Genetic structure of the European hedgehog (Erinaceus europaeus) in Denmark

Autoři: Sophie Lund Rasmussen aff001;  Jeppe Lund Nielsen aff002;  Owen R. Jones aff001;  Thomas B. Berg aff001;  Cino Pertoldi aff002
Působiště autorů: Department of Biology, University of Southern Denmark, Odense, Denmark aff001;  Department of Chemistry and Bioscience, Section of Biotechnology, Aalborg University, Aalborg, Denmark aff002;  Interdisciplinary Centre on Population Dynamics (CPop), Department of Biology, University of Southern Denmark, Odense, Denmark aff003;  Naturama, Svendborg, Denmark aff004;  Aalborg Zoo, Aalborg, Denmark aff005
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article



Low genetic diversity can lead to reduced average fitness in a population or even extinction. Preserving genetic connectivity across fragmented landscapes is therefore vital to counteract the negative consequences of genetic drift and inbreeding. This study aimed to assess the genetic composition and consequently the conservation status of a nationwide sample of European hedgehogs (Erinaceus europaeus) in Denmark.


We applied an adaptation of the genotyping by sequencing (GBS) technique to 178 individuals from six geographically distinct populations. We used a Bayesian clustering method to subdivide individuals into genetically distinct populations. We estimated individual observed (iHO), observed (HO), and unbiased expected (uHE) heterozygosity, inbreeding coefficient (FIS), percentage of polymorphic loci (P%) and tested for deviations from Hardy-Weinberg equilibrium (HWE). We used linear models to test for potential anthropogenic effects on the genetic variability of hedgehogs with iHO, uHE, P% and FIS as response variables, and assessed the demographic history of the population.


The Danish hedgehog population is composed of three genetic clusters. We found a mean P% of 54.44–94.71, a mean uHE of 0.126–0.318 and a mean HO of 0.124–0.293 in the six populations. The FIS was found to be significantly positive for three of the six populations. We detected a large heterogeneity of iHO values within populations, which can be due to inbreeding and/or fragmentation. FIS values decreased with increasing farmland density, but there was no significant association with human population or road density.


We found a low level of genetic variability and evidence for genetic substructure and low effective population size, which are all consequences of habitat fragmentation. We failed to detect signs of a recent population bottleneck or population increase or decline. However, because the test only identifies recent changes in population size, we cannot reject the possibility of a longer-term decline in the Danish hedgehog population.

Klíčová slova:

Denmark – Europe – Genetic polymorphism – Heterozygosity – Islands – Population density – Population genetics – Hedgehogs


1. Reeve N. Hedgehogs. London: Poyser; 1994.

2. Morris P. Hedgehogs. Stansted, Essex: Whittet Books Ltd.; 2014.

3. SoBH. The state of Britain's Hedgehogs 2011. British Trust for Ornithology (BTO) commissioned by People's Trust for Endangered Species (PTES) and the British Hedgehog Preservation Society (BHPS): 2011.

4. SoBH. The State of Britain’s Hedgehogs 2015. British Hedgehog Preservation Society and People’s Trust for Endangered Species, 2015.

5. SoBH. The State of Britain’s Hedgehogs 2018. British Hedgehog Preservation Society and People’s Trust for Endangered Species: 2018.

6. Hof AR, Bright PW. Quantifying the long-term decline of the West European hedgehog in England by subsampling citizen-science datasets. Eur J Wildl Res. 2016;62(4):407–13. doi: 10.1007/s10344-016-1013-1 WOS:000380127300003.

7. Williams BM, Baker PJ, Thomas E, Wilson G, Judge J, Yarnell RW. Reduced occupancy of hedgehogs (Erinaceus europaeus) in rural England and Wales: The influence of habitat and an asymmetric intra-guild predator. Sci Rep. 2018;8(1):12156. Epub 2018/09/08. doi: 10.1038/s41598-018-30130-4 30190482; PubMed Central PMCID: PMC6127255.

8. Holsbeek L, Rodts J, Muyldermans S. Hedgehog and other animal traffic victims in Belgium: Results of a countrywide survey. Lutra. 1999;42(1):111–9. BIOSIS:PREV200000071214.

9. van de Poel JL, Dekker J, van Langevelde F. Dutch hedgehogs Erinaceus europaeus are nowadays mainly found in urban areas, possibly due to the negative effects of badgers Meles meles. Wildlife Biol. 2015;21(1):51–5. doi: 10.2981/wlb.00072 WOS:000347398500006.

