Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The genetic legacy of the Quaternary ice ages


Global climate has fluctuated greatly during the past three million years, leading to the recent major ice ages. An inescapable consequence for most living organisms is great changes in their distribution, which are expressed differently in boreal, temperate and tropical zones. Such range changes can be expected to have genetic consequences, and the advent of DNA technology provides most suitable markers to examine these. Several good data sets are now available, which provide tests of expectations, insights into species colonization and unexpected genetic subdivision and mixture of species. The genetic structure of human populations may be viewed in the same context. The present genetic structure of populations, species and communities has been mainly formed by Quaternary ice ages, and genetic, fossil and physical data combined can greatly help our understanding of how organisms were so affected.

This is a preview of subscription content

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: The maximum extent of ice and permafrost at the end of the last ice age 20,000 yr BP.
Figure 2: Three paradigm postglacial colonizations from southern Europe deduced from DNA differences for the grasshopper, Chorthippus parallelus, the hedgehog, Erinaceus europeus/concolor, and the bear, Ursos arctos .
Figure 3: The general position of some well-known hybrid zones in Europe, which show major clustering in Scandinavia, central Europe and the Alps.


  1. 1

    Bennett, K. J. Evolution and Ecology: The Pace of Life (Cambridge Univ. Press, Cambridge, 1997).

    Google Scholar 

  2. 2

    Williams, D., Dunkerley, D., DeDeckker, P., Kershaw, P. & Chappell, M. Quaternary Environments (Arnold, London, 1998).

    Google Scholar 

  3. 3

    Webb, R. S., Rind, D. H., Lehman, S. J., Healy, R. J. & Sigman, D. The influence of ocean heat transport on the climate of the last Glacial Maximum. Nature 385, 695–699 (1997).

    ADS  CAS  Google Scholar 

  4. 4

    Stauffer, B. Cornucopia of ice core results. Nature 399, 412–413 (1999).

    ADS  CAS  Google Scholar 

  5. 5

    Reille, M., Andrieu, V., De Beaulieu, J. -L., Guenet, P. & Goeury, C. A long pollen record from Lac du Bouchet, Massif Central, France: for the period ca. 325 to 100 ka BP (OIS 9c to OIS 5e). Quat. Sci. Rev. 17, 1107– 1123 (1998).

    ADS  Google Scholar 

  6. 6

    Behl, R. J. & Kennett, J. P. Brief interstadial events in the Santa Barbara basin, NE Pacific, during the past 60 kyr. Nature 379, 243–246. ( 1996).

    ADS  CAS  Google Scholar 

  7. 7

    Schulz, A., von Rad, V. & Erlenkeuser, H. Correlation between Arabian Sea and Greenland climatic oscillations of the past 110,000 years. Nature 393, 54–57 (1998).

    ADS  CAS  Google Scholar 

  8. 8

    Van Andel, T. H. & Tzedakis, P. C. Palaeolithic landscapes of Europe and environs, 150,000–25,000 years ago: an overview. Quat. Sci. Rev. 15, 481– 500 (1996).

    ADS  Google Scholar 

  9. 9

    Coope, G. R. The response of insect faunas to glacial-interglacial climatic fluctuations. Phil. Trans. R. Soc. Lond. B 344, 19– 26. (1994).

    ADS  Google Scholar 

  10. 10

    Rohling, R. J. et al. Magnitudes of sea-level lowstands of the past 500,000 years. Nature 394, 162–165 (1998).

    ADS  CAS  Google Scholar 

  11. 11

    Colinvaux, P. A. An arid Amazon? Trends in Ecology and Evolution 12, 318–319 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 12

    Hewitt, G. M. in Speciation and its Consequences (eds. Otte, D. & Endler, J.) 85–110 (Sinauer Associates, Sunderland, MA, 1989).

    Google Scholar 

  13. 13

    Hewitt, G. M. in Hybrid zones and Evolutionary Process (ed. Harrison, R. G.) 140 –164 (Oxford Univ. Press, Oxford, 1993).

    Google Scholar 

  14. 14

    Ibrahim, K. M., Nichols, R. A. & Hewitt, G. M. Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77, 282–291 (1996).

