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Conservation Genetics

, 6:665 | Cite as

Does time since colonization influence isolation by distance? A meta-analysis

  • E. Crispo
  • A. P. Hendry
Article

Abstract

Isolation by distance (IBD) is a phenomenon characterized by increasing genetic divergence and decreasing gene flow with increasing geographic distance. IBD is often used in conservation biology to infer the extent of gene flow among populations. An assumption inherent to this approach is equilibrium between genetic drift and gene flow, which may take thousands of years to achieve. This implies that empirical IBD studies of recently colonized areas, such as postglacial systems, should be concerned with whether or not equilibrium has been reached. Short of equilibrium, IBD should increase with the length of time since a geographical area was colonized. We test the prediction that IBD increases with increasing time since colonization through a meta-analysis based on a diverse range of empirical systems. P and r 2 values from published IBD studies were analyzed with respect to time since colonization (in generations and years), taking into account variation in sample sizes, molecular markers, divergence metrics (genetic distance, F st, Nm), and dispersal patterns (one or two dimensional). Overall, we found weak evidence for associations between time since colonization and IBD. Sample sizes, molecular markers, divergence metrics, and dispersal patterns did not appreciably influence IBD. We propose that the expected relationship between IBD and time since colonization is obscured by the influence of other factors, such as dispersal ability, geographical barriers, and proximity to glacial refugia. The possible effects of time since colonization should continue to be evaluated in empirical studies, but other potential factors should also be thoroughly explored.

Keywords

dispersal gene flow glaciation migration equilibrium 

Notes

Acknowledgements

We thank J. Correa for providing assistance with the statistics and K. Räsänen, S. A. Pavey, McGill Department of Biology graduate student discussion group members, and anonymous reviewers for providing comments. We also thank all individuals who provided information on generation lengths (see Appendix A). Financial support was provided by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to A. P. Hendry.

