Glacial allopatry vs. postglacial parapatry and peripatry: the case of hedgehogs
Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
28462018
PubMed Central
PMC5407276
DOI
10.7717/peerj.3163
PII: 3163
Knihovny.cz E-zdroje
- Klíčová slova
- Balkan, Erinaceus roumanicus, Founder effect, Genetic differentiation, Interspecies interactions, Landscape genetic, Phylogeography,
- Publikační typ
- časopisecké články MeSH
Although hedgehogs are well-known examples of postglacial recolonisation, the specific processes that shape their population structures have not been examined by detailed sampling and fast-evolving genetic markers in combination with model based clustering methods. This study aims to analyse the impacts of isolation within glacial refugia and of postglacial expansion on the population structure of the Northern White-breasted hedgehog (Erinaceus roumanicus). It also discusses the role of the processes at edges of species distribution in its evolutionary history. The maternally inherited mitochondrial control region and the bi-parentally inherited nuclear microsatellites were used to examine samples within the Central Europe, Balkan Peninsula and adjacent islands. Bayesian coalescent inference and neutrality tests proposed a recent increase in the population size. The most pronounced pattern of population structure involved differentiation of the insular populations in the Mediterranean Sea and the population within the contact zone with E. europaeus in Central Europe. An interspecies hybrid was detected for the first time in Central Europe. A low genetic diversity was observed in Crete, while the highest genetic distances among individuals were found in Romania. The recent population in the post-refugial area related to the Balkan Peninsula shows a complex pattern with pronounced subpopulations located mainly in the Pannonian Basin and at the Adriatic and Pontic coasts. Detailed analyses indicate that parapatry and peripatry may not be the only factors that limit range expansion, but also strong microevolutionary forces that may change the genetic structure of the species. Here we present evidence showing that population differentiation may occur not only during the glacial restriction of the range into the refugia, but also during the interglacial range expansion. Population differentiation at the Balkan Peninsula and adjacent regions could be ascribed to diversification in steppe/forest biomes and complicated geomorphology, including pronounced geographic barriers as Carpathians.
Department of Zoology National Museum Prague Czech Republic
Faculty of Science Charles University Prague Prague Czech Republic
Faculty of Science University of Ostrava Ostrava Czech Republic
Faculty of Tropical AgriSciences Czech University of Life Sciences Prague Prague Czech Republic
Natural History Museum of Crete University of Crete Heraklion Greece
Zobrazit více v PubMed
Amori G, Hutterer R, Kryštufek B, Yigit N, Mitsain G, Palomo LJ. Erinaceus roumanicus. The IUCN Red List of Threatened Species 2016: e.T136344A22325720. 2016 doi: 10.2305/IUCN.UK.2016-3.RLTS.T136344A22325720.en. DOI
Anderson EC, Thompson E. A model-based method for identifying species hybrids using multilocus genetic data. Genetics. 2002;160:1217–1229. PubMed PMC
Balkenhol N, Cushman S, Storfer A, Waits L. Landscape genetics: concepts, methods, applications. Wiley-Blackwell; Hoboken: 2015.
Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution. 1999;16:37–48. doi: 10.1093/oxfordjournals.molbev.a026036. PubMed DOI
Bannikova AA, Lebedev VS, Abramov AV, Rozhnov VV. Contrasting evolutionary history of hedgehogs and gymnures (Mammalia: Erinaceomorpha) as inferred from a multigene study. Biological Journal of Linnean Society. 2014;112:499–519. doi: 10.1111/bij.12299. DOI
Becher SA, Griffiths R. Isolation and characterization of six polymorphic microsatellite loci in the European hedgehog Erinaceus europaeus. Molecular Ecology. 1997;6:89–90. doi: 10.1046/j.1365-294X.1997.00159.x. PubMed DOI
Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F. 1999. GENETIX v.405 logiciel sous Windows pour la génetique des populations. http://kimura.univ-montp2fr/genetix/
Blair C, Weigel DE, Balazik M, Keeley AT, Walker FM, Landguth E, Cushman S, Murphy M, Waits L, Balkenhol N. A simulation-based evaluation of methods for inferring linear barriers to gene flow. Molecular Ecology Resources. 2012;12:822–833. doi: 10.1111/j.1755-0998.2012.03151.x. PubMed DOI
Bogdanov AS, Bannikova AA, Pirusskii YM, Formozov NA. The first genetic evidence of hybridization between West European and Northern White-breasted hedgehogs (Erinaceus europaeus and E. roumanicus) in Moscow region. Biological Bulletin. 2009;36:647–651. doi: 10.1134/S106235900906017X. 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
Bolfíková B, Konečný A, Pfäffle M, Skuballa J. Population biology of establishment in New Zealand hedgehogs inferred from genetic and historical data: conflict or compromise? Molecular Ecology. 2013;22:3709–3720. doi: 10.1111/mec.12331. PubMed DOI
Brewer S, Cheddadi R, Beaulieu JL, Reille M. The spread of deciduous Quercus throughout Europe since the last glacial period. Forest Ecology and Management. 2002;156:27–48. doi: 10.1016/S0378-1127(01)00646-6. DOI
Chen C, Durand E, Forbes F, Francois O. Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Molecular Ecology Notes. 2007;7:747–756. doi: 10.1111/j.1471-8286.2007.01769.x. DOI
Coyne JA, Orr HA. Speciation. Sinauer Associates; Sunderland: 2004.
Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology. 2007;7:214. doi: 10.1186/1471-2148-7-214. PubMed DOI PMC
Drummond AJ, Rambaut A, Shapiro B, Pybus OG. Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution. 2005;22:1185–1192. doi: 10.1093/molbev/msi103. PubMed DOI
Durand E, Jay F, Gaggiotti OE, François O. Spatial inference of admixture proportions and secondary contact zones. Molecular Biology and Evolution. 2009;26:1963–1973. doi: 10.1093/molbev/msp106. PubMed DOI
Earl DA, VonHoldt BM. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetic Resources. 2012;4:359–361. doi: 10.1007/s12686-011-9548-7. DOI
ESRI . ArcGIS desktop: release 10. Redlands: Environmental Systems Research Institute; 2014.
Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology. 2005;14(261):1–2620. doi: 10.1111/j.1365-294X.2005.02553.x. PubMed DOI
Excoffier L, Foll M, Petit RJ. Genetic consequences of range expansions. Annual Review of Ecology, Evolution, and Systematics. 2009;40(48):1–501. doi: 10.1146/annurev.ecolsys.39.110707.173414. DOI
Excoffier L, Ray N. Surfing during population expansions promotes genetic revolutions and structuration. Trends in Ecology & Evolution. 2008;23(34):7–351. doi: 10.1016/j.tree.2008.04.004. PubMed DOI
Fijarczyk A, Nadachowska K, Hofman S, Litvinchuk SN, Babik W, Stuglik M, Gollmann G, Choleva L, Cogălniceanu D, Vukov T, Džukić G, Szymura JM. Nuclear and mitochondrial phylogeography of the European fire-bellied toads Bombina bombina and Bombina variegata supports their independent histories. Molecular Ecology. 2011;20:3381–3398. doi: 10.1111/j.1365-294X.2011.05175.x. PubMed DOI
Giagia-Athanasopoulou EB, Markakis G. Multivariate analysis of morphometric characters in the Eastern hedgehog Erinaceus concolor from Greece and adjacent areas. Zeitschrift Fuer Saeugetierkunde. 1996;61:129–139.