    Google Scholar 

  15. 15

    Hewitt, G. M. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linnean Soc. 58, 247– 276 (1996).

    Google Scholar 

  16. 16

    Bernatchez, L. & Wilson, C. C. Comparative phylogeography of nearctic and palearctic fishes. Mol. Ecol. 7, 431–452 (1998).

    Google Scholar 

  17. 17

    Gray, A. J. in Past and Future Rapid Environmental Changes NATO ASI Series, vol. I47 (eds Huntley B. et al.) 371–380 (Springer, Berlin, 1997).

    Google Scholar 

  18. 18

    Showers, W. B. in Insect Life History Patterns (eds Denno, R. & Dingle, H.) 97–111 (Springer, New York, 1981).

    Google Scholar 

  19. 19

    Wade, M. J. & Goodnight, C. J. The theories of Fisher and Wright in the context of metapopulations: when nature does many small experiments. Evolution 52, 1537–1553 (1998).

    PubMed  PubMed Central  Google Scholar 

  20. 20

    Armbruster, P., Bradshaw, W. E. & Holzapfel, C. M. Effects of postglacial range expansion on allozyme and quantitative genetic variation of the pitcher-plant mosquito Wyeomyia smithii. Evolution 52, 1697– 1704 (1998).

    PubMed  PubMed Central  Google Scholar 

  21. 21

    Templeton, A. R. Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol. Ecol. 7, 381–397 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22

    Hewitt, G. M. Post-glacial recolonization of European biota. Biol. J. Linnean Soc. 68, 87–112 ( 1999).

    Google Scholar 

  23. 23

    Harpending, H. C. et al. Genetic traces of ancient demography. Proc. Natl Acad. Sci. USA 95, 1961–1967 (1998).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  24. 24

    Bandelt, H-J., Forster, P. & Rohl, A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37– 48 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 25

    Taberlet, P., Fumagalli, L., Wust-Saucy, A. G. & Cossons, J.-F. Comparative phylogeography and postglacial colonization routes in Europe. Mol. Ecol. 7, 453–464 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26

    Cooper, S. J. B., Ibrahim, K. M. & Hewitt, G. M. Postglacial expansion and genome subdivision in the European grasshopper Chorthippus parallelus. Mol. Ecol. 4, 49–60 (1995 ).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27

    Flanagan, N. S., Mason, P. L., Gosalvez, J. & Hewitt, G. M. Chromosomal differentiation through an Alpine hybrid zone in the grasshopper Chorthippus parallelus. Evol. Biol. 12, 577–585 (1999).

    Google Scholar 

  28. 28

    King, R. A. & Ferris, C. Chloroplast DNA phylogeography of Alnus glutinosa (L.) Gaertn. Mol. Ecol. 4, 95–103 (1998).

    Google Scholar 

  29. 29

    Santucci, F., Emerson, B. & Hewitt, G. M. Mitochondrial DNA phylogeography of European hedgehogs. Mol. Ecol. 7, 1163–1172 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. 30

    Ferris, C., King, R. A., Vainola, R. & Hewitt, G. M. Chloroplast DNA recognises three refugial sources of European oaks and shows independent eastern and western immigrations to Finland. Heredity 80, 584–593 (1998).

    PubMed  PubMed Central  Google Scholar 

  31. 31

    Taberlet, P. & Bouvet, J. Mitochondrial DNA polymorphism, phylogeography, and conservation genetics of the brown bear (Ursus arctos) in Europe. Proc. R. Soc. Lond. B 255, 195– 200 (1994).

    ADS  CAS  Google Scholar 

  32. 32

    Jaarola, M., Tegelstrom, H. & Fredga, K. Colonization history in Fenno scandian rodents. Biol. J. Linnean Soc. 68, 113–127 (1999).

    Google Scholar 

  33. 33

    Remington, C. L. Suture-zones of hybrid interaction between recently joined biotas. Evol. Biol. 2, 321–428 ( 1968).

    Google Scholar 

  34. 34

    Avise, J. C. The history and purview of phylogeography: a personal reflection. Mol. Ecol. 7, 371–379. ( 1998).

