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

doi:10.24272/j.issn.2095-8137.2022.414

Volume 44 Issue 3

May 2023

Turn off MathJax

Article Contents

Article Navigation > Zoological Research > 2023 > 44(3): 483-493

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. Defining honeybee subspecies in an evolutionary context warrants strategized conservation. Zoological Research, 2023, 44(3): 483-493. doi: 10.24272/j.issn.2095-8137.2022.414

Citation:

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. Defining honeybee subspecies in an evolutionary context warrants strategized conservation. Zoological Research, 2023, 44(3): 483-493. doi: 10.24272/j.issn.2095-8137.2022.414

Citation:

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. Defining honeybee subspecies in an evolutionary context warrants strategized conservation. Zoological Research, 2023, 44(3): 483-493. doi: 10.24272/j.issn.2095-8137.2022.414

PDF( 4603 KB)

Defining honeybee subspecies in an evolutionary context warrants strategized conservation

doi: 10.24272/j.issn.2095-8137.2022.414

1.
Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China
2.
Key Laboratory for Bee Genetics and Breeding, Jilin Provincial Institute of Apicultural Sciences, Jilin, Jilin 132108, China
3.
Department of Zoology, School of Biosciences and Biotechnology, Baba Ghulam Shah Badshah University, Rajouri (Jammu and Kashmir) 185234, India
4.
CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Xishuangbanna, Yunnan 650000, China
5.
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
6.
Department of Entomology, University of Kentucky, Lexington, KY 40546, USA
7.
Yangzhou University, Yangzhou, Jiangsu 225009, China

The newly sequenced data have been archived at the NCBI SRA under accession No. PRJNA870246, as well as the Genome Sequence Archive (https://ngdc.cncb.ac.cn./gsz) and Science Data Bank (https://www.scidb.cn/en) under accessions PRJCA015358 and 10.57760/sciencedb.07636, respectively.
Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
Xin Z. and S.L. designed the study. L.Q. performed morphometrics analysis. S.L. conducted population genomics and mitochondrial analyses. J.D. assisted with sequencing data analysis. S.H.P. and A.M. acquired Indian specimens. Q.N., T.J., X.L., and Xin Z. organized sampling. X.L. provided samples from Northeast China and Japan. M.O., C.Z., X Zhang., Xuguo Z., and S. Luo assisted in manuscript writing. K.T. provided morphological data for a series of geographic populations. Xin Z., S.L., and L.Q. wrote the first drafts, and all authors contributed to and proof-read the manuscript. All authors read and approved the final version of the manuscript.

Funds: The work was supported by the National Natural Science Foundation (NSF) of China (32270475), Program of Ministry of Science and Technology of China (2018FY100403), National Special Support Program for High-level Talents (Ten-Thousand Talents Program), and 2115 Talent Development Program of China Agricultural University through Xin Z. S.L. is supported by Funds for International Cooperation and Exchange of the National Natural Science Foundation of China (3211001043). Sample collection was also supported by the NSF of China (31470123) and Jilin Science and Technology Program (20030561) through X.L. S.H.P. is supported by the National Mission on Himalayan Studies (NMHS) - Almora, Ministry of Environment, Forest and Climate Change, Government of India, through grant GBPNI/NMHS-2017-18/MG-12

More Information

Corresponding author: E-mail: shanlin.liu@cau.edu.cn; xinzhou@cau.edu.cn
Received Date: 2023-01-14
Accepted Date: 2023-03-01

Published Online: 2023-03-14

Publish Date: 2023-05-18

Abstract

Abstract

Despite the urgent need for conservation consideration, strategic action plans for the preservation of the Asian honeybee, Apis cerana 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 A. cerana 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 A. cerana. 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.
- Apis cerana,
- Integrative taxonomy,
- Species concept,
- Pollinator insect,
- Centrifugal diversification,
- Morphology,
- Genomics

FullText(HTML)

References(76)