Goudet J. FSTAT (Version 1.2): a computer note computer program to calculate F-statistics. Journal of Heredity. 1995;86:485–486. doi: 10.1093/oxfordjournals.jhered.a111627. DOI
Guillot G, Mortier F, Estoup A. GENELAND: a computer package for landscape genetics. Molecular Ecology Notes. 2005;5:712–715. doi: 10.1111/j.1471-8286.2005.01031.x. DOI
Gvoždík V, Jandzik D, Lymberakis P, Jablonski D, Moravec J. Slow worm, Anguis fragilis (Reptilia: Anguidae) as a species complex: genetic structure reveals deep divergences. Molecular Phylogenetics and Evolution. 2010;55:460–472. doi: 10.1016/j.ympev.2010.01.007. PubMed DOI
Henderson M, Becher SA, Doncaster CP, Maclean N. Five new polymorphic microsatellite loci in the European hedgehog, Erinaceus europaeus. Molecular Ecology. 2000;9:1949–1950. doi: 10.1046/j.1365-294x.2000.01098-18.x. PubMed DOI
Hewitt GM. The genetic legacy of the quaternary ice ages. Nature. 2000;405:907–913. doi: 10.1038/35016000. PubMed DOI
Hewitt GM. Speciation, hybrid zones and phylogeography—or seeing genes in space and time. Molecular Ecology. 2001;10:537–549. doi: 10.1046/j.1365294x.2001.01202.x. PubMed DOI
Hulva P, Benda P, Hanák V, Evin A, Horáček I. New mitochondrial lineages within the Pipistrellus pipistrellus complex from Mediterranean Europe. Folia Zoologica. 2007;56:378–388.
Hulva P, Fornůsková A, Chudárková A, Evin A, Allegrini B, Benda P, Bryja J. Mechanisms of radiation in a bat group from the genus Pipistrellus inferred by phylogeography, demography and population genetics. Molecular Ecology. 2010;19:5417–5431. doi: 10.1111/j.1365-294X.2010.04899.x. PubMed DOI
Huntley B. Climatic change and reconstruction. Journal of Quarternary Science. 1999;14:513–520. doi: 10.1002/(SICI)1099-1417(199910)14:6<513::AID-JQS486>3.0.CO;2-E. DOI
Huntley B, Birks HJB. Cambridge University Press; Cambridge: 1983. An atlas of past and present pollen maps for Europe: 0–13000 years ago.
Jarman MR. Human influence in the development of the cretan mammalian Fauna. In: Reese DS, editor. Pleistocene and holocene fauna of crete and its first settlers. Prehistoric Press; Madison: 1996.
Jensen AB. Overwintering of European hedgehogs Erinaceus europaeus in a Danish rural area. Acta Theriologica. 2004;49:145–155. doi: 10.1007/BF03192516. DOI
Joger U, Fritz U, Guicking D, Kalyabina-Hauf S, Nagy ZT, Wink M. Phylogeography of western Palaearctic reptiles—Spatial and temporal speciation patterns. Zoologischer Anzeiger—A Journal of Comparative Zoology. 2007;246:293–313. doi: 10.1016/j.jcz.2007.09.002. DOI
Katoh K, Standley DM. MAFFT multiple sequence alignment software, version 7: improvements in performance and usability. Molecular Biology and Evolution. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. doi: 10.1093/bioinformatics/bts199. PubMed DOI PMC
King RA, Ferris C. Chloroplast DNA phylogeography of Alnus glutinosa (L.) Gaertn. Molecular Ecology. 1998;7:1151–1161. doi: 10.1046/j.1365-294x.1998.00432.x. DOI
Klopfstein S, Currat M, Excoffier L. The fate of mutations surfing on the wave of a range expansion. Molecular Biology and Evolution. 2006;23:482–490. doi: 10.1093/molbev/msj057. PubMed DOI
Kryštufek B, Reed JM. Pattern and process in Balkan biodiversity—an overview. In: Griffiths HI, Kryštufek B, Reed JM, editors. Balkan biodiversity: pattern and process in the European hotspot. Dordrecht: Springer Netherlands; 2004. pp. 1–8.
Kryštufek B, Tvrtković N, Paunović M, Ozkan 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
Lax E, Strasser TF. Early holocene extinctions on crete; the search for the cause. Journal of Meditteranean Archaeology. 1992;5:203–224. doi: 10.1558/jmea.v5i1.203. DOI
Mantel N. The detection of disease clustering and a generalized regression approach. Cancer Research. 1967;27:209–220. PubMed
Miller MP. Alleles In Space (AIS): computer software for the joint analysis of interindividual spatial and genetic information. Journal of Heredity. 2005;96:722–724. doi: 10.1093/jhered/esi119. PubMed DOI
Posada D, Crandall K. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14:817–818. doi: 10.1093/bioinformatics/14.9.817. PubMed DOI
Pritchard JK, Stephens M, Donnely PJ. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–959. PubMed PMC
Rambaut A, Suchard MA, Xie D, Drummond AJ. 2014. Tracer v1.6. http://beast.bio.ed.ac.uk/Tracer .