10. Huijser MP, Bergers PJM. The effect of roads and traffic on hedgehog (Erinaceus europaeus) populations. Biological Conservation. 2000;95(1):111–6. BIOSIS:PREV200000306409.

11. Krange M. Change in the occurrence of the West European Hedgehog (Erinaceus europaeus) in western Sweden during 1950–2010. [MSc thesis]. Sweden: Karlstad University; 2015.

12. Müller F. Langzeit-Monitoring der Strassenverkehrsopfer beim Igel (Erinaceus europaeus L.) zur Indikation von Populationsdichteveränderungen entlang zweier Teststrecken im Landkreis Fulda. Beiträge zur Naturkunde in Osthessen. 2018;54:21–6.

13. Brooks TM, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Rylands AB, Konstant WR, et al. Habitat loss and extinction in the hotspots of biodiversity. Conservation Biology. 2002;16(4):909–23. doi: 10.1046/j.1523-1739.2002.00530.x WOS:000177199500009.

14. Crooks KR, Burdett CL, Theobald DM, King SRB, Di Marco M, Rondinini C, et al. Quantification of habitat fragmentation reveals extinction risk in terrestrial mammals. Proceedings of the National Academy of Sciences of the United States of America. 2017;114(29):7635–40. doi: 10.1073/pnas.1705769114 WOS:000405662300064. 28673992

15. Stoate C, Boatman ND, Borralho RJ, Carvalho CR, de Snoo GR, Eden P. Ecological impacts of arable intensification in Europe. Journal of Environmental Management. 2001;63(4):337–65. doi: 10.1006/jema.2001.0473 WOS:000173317500001. 11826719

16. Hof AR, Bright PW. The value of agri-environment schemes for macro-invertebrate feeders: hedgehogs on arable farms in Britain. Animal Conservation. 2010;13(5):467–73. doi: 10.1111/j.1469-1795.2010.00359.x WOS:000282370500008.

17. Riber AB. Habitat use and behaviour of European hedgehog Erinaceus europaeus in a Danish rural area. Acta Theriologica. 2006;51(4):363–71. doi: 10.1007/bf03195183 WOS:000241390700004.

18. Michel N, Burel F, Butet A. How does landscape use influence small mammal diversity, abundance and biomass in hedgerow networks of farming landscapes? Acta Oecologica-International Journal of Ecology. 2006;30(1):11–20. doi: 10.1016/j.actao.2005.12.006 WOS:000239342400002.

19. Dowding CV, Harris S, Poulton S, Baker PJ. Nocturnal ranging behaviour of urban hedgehogs, Erinaceus europaeus, in relation to risk and reward. Animal Behaviour. 2010;80(1):13–21. doi: 10.1016/j.anbehav.2010.04.007 WOS:000279153100004.

20. Rondinini C, Doncaster CP. Roads as barriers to movement for hedgehogs. Functional Ecology. 2002;16(4):504–9. doi: 10.1046/j.1365-2435.2002.00651.x WOS:000177256800009.

21. Rautio A, Isomursu M, Valtonen A, Hirvela-Koski V, Kunnasranta M. Mortality, diseases and diet of European hedgehogs (Erinaceus europaeus) in an urban environment in Finland. Mammal Research. 2016;61(2):161–9. doi: 10.1007/s13364-015-0256-7 WOS:000372880400008.

22. Reed DH. Extinction risk in fragmented habitats. Animal Conservation. 2004;7:181–91. doi: 10.1017/s1367943004001313 WOS:000221970100009.

23. Braaker S, Kormann U, Bontadina F, Obrist M K,. Prediction of genetic connectivity in urban ecosystems by combining detailed movement data, genetic data and multi-path modelling. Landscape and Urban Planning. 2017;160:107–14. doi: 10.1016/j.landurbplan.2016.12.011 WOS:000394403300011.

24. Grimm NB, Faeth SH, Golubiewski NE, Redman CL, Wu J, Bai X, et al. Global change and the ecology of cities. Science. 2008;319(5864):756–60. doi: 10.1126/science.1150195 WOS:000252963000045. 18258902

25. Hof AR, Bright PW. The value of green-spaces in built-up areas for western hedgehogs. Lutra. 2009;52(2):69–82. BIOSIS:PREV201000094991.

26. Sæther HM. Overlevelse og tidlig spredning hos juvenile piggsvin (Erinaceus europaeus). [MSc thesis]. Norway: Norges Teknisk-Naturvitenskapelige Universitet; 1997.

