Abstract
An appreciation of the scale and frequency of climatic oscillations in the past few million years is modifying our views on how evolution proceeds. Such major events caused extinction and repeated changes in the ranges of those taxa that survived. Their spatial effects depend on latitude and topography, with extensive extinction and recolonization in higher latitudes and altitudinal shifts and complex refugia nearer the tropics. The associated population dynamics varied with life history and geography, and the present genetic constitution of the populations and species carry attenuated signals of these past dynamics. Phylogeographic studies with DNA have burgeoned recently and studies are reviewed from the arctic, temperate and tropical regions, seeking commonalities of cause in the resulting genetic patterns. Arctic species show distinct shallow genetic clades with common geographical boundaries. Thus Beringia is distinct phylogeographically, but its role as a refugial source is complex. Arctic taxa do not show the common genetic pattern of southern richness and northern purity in north-temperate species. Temperate refugial regions in Europe and North America show relatively deep DNA divergence for many taxa, indicating their presence over several Ice Ages, and suggesting a mode of speciation by repeated allopatry. DNA evidence indicates temperate species in Europe had different patterns of postglacial colonization across the same area and different ones in previous oscillations, whereas the northwest region of North America was colonized from the north, east and south. Tropical montane regions contain deeply diverged lineages, often in a relatively small geographical area, suggesting their survival there from the Pliocene. Our poor understanding of refugial biodiversity would benefit from further combined fossil and genetic studies.
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- Abbott R. J., Smith L. C., Milne R. I., Crawford R. M., Wolff K., Balfour J. Molecular analysis of plant migration and refugia in the Arctic. Science. 2000 Aug 25;289(5483):1343–1346. doi: 10.1126/science.289.5483.1343. [DOI] [PubMed] [Google Scholar]
- Abbott Richard J., Brochmann Christian. History and evolution of the arctic flora: in the footsteps of Eric Hultén. Mol Ecol. 2003 Feb;12(2):299–313. doi: 10.1046/j.1365-294x.2003.01731.x. [DOI] [PubMed] [Google Scholar]
- Alexandrino J., Arntzen J. W., Ferrand N. Nested clade analysis and the genetic evidence for population expansion in the phylogeography of the golden-striped salamander, Chioglossa lusitanica (Amphibia: Urodela). Heredity (Edinb) 2002 Jan;88(1):66–74. doi: 10.1038/sj.hdy.6800010. [DOI] [PubMed] [Google Scholar]
- Austin James D., Lougheed Stephen C., Neidrauer Lindsay, Chek Andrew A., Boag Peter T. Cryptic lineages in a small frog: the post-glacial history of the spring peeper, Pseudacris crucifer (Anura: Hylidae). Mol Phylogenet Evol. 2002 Nov;25(2):316–329. doi: 10.1016/s1055-7903(02)00260-9. [DOI] [PubMed] [Google Scholar]
- Avise J. C., Walker D., Johns G. C. Speciation durations and Pleistocene effects on vertebrate phylogeography. Proc Biol Sci. 1998 Sep 22;265(1407):1707–1712. doi: 10.1098/rspb.1998.0492. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barnes I., Matheus P., Shapiro B., Jensen D., Cooper A. Dynamics of Pleistocene population extinctions in Beringian brown bears. Science. 2002 Mar 22;295(5563):2267–2270. doi: 10.1126/science.1067814. [DOI] [PubMed] [Google Scholar]