References

[1]	Abrol DP. 2013. Asiatic Honeybee Apis cerana: Biodiversity Conservation and Agricultural Production. Dordrecht: Springer.
[2]	Barr CM, Neiman M, Taylor DR. 2005. Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytologist, 168(1): 39−50. doi: 10.1111/j.1469-8137.2005.01492.x
[3]	Braby MF, Eastwood R, Murray N. 2012. The subspecies concept in butterflies: has its application in taxonomy and conservation biology outlived its usefulness?. Biological Journal of the Linnean Society, 106(4): 699−716. doi: 10.1111/j.1095-8312.2012.01909.x
[4]	Casacci LP, Barbero F, Balletto E. 2014. The “Evolutionarily Significant Unit” concept and its applicability in biological conservation. Italian Journal of Zoology, 81(2): 182−193. doi: 10.1080/11250003.2013.870240
[5]	Chen C, Wang HH, Liu ZG, et al. 2018a. Population genomics provide insights into the evolution and adaptation of the Eastern Honey Bee (Apis cerana). Molecular Biology and Evolution, 35(9): 2260−2271. doi: 10.1093/molbev/msy130
[6]	Chen SF, Zhou YQ, Chen YR, et al. 2018b. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34(17): i884−i890. doi: 10.1093/bioinformatics/bty560
[7]	Chen YC. 1993. Apiculture of China. Beijing: China Agricultural Publication. (in Chinese)
[8]	Christmas MJ, Jones JC, Olsson A, et al. 2021. Genetic barriers to historical gene flow between cryptic species of Alpine Bumblebees revealed by comparative population genomics. Molecular Biology and Evolution, 38(8): 3126−3143. doi: 10.1093/molbev/msab086
[9]	Danecek P, Auton A, Abecasis G, et al. 2011. The variant call format and VCFtools. Bioinformatics, 27(15): 2156−2158. doi: 10.1093/bioinformatics/btr330
[10]	De Guia APO, Saitoh T. 2007. The gap between the concept and definitions in the Evolutionarily Significant Unit: the need to integrate neutral genetic variation and adaptive variation. Ecological Research, 22(4): 604−612. doi: 10.1007/s11284-006-0059-z
[11]	De Queiroz K. 2007. Species concepts and species delimitation. Systematic Biology, 56(6): 879−886. doi: 10.1080/10635150701701083
[12]	De Queiroz K. 2020. An updated concept of subspecies resolves a dispute about the taxonomy of incompletely separated lineages. Herpetological Review, 51(3): 459−461.
[13]	Dogantzis KA, Tiwari T, Conflitti IM, et al. 2021. Thrice out of Asia and the adaptive radiation of the western honey bee. Science Advances, 7(49): eabj2151. doi: 10.1126/sciadv.abj2151
[14]	Dogantzis KA, Zayed A. 2019. Recent advances in population and quantitative genomics of honey bees. Current Opinion in Insect Science, 31: 93−98. doi: 10.1016/j.cois.2018.11.010
[15]	Engel MS. 1999. The taxonomy of recent and fossil honey bees (Hymenoptera: Apidae; Apis). Journal of Hymenoptera Research, 8(2): 165−196.
[16]	Garnery L, Cornuet JM, Solignac M. 1992. Evolutionary history of the honey bee Apis mellifera inferred from mitochondrial DNA analysis. Molecular Ecology, 1(3): 145−154. doi: 10.1111/j.1365-294X.1992.tb00170.x
[17]	Groves CP, Cotterill FPD, Gippoliti S, et al. 2017. Species definitions and conservation: a review and case studies from African mammals. Conservation Genetics, 18(6): 1247−1256. doi: 10.1007/s10592-017-0976-0
[18]	Guillot G, Renaud S, Ledevin R, et al. 2012. A unifying model for the analysis of phenotypic, genetic, and geographic data. Systematic Biology, 61(6): 897−911. doi: 10.1093/sysbio/sys038
[19]	Gutiérrez EE, Helgen KM. 2013. Outdated taxonomy blocks conservation. Nature, 495(7441): 314.