    Google Scholar 

  35. 35

    Avise, J. C. et al. Intraspecific phylogeography: The mitochondrial DNA bridge between population genetics and systematics. Annu. Rev. Ecol. System. 18, 489–522 ( 1987).

    Google Scholar 

  36. 36

    Avise, J. C. in Conservation Genetics (eds Avise, J. C. & Hamrick, J. L.) 431–470 (Chapman & Hall, New York, 1996).

    Google Scholar 

  37. 37

    Walker, D. & Avise, J. C. Principles of phylogoegraphy as illustrated by freshwater and terrestrial turtles in the southeastern United States. Annu. Rev. Ecol. System. 29, 23– 58 (1998).

    Google Scholar 

  38. 38

    Weisrock, D. W. & Janzen, F. J. Comparative molecular phylogeography of North American softshell turtles (Apalone): implications for regional and wide-scale historical evolutionary forces. Mol. Phylogenetics Evol. 14, 152–164 (2000).

    CAS  Google Scholar 

  39. 39

    Soltis, D. E., Gitzendanner, M. A., Strenge, D. D. & Soltis, P. S. Chloroplast DNA intraspecific phylogeography of plants from the Pacific Northwest of North America. Plant System. Evol. 206, 353–373 (1997).

    Google Scholar 

  40. 40

    Conroy, C. J. & Cook, J. A. Phylogeography of a post-glacial colonizer: Microtus longicaudus (Rodentia:Muridae). Mol. Ecol. 9, 165–175 ( 2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. 41

    Zink, R. M. Comparative phylogeography in North American birds. Evolution 50, 308–317 (1996).

    PubMed  PubMed Central  Google Scholar 

  42. 42

    Orange, D. I., Riddle, B. R. & Nickle, D. C. Phylogeography of a wide ranging desert lizard, Gambelia wislizenii (Crotaphytidae). Copeia 1999 , 267–273 (1999).

    Google Scholar 

  43. 43

    Ashworth, A. C. in Past and Future Rapid Environmental Changes. NATO ASI Series, vol. I47 (eds Huntley, B., et al.) 119–128 (Springer, Berlin, 1997).

    Google Scholar 

  44. 44

    Kidd, M. G. & Friesen, V. L. Analysis of mechanisms of microevolutionary change in Cepphus guillemots using patterns of control region variation. Evolution 52, 1158–1168 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. 45

    Wenink, P. W., Barker, A. J., Rosner, H. -U. & Tilanus, M. G. J. Global mitochondrial DNA phylogeography of holarctic breeding dunlins ( Calidris alpina). Evolution 50, 318– 330 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. 46

    Gravlund, P., Meldgaard, M., Paabo, S. & Arctander, P. Polyphyletic origin of the small-bodied, high-arctic subspecies of tundra reindeer ( Rangifer tarandus). Mol. Phylogenetics Evol. 10 , 151–159 (1998).

    CAS  Google Scholar 

  47. 47

    Talbot, S. L. & Shields, S. L. Phylogeography of Brown Bears (Ursos arctos) of Alaska and paraphyly within the Ursidae. Mol. Phylogenetics Evol. 5, 477–494 (1996).

    CAS  Google Scholar 

  48. 48

    Colbourne, J. K. et al. Phylogenetics and evolution of a circumarctic species complex (Cladocera: Daphnia pulex). Biol. J. Linnean Soc. 65, 347–365 (1998).

    Google Scholar 

  49. 49

    Colinvaux, P. A., Oliviera, P. E., Moreno, J. E., Miller, M. C. & Bush, M. B. A long pollen record from lowland Amazonia: forest and cooling in glacial times. Science 274, 85–88 (1996).

    ADS  CAS  Google Scholar 

  50. 50

    Schneider, C. J., Cunningham, M. & Moritz, C. Comparative phylogeography and the history of endemic vertebrates in the Wet Tropics rainforests of Australia. Mol. Ecol. 7, 487–498 ( 1998).

