Hedgehogs, as medium-sized plantigrade insectivores with low basal metabolic rates and related defensive anti-predator strategies, are quite sensitive to temperature and ecosystem productivity. Their ranges therefore changed dramatically due to Pleistocene climate oscillations, resulting in allopatric speciation and the subsequent formation of secondary contact zones. Such interactions between closely related species are known to generate strong evolutionary forces responsible for niche differentiation. In this connection, here, we detail the results of research on the phenotypic evolution in the two species of hedgehog present in central Europe, as based on genetics and geometric morphometrics in samples along a longitudinal transect that includes the contact zone between the species. While in allopatry, Erinaceus europaeus is found to have a larger skull than E. roumanicus and distinct cranial and mandibular shapes; the members of the two species in sympatry are smaller and more similar to each other, with a convergent shape of the mandible. The relevant data fail to reveal any major role for either hybridisation or clinal variation. We, therefore, hypothesise that competitive pressure exerted on the studied species does not generate divergent selection sufficient for divergent character displacement to evolve, instead giving rise to convergent selection in the face of resource limitation in the direction of smaller skull size. Considering the multi-factorial constraints present in the relevant adaptive landscape, reduction in size could also be facilitated by predator pressure in ecosystems characterised by mesopredator release and other anthropogenic factors. As the function of the animals' lower jaw is mainly connected with feeding (in contrast to the cranium whose functions are obviously more complex), we interpret the similarity in shape as reflecting local adaptations to overlapping dietary resources in the two species and hence as convergent character displacement.

Department of Zoology Faculty of Science Charles University Prague Viničná 7 128 00 Prague Czech Republic

Faculty of Science University of Ostrava Chittussiho 10 710 00 Ostrava Czech Republic

Faculty of Tropical AgriSciences Czech University of Life Sciences Prague Kamýcká 129 165 21 Prague Czech Republic

Institut des Sciences de l'Evolution Montpellier Univ Montpellier CNRS EPHE IRD 2 place Eugène Bataillon CC065 CEDEX 5 34095 Montpellier France

Museum and Institute of Zoology Polish Academy of Sciences Wilcza 64 00 679 Warszawa Poland

Zobrazit více v PubMed

Hewitt G.M. Post-Glacial Re-Colonization of European Biota. Biol. J. Linn. Soc. 1999;68:87–112. doi: 10.1111/j.1095-8312.1999.tb01160.x. DOI

Seddon J.M., Santucci F., Reeve N.J., Hewitt G.M. DNA Footprints of European Hedgehogs, Erinaceus europaeus and E. concolor: Pleistocene Refugia, Postglacial Expansion and Colonization Routes. Mol. Ecol. 2001;10:2187–2198. doi: 10.1046/j.0962-1083.2001.01357.x. PubMed DOI

Bolfíková B., Hulva P. Microevolution of Sympatry: Landscape Genetics of Hedgehogs Erinaceus europaeus and E. roumanicus in Central Europe. Heredity. 2012;108:248–255. doi: 10.1038/hdy.2011.67. PubMed DOI PMC

Černá Bolfíková B., Eliášová K., Loudová M., Kryštufek B., Lymberakis P., Sándor A.D., Hulva P. Glacial Allopatry vs. Postglacial Parapatry and Peripatry: The Case of Hedgehogs. PeerJ. 2017;5:e3163:1–e3163:21. doi: 10.7717/peerj.3163. PubMed DOI PMC

Curto M., Winter S., Seiter A., Schmid L., Scheicher K., Barthel L.M.F., Plass J., Meimberg H. Application of a SSR-GBS Marker System on Investigation of European Hedgehog Species and Their Hybrid Zone Dynamics. Ecol. Evol. 2019;9:2814–2832. doi: 10.1002/ece3.4960. PubMed DOI PMC

Evin A., Horáček I., Hulva P. Phenotypic Diversification and Island Evolution of Pipistrelle Bats (Pipistrellus pipistrellus Group) in the Mediterranean Region Inferred from Geometric Morphometrics and Molecular Phylogenetics. J. Biogeogr. 2011;38:2091–2105. doi: 10.1111/j.1365-2699.2011.02556.x. DOI

Coyne J., Orr H. Speciation. Sinauer Associates; Sunderland, MA, USA: 2004.