[20]	Hausdorf B, Wilkens H, Strecker U. 2011. Population genetic patterns revealed by microsatellite data challenge the mitochondrial DNA based taxonomy of Astyanax in Mexico (Characidae, Teleostei). Molecular Phylogenetics and Evolution, 60(1): 89−97. doi: 10.1016/j.ympev.2011.03.009
[21]	Hepburn HR, Radloff SE, Verma S, et al. 2001a. Morphometric analysis of Apis cerana populations in the southern Himalayan region. Apidologie, 32(5): 435−447. doi: 10.1051/apido:2001142
[22]	Hepburn HR, Smith DR, Radloff SE, et al. 2001b. Infraspecific categories of Apis cerana: morphometric, allozymal and mtDNA diversity. Apidologie, 32(1): 3−23. doi: 10.1051/apido:2001108
[23]	Hillis DM. 2019. Species delimitation in herpetology. Journal of Herpetology, 53(1): 3−12. doi: 10.1670/18-123
[24]	Hou CS, Li BB, Luo YX, et al. 2016. First detection of Apis mellifera filamentous virus in Apis cerana cerana in China. Journal of Invertebrate Pathology, 138: 112−115. doi: 10.1016/j.jip.2016.06.011
[25]	Ilyasov RA, Park J, Takahashi J, et al. 2018. Phylogenetic uniqueness of Honeybee Apis cerana from the Korean peninsula inferred from the mitochondrial, nuclear, and morphological Data. Journal of Apicultural Science, 62(2): 189−214. doi: 10.2478/jas-2018-0018
[26]	Ilyasov RA, Youn HG, Lee ML, et al. 2019. Phylogenetic relationships of Russian Far-East Apis cerana with other north Asian populations. Journal of Apicultural Science, 63(2): 289−314. doi: 10.2478/jas-2019-0024
[27]	Ji YK, Li XG, Ji T, et al. 2020. Gene reuse facilitates rapid radiation and independent adaptation to diverse habitats in the Asian honeybee. Science Advances, 6(51): eabd3590. doi: 10.1126/sciadv.abd3590
[28]	Kalyaanamoorthy S, Minh BQ, Wong TKF, et al. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6): 587−589. doi: 10.1038/nmeth.4285
[29]	Klingenberg CP. 2011. MORPHOJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11(2): 353−357. doi: 10.1111/j.1755-0998.2010.02924.x
[30]	Korneliussen TS, Albrechtsen A, Nielsen R. 2014. ANGSD: Analysis of next generation sequencing data. BMC Bioinformatics, 15(1): 356. doi: 10.1186/s12859-014-0356-4
[31]	Larson G, Karlsson EK, Perri A, et al. 2012. Rethinking dog domestication by integrating genetics, archeology, and biogeography. Proceedings of the National Academy of Sciences of the United States of America, 109(23): 8878−8883. doi: 10.1073/pnas.1203005109
[32]	Lefort V, Desper R, Gascuel O. 2015. FastME 2.0: A comprehensive, accurate, and fast distance-based phylogeny inference program. Molecular Biology and Evolution, 32(10): 2798−2800. doi: 10.1093/molbev/msv150
[33]	Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14): 1754−1760. doi: 10.1093/bioinformatics/btp324
[34]	Li YY, Zhang R, Liu SL, et al. 2017. The molecular evolutionary dynamics of oxidative phosphorylation (OXPHOS) genes in Hymenoptera. BMC Evolutionary Biology, 17(1): 269. doi: 10.1186/s12862-017-1111-z
[35]	Liu NN, Liu HM, Ju Y, et al. 2022. Geometric morphology and population genomics provide insights into the adaptive evolution of Apis cerana in Changbai Mountain. BMC Genomics, 23(1): 64. doi: 10.1186/s12864-022-08298-x
[36]	Lo N, Gloag RS, Anderson DL, et al. 2010. A molecular phylogeny of the genus Apis suggests that the giant honey bee of the Philippines, A. breviligula Maa, and the plains honey bee of southern India, A. indica Fabricius, are valid species. Systematic Entomology, 35(2): 226−233. doi: 10.1111/j.1365-3113.2009.00504.x
[37]	Ma DF, Huang WC. 1981. Apiculture in the New China. Bee World, 62(4): 163−166. doi: 10.1080/0005772X.1981.11097840
[38]	Maa TC. 1953. An inquiry into the systematics of the tribus Apidini or honeybees (Hym. ). Treubia, 21(3): 525−640.