27. Rasmussen SL. Personality, survivability and spatial behaviour of juvenile hedgehogs (Erinaceus europaeus): a comparison between rehabilitated and wild individuals. [MSc thesis]. Denmark: University of Copenhagen; 2013.

28. Doncaster CP, Rondinini C, Johnson PCD. Field test for environmental correlates of dispersal in hedgehogs Erinaceus europaeus. Journal of Animal Ecology. 2001;70(1):33–46. WOS:000167677400005.

29. Dowding CV, Shore RF, Worgan A, Baker PJ, Harris S. Accumulation of anticoagulant rodenticides in a non-target insectivore, the European hedgehog (Erinaceus europaeus). Environmental Pollution. 2010;158(1):161–6. doi: 10.1016/j.envpol.2009.07.017 WOS:000273245000022. 19674821

30. Robinson RA, Sutherland WJ. Post-war changes in arable farming and biodiversity in Great Britain. Journal of Applied Ecology. 2002;39(1):157–76. doi: 10.1046/j.1365-2664.2002.00695.x WOS:000174307300014.

31. Brakes CR, Smith RH. Exposure of non-target small mammals to rodenticides: short-term effects, recovery and implications for secondary poisoning. Journal of Applied Ecology. 2005;42(1):118–28. doi: 10.1111/j.1365-2664.2005.00997.x WOS:000227175200013.

32. Haigh A, Butler F, O'Riordan RM. Intra- and interhabitat differences in hedgehog distribution and potential prey availability. Mammalia. 2012;76(3):261–8. doi: 10.1515/mammalia-2011-0110 WOS:000308551400004.

33. Micol T, Doncaster CP, Mackinlay LA. Correlates of local variation in the abundance of hedgehogs Erinaceus europeaus. Journal of Animal Ecology. 1994;63(4):851–60. doi: 10.2307/5262 WOS:A1994PM01600011.

34. Young RP, Davison J, Trewby ID, Wilson GJ, Delahay RJ, Doncaster CP. Abundance of hedgehogs (Erinaceus europaeus) in relation to the density and distribution of badgers (Meles meles). Journal of Zoology. 2006;269(3):349–56. doi: 10.1111/j.1469-7998.2006.00078.x WOS:000238186400009.

35. Hubert P, Julliard R, Biagianti S, Poulle M-L. Ecological factors driving the higher hedgehog (Erinaceus europeaus) density in an urban area compared to the adjacent rural area. Landscape and Urban Planning. 2011;103(1):34–43. doi: 10.1016/j.landurbplan.2011.05.010 WOS:000295771500004.

36. Pettett CE, Moorhouse TP, Johnson PJ, Macdonald DW. Factors affecting hedgehog (Erinaceus europaeus) attraction to rural villages in arable landscapes. Eur J Wildl Res. 2017;63(54). doi: 10.1007/s10344-017-1113-6 WOS:000403084900013.

37. Morris PA. The effects of supplementary feeding on the movements of hedgehogs (Erinaceus europaeus) Mammal Rev. 1985;15(1):23–33. doi: 10.1111/j.1365-2907.1985.tb00383.x WOS:A1985ADU2800006.

38. Keller LF, Waller DM. Inbreeding effects in wild populations. Trends in Ecology & Evolution. 2002;17(5):230–41. doi: 10.1016/s0169-5347(02)02489-8 WOS:000175024300013.

39. Lacy RC. Importance of genetic variation to the viability of mammalian populations. Journal of Mammalogy. 1997;78(2):320–35. doi: 10.2307/1382885 WOS:A1997XB31600005.

40. Ralls K, Ballou JD, Dudash MR, Eldridge MDB, Fenster CB, Lacy RC, et al. Call for a Paradigm Shift in the Genetic Management of Fragmented Populations. Conservation Letters. 2018;11(2). doi: 10.1111/conl.12381 WOS:000430118100022. 29937920

41. Moran S, Turner PD, O'Reilly C. Multiple paternity in the European hedgehog. Journal of Zoology. 2009;278(4):349–53. doi: 10.1111/j.1469-7998.2009.00583.x WOS:000268222100011.