Reifová R., Reif J., Antczak M., Nachman M.W. Ecological Character Displacement in the Face of Gene Flow: Evidence from Two Species of Nightingales. BMC Evol. Biol. 2011;11:138:1–138:11. doi: 10.1186/1471-2148-11-138. PubMed DOI PMC

Kryštufek B., Tvrtković N., Paunović M., Özkan B. Size Variation in the Northern White-Breasted Hedgehog Erinaceus roumanicus: Latitudinal Cline and the Island Rule. Mammalia. 2009;73:299–306. doi: 10.1515/MAMM.2009.055. DOI

Reeve N. Hedgehogs. T & AD Poyser; London, UK: 1994.

Ruprecht A. Correlation Structure of Skull Dimensions in European Hedgehogs. Acta Theriol. 1972;17:419–442. doi: 10.4098/AT.arch.72-34. DOI

Holz H., Niethammer J. Erianceus concolor Martin, 1838—Weissbrustigel, Ostigel. In: Niethammer J., Krapp F., editors. Handbuch der Säugetiere Europas 3/1. Aula-Verlag; Wiesbaden, Germany: 1990. pp. 50–64.

Holz H., Niethammer J. Erinaceus europaeus Linnaeus, 1758—Braunbrustigel, Westigel. In: Niethammer J., Krapp F., editors. Handbuch der Säugetiere Europas 3/1. Aula-Verlag; Wiesbaden, Germany: 1990. pp. 26–49.

Kryštufek B. Cranial Variability in the Eastern Hedgehog Erinaceus concolor (Mammalia: Insectivora) J. Zool. 2002;258:365–373. doi: 10.1017/S0952836902001516. DOI

Hrabě V. Variation in Cranial Measurement of Erinaceus concolor roumanicus (Insectivora, Mammalia) Zool. List. 1976;25:315–326.

Niethammer J., Krapp F. In: Handbuch Der Säugetiere Europas. Bd. 3/1, Insektenfresser-Insectivora, Herrentiere-Primates. Niethammer J., Krapp F., editors. Aula-Verlag; Wiesbaden, Germany: 1990.

Hrabě V. Variation in Somatic Characters of Two Species of Erinaceus (Insectivora, Mammalia) in Relation to Individual Age. Zool. List. 1975;24:335–351.

Wolff P. Unterscheidungsmerkmale am Unterkiefer von Erinaceus europaeus L. und Erinaceus concolor Martin. Ann. Naturhist. Mus. Wien. 1976;80:337–341. doi: 10.2307/41769613. DOI

Kratochvíl J. Die Hirnmasse Der Mitteleuropäischen Arten Der Gattung Erinaceus (Insectivora, Mamm.) Folia Zool. 1980;29:1–20.

Hrabě V. Notes on the Dentition of Two Erinaceus Spp. from Czechoslovakia (Insectivora, Mammalia) Folia Zool. 1981;30:311–316.

Hanken J., Hall B.K. The Skull, Volume 3: Functional and Evolutionary Mechanisms. University of Chicago Press; Chicago, IL, USA: 1993.

Škoudlín J. Zur Altersbestimmung Bei Erinaceus europaeus Und Erinaceus concolor (Insectivora: Erinaceidae) Věst. Českosl. Spol. Zool. 1976;40:300–306.

Herter K. Studien Zur Verbreitung Der Europäischen Igel. Arch. Naturgesch. 1934;3:21–382.

Rohlf F.J., Slice D. Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks. Syst. Zool. 1990;39:40–59. doi: 10.2307/2992207. DOI

Goodall C.R. Procrustes Methods in the Statistical Analysis of Shape Revisited. In: Mardia K.V., Gill C.A., editors. Current Issues in Statistical Shape Analysis. Leeds University Press; Leeds, UK: 1995. pp. 18–33.

Bookstein F. Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge University Press; New York, NY, USA: 1991. DOI

Evin A., Cucchi T., Cardini A., Strand Vidarsdottir U., Larson G., Dobney K. The Long and Winding Road: Identifying Pig Domestication through Molar Size and Shape. J. Archaeol. Sci. 2013;40:735–743. doi: 10.1016/j.jas.2012.08.005. DOI

Monteiro L.R. Multivariate Regression Models and Geometric Morphometrics: The Search for Causal Factors in the Analysis of Shape. Syst. Biol. 1999;48:192–199. doi: 10.1080/106351599260526. PubMed DOI

Schlager S. Morpho and Rvcg—Shape Analysis in R. In: Zheng G., Li S., Szekely G., editors. Statistical Shape and Deformation Analysis: Methods, Implementation and Applications. Academic Press; San Diego, CA, USA: 2017. pp. 217–256.