Ramírez-Soriano A, Ramos-Onsins SE, Rozas J, Calafell F, Navarro A. Statistical power analysis of neutrality tests under demographic expansions, contractions and bottlenecks with recombination. Genetics. 2008;179:555–567. doi: 10.1534/genetics.107.083006. PubMed DOI PMC
Ramos-Onsins SE, Rozas J. Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution. 2002;19:2092–2100. doi: 10.1093/molbev/msl052. PubMed DOI
Rautio A, Valtonen A, Auttila M, Kunnasranta M. Nesting patterns of European hedgehogs (Erinaceus europaeus) under northern conditions. Acta Theriologica. 2014;59:173–181. doi: 10.1007/s13364-013-0150-0. DOI
Říčanová S, Bryja J, Cosson JF, Gedeon C, Choleva L, Ambros M, Sedláček F. Depleted genetic variation of the European ground squirrel in Central Europe in both microsatellites and the major histocompatibility complex gene: implication for conservation. Conservation Genetics. 2011;12:1115–1129. doi: 10.1007/s10592-011-0213-1. DOI
Rosenberg N. Distruct: a program for the graphical display of population structure. Molecular Ecology Notes. 2004;4:137–138. doi: 10.1046/j.1471-8286.2003.00566.x. DOI
Rousset F. GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources. 2008;8:103–106. doi: 10.1111/j.1471-8286.2007.01931.x. PubMed DOI
Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003;19:2496–2497. doi: 10.1093/bioinformatics/btg359. PubMed DOI
Santucci F, Emerson BC, Hewitt GM. Mitochondrial DNA phylogeography of European hedgehogs. Molecular Ecology. 1998;7:1163–1172. doi: 10.1046/j.1365-294x.1998.00436.x. PubMed DOI
Schaschl H, Lymberakis P, Suchentruck F. On allozyme and cyt-b gene characteristics of Cretan hedgehogs, Erinaceus consolor nesiotes Bate, 1906. Mammalian Biology. 2002;67:257–267. doi: 10.1078/1616-5047-00040. DOI
Schule W. Mammals, vegetation and the initial human settlement of the Mediterranean islands: a palaeoecological approach. Journal of Biogeography. 1993;20:399–412. doi: 10.2307/2845588. DOI
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;10:2187–2198. doi: 10.1046/j.0962-1083.2001.01357.x. PubMed DOI
Seddon JM, Santucci F, Reeve N, Hewitt GM. Caucasus Mountains divide postulated postglacial colonization routes in the white-breasted hedgehog, Erinaceus concolor. Journal of Evolutionary Biology. 2002;15:463–467. doi: 10.1046/j.1420-9101.2002.00408.x. DOI
Stewart JR, Lister AM, Barnes I, Dalén L. Refugia revisited: individualistic responses of species in space and time. Proceedings of the Royal Society. 2010;277:661–666. doi: 10.1098/rspb.2009.1272. PubMed DOI PMC
Tyrberg T. Arctic, montane and steppe birds as glacial relicts in the west palearctic. Ornithologische Verhandlungen. 1991;25:29–49.
Tzedakis PC. The Balkans as prime glacial refugial territory of European temperate trees. In: Griffiths HI, Kryštufek B, Reed JM, editors. Balkan biodiversity: pattern and process in the European hotspot. Dordrecht: Springer Netherlands; 2004. pp. 49–65.
Van der Geer A, Lyras G, De Vos J, Dermitzakis M. Evolution of Island mammals. Wiley-Blackwell; London: 2010.
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes. 2004;4:535–538. doi: 10.1111/j.1471-8286.2004.00684.x. DOI