Genome-wide developed microsatellites reveal a weak population differentiation in the hoverfly Eupeodes corollae (Diptera: Syrphidae) across China

Autoři: Mengjia Liu aff001;  Xiaoqiang Wang aff001;  Ling Ma aff002;  Lijun Cao aff002;  Hongling Liu aff003;  Deqiang Pu aff001;  Shujun Wei aff002
Působiště autorů: Industrial Crop Research Institute, Sichuan Academy of Agricultural Sciences, Chengdu, China aff001;  Institute of Plant and Environmental Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China aff002;  Institute of Plant Protection, Sichuan Academy of Agricultural Sciences, Chengdu, China aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0215888


The hoverfly, Eupeodes corollae, is a worldwide natural enemy of aphids and a plant pollinator. To provide insights into the biology of this species, we examined its population genetic structure by obtaining 1.15-GB random genomic sequences using next-generation sequencing and developing genome-wide microsatellite markers. A total of 79,138 microsatellite loci were initially isolated from the genomic sequences; after strict selection and further testing of 40 primer pairs in eight individuals, 24 polymorphic microsatellites with high amplification rates were developed. These microsatellites were used to examine the population genetic structure of 96 individuals from four field populations collected across southern to northern China. The number of alleles per locus ranged from 5 to 13 with an average of 8.75; the observed and expected heterozygosity varied from 0.235 to 0.768 and from 0.333 to 0.785, respectively. Population genetic structure analysis showed weak genetic differentiation among the four geographical populations of E. corollae, suggesting a high rate of gene flow reflecting likely widespread migration of E. corollae in China.

Klíčová slova:

Genetic loci – Genomic library construction – Genomics – China – Invertebrate genomics – Population genetics – Microsatellite loci – Structural genomics


1. Van Veen MP, Moore SJ. Hoverflies of Northwest Europe: identification keys to the Syrphidae: KNNV Publishing Utrecht; 2004.

2. Rojo S, Isidro P, Perez-Bañón M, Marcos-García M. Revision of the hoverflies (Diptera: Syrphidae) from the Azores archipelago with notes on Macaronesian Syrphid fauna. ARQUIPÉLAGO Ciências Biológicas e Marinhas = Life and Marine Sciences. 1997;15:65–82.

3. Rojo S, Hopper KR, Marcos‐García MA. Fitness of the hover flies Episyrphus balteatus and Eupeodes corollae faced with limited larval prey. Entomologia Experimentalis et Applicata. 1996;81(1):53–9.

4. Mengual X, Ståhls G, Rojo S. Molecular phylogeny of Allograpta (Diptera, Syrphidae) reveals diversity of lineages and non-monophyly of phytophagous taxa. Molecular phylogenetics and evolution. 2008;49(3):715–27. doi: 10.1016/j.ympev.2008.09.011 18848633

5. Scott S, Barlow C. Effect of hunger on the allocation of time among pea plants by the larvae of an aphidophagous hover fly, Eupeodes corollae [Dipt: Syrphidae]. Entomophaga. 1990;35(2):163–72.

6. Barbir J, Dorado J, Fernández-Quintanilla C, Blanusa T, Maksimovic C, Badenes-Pérez FR. Wild rocket–effect of water deficit on growth, flowering, and attractiveness to pollinators. Acta Agriculturae Scandinavica, Section B—Soil & Plant Science. 2014;64(6):482–92. doi: 10.1080/09064710.2014.925575

7. Jauker F, Wolters V. Hover flies are efficient pollinators of oilseed rape. Oecologia. 2008;156(4):819–23. doi: 10.1007/s00442-008-1034-x 18438687.

8. Dq Pu, Shi M, Wu Q, Gao Mq, Liu JF, Ren Sp, et al. Flower‐visiting insects and their potential impact on transgene flow in rice. Journal of Applied Ecology. 2014;51(5):1357–65.

9. Putra NS, Yasuda H. Effects of prey species and its density on larval performance of two species of hoverfly larvae, Episyrphus balteatus de Geer and Eupeodes corollae Fabricius (Diptera: Syrphidae). Applied Entomology and Zoology. 2006;41(3):389–97.

10. Hu G, Lim KS, Horvitz N, Clark SJ, Reynolds DR, Sapir N, et al. Mass seasonal bioflows of high-flying insect migrants. Science. 2016;354(6319):1584–7. doi: 10.1126/science.aah4379 28008067

11. Raymond L, Vialatte A, Plantegenest M. Combination of morphometric and isotopic tools for studying spring migration dynamics in Episyrphus balteatus. Ecosphere. 2014;5(7):1–16.

12. Wei SJ, Shi BC, Gong YJ, Jin GH, Chen XX, Meng XF. Genetic structure and demographic history reveal migration of the diamondback moth Plutella xylostella (Lepidoptera: Plutellidae) from the southern to northern regions of China. PLoS ONE. 2013;8(4):e59654. doi: 10.1371/journal.pone.0059654 23565158; PubMed Central PMCID: PMC3614937.