[39]	Malinsky M, Challis RJ, Tyers AM, et al. 2015. Genomic islands of speciation separate cichlid ecomorphs in an East African crater lake. Science, 350(6267): 1493−1498. doi: 10.1126/science.aac9927
[40]	Manichaikul A, Mychaleckyj JC, Rich SS, et al. 2010. Robust relationship inference in genome-wide association studies. Bioinformatics, 26(22): 2867−2873. doi: 10.1093/bioinformatics/btq559
[41]	McKenna A, Hanna M, Banks E, et al. 2010. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20(9): 1297−1303. doi: 10.1101/gr.107524.110
[42]	Minh BQ, Schmidt HA, Chernomor O, et al. 2020. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37(5): 1530−1534. doi: 10.1093/molbev/msaa015
[43]	Morrison III WR, Lohr JL, Duchen P, et al. 2009. The impact of taxonomic change on conservation: Does it kill, can it save, or is it just irrelevant?. Biological Conservation, 142(12): 3201−3206. doi: 10.1016/j.biocon.2009.07.019
[44]	Nakamura T, Yamada KD, Tomii K, et al. 2018. Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics, 34(14): 2490−2492. doi: 10.1093/bioinformatics/bty121
[45]	National Animal Genetic Resources Committee. 2011. Animal Genetic Resources in China: Bees. Beijing: China Agriculture Press. (in Chinese)
[46]	Neuditschko M, Khatkar MS, Raadsma HW. 2012. NetView: a high-definition network-visualization approach to detect fine-scale population structures from genome-wide patterns of variation. PLoS One, 7(10): e48375. doi: 10.1371/journal.pone.0048375
[47]	Oldroyd BP, Reddy MS, Chapman NC, et al. 2006. Evidence for reproductive isolation between two colour morphs of cavity nesting honey bees (Apis) in south India. Insectes Sociaux, 53(4): 428−434. doi: 10.1007/s00040-005-0889-2
[48]	Orr MC, Ferrari RR, Hughes AC, et al. 2021. Taxonomy must engage with new technologies and evolve to face future challenges. Nature Ecology & Evolution, 5(1): 3−4.
[49]	Peng YS, Nasr ME, Locke SJ. 1989. Geographical races of Apis cerana Fabricius in China and their distribution. Review of recent Chinese publications and a preliminary statistical analysis. Apidologie, 20(1): 9−20. doi: 10.1051/apido:19890102
[50]	Phillimore AB, Owens IPF. 2006. Are subspecies useful in evolutionary and conservation biology?. Proceedings of the Royal Society B:Biological Sciences, 273(1590): 1049−1053. doi: 10.1098/rspb.2005.3425
[51]	Purcell S, Neale B, Todd-Brown K, et al. 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. The American Journal of Human Genetics, 81(3): 559−575. doi: 10.1086/519795
[52]	Radloff SE, Hepburn C, Hepburn HR, et al. 2010. Population structure and classification of Apis cerana. Apidologie, 41(6): 589–601.
[53]	Radoszkowski O. 1887. Hyménoptères de Korée. Horae Societatis Entomologicae Rossicae, 21: 428−436.
[54]	Requier F, Garnery L, Kohl PL, et al. 2019. The conservation of native Honey Bees is crucial. Trends in Ecolgy & Evolution, 34(9): 789−798.
[55]	Rodríguez F, Pérez T, Hammer SE, et al. 2010. Integrating phylogeographic patterns of microsatellite and mtDNA divergence to infer the evolutionary history of chamois (genus Rupicapra). BMC Evolutionary Biology, 10(1): 222. doi: 10.1186/1471-2148-10-222
[56]	Ruttner F. 1988. Biogeography and Taxonomy of Honeybees. Berlin: Springer.
[57]	Ryder OA. 1986. Species conservation and systematics: the dilemma of subspecies. Trends in Ecology & Evolution, 1(1): 9−10.
[58]	Shanas S, Anju KG, Mashhoor K. 2022. Identity of cavity nesting honey bees of the Indian subcontinent with description of a new species (Hymenoptera: Apidae: Apinae: Apini: Apis). Entomon, 47(3): 197−220. doi: 10.33307/entomon.v47i3.755