    Google Scholar 

  51. 51

    Patton, J. L. & da Silva, M. N. F. in Endless Forms: Species and Speciation. (eds Howard, D. & Berlocher, S.) 202– 213 (Oxford Univ. Press, Oxford, 1997).

    Google Scholar 

  52. 52

    Da Silva, M. N. F. & Patton, J. L. Molecular phylogeography and the evolution and conservation of Amazonian mammals. Mol. Ecol. 7, 475–486 ( 1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. 53

    Bermingham, E. & Martin, A. P. Comparative mtDNA phylogoegraphy of neotropical freshwater fishes: testing shared history to infer the evolutionary landscape of lower Central America. Mol. Ecol. 7, 499–517 ( 1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54

    Arctander, P., Johansen, C. & Coutellec-Vreto, M. A. Phylogeography of three closely related African bovids (tribe Alcelaphini). Mol. Biol. Evol. 16, 1724–1739 (2000)..

    Google Scholar 

  55. 55

    Fjeldsa, J. Geographical patterns for relict and young species of birds in Africa and South America and implications for conservation priorities. Biodivers. Conserv. 3, 207–226 ( 1994).

    Google Scholar 

  56. 56

    Fjeldsa, J. & Lovett, J. C. Geographical patterns of old and young species in African forest biota: the significance of specific montane areas as evolutionary centres. Biodivers. Conserv. 6, 323–244 (1997).

    Google Scholar 

  57. 57

    Roy, M. S. Recent diversification in African greenbuls (Pycnonotidae: Andropadus) supports a montane speciation model. Proc. R. Soc. Lond. B 264, 1337–1344 (1997).

    ADS  Google Scholar 

  58. 58

    Garcia-Moreno, J., Arctander, P. & Fjeldsa, J. A case of rapid diversification in the Neotropics: Phylogenetic relationships among Cranioleuca spinetails (Aves, Furnariidae). Mol. Phylogenetics Evol. 12, 273–281 (1999).

    CAS  Google Scholar 

  59. 59

    Ruedi, M. & Fumagalli, L. Genetic structure of Gymnures (genus Hylomys: Erinaceidae) on continental islands of Southeast Asia: historical effects of fragmentation. J. Zool. System. Evol. Res. 34, 153–162 ( 1996).

    Google Scholar 

  60. 60

    Dodson, J. J., Colombani, F. & Ng, P. K. L. Phylogeographic structure in mitochondrial DNA of a Southeast Asian freshwater fish, Hemibagrus nemurus (Siluroidei: Bagridae) and Pleistocene sea-level changes on the Sunda shelf. Mol. Ecol. 4, 331–346 ( 1995).

    CAS  Google Scholar 

  61. 61

    Surridge, A. K., Timmins, R. J., Hewitt, G. M. & Bell, D. J. Striped rabbits in Southeast Asia. Nature 400, 726 (1999).

    ADS  CAS  Google Scholar 

  62. 62

    Hisheh, S., Westerman, M. & Schmitt, L. H. Biogeography of the Indonesian archipelago: mitochondrial DNA variation in the fruitbat, Eonycteris spelaea. Biol. J. Linnean Soc. 65, 329–345 (1998).

    Google Scholar 

  63. 63

    Palumbi, S. R. Molecular biogeography of the Pacific. Coral Reefs 16, S47–S52 (1997).

    Google Scholar 

  64. 64

    Williams, S. T. & Benzie, J. A. H. Evidence of a biogeographic break between populations of a high dispersal starfish: congruent regions within the Indo-West Pacific defined by color morphs, mt DNA, and allozyme data. Evolution 52, 87 –99 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. 65

    Chenoweth, S. F., Hughes, J. M., Keenan, C. P. & Lavery, S. When oceans meet: a teleost shows secondary intergradation at an Indian-Pacific interface. Proc. R. Soc. Lond. B 265, 415 –420 (1998).

    Google Scholar 

  66. 66

    Duke, N. C., Benzie, J. A. H., Goodall, J. A. & Ballment, E. R. Genetic structure and evolution of species of the mangrove genus Avicennia (Avicenniaceae) in the Indo-West Pacific. Evolution 52, 1612–1626 (1998).

