Divergent evolutionary processes associated with colonization of offshore islands

. 2013 Oct ; 22 (20) : 5205-20. [epub] 20130903

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid23998800

Grantová podpora
Wellcome Trust - United Kingdom
GR071037 Wellcome Trust - United Kingdom

Oceanic islands have been a test ground for evolutionary theory, but here, we focus on the possibilities for evolutionary study created by offshore islands. These can be colonized through various means and by a wide range of species, including those with low dispersal capabilities. We use morphology, modern and ancient sequences of cytochrome b (cytb) and microsatellite genotypes to examine colonization history and evolutionary change associated with occupation of the Orkney archipelago by the common vole (Microtus arvalis), a species found in continental Europe but not in Britain. Among possible colonization scenarios, our results are most consistent with human introduction at least 5100 bp (confirmed by radiocarbon dating). We used approximate Bayesian computation of population history to infer the coast of Belgium as the possible source and estimated the evolutionary timescale using a Bayesian coalescent approach. We showed substantial morphological divergence of the island populations, including a size increase presumably driven by selection and reduced microsatellite variation likely reflecting founder events and genetic drift. More surprisingly, our results suggest that a recent and widespread cytb replacement event in the continental source area purged cytb variation there, whereas the ancestral diversity is largely retained in the colonized islands as a genetic 'ark'. The replacement event in the continental M. arvalis was probably triggered by anthropogenic causes (land-use change). Our studies illustrate that small offshore islands can act as field laboratories for studying various evolutionary processes over relatively short timescales, informing about the mainland source area as well as the island.

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Angerbjorn A (1986) Gigantism in island populations of wood mice (Apodemus) in Europe. Oikos, 47, 47–56

Bandelt HJ, Forster P, Röhl A (1999) Median‐joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48 PubMed

Barnes I, Matheus P, Shapiro B, Jensen D, Cooper A (2002) Dynamics of Pleistocene population extinctions in Beringian brown bears. Science, 295, 2267–2270 PubMed

Beirne BP (1952) The Origin and History of the British Fauna. Methuen, London

Berry RJ (1996) Small mammal differentiation on islands. Philosophical Transactions of the Royal Society of London. B, Biological Sciences, 351, 753–764 PubMed

Berry RJ (2000) Orkney Nature. Poyser, London

Berry RJ, Rose FEN (1975) Islands and the evolution of Microtus arvalis (Microtinae). Journal of Zoology, 177, 395–409

Boessenkool S, Taylor SS, Tepolt CK, Komdeur J, Jamieson IG (2007) Large mainland populations of South Island robins retain greater genetic diversity than offshore island refuges. Conservation Genetics, 8, 705–714

Bookstein FL (1997) Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Medical Image Analysis, 1, 225–243 PubMed

Borkowska A, Ratkiewicz M (2008) Sex‐related spatial structure and effective population size in the common vole, Microtus arvalis, as revealed by mtDNA analysis. Annales Zoologici Fennici, 45, 255–262

Bowen DQ, Phillips FM, McCabe AM, Knutz PC, Sykes GA (2002) New data for the last glacial maximum in Great Britain and Ireland. Quaternary Science Reviews, 21, 89–101

Broodbank C (2006) The origins and early development of Mediterranean maritime activity. Journal of Mediterranean Archaeology, 19, 199–230

de Bruyn M, Hoelzel AR, Carvalho GR, Hofreiter M (2011) Faunal histories from Holocene ancient DNA. Trends in Ecology and Evolution, 26, 405–413 PubMed

Bunting MJ (1996) The development of heathland in Orkney, Scotland: pollen records from Loch of Knitchen (Rousay) and Loch of Torness (Hoy). The Holocene, 6, 193–212

Chan YF, Jones FC, McConnell Eet al (2012) Parallel selection mapping using artificially selected mice reveals body weight control loci. Current Biology, 22, 794–800 PubMed

Corbet GB (1961) Origin of British insular races of small mammals and of Lusitanian fauna. Nature, 191, 1037–1040