- Bermingham E., Martin A. P. Comparative mtDNA phylogeography of neotropical freshwater fishes: testing shared history to infer the evolutionary landscape of lower Central America. Mol Ecol. 1998 Apr;7(4):499–517. doi: 10.1046/j.1365-294x.1998.00358.x. [DOI] [PubMed] [Google Scholar]
- Bernatchez L. The evolutionary history of brown trout (Salmo trutta L.) inferred from phylogeographic, nested clade, and mismatch analyses of mitochondrial DNA variation. Evolution. 2001 Feb;55(2):351–379. doi: 10.1111/j.0014-3820.2001.tb01300.x. [DOI] [PubMed] [Google Scholar]
- Brunhoff C., Galbreath K. E., Fedorov V. B., Cook J. A., Jaarola M. Holarctic phylogeography of the root vole (Microtus oeconomus): implications for late Quaternary biogeography of high latitudes. Mol Ecol. 2003 Apr;12(4):957–968. doi: 10.1046/j.1365-294x.2003.01796.x. [DOI] [PubMed] [Google Scholar]
- Clarke T. E., Levin D. B., Kavanaugh D. H., Reimchen T. E. Rapid evolution in the Nebria gregaria group (Coleoptera: Carabidae) and the paleogeography of the Queen Charlotte Islands. Evolution. 2001 Jul;55(7):1408–1418. doi: 10.1111/j.0014-3820.2001.tb00662.x. [DOI] [PubMed] [Google Scholar]
- Conroy C. J., Cook J. A. Phylogeography of a post-glacial colonizer: Microtus longicaudus (Rodentia: muridae). Mol Ecol. 2000 Feb;9(2):165–175. doi: 10.1046/j.1365-294x.2000.00846.x. [DOI] [PubMed] [Google Scholar]
- Demboski J. R., Cook J. A. Phylogeography of the dusky shrew, Sorex monticolus (Insectivora, Soricidae): insight into deep and shallow history in northwestern North America. Mol Ecol. 2001 May;10(5):1227–1240. doi: 10.1046/j.1365-294x.2001.01260.x. [DOI] [PubMed] [Google Scholar]
- Despres Laurence, Loriot Sandrine, Gaudeul Myriam. Geographic pattern of genetic variation in the European globeflower Trollius europaeus L. (Ranunculaceae) inferred from amplified fragment length polymorphism markers. Mol Ecol. 2002 Nov;11(11):2337–2347. doi: 10.1046/j.1365-294x.2002.01618.x. [DOI] [PubMed] [Google Scholar]
- Durand J. D., Persat H., Bouvet Y. Phylogeography and postglacial dispersion of the chub (Leuciscus cephalus) in Europe. Mol Ecol. 1999 Jun;8(6):989–997. doi: 10.1046/j.1365-294x.1999.00654.x. [DOI] [PubMed] [Google Scholar]
- Fedorov V. B., Goropashnaya A. V., Jaarola M., Cook J. A. Phylogeography of lemmings (Lemmus): no evidence for postglacial colonization of Arctic from the Beringian refugium. Mol Ecol. 2003 Mar;12(3):725–731. doi: 10.1046/j.1365-294x.2003.01776.x. [DOI] [PubMed] [Google Scholar]
- Fedorov Vadim B., Stenseth Nils Chr. Multiple glacial refugia in the North American Arctic: inference from phylogeography of the collared lemming (Dicrostonyx groenlandicus). Proc Biol Sci. 2002 Oct 22;269(1505):2071–2077. doi: 10.1098/rspb.2002.2126. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Flagstad Oystein, Røed Knut H. Refugial origins of reindeer (Rangifer tarandus L.) inferred from mitochondrial DNA sequences. Evolution. 2003 Mar;57(3):658–670. doi: 10.1111/j.0014-3820.2003.tb01557.x. [DOI] [PubMed] [Google Scholar]