    PubMed  PubMed Central  Google Scholar 

  67. 67

    Bowen, B. W. & Grant, W. S. Phylogeography of the sardines (Sardinops spp.): assessing biogeographic models and population histories in temperate upwelling zones. Evolution 51, 1601–1610 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. 68

    Hauser, L. & Ward, R. in Advances in Molecular Ecology (ed. Cavalho, G.) 191–223 (IOS Press, Amsterdam, 1998).

    Google Scholar 

  69. 69

    Avise, J. C., Walker, D. & Johns, G. C. Speciation durations and Pleistocene effects on vertebrate phylogeography. Proc. R. Soc. Lond. B 265, 1707–1712 (1998).

    CAS  Google Scholar 

  70. 70

    Klicka, J. & Zink, R. M. Pleistocene effects on North American songbird evolution. Proc. R. Soc. Lond. B 266, 695–700 (1999).

    Google Scholar 

  71. 71

    Orr, M. R. & Smith, T. B. Ecology and Speciation. Trends Ecol. Evol. 13, 502–506 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. 72

    Schluter, D. in Endless Forms: Species and Speciation. (eds Howard, D. & Berlocher, S.) 114–129. (Oxford Univ. Press, Oxford, 1998).

    Google Scholar 

  73. 73

    Jorde, L. B., Bamshad, M. & Rogers, A. R. Using mitochondrial and nuclear DNA markers to reconstruct human evolution. BioEssays 20, 126– 136 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. 74

    Templeton, A. R. Out of Africa? What do genes tell us? Curr. Opin. Genet. Dev. 7, 841–847 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  75. 75

    Stringer, C. B. African Exodus: The Origins of Modern Humanity (Jonathan Cape, London, 1996).

    Google Scholar 

  76. 76

    Hublin, J.-J. in Neandertals and Modern Humans in Western Asia (eds Akazawa, T. et al.) (Plenum, New York, 1998).

    Google Scholar 

  77. 77

    Krings, M., Stone, A., Schmitz, R. W. & Krainitzki, H. Neandertal DNA sequences and the origins of modern humans. Cell 90, 19–30 ( 1997).

    CAS  Google Scholar 

  78. 78

    Tchernov, E. in Neandertals and Modern Humans in Western Asia (eds Akazawa, T. et al.) (Plenum, New York, 1998).

    Google Scholar 

  79. 79

    Ambrose, S. H. Late Pleistocene human population bottlenecks, volcanic winter, and differentiation of modern humans. J. Hum. Evol. 34, 623– 651 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. 80

    Mellars, P. in Neanderthals and Modern Humans in Western Asia (eds Akazawa, T. et al.) (Plenum, New York, 1998).

    Google Scholar 

  81. 81

    Cavalli-Sforza, L. L., Menozzi, P. & Piazza, A. The History and Geography of Human Genes (Princeton Univ. Press, Princeton NJ, 1994).

    MATH  Google Scholar 

  82. 82

    Richards, M. et al. Paleolithic and neolithic lineages in the European mitochondrial gene pool. Am. Hum. Genet. 59, 185– 203 (1996).

    CAS  Google Scholar 

  83. 83

    Richards, M., MacAulay, V., Bandelt, H. -J. & Sykes, B. Phylogeography of mitochondrial DNA in western Europe. Ann. Hum. Genet. 62, 241–260 ( 1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. 84

    Li, W. H. Molecular Evolution, (Sinauer Associates, Sunderland, MA, 1997).

    Google Scholar 

  85. 85

    Parsons, T. J. & Holland, M. M. Mitochondrial mutation rate revisited: hotspots and polymorphism. Nature Genet. 18, 110 (1998).

    CAS  Google Scholar 

  86. 86

    Schug, M. D., Mackay, T. F. C. & Aquadro, C. F. Low mutation rates of microsatellite loci in Drosophila melanogaster. Nature Genet. 15, 99–102 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information



Corresponding author

Correspondence to Godfrey Hewitt.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Hewitt, G. The genetic legacy of the Quaternary ice ages. Nature 405, 907–913 (2000).

Download citation

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links