Corbet GB (1986) Temporal and spatial variation of dental pattern in the voles, Microtus arvalis, of the Orkney Islands. Journal of Zoology, 208, 395–402

Currant A, Jacobi R (2001) A formal mammalian biostratigraphy for the Late Pleistocene of Britain. Quaternary Science Reviews, 20, 1707–1716

Cyprien AL, Visset L, Carcaud N (2004) Evolution of vegetation landscapes during the Holocene in the central and downstream Loire basin (Western France). Vegetation History and Archaeobotany, 13, 181–196

Delattre P, Giraudoux P, Baudry Jet al (1992) Land use patterns and types of common vole (Microtus arvalis) population kinetics. Agriculture, Ecosystems & Environment, 39, 153–168

DeWoody JA, Chesser RK, Baker RJ (1999) A translocated mitochondrial cytochrome b pseudogene in voles (Rodentia: Microtus). Journal of Molecular Evolution, 48, 380–382 PubMed

Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214. PubMed PMC

Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biology, 4, e88. PubMed PMC

Ehlers J, Gibbard PL (2004) Quaternary Glaciations – Extent and Chronology. Part I: Europe. Elsevier, Amsterdam

Emerson BC (2002) Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Molecular Ecology, 11, 951–966 PubMed

Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50 PubMed PMC

Fink S, Fischer MC, Excoffier L, Heckel G (2010) Genomic scans support repetitive continental colonization events during the rapid radiation of voles (Rodentia: Microtus): the utility of AFLPs versus mitochondrial and nuclear sequence markers. Systematic Biology, 59, 548–572 PubMed

Finnegan LA, Edwards CJ, Rochford JM (2008) Origin of, and conservation units in, the Irish red squirrel (Sciurus vulgaris) population. Conservation Genetics, 9, 1099–1109

Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity, 78, 311–327 PubMed

Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915–925 PubMed PMC

Gorman ML, Reynolds P (2008) Orkney and Guernsey vole In: Mammals of the British Isles: Handbook, 4th edn (eds Harris S, Yalden DW), pp. 107–110 The Mammal Society, Southampton

Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F‐statistics. Journal of Heredity, 86, 485–486

Grant PR (ed.) (2008) Evolution on Islands. Oxford University Press, Oxford

Hall TA (1999) BioEdit: a user‐friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symposium Series, 41, 95–98

Haynes S, Jaarola M, Searle JB (2003) Phylogeography of the common vole (Microtus arvalis) with particular emphasis on the colonization of the Orkney archipelago. Molecular Ecology, 12, 951–956 PubMed

Heckel G, Burri R, Fink S, Desmet JF, Excoffier L (2005) Genetic structure and colonization processes in European populations of the common vole, Microtus arvalis. Evolution, 59, 2231–2242 PubMed

Hedges REM, Housley RA, Law IA, Perry C, Gowlett JAJ (1987) Radiocarbon dates from the Oxford AMS system: archaeometry datelist 6. Archaeometry, 29, 289–306

Herman JS, Searle JB (2011) Post‐glacial partitioning of mitochondrial genetic variation in the field vole. Proceedings of the Royal Society. B, Biological Sciences, 278, 3601–3607 PubMed PMC

Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proceedings of the National Academy of Sciences USA, 104, 2785–2790 PubMed PMC

Ho SYW, Larson G (2006) Molecular clocks: when times are a‐changin’. Trends in Genetics, 22, 79–83 PubMed

Ho SYW, Lanfear R, Phillips MJet al (2011) Bayesian estimation of substitution rates from ancient DNA sequences with low information content. Systematic Biology, 60, 366–375 PubMed

Hofreiter M, Munzel S, Conard NJet al (2007) Sudden replacement of cave bear mitochondrial DNA in the late Pleistocene. Current Biology, 17, R122–R123 PubMed

Jaarola M, Martínková N, Gündüz İet al (2004) Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 33, 647–663 PubMed