Baylac M., Frieß M. Fourier Descriptors, Procrustes Superimposition, and Data Dimensionality: An Example of Cranial Shape Analysis in Modern Human Populations. In: Slice D.E., editor. Modern Morphometrics in Physical Anthropology. Springer; Boston, MA, USA: 2005. pp. 145–162. DOI

Benjamini Y., Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J. R. Stat. Soc. Ser. B. 1995;57:289–300. doi: 10.1111/j.2517-6161.1995.tb02031.x. DOI

Mahalanobis P. On the Generalized Distance in Statistics. Proc. Natl. Acad. Sci. India. 1936;2:49–55.

Mantel N. The Detection of Disease Clustering and a Generalized Regression Approach. Cancer Res. 1967;27:209–220. PubMed

Sokal R.R., Rohlf F.J. Biometry: The Principles and Practice of Statistics in Biological Research. 3rd ed. W.H. Freeman and Co.; New York, NY, USA: 1995.

Stayton C.T. The Definition, Recognition, and Interpretation of Convergent Evolution, and Two New Measures for Quantifying and Assessing the Significance of Convergence. Evolution. 2015;69:2140–2153. doi: 10.1111/evo.12729. PubMed DOI

Stayton C.T. Testing Hypotheses of Convergence with Multivariate Data: Morphological and Functional Convergence among Herbivorous Lizards. Evolution. 2006;60:824–841. doi: 10.1111/j.0014-3820.2006.tb01160.x. PubMed DOI

Zelditch M.L., Swiderski D.L., Sheets H.D. Geometric Morphometrics for Biologists: A Primer. 2nd ed. Elsevier, Academic Press; Amsterdam, The Netherlands: 2012.

Adams D., Collyer M., Kaliontzopoulou A., Sherratt E. Geomorph: Software for Geometric Morphometric Analyses. [(accessed on 20 December 2019)];2019 R Package Version 3.1.0. Available online: https://github.com/geomorphR/geomorph.

Dray S., Dufour A.-B. The Ade4 Package: Implementing the Duality Diagram for Ecologists. J. Stat. Softw. 2007;22:1–20. doi: 10.18637/jss.v022.i04. DOI

R Core Team R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. [(accessed on 29 February 2020)];2020 Available online: https://www.r-project.org.

Poduschka W., Poduschka C. Kreuzungsversuche an Mitteleuropäischen Igeln. Säugetierk. Mitt. 1983;31:1–12.

O’Regan H.J., Kitchener A.C. The Effects of Captivity on the Morphology of Captive, Domesticated and Feral Mammals. Mamm. Rev. 2005;35:215–230. doi: 10.1111/j.1365-2907.2005.00070.x. DOI

Evin A., Dobney K., Schafberg R., Owen J., Strand Vidarsdottir U., Larson G., Cucchi T. Phenotype and Animal Domestication: A Study of Dental Variation between Domestic, Wild, Captive, Hybrid and Insular Sus scrofa. BMC Evol. Biol. 2015;15:6. doi: 10.1186/s12862-014-0269-x. PubMed DOI PMC

Meiri S., Simberloff D., Dayan T. Community-Wide Character Displacement in the Presence of Clines: A Test of Holarctic Weasel Guilds. J. Anim. Ecol. 2011;80:824–834. doi: 10.1111/j.1365-2656.2011.01827.x. PubMed DOI

Škoudlín J. Craniometric Analysis of a Czechoslovak and a Polish Population of Erinaceus concolor (Mammalia: Erinaceidae) Věst. Českosl. Spol. Zool. 1982;46:304–316.

Smith K.K. The Form of the Feeding Apparatus in Terrestrial Vertebrates: Studies of Adaptation and Constraint. In: Hanken J., Hall B.K., editors. The Skull. University of Chicago Press; Chicago, IL, USA: 1993. pp. 150–196.