- Fleming Melissa A., Cook Joseph A. Phylogeography of endemic ermine (Mustela erminea) in southeast Alaska. Mol Ecol. 2002 Apr;11(4):795–807. doi: 10.1046/j.1365-294x.2002.01472.x. [DOI] [PubMed] [Google Scholar]
- Garcia-Paris M., Good D. A., Parra-Olea G., Wake D. B. Biodiversity of Costa Rican salamanders: implications of high levels of genetic differentiation and phylogeographic structure for species formation. Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1640–1647. doi: 10.1073/pnas.97.4.1640. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gravlund P., Meldgaard M., Päbo S., Arctander P. Polyphyletic origin of the small-bodied, high-arctic subspecies of tundra reindeer (Rangifer tarandus). Mol Phylogenet Evol. 1998 Oct;10(2):151–159. doi: 10.1006/mpev.1998.0525. [DOI] [PubMed] [Google Scholar]
- Gugerli F., Sperisen C., Büchler U., Magni F., Geburek T., Jeandroz S., Senn J. Haplotype variation in a mitochondrial tandem repeat of Norway spruce (Picea abies) populations suggests a serious founder effect during postglacial re-colonization of the western Alps. Mol Ecol. 2001 May;10(5):1255–1263. doi: 10.1046/j.1365-294x.2001.01279.x. [DOI] [PubMed] [Google Scholar]
- Gutiérrez Larena B., Fuertes Aguilar J., Nieto Feliner G. Glacial-induced altitudinal migrations in Armeria (Plumbaginaceae) inferred from patterns of chloroplast DNA haplotype sharing. Mol Ecol. 2002 Oct;11(10):1965–1974. doi: 10.1046/j.1365-294x.2002.01594.x. [DOI] [PubMed] [Google Scholar]
- Gómez-Zurita J., Petitpierre E., Juan C. Nested cladistic analysis, phylogeography and speciation in the Timarcha goettingensis complex (Coleoptera, chrysomelidae). Mol Ecol. 2000 May;9(5):557–570. doi: 10.1046/j.1365-294x.2000.00900.x. [DOI] [PubMed] [Google Scholar]
- Harpending H. C., Batzer M. A., Gurven M., Jorde L. B., Rogers A. R., Sherry S. T. Genetic traces of ancient demography. Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1961–1967. doi: 10.1073/pnas.95.4.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hewitt G. M. Speciation, hybrid zones and phylogeography - or seeing genes in space and time. Mol Ecol. 2001 Mar;10(3):537–549. doi: 10.1046/j.1365-294x.2001.01202.x. [DOI] [PubMed] [Google Scholar]
- Hewitt G. The genetic legacy of the Quaternary ice ages. Nature. 2000 Jun 22;405(6789):907–913. doi: 10.1038/35016000. [DOI] [PubMed] [Google Scholar]
- Holder K., Montgomerie R., Friesen V. L. Glacial vicariance and historical biogeography of rock ptarmigan (Lagopus mutus) in the Bering region. Mol Ecol. 2000 Sep;9(9):1265–1278. doi: 10.1046/j.1365-294x.2000.01005.x. [DOI] [PubMed] [Google Scholar]
- Hugall Andrew, Moritz Craig, Moussalli Adnan, Stanisic John. Reconciling paleodistribution models and comparative phylogeography in the Wet Tropics rainforest land snail Gnarosophia bellendenkerensis (Brazier 1875). Proc Natl Acad Sci U S A. 2002 Apr 23;99(9):6112–6117. doi: 10.1073/pnas.092538699. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hänfling B., Hellemans B., Volckaert F. A. M., Carvalho G. R. Late glacial history of the cold-adapted freshwater fish Cottus gobio, revealed by microsatellites. Mol Ecol. 2002 Sep;11(9):1717–1729. doi: 10.1046/j.1365-294x.2002.01563.x. [DOI] [PubMed] [Google Scholar]
- Jaarola Maarit, Searle Jeremy B. Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences. Mol Ecol. 2002 Dec;11(12):2613–2621. doi: 10.1046/j.1365-294x.2002.01639.x. [DOI] [PubMed] [Google Scholar]