Jaarola M, Ashford RT, Ratkiewicz M, Brunhoff C, Borkowska A (2007) Isolation and characterization of polymorphic microsatellite loci in the field vole, Microtus agrestis, and their cross‐utility in the common vole, Microtus arvalis. Molecular Ecology Notes, 7, 1029–1031

Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353–357 PubMed

Lachaise D, Harry M, Solignac Met al (2000) Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from Sao Tome. Proceedings of the Royal Society of London. B, Biological Sciences, 267, 1487–1495 PubMed PMC

Lee DHJ, Woodward NL (2009) Links House, Stronsay, Orkney (Phase III). Data Structure Report, ORCA.

Lomolino MV (1985) Body size of mammals on islands ‐ the island rule reexamined. American Naturalist, 125, 310–316

Marshall DC (2010) Cryptic failure of partitioned Bayesian phylogenetic analyses: lost in the land of long trees. Systematic Biology, 59, 108–117 PubMed

Martin Y, Gerlach G, Schlötterer C, Meyer A (2000) Molecular phylogeny of European muroid rodents based on complete cytochrome b sequences. Molecular Phylogenetics and Evolution, 16, 37–47 PubMed

Martínková N, Moravec J (2012) Multilocus phylogeny of arvicoline voles (Arvicolini, Rodentia) shows small tree terrace size. Folia Zoologica, 61, 254–267

Martínková N, McDonald RA, Searle JB (2007) Stoats (Mustela erminea) provide evidence of natural overland colonization of Ireland. Proceedings of the Royal Society. B, Biological Sciences, 274, 1387–1393 PubMed PMC

Matisoo‐Smith E, Robins JH (2004) Origins and dispersals of Pacific peoples: evidence from mtDNA phylogenies of the Pacific rat. Proceedings of the National Academy of Sciences USA, 101, 9167–9172 PubMed PMC

Michaux JR, Libois R, Fons R (1996) Différenciation génétique et morphologique du mulot, Apodemus sylvaticus, dans le bassin méditerranéen occidental. Vie Milieu, 46, 193–203

Millien V (2011) Mammals evolve faster on smaller islands. Evolution, 65, 1935–1944 PubMed

Morrison ML, Block WM, Jehl JR Jr, Hall LS (1992) Terrestrial vertebrates of the Mono Lake Islands, California. Great Basin Naturalist, 52, 328–334

Navascués M, Emerson BC (2009) Elevated substitution rate estimates from ancient DNA: model violation and bias of Bayesian methods. Molecular Ecology, 18, 4390–4397 PubMed

Nei M (1987) Molecular Evolutionary Genetics. Colombia University Press, New York

Nichols C, Herman J, Gaggiotti OEet al (2007) Genetic isolation of a now extinct population of bottlenose dolphins (Tursiops truncatus). Proceedings of the Royal Society. B, Biological Sciences, 274, 1611–1616 PubMed PMC

Niethammer J, Krapp F (1982) Microtus arvalis (Pallas, 1779) ‐ Feldmaus In: Handbuch der Säugetiere Europas 2 (1). Rodentia: II (eds Niethammer J, Krapp F), pp. 284–318 Akademische Verlagsgesellschaft, Wiesbaden

Nylander JAA (2004) MrModeltest v2. Evolutionary Biology Centre, Uppsala University, Uppsala

Pergams ORW, Barnes WM, Nyberg D (2003) Rapid change in mouse mitochondrial DNA. Nature, 423, 397. PubMed

Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817–818 PubMed

R Development Core Team (2011) R: A Language and Environment for Statistical Computing. Retrieved from http://www.r-project.org

Rackham O (1998) Implications of historical ecology for conservation In: Conservation Science and Action (ed. Sutherland W), pp. 152–175 Blackwell, Oxford

Rambaut A, Drummond AJ (2007) Tracer v1.4. University of Oxford, Oxford

Rambaut A, Ho SYW, Drummond AJ, Shapiro B (2009) Accommodating the effect of ancient DNA damage on inferences of demographic histories. Molecular Biology and Evolution, 26, 245–248 PubMed