[59]	Shaw KL. 2002. Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: What mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proceedings of the National Academy of Sciences of the United States of America, 99(25): 16122−16127. doi: 10.1073/pnas.242585899
[60]	Skotte L, Korneliussen TS, Albrechtsen A. 2013. Estimating individual admixture proportions from next generation sequencing data. Genetics, 195(3): 693−702. doi: 10.1534/genetics.113.154138
[61]	Smith DR, Hagen RH. 1996. The biogeography of Apis cerana as revealed by mitochondrial DNA sequence data. Journal of the Kansas Entomological Society, 69(4): 294−310.
[62]	Tan HW, Naeem M, Ali H, et al. 2021. Genome sequence of the Asian honeybee in Pakistan sheds light on its phylogenetic relationship with other honeybees. Insects, 12(7): 652. doi: 10.3390/insects12070652
[63]	Tan K, Fuchs S, Koeniger N, et al. 2003. Morphological characterization of Apis cerana in the Yunnan province of China. Apidologie, 34(6): 553−561. doi: 10.1051/apido:2003049
[64]	Tan K, Hepburn HR, Radloff SE, et al. 2008. Multivariate morphometric analysis of the Apis cerana of China. Apidologie, 39(3): 343−353. doi: 10.1051/apido:2008014
[65]	Tan K, Meixner MD, Fuchs S, et al. 2006. Geographic distribution of the eastern honeybee, Apis cerana (Hymenoptera: Apidae), across ecological zones in China: Morphological and molecular analyses. Systematics and Biodiversity, 4(4): 473−482. doi: 10.1017/S1477200006002015
[66]	Tarasov A, Vilella AJ, Cuppen E, et al. 2015. Sambamba: fast processing of NGS alignment formats. Bioinformatics, 31(12): 2032−2034. doi: 10.1093/bioinformatics/btv098
[67]	Toews DPL, Brelsford A. 2012. The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology, 21(16): 3907−3930. doi: 10.1111/j.1365-294X.2012.05664.x
[68]	Vung NN, Kim I, Lee MY, et al. 2018. Controlling sacbrood virus disease in Apis cerana colonies with biological methods in Korea. Journal of Apiculture, 33(4): 283−295. doi: 10.17519/apiculture.2018.11.33.4.283
[69]	Wang XY, Wang T, Xu JF, et al. 2022. Enhanced habitat loss of the Himalayan endemic flora driven by warming-forced upslope tree expansion. Nature Ecology & Evolution, 6(7): 890−899.
[70]	Wang Z, Chen DH, Wang Q, et al. 2021. Research on the development status and countermeasures of the bee seed industry in China. Journal of Bee, 41(11): 12−18. (in Chinese)
[71]	Yang GH. 2009. The effect of Apis cerana cerana on forest ecosystem. Apiculture of China, 60(4): 5−7,10. (in Chinese)
[72]	Yang GH, Lin GL, Sun QH, et al. 1995. The distribution, morphological variation and behavior of Chinese honeybee in northwestern plateau of Sichuan province. Scientia Agricultura Sinica, 28(S1): 202−206. (in Chinese)
[73]	Yang GH, Xu SY, Kuang BY, et al. 1986. The distribution of the genus Apis cerana Fab. in China and some of its subspecies. Journal of Yunnan Agricultural University, 1(1): 89−92. (in Chinese)
[74]	Zhao HL. 2018. Problems and countermeasures of bee cultivation in poor mountainous areas of Hainan. Anhui Agricultural Science Bulletin, 24(12): 10−12. (in Chinese)
[75]	Zhao WZ, Wang M, Liu YQ, et al. 2017. Phylogeography of Apis cerana populations on Hainan island and southern mainland China revealed by microsatellite polymorphism and mitochondrial DNA. Apidologie, 48(1): 63−74. doi: 10.1007/s13592-016-0450-x
[76]	Zhuang DA. 1989. New subspecies of Apis cerana. Southwest China Journal of Agricultural Sciences, 2(4): 61–65. (in Chinese)