13. Liedvogel M, Akesson S, Bensch S. The genetics of migration on the move. Trends Ecol Evol. 2011;26(11):561–9. doi: 10.1016/j.tree.2011.07.009 21862171.

14. Zhan S, Merlin C, Boore JL, Reppert SM. The monarch butterfly genome yields insights into long-distance migration. Cell. 2011;147(5):1171–85. doi: 10.1016/j.cell.2011.09.052 22118469; PubMed Central PMCID: PMC3225893.

15. Zhan S, Zhang W, Niitepold K, Hsu J, Haeger JF, Zalucki MP, et al. The genetics of monarch butterfly migration and warning coloration. Nature. 2014;514(7522):317. doi: 10.1038/nature13812 25274300

16. Milankov V, Francuski L, Ludoski J, Ståhls G, Vujic A. Genetic structure and phenotypic diversity of two northern populations of Cheilosia aff. longula (Diptera: Syrphidae) has implications for evolution and conservation. European Journal of Entomology. 2010;107(3):305.

17. Rotheray E, Lepais O, Nater A, Krützen M, Greminger M, Goulson D, et al. Genetic variation and population decline of an endangered hoverfly Blera fallax (Diptera: Syrphidae). Conservation genetics. 2012;13(5):1283–91.

18. Raymond L, Plantegenest M, Vialatte A. Migration and dispersal may drive to high genetic variation and significant genetic mixing: the case of two agriculturally important, continental hoverflies (E pisyrphus balteatus and S phaerophoria scripta). Molecular ecology. 2013;22(21):5329–39. doi: 10.1111/mec.12483 24138027

19. Raymond L, Plantegenest M, Gauffre B, Sarthou JP, Vialatte A. Lack of genetic differentiation between contrasted overwintering strategies of a major pest predator Episyrphus balteatus (Diptera: Syrphidae): implications for biocontrol. PloS one. 2013;8(9):e72997. doi: 10.1371/journal.pone.0072997 24023799; PubMed Central PMCID: PMC3759392.

20. Odermatt J, Frommen JG, Menz MH. Consistent behavioural differences between migratory and resident hoverflies. Animal Behaviour. 2017;127:187–95.

21. Stubbs AE, Falk SJ. British hoverflies: An illustrated identification guide: British Entomological and Natural History Society; 2002.

22. Svensson BG, Janzon LÅ. Why does the hoverfly Metasyrphus corollae migrate? Ecological entomology. 1984;9(3):329–35.

23. Speight MC. A mass migration of Episyrphus balteatus and Eupeodes corollae arriving in the south-west and remarks on other migrant hoverflies (Diptera: Syrphidae) in Ireland. Irish Naturalists' Journal. 1996;25(5):182–3.

24. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. doi: 10.1093/bioinformatics/btu170 24695404

25. Andrews S. FastQC: a quality control tool for high throughput sequence data. 2010.

26. Marçais G, Kingsford C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics. 2011;27(6):764. doi: 10.1093/bioinformatics/btr011 21217122

27. Peng Y, Leung HCM, Yiu SM, Chin FYL, editors. IDBA–A practical iterative de bruijn graph De Novo assembler2010; Berlin, Heidelberg: Springer Berlin Heidelberg.

28. Castoe TA, Poole AW, Gu W, Jason de Koning A, Daza JM, Smith EN, et al. Rapid identification of thousands of copperhead snake (Agkistrodon contortrix) microsatellite loci from modest amounts of 454 shotgun genome sequence. Molecular Ecology Resources. 2010;10(2):341–7. doi: 10.1111/j.1755-0998.2009.02750.x 21565030

29. Gardner MG, Fitch AJ, Bertozzi T, Lowe AJ. Rise of the machines–recommendations for ecologists when using next generation sequencing for microsatellite development. Molecular Ecology Resources. 2011;11(6):1093–101. doi: 10.1111/j.1755-0998.2011.03037.x 21679314

30. Abdelkrim J, Robertson BC, Stanton J-AL, Gemmell NJ. Fast, cost-effective development of species-specific microsatellite markers by genomic sequencing. BioTechniques. 2009;46(3):185–92. doi: 10.2144/000113084 19317661

31. Du L, Li Y, Zhang X, Yue B. MSDB: A user-friendly program for reporting distribution and building databases of microsatellites from genome sequences. Journal of Heredity. 2013;104(1):154–7. doi: 10.1093/jhered/ess082 23144492

32. Meglécz E, Costedoat C, Dubut V, Gilles A, Malausa T, Pech N, et al. QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects. Bioinformatics. 2010;26(3):403–4. doi: 10.1093/bioinformatics/btp670 20007741

33. Wang YZ, Cao LJ, Zhu JY, Wei SJ. Development and characterization of novel microsatellite markers for the peach fruit moth Carposina sasakii (Lepidoptera: Carposinidae) using next-generation sequencing. International Journal of Molecular Sciences. 2016;17(3):362. doi: 10.3390/ijms17030362 26999103

34. Song W, Cao LJ, Wang YZ, Li BY, Wei SJ. Novel microsatellite markers for the oriental fruit moth Grapholita molesta (Lepidoptera: Tortricidae) and effects of null alleles on population genetics analyses. Bulletin of entomological research. 2017;107(3):349–58. Epub 2016/11/08. doi: 10.1017/S0007485316000936 27819214.

