delineation. Conversely, wing vein characters showed relative independence to the environment and supported the subspecies boundaries inferred from nuclear genomes. Mitochondrial phylogeny further indicated that the present subspecies structure was a result of multiple waves of population divergence from a common ancestor. Based on our findings, we propose that criteria for subspecies delineation should be based on evolutionary independence, trait distinction, and geographic isolation. We formally defined and described eight subspecies of mainland . Elucidation of the evolutionary history and subspecies boundaries enables a customized conservation strategy for both widespread and endemic honeybee conservation units, guiding colony introduction and breeding.

Keywords

Associated Data

SRA | PRJNA870246

References

  1. Mol Biol Evol. 2018 Sep 1;35(9):2260-2271 [PMID: 29931308]
  2. Mol Ecol. 1992 Oct;1(3):145-54 [PMID: 1364272]
  3. Mol Biol Evol. 2021 Jul 29;38(8):3126-3143 [PMID: 33823537]
  4. Nat Ecol Evol. 2021 Jan;5(1):3-4 [PMID: 33173204]
  5. Bioinformatics. 2010 Nov 15;26(22):2867-73 [PMID: 20926424]
  6. Syst Biol. 2012 Dec 1;61(6):897-911 [PMID: 22398122]
  7. Bioinformatics. 2009 Jul 15;25(14):1754-60 [PMID: 19451168]
  8. Mol Biol Evol. 2015 Oct;32(10):2798-800 [PMID: 26130081]
  9. Bioinformatics. 2018 Jul 15;34(14):2490-2492 [PMID: 29506019]
  10. Genome Res. 2010 Sep;20(9):1297-303 [PMID: 20644199]
  11. Sci Adv. 2020 Dec 18;6(51): [PMID: 33355133]
  12. PLoS One. 2012;7(10):e48375 [PMID: 23152744]
  13. BMC Evol Biol. 2017 Dec 28;17(1):269 [PMID: 29281964]
  14. BMC Genomics. 2022 Jan 19;23(1):64 [PMID: 35045823]
  15. BMC Evol Biol. 2010 Jul 22;10:222 [PMID: 20649956]
  16. Trends Ecol Evol. 2019 Sep;34(9):789-798 [PMID: 31072605]
  17. Insects. 2021 Jul 16;12(7): [PMID: 34357312]
  18. Mol Ecol Resour. 2011 Mar;11(2):353-7 [PMID: 21429143]
  19. Bioinformatics. 2018 Sep 1;34(17):i884-i890 [PMID: 30423086]
  20. Nature. 2013 Mar 21;495(7441):314 [PMID: 23518556]
  21. Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):16122-7 [PMID: 12451181]
  22. Mol Phylogenet Evol. 2011 Jul;60(1):89-97 [PMID: 21419231]
  23. Mol Ecol. 2012 Aug;21(16):3907-30 [PMID: 22738314]
  24. New Phytol. 2005 Oct;168(1):39-50 [PMID: 16159319]
  25. Bioinformatics. 2011 Aug 1;27(15):2156-8 [PMID: 21653522]
  26. Trends Ecol Evol. 1986 Oct;1(4):104 [PMID: 21227791]
  27. Syst Biol. 2007 Dec;56(6):879-86 [PMID: 18027281]
  28. Mol Biol Evol. 2020 May 1;37(5):1530-1534 [PMID: 32011700]
  29. Proc Biol Sci. 2006 May 7;273(1590):1049-53 [PMID: 16600880]
  30. Genetics. 2013 Nov;195(3):693-702 [PMID: 24026093]
  31. BMC Bioinformatics. 2014 Nov 25;15:356 [PMID: 25420514]
  32. Am J Hum Genet. 2007 Sep;81(3):559-75 [PMID: 17701901]
  33. Sci Adv. 2021 Dec 03;7(49):eabj2151 [PMID: 34860547]
  34. Science. 2015 Dec 18;350(6267):1493-1498 [PMID: 26680190]
  35. Nat Ecol Evol. 2022 Jul;6(7):890-899 [PMID: 35654898]
  36. Proc Natl Acad Sci U S A. 2012 Jun 5;109(23):8878-83 [PMID: 22615366]
  37. Nat Methods. 2017 Jun;14(6):587-589 [PMID: 28481363]
  38. Bioinformatics. 2015 Jun 15;31(12):2032-4 [PMID: 25697820]
  39. Curr Opin Insect Sci. 2019 Feb;31:93-98 [PMID: 31109680]
  40. J Invertebr Pathol. 2016 Jul;138:112-5 [PMID: 27369386]

MeSH Term

Bees
Animals
Phylogeny
Phenotype
Mitochondria

Word Cloud

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