42. Becher SA, Griffiths R. Isolation and characterization of six polymorphic microsatellite loci in the European hedgehog Erinaceus europaeus. Molecular Ecology. 1997;6(1):89–90. doi: 10.1046/j.1365-294x.1997.00159.x WOS:A1997WH49800010. 9004520

43. Becher SA, Griffiths R. Genetic differentiation among local populations of the European hedgehog (Erinaceus europaeus) in mosaic habitats. Molecular Ecology. 1998;7(11):1599–604. doi: 10.1046/j.1365-294x.1998.00457.x WOS:000076933000018. 9819909

44. Santucci F, Emerson BC, Hewitt GM. Mitochondrial DNA phylogeography of European hedgehogs. Molecular Ecology. 1998;7(9):1163–72. doi: 10.1046/j.1365-294x.1998.00436.x WOS:000075779100007. 9734073

45. Henderson M, Becher SA, Doncaster CP, Maclean N. Five new polymorphic microsatellite loci in the European hedgehog Erinaceus europaeus. Molecular Ecology. 2000;9(11):1949–51. doi: 10.1046/j.1365-294x.2000.01098-18.x WOS:000165404800041. 11091346

46. Seddon JM, Santucci F, Reeve NJ, Hewitt GM. DNA footprints of European hedgehogs, Erinaceus europaeus and E-concolor. Pleistocene refugia, postglacial expansion and colonization routes. Molecular Ecology. 2001;10(9):2187–98. doi: 10.1046/j.0962-1083.2001.01357.x WOS:000171127700007. 11555261

47. Berggren KT, Ellegren H, Hewitt GM, Seddon JM. Understanding the phylogeographic patterns of European hedgehogs, Erinaceus concolor and E-europaeus using the MHC. Heredity. 2005;95(1):84–90. doi: 10.1038/sj.hdy.6800694 WOS:000230110700013. 16077505

48. Bolfikova B, Hulva P. Microevolution of sympatry: landscape genetics of hedgehogs Erinaceus europaeus and E. roumanicus in Central Europe. Heredity. 2012;108(3):248–55. doi: 10.1038/hdy.2011.67 WOS:000300596100012. 21863052

49. Fraser M, Sten S, Gotherstrom A. Neolithic Hedgehogs (Erinaceus europaeus) from the Island of Gotland show early contacts with the Swedish mainland. Journal of Archaeological Science. 2012;39(2):229–33. doi: 10.1016/j.jas.2011.08.006 WOS:000298464300003.

50. Bolfikova B, Konecny A, Pfaeffle M, Skuballa J, Hulva P. Population biology of establishment in New Zealand hedgehogs inferred from genetic and historical data: conflict or compromise? Molecular Ecology. 2013;22(14):3709–20. doi: 10.1111/mec.12331 WOS:000321552800007. 23711046

51. Bolfikova BC, Eliasova K, Loudova M, Krystufek B, Lymberakis P, Sandor AD, et al. Glacial allopatry vs. postglacial parapatry and peripatry: the case of hedgehogs. Peerj. 2017;5. doi: 10.7717/peerj.3163 WOS:000400303800001. 28462018

52. O’Reilly C. Genetic Analysis of hedgehogs in Regent’s Park. Unpublished report.: The Royal Parks, 2016.

53. Barthel L. Population structure and behaviour of the European hedgehog in an urbanized world. [PhD thesis]. Berlin: Freie Universität Berlin; 2019.

54. Aaris-Sorensen K. Diversity and dynamics of the mammalian fauna in Denmark throughout the last glacial-interglacial cycle, 115–0 kyr BP. Fossils and Strata. 2009;57:i–iv, 1–59. ZOOREC:ZOOR14603022625.

55. Statistics Denmark. Areal 2019 [cited 2019 May]. Available from:

56. Statistics Denmark. Afgrøder i dansk landbrug 2017 [cited 2019 May]. Available from:

57. Statistics Denmark. Population in Denmark 2019 [cited 2019 May]. Available from:

58. The Danish Road Directorate. Længden af offentlige veje i kommuner (xls) 2019 [cited 2019 October]. Available from:

59. Statistics Denmark. Vejnet 2018 [cited 2019 May]. Available from:

60. Elmeros M, Andersen, P.N., Sunde, P. Haugaard, L., Skov, F. & Madsen, A.B. Påkørte større vilde dyr i Danmark 2003–2012. Aarhus Universitet, DCE–Nationalt Center for Miljø og Energi, 2014.

61. Rasmussen SL, Nielsen JL, Jones OR, Berg TB, Pertoldi C. Supplementary material for the manuscript: Genetic structure of the European hedgehog (Erinaceus europaeus) in Denmark. December 12 2019 ed. Zenodo; 2019.

62. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, et al. A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species. Plos One. 2011;6(5). doi: 10.1371/journal.pone.0019379 WOS:000290224800026. 21573248

63. Rasmussen SL, Yashiro E, Sverrisdóttir E, Nielsen KL, Lukassen MB, Nielsen JL, et al. Applying the GBS Technique for the Genomic Characterization of a Danish Population of European Hedgehogs (Erinaceus europaeus). Genetics and Biodiversity (GABJ). 2019;3(2):78–86.

64. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genetics. 2011;43(5):491–501. doi: 10.1038/ng.806 WOS:000289972600023. 21478889

65. Peakall R, Smouse PE. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics. 2012;28(19):2537–9. doi: 10.1093/bioinformatics/bts460 WOS:000309687500024. 22820204

66. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155(2):945–59. WOS:000087475100039. 10835412

67. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology. 2005;14(8):2611–20. doi: 10.1111/j.1365-294X.2005.02553.x WOS:000229961500029. 15969739

68. Meirmans PG, Van Tienderen PH. GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes. 2004;4(4):792–4. doi: 10.1111/j.1471-8286.2004.00770.x WOS:000225496600081.

69. Hammer O, Harper DAT, Ryan PD. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica. 2001;4(1). ZOOREC:ZOOR13700068172.

70. Luikart G, Cornuet JM. Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conservation Biology. 1998;12(1):228–37. doi: 10.1046/j.1523-1739.1998.96388.x WOS:000072094300025.

71. Luikart G, Ryman N, Tallmon DA, Schwartz MK, Allendorf FW. Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conservation Genetics. 2010;11(2):355–73. doi: 10.1007/s10592-010-0050-7 WOS:000275455700003.

72. R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2019.

73. Statistics Denmark. By2: Population 1. January by municipality, size of the city, age and sex 2019 [cited 2019 August]. Available from:

74. Statistics Denmark. ARE207: Area 1. January by region 2019 [cited 2019 August]. Available from:

75. Statistics Denmark. AFG07: CULTIVATED AREA BY REGION, UNIT AND CROP 2019 [cited 2019 October]. Available from:

76. Schaid DJ, Guenther JC, Christensen GB, Hebbring S, Rosenow C, Hilker CA, et al. Comparison of microsatellites versus single-nucleotide polymorphisms in a genome linkage screen for prostate cancer-susceptibility loci. American Journal of Human Genetics. 2004;75(6):948–65. doi: 10.1086/425870 WOS:000224866400002. 15514889

77. 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. doi: 10.1186/1471-2164-11-218 WOS:000277271000001. 20359323

78. Putman AI, Carbone I. Challenges in analysis and interpretation of microsatellite data for population genetic studies. Ecology and Evolution. 2014;4(22):4399–428. doi: 10.1002/ece3.1305 WOS:000345316200017. 25540699

79. Aaris-Sørensen K. Danmarks forhistoriske dyreverden. 3rd ed. Denmark: Gyldendal; 1998.

80. Bennike O, Jensen JB. Postglacial, relative shore-level changes in Lillebaelt, Denmark. Geological Survey of Denmark and Greenland Bulletin. 2011;(23):37–40. WOS:000294389700009.

81. Jakobsen EM. Fribrødre Å: Geologi i vikingetid. VARV. 1987;4:104–15.

82. Bennike O, Nørgaard-Pedersen N, Jensen JB, Andresen KJ, Seidenkrantz M-S. Development of the western Limfjord, Denmark after the last deglaciation: a review with new data. Bulletin of the Geological Society of Denmark. 2019;in press.

83. Morris P. Hedgehog. Hedgehog [New Naturalist Vol 137]. 2018:i-ix, 1–404. ZOOREC:ZOOR15502009962.

84. Danish Nature Agency. Vejledning for vildtplejestationer 2013 [cited 2019 May]. Available from:

85. Kristiansson H. Distribution of the European hedgehog (Erinaceau europaeus L.) in Sweden and Finland. Ann Zool Fenn. 1981;18(2):115–9. WOS:A1981MK35200003.

86. Eurostat. Land cover, 2015: European Union; 2015 [cited 2019 May]. Available from:,_2015.png.

87. Provine WB. Ernst Mayr: genetics and speciation. Genetics. 2004;167(3):1041–6. WOS:000223109300001. 15280221

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