Zelditch M.L., Ye J., Mitchell J.S., Swiderski D.L. Rare Ecomorphological Convergence on a Complex Adaptive Landscape: Body Size and Diet Mediate Evolution of Jaw Shape in Squirrels (Sciuridae) Evolution. 2017;71:633–649. doi: 10.1111/evo.13168. PubMed DOI

Hendry A.P., Kinnison M.T. Perspective: The Pace of Modern Life: Measuring Rates of Contemporary Microevolution. Evolution. 1999;53:1637–1653. doi: 10.1111/j.1558-5646.1999.tb04550.x. PubMed DOI

Carroll S.P., Hendry A.P., Reznick D.N., Fox C.W. Evolution on Ecological Time-Scales. Funct. Ecol. 2007;21:387–393. doi: 10.1111/j.1365-2435.2007.01289.x. DOI

Herrel A., Huyghe K., Vanhooydonck B., Backeljau T., Breugelmans K., Grbac I., Van Damme R., Irschick D.J. Rapid Large-Scale Evolutionary Divergence in Morphology and Performance Associated with Exploitation of a Different Dietary Resource. Proc. Natl. Acad. Sci. USA. 2008;105:4792–4795. doi: 10.1073/pnas.0711998105. PubMed DOI PMC

Lovegrove B.G. The Evolution of Body Armor in Mammals: Plantigrade Constraints of Large Body Size. Evolution. 2001;55:1464–1473. doi: 10.1111/j.0014-3820.2001.tb00666.x. PubMed DOI

Morris P.J.R., Cobb S.N.F., Cox P.G. Convergent Evolution in the Euarchontoglires. Biol. Lett. 2018;14:20180366:1–20180366:4. doi: 10.1098/rsbl.2018.0366. PubMed DOI PMC

Cheverud J.M. Phenotypic, Genetic, and Environmental Morphological Integration in the Cranium. Evolution. 1982;36:499–516. doi: 10.1111/j.1558-5646.1982.tb05070.x. PubMed DOI

Goswami A. Cranial Modularity Shifts during Mammalian Evolution. Am. Nat. 2006;168:270–280. doi: 10.1086/505758. PubMed DOI

Alroy J. Cope’s Rule and the Dynamics of Body Mass Evolution in North American Fossil Mammals. Science. 1998;280:731–734. doi: 10.1126/science.280.5364.731. PubMed DOI

Stankowich T., Campbell L.A. Living in the Danger Zone: Exposure to Predators and the Evolution of Spines and Body Armor in Mammals. Evolution. 2016;70:1501–1511. doi: 10.1111/evo.12961. PubMed DOI

Williams B.M., Baker P.J., Thomas E., Wilson G., Judge J., Yarnell R.W. Reduced Occupancy of Hedgehogs (Erinaceus europaeus) in Rural England and Wales: The Influence of Habitat and an Asymmetric Intra-Guild Predator. Sci. Rep. 2018;8:1–10. doi: 10.1038/s41598-018-30130-4. PubMed DOI PMC

Ritchie E.G., Johnson C.N. Predator interactions, mesopredator release and biodiversity conservation. Ecol. Lett. 2009;12:982–998. doi: 10.1111/j.1461-0248.2009.01347.x. PubMed DOI

Hof A.R., Bright P.W. Quantifying the Long-Term Decline of the West European Hedgehog in England by Subsampling Citizen-Science Datasets. Eur. J. Wildl. Res. 2016;62:407–413. doi: 10.1007/s10344-016-1013-1. DOI

Hulva P., Černá Bolfíková B., Woznicová V., Jindřichová M., Benešová M., Mysłajek R.W., Nowak S., Szewczyk M., Niedźwiecka N., Figura M., et al. Wolves at the Crossroad: Fission–Fusion Range Biogeography in the Western Carpathians and Central Europe. Divers. Distrib. 2018;24:179–192. doi: 10.1111/ddi.12676. DOI

Ploi K., Curto M., Bolfíková B.Č., Loudová M., Hulva P., Seiter A., Fuhrmann M., Winter S., Meimberg H. Evaluating the Impact of Wildlife Shelter Management on the Genetic Diversity of Erinaceus europaeus and E. roumanicus in Their Contact Zone. Animals. 2020;10:1452. doi: 10.3390/ani10091452. PubMed DOI PMC

Host-driven subspeciation in the hedgehog fungus, Trichophyton erinacei, an emerging cause of human dermatophytosis