- Knowles L. L. Tests of pleistocene speciation in montane grasshoppers (genus Melanoplus) from the sky islands of western North America. Evolution. 2000 Aug;54(4):1337–1348. doi: 10.1111/j.0014-3820.2000.tb00566.x. [DOI] [PubMed] [Google Scholar]
- Knowles L. Lacey, Maddison Wayne P. Statistical phylogeography. Mol Ecol. 2002 Dec;11(12):2623–2635. doi: 10.1046/j.1365-294x.2002.01637.x. [DOI] [PubMed] [Google Scholar]
- Koskinen Mikko T., Knizhin Igor, Primmer Craig R., Schlötterer Christian, Weiss Steven. Mitochondrial and nuclear DNA phylogeography of Thymallus spp (grayling) provides evidence of ice-age mediated environmental perturbations in the world's oldest body of fresh water, Lake Baikal. Mol Ecol. 2002 Dec;11(12):2599–2611. doi: 10.1046/j.1365-294x.2002.01642.x. [DOI] [PubMed] [Google Scholar]
- Kotlík P., Berrebi P. Phylogeography of the barbel (Barbus barbus) assessed by mitochondrial DNA variation. Mol Ecol. 2001 Sep;10(9):2177–2185. doi: 10.1046/j.0962-1083.2001.01344.x. [DOI] [PubMed] [Google Scholar]
- Kropf Matthias, Kadereit Joachim W., Comes Hans Peter. Differential cycles of range contraction and expansion in European high mountain plants during the Late Quaternary: insights from Pritzelago alpina (L.) O. Kuntze (Brassicaceae). Mol Ecol. 2003 Apr;12(4):931–949. doi: 10.1046/j.1365-294x.2003.01781.x. [DOI] [PubMed] [Google Scholar]
- Lenk P., Fritz U., Joger U., Wink M. Mitochondrial phylogeography of the European pond turtle, Emys orbicularis (Linnaeus 1758). Mol Ecol. 1999 Nov;8(11):1911–1922. doi: 10.1046/j.1365-294x.1999.00791.x. [DOI] [PubMed] [Google Scholar]
- Leonard J. A., Wayne R. K., Cooper A. Population genetics of ice age brown bears. Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1651–1654. doi: 10.1073/pnas.040453097. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maldonado J. E., Vilà C., Wayne R. K. Tripartite genetic subdivisions in the ornate shrew (Sorex ornatus). Mol Ecol. 2001 Jan;10(1):127–147. doi: 10.1046/j.1365-294x.2001.01178.x. [DOI] [PubMed] [Google Scholar]
- Mardulyn P. Phylogeography of the Vosges mountains populations of Gonioctena pallida (Coleoptera: Chrysomelidae): a nested clade analysis of mitochondrial DNA haplotypes. Mol Ecol. 2001 Jul;10(7):1751–1763. doi: 10.1046/j.0962-1083.2001.01307.x. [DOI] [PubMed] [Google Scholar]
- Matocq Marjorie D. Phylogeographical structure and regional history of the dusky-footed woodrat, Neotoma fuscipes. Mol Ecol. 2002 Feb;11(2):229–242. doi: 10.1046/j.0962-1083.2001.01430.x. [DOI] [PubMed] [Google Scholar]
- Michaux J. R., Magnanou E., Paradis E., Nieberding C., Libois R. Mitochondrial phylogeography of the Woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Mol Ecol. 2003 Mar;12(3):685–697. doi: 10.1046/j.1365-294x.2003.01752.x. [DOI] [PubMed] [Google Scholar]
- Molecular phylogeography of Dryas integrifolia: glacial refugia and postglacial recolonization. Mol Ecol. 1999 Jul;8(7):1187–1198. doi: 10.1046/j.1365-294x.1999.00680.x. [DOI] [PubMed] [Google Scholar]
- Nesbø C. L., Fossheim T., Vollestad L. A., Jakobsen K. S. Genetic divergence and phylogeographic relationships among european perch (Perca fluviatilis) populations reflect glacial refugia and postglacial colonization. Mol Ecol. 1999 Sep;8(9):1387–1404. doi: 10.1046/j.1365-294x.1999.00699.x. [DOI] [PubMed] [Google Scholar]