35. Blacket MJ, Robin C, Good RT, Lee SF, Miller AD. Universal primers for fluorescent labelling of PCR fragments—an efficient and cost‐effective approach to genotyping by fluorescence. Molecular ecology resources. 2012;12(3):456–63. doi: 10.1111/j.1755-0998.2011.03104.x 22268566

36. Raymond M. GENEPOP: population genetics software for exact tests and ecumenism. Vers. 1.2. J Hered. 1995;86:248–9.

37. Cao LJ, Wang ZH, Gong YJ, Zhu L, Hoffmann AA, Wei SJ. Low genetic diversity but strong population structure reflects multiple introductions of western flower thrips (Thysanoptera: Thripidae) into China followed by human‐mediated spread. Evolutionary applications. 2017;10(4):391–401. doi: 10.1111/eva.12461 28352298

38. Pritchard JK, Stephens M, Donnelly P. Inference of Population Structure Using Multilocus Genotype Data. Genetics. 2000;155(2):945–59. 10835412

39. Earl DA, vonHoldt BM. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources. 2012;4(2):359–61. doi: 10.1007/s12686-011-9548-7

40. Jakobsson M, Rosenberg NA. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007;23(14):1801–6. doi: 10.1093/bioinformatics/btm233 17485429

41. Rosenberg NA. DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes. 2004;4(1):137–8. doi: 10.1046/j.1471-8286.2003.00566.x

42. Bai X, Zhang W, Orantes L, Jun T-H, Mittapalli O, Mian MAR, et al. Combining next-generation sequencing strategies for rapid molecular resource development from an invasive aphid species, Aphis glycines. PloS one. 2010;5(6):e11370. doi: 10.1371/journal.pone.0011370 20614011

43. Yao Y, Zhao W, Shang X. Development of polymorphic microsatellite markers of Obolodiplosis robiniae (Haldeman) (Diptera: Cecidomyiidae), a North American pest invading asia. Journal of insect science. 2015;15(1):127-. doi: 10.1093/jisesa/iev104 26386040

44. Ellegren H. Microsatellites: simple sequences with complex evolution. Nature Reviews Genetics. 2004;5:435. doi: 10.1038/nrg1348 15153996

45. Selkoe KA, Toonen RJ. Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology letters. 2006;9(5):615–29. doi: 10.1111/j.1461-0248.2006.00889.x 16643306

46. Queirós J, Godinho R, Lopes S, Gortazar C, De la Fuente J, Alves P. Effect of microsatellite selection on individual and population genetic inferences: an empirical study using cross‐specific and species‐specific amplifications. Molecular ecology resources. 2015;15(4):747–60. doi: 10.1111/1755-0998.12349 25403329

47. Cao LJ, Li ZM, Wang ZH, Zhu L, Gong YJ, Chen M, et al. Bulk development and stringent selection of microsatellite markers in the western flower thrips Frankliniella occidentalis. Scientific Reports. 2016;6:26512. doi: 10.1038/srep26512 27197749

48. Rice WR. Analyzing tables of statistical tests. Evolution; international journal of organic evolution. 1989;43(1):223–5. doi: 10.1111/j.1558-5646.1989.tb04220.x 28568501

49. Milankov V, Francuski L, Ludoški J, Ståhls G, Vujić A. Estimating genetic and phenotypic diversity in a northern hoverfly reveals lack of heterozygosity correlated with significant fluctuating asymmetry of wing traits. Journal of Insect Conservation. 2010;14(1):77–88. doi: 10.1007/s10841-009-9226-1

50. Verhoeven KJ, Macel M, Wolfe LM, Biere A. Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proceedings of the Royal Society of London B: Biological Sciences. 2011;278(1702):2–8.

51. Behura SK. Molecular marker systems in insects: current trends and future avenues. Molecular ecology. 2006;15(11):3087–113. doi: 10.1111/j.1365-294X.2006.03014.x 16968257

52. Ball AD, Stapley J, Dawson DA, Birkhead TR, Burke T, Slate J. A comparison of SNPs and microsatellites as linkage mapping markers: lessons from the zebra finch (Taeniopygia guttata). BMC genomics. 2010;11(1):218.

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