Ramos‐Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution, 19, 2092–2100 PubMed

Reimer PJ, Baillie MGL, Bard Eet al (2004) IntCal04 terrestrial radiocarbon age calibration, 0‐26 cal kyr BP. Radiocarbon, 46, 1029–1058

Rice WR (1989) Analyzing tables of statistical tests. Evolution, 43, 223–225 PubMed

Ritchie A (2001) Knap of Howar, Papa Westray. Discovery and Excavation in Scotland, 2000, 124–125

Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552–569 PubMed

Rohlf FJ (2010a) TpsDig 2‐Thin Plate Spline Digitizer. Ecology & Evolution, State University at Stony Brook, New York

Rohlf FJ (2010b) TpsRelw 1.49‐Thin Plate Spline Relative Warp. Ecology & Evolution, State University at Stony Brook, New York

Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574 PubMed

Rozas J, Sánchez‐DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19, 2496–2497 PubMed

Schulting RA, Sheridan A, Crozier R, Murphy E (2010) Revisiting Quanterness: new AMS dates and stable isotope data from an Orcadian chamber tomb. Proceedings of the Society of Antiquaries of Scotland, 140, 1–50

Searle JB (2008) The genetics of mammalian invasions: a review. Wildlife Research, 35, 185–192

Shenbrot GI, Krasnov BR (2005) An Atlas of the Geographic Distribution of the Arvicoline Rodents of the World (Rodentia, Muridae: Arvicolinae). Pensoft Publishers, Sofia, Moscow

Simpson GG (1940) Mammals and land bridges. Journal of the Washington Academy of Sciences, 30, 137–163

Stamatakis A (2006) RAxML‐VI‐HPC: Maximum likelihood‐based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690 PubMed

Stewart DT, Baker AJ (1992) Genetic differentiation and biogeography of the masked shrew in Atlantic Canada. Canadian Journal of Zoology, 70, 106–114

Stuiver M, Reimer PJ (1993) Extended 14C database and revised CALIB radiocarbon calibration program. Radiocarbon, 35, 215–230

Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595 PubMed PMC

Thaw S, Jaarola M, Searle JB, Dobney KM (2004) The origin of the Orkney vole Microtus arvalis orcadensis: a proxy for reconstructing human movements In: Atlantic Connections and Adaptations (eds Housley RA, Coles G), pp. 114–119 Oxbow, Oxford

Tougard C, Renvoisé E, Petitjean A, Quéré J‐P (2008) New insight into the colonization processes of common voles: inferences from molecular and fossil evidence. PLoS ONE, 3, e3532. PubMed PMC

Triant DA, DeWoody JA (2006) Accelerated molecular evolution in Microtus (Rodentia) as assessed via complete mitochondrial genome sequences. Genetica, 128, 95–108 PubMed

Wallace AR (1880) Island Life. Macmillan, London

Walser B, Heckel G (2008) Microsatellite markers for the common vole (Microtus arvalis) and their cross‐species utility. Conservation Genetics, 9, 479–481

Weninger B, Schulting R, Bradtmöller Met al (2008) The catastrophic final flooding of Doggerland by the Storegga Slide tsunami. Documenta Praehistorica, 35, 1–24

White TA, Searle JB (2007a) Genetic diversity and population size: island populations of the common shrew, Sorex araneus. Molecular Ecology, 16, 2005–2016 PubMed

White TA, Searle JB (2007b) Factors explaining increased body size in common shrews (Sorex araneus) on Scottish islands. Journal of Biogeography, 34, 356–363

White TA, Searle JB (2008) The colonization of Scottish islands by the common shrew, Sorex araneus (Eulipotyphla: Soricidae). Biological Journal of the Linnean Society, 94, 797–808

Yalden DW (1982) When did the mammal fauna of the British Isles arrive? Mammal Review, 12, 1–57

Yalden DW (1999) The History of British Mammals. Poyser, London

Zobrazit více v PubMed

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