- Nielson M., Lohman K., Sullivan J. Phylogeography of the tailed frog (Ascaphus truei): implications for the biogeography of the Pacific Northwest. Evolution. 2001 Jan;55(1):147–160. doi: 10.1111/j.0014-3820.2001.tb01280.x. [DOI] [PubMed] [Google Scholar]
- Ochman H., Jones J. S., Selander R. K. Molecular area effects in Cepaea. Proc Natl Acad Sci U S A. 1983 Jul;80(13):4189–4193. doi: 10.1073/pnas.80.13.4189. [DOI] [PMC free article] [PubMed] [Google Scholar]
- doi: 10.1098/rspb.1999.0691. [DOI] [PMC free article] [Google Scholar]
- Paulo Octávio S., Jordan William C., Bruford Michael W., Nichols Richard A. Using nested clade analysis to assess the history of colonization and the persistence of populations of an Iberian Lizard. Mol Ecol. 2002 Apr;11(4):809–819. doi: 10.1046/j.1365-294x.2002.01484.x. [DOI] [PubMed] [Google Scholar]
- Quinn T. W. The genetic legacy of Mother Goose--phylogeographic patterns of lesser snow goose Chen caerulescens caerulescens maternal lineages. Mol Ecol. 1992 Aug;1(2):105–117. doi: 10.1111/j.1365-294x.1992.tb00162.x. [DOI] [PubMed] [Google Scholar]
- Richards M., Macaulay V., Hickey E., Vega E., Sykes B., Guida V., Rengo C., Sellitto D., Cruciani F., Kivisild T. Tracing European founder lineages in the Near Eastern mtDNA pool. Am J Hum Genet. 2000 Oct 16;67(5):1251–1276. [PMC free article] [PubMed] [Google Scholar]
- Rosser Z. H., Zerjal T., Hurles M. E., Adojaan M., Alavantic D., Amorim A., Amos W., Armenteros M., Arroyo E., Barbujani G. Y-chromosomal diversity in Europe is clinal and influenced primarily by geography, rather than by language. Am J Hum Genet. 2000 Nov 9;67(6):1526–1543. doi: 10.1086/316890. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Santucci F., Emerson B. C., Hewitt G. M. Mitochondrial DNA phylogeography of European hedgehogs. Mol Ecol. 1998 Sep;7(9):1163–1172. doi: 10.1046/j.1365-294x.1998.00436.x. [DOI] [PubMed] [Google Scholar]
- Schmitt T., Giessl A., Seitz A. Postglacial colonisation of western Central Europe by Polyommatus coridon (Poda 1761) (Lepidoptera: Lycaenidae): evidence from population genetics. Heredity (Edinb) 2002 Jan;88(1):26–34. doi: 10.1038/sj.hdy.6800003. [DOI] [PubMed] [Google Scholar]
- Schönswetter P., Tribsch A., Barfuss M., Niklfeld H. Several Pleistocene refugia detected in the high alpine plant Phyteuma globulariifolium sternb & hoppe (Campanulaceae) in the European Alps. Mol Ecol. 2002 Dec;11(12):2637–2647. doi: 10.1046/j.1365-294x.2002.01651.x. [DOI] [PubMed] [Google Scholar]
- 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 Sep;10(9):2187–2198. doi: 10.1046/j.0962-1083.2001.01357.x. [DOI] [PubMed] [Google Scholar]
- Semino O., Passarino G., Oefner P. J., Lin A. A., Arbuzova S., Beckman L. E., De Benedictis G., Francalacci P., Kouvatsi A., Limborska S. The genetic legacy of Paleolithic Homo sapiens sapiens in extant Europeans: a Y chromosome perspective. Science. 2000 Nov 10;290(5494):1155–1159. doi: 10.1126/science.290.5494.1155. [DOI] [PubMed] [Google Scholar]
- Starkey David E., Shaffer H. Bradley, Burke Russell L., Forstner Michael R. J., Iverson John B., Janzen Fredric J., Rhodin Anders G. J., Ultsch Gordon R. Molecular systematics, phylogeography, and the effects of Pleistocene glaciation in the painted turtle (Chrysemys picta) complex. Evolution. 2003 Jan;57(1):119–128. doi: 10.1111/j.0014-3820.2003.tb00220.x. [DOI] [PubMed] [Google Scholar]
- Stehlik I., Blattner F. R., Holderegger R., Bachmann K. Nunatak survival of the high Alpine plant Eritrichium nanum (L.) Gaudin in the central Alps during the ice ages. Mol Ecol. 2002 Oct;11(10):2027–2036. doi: 10.1046/j.1365-294x.2002.01595.x. [DOI] [PubMed] [Google Scholar]
- Steinfartz S., Veith M., Tautz D. Mitochondrial sequence analysis of Salamandra taxa suggests old splits of major lineages and postglacial recolonizations of central Europe from distinct source populations of Salamandra salamandra. Mol Ecol. 2000 Apr;9(4):397–410. doi: 10.1046/j.1365-294x.2000.00870.x. [DOI] [PubMed] [Google Scholar]
- Stenström A., Jonsson B. O., Jónsdóttir I. S., Fagerström T., Augner M. Genetic variation and clonal diversity in four clonal sedges (Carex) along the Arctic coast of Eurasia. Mol Ecol. 2001 Feb;10(2):497–513. doi: 10.1046/j.1365-294x.2001.01238.x. [DOI] [PubMed] [Google Scholar]
- Stone Karen D., Flynn Rodney W., Cook Joseph A. Post-glacial colonization of northwestern North America by the forest-associated American marten (Martes americana, Mammalia: Carnivora: Mustelidae). Mol Ecol. 2002 Oct;11(10):2049–2063. doi: 10.1046/j.1365-294x.2002.01596.x. [DOI] [PubMed] [Google Scholar]
- Taberlet P., Fumagalli L., Wust-Saucy A. G., Cosson J. F. Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol. 1998 Apr;7(4):453–464. doi: 10.1046/j.1365-294x.1998.00289.x. [DOI] [PubMed] [Google Scholar]
- Torroni A., Bandelt H. J., Macaulay V., Richards M., Cruciani F., Rengo C., Martinez-Cabrera V., Villems R., Kivisild T., Metspalu E. A signal, from human mtDNA, of postglacial recolonization in Europe. Am J Hum Genet. 2001 Aug 21;69(4):844–852. doi: 10.1086/323485. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tzedakis P. C., Lawson I. T., Frogley M. R., Hewitt G. M., Preece R. C. Buffered tree population changes in a quaternary refugium: evolutionary implications. Science. 2002 Sep 20;297(5589):2044–2047. doi: 10.1126/science.1073083. [DOI] [PubMed] [Google Scholar]
- Underhill P. A., Shen P., Lin A. A., Jin L., Passarino G., Yang W. H., Kauffman E., Bonné-Tamir B., Bertranpetit J., Francalacci P. Y chromosome sequence variation and the history of human populations. Nat Genet. 2000 Nov;26(3):358–361. doi: 10.1038/81685. [DOI] [PubMed] [Google Scholar]
- Wake D. B. Incipient species formation in salamanders of the Ensatina complex. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7761–7767. doi: 10.1073/pnas.94.15.7761. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wares J. P. Community genetics in the Northwestern Atlantic intertidal. Mol Ecol. 2002 Jul;11(7):1131–1144. doi: 10.1046/j.1365-294x.2002.01510.x. [DOI] [PubMed] [Google Scholar]
- Weider L. J., Hobaek A. Glacial refugia, haplotype distributions, and clonal richness of the Daphnia pulex complex in arctic Canada. Mol Ecol. 2003 Feb;12(2):463–473. doi: 10.1046/j.1365-294x.2003.01746.x. [DOI] [PubMed] [Google Scholar]
- Wennerberg L. Breeding origin and migration pattern of dunlin (Calidris alpina) revealed by mitochondrial DNA analysis. Mol Ecol. 2001 May;10(5):1111–1120. doi: 10.1046/j.1365-294x.2001.01256.x. [DOI] [PubMed] [Google Scholar]