References

  1. Baer CF (1998) Species-wide population structure in a southeastern U.S. freshwater fish, Heterandria formosa: gene flow and biogeography. Evolution 52: 183–193CrossRefGoogle Scholar
  2. Baker AM, Mather PB, Hughes JM (2001) Evidence for long-distance dispersal in a sedentary passerine, Gymnorhina tibicen (Artamidae). Biol. J. Linn. Soc. 72: 333–343CrossRefGoogle Scholar
  3. Barber PH (1999) Patterns of gene flow and population genetic structure in the canyon tree frog, Hyla arenicolor (Cope). Mol. Ecol. 8: 563–576CrossRefPubMedGoogle Scholar
  4. Burton C, Krebs CJ, Taylor EB (2002) Population genetic structure of the cyclic snowshoe hare (Lepus americanus) in southwestern Yukon, Canada. Mol. Ecol. 11: 1689–1701CrossRefPubMedGoogle Scholar
  5. Caizergues A, Dubois S, Mondor G et al. (2001) Genetic structure of black grouse (Tetrao tetrix) populations of the French Alps. Genet. Select. Evol. 33: S177–S191Google Scholar
  6. Castric V, Bernatchez L (2003) The rise and fall of isolation by distance in the anadromous brook charr (Salvelinus fontinalis Mitchill). Genetics 163: 983–996PubMedGoogle Scholar
  7. Castric V, Bonney F, Bernatchez L (2001) Landscape structure and hierarchical genetic diversity in the brook charr, Salvelinus fontinalis. Evolution 55: 1016–1028PubMedCrossRefGoogle Scholar
  8. Chiappero MB, Calderon GE, Gardenal CN (1997) Oligoryzomys flavescens (Rodentia, Muridae): gene flow among populations from central-eastern Argentina. Genetica 101: 105–113CrossRefPubMedGoogle Scholar
  9. Costello AB, Down TE, Pollard SM, Pacas CJ, Taylor EB (2003) The influence of history and contemporary stream hydrology on the evolution of genetic diversity within species: an examination of microsatellite DNA variation in bull trout, Salvelinus confluentus (Pisces: Salmonidae). Evolution 57: 328–344PubMedGoogle Scholar
  10. de Innocentiis S, Sola L, Cataudella S, Bentzen P (2001) Allozyme and microsatellite loci provide discordant estimates of population differentiation in the endangered dusky grouper (Epinephelus marginatus) within the Mediterranean Sea. Mol. Ecol. 10: 2163–2175CrossRefPubMedGoogle Scholar
  11. Ellis WA, Hale PT, Carrick F (2002) Breeding dynamics of koalas in open woodlands. Wildl. Res. 29: 19–25CrossRefGoogle Scholar
  12. Fuller SJ, Mather PB, Wilson JC (1996) Limited genetic differentiation among wild Oryctolagus cuniculus L. (rabbit) populations in arid eastern Australia. Heredity 77: 138–145PubMedGoogle Scholar
  13. Gavin TA, Sherman PW, Yensen E, May B (1999) Population genetic structure of the northern Idaho ground squirrel (Spermophilus brunneus brunneus). J. Mammal. 80: 156–168CrossRefGoogle Scholar
  14. Gold JR, Richardson LR, Turner TF (1999) Temporal stability and spatial divergence of mitochondrial DNA haplotype frequencies in red drum (Sciaenops ocellatus) from coastal regions of the western Atlantic Ocean and Gulf of Mexico. Mar. Biol. 133: 593–602CrossRefGoogle Scholar
  15. Goossens B, Chikhi L, Taberlet P, Waits LP, Allaine D (2001) Microsatellite analysis of genetic variation among and within Alpine marmot populations in the French Alps. Mol. Ecol. 10: 41–52CrossRefPubMedGoogle Scholar
  16. Green DM, Sharbel TF, Kearsley J, Kaiser H (1996) Postglacial range fluctuation, genetic subdivision and speciation in the western North American spotted frog complex, Rana pretiosa. Evolution 50: 374–390CrossRefGoogle Scholar
  17. Hewitt GM (1993) Postglacial distribution and species substructure: lessons from pollen, insects and hybrid zones. In: Lees DR, Edwards D., (eds) Evolutionary Patterns and Process. Academic Press, London, pp. 97–123Google Scholar
  18. Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58: 247–276CrossRefGoogle Scholar
  19. Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. 68: 87–112CrossRefGoogle Scholar
  20. Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405: 907–913CrossRefPubMedGoogle Scholar
  21. Holder K, Montgomerie R, Friesen VL (2000) Glacial vicariance and historical biogeography of rock ptarmigan (Lagopus mutus) in the Bering region. Mol. Ecol. 9: 1265–1278CrossRefPubMedGoogle Scholar
  22. Hundertmark KJ, Bowyer RT, Shields GF, Schwartz CC (2003) Mitochondrial phylogeography of moose (Alces alces) in North America. J. Mammal. 84: 718–728CrossRefGoogle Scholar
  23. Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53: 1898–1914CrossRefGoogle Scholar
  24. Jennions MD, Møller AP (2002) Publication bias in ecology and evolution: an empirical assessment using the ȁ8trim and fillȁ9 method. Biol. Rev. 77: 221–222CrossRefGoogle Scholar
  25. Kark S, Alkon PU, Safriel UN, Randi E (1999) Conservation priorities for Chukar partridge in Israel based on genetic diversity across an ecological gradient. Conserv. Biol. 13: 542–552CrossRefGoogle Scholar
  26. Kimura M, Weiss GH (1964) The stepping stone model of population structure and the decrease in genetic correlation with distance. Genetics 49: 561–576PubMedGoogle Scholar
  27. King RB, Lawson R (2001) Patterns of population subdivision and gene flow in three species of sympatric natricine snakes. Copeia 2001: 602–614CrossRefGoogle Scholar
  28. Kinnison MT, Bentzen P, Unwin MJ, Quinn TP (2002) Reconstructing recent divergence: evaluating nonequilibrium population structure in New Zealand chinook salmon. Mol. Ecol. 11: 739–754CrossRefPubMedGoogle Scholar
  29. Knutsen H, Knutsen JA, Jorde PE (2001) Genetic evidence for mixed origin of recolonized sea trout populations. Heredity 87: 207–214CrossRefPubMedGoogle Scholar
  30. Koljonen M-L, Jansson H, Paaver T, Vasin O, Koskiniemi J (1999) Phylogeographic lineages and differentiation pattern of Atlantic salmon (Salmo salar) in the Baltic Sea with management implications. Can. J. Fish. Aquat. Sci. 56: 1766–1780CrossRefGoogle Scholar
  31. Lougheed SC, Gibbs HL, Prior KA, Weatherhead PJ (1999) Hierarchical patterns of genetic population structure in black rat snakes (Elaphe obsoleta obsoleta) as revealed by microsatellite DNA analysis. Evolution 53: 1995–2001CrossRefGoogle Scholar
  32. Lugon-Moulin N, Hausser J (2002) Phylogeographical structure, postglacial recolonization and barriers to gene flow in the distinctive Valais chromosome race of the common shrew (Sorex araneus). Mol. Ecol. 11: 785–794CrossRefPubMedGoogle Scholar
  33. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res. 27: 209–220PubMedGoogle Scholar
  34. Maruyama T (1970) On the rate of decrease of heterozygosity in circular stepping stone models of populations. Theor. Popul. Biol. 1: 101–119CrossRefPubMedGoogle Scholar
  35. Maruyama T (1971) Analysis of population structure. II. Two-dimensional stepping stone models of finite length and other geographically structured populations. Ann. Human Genet. 35: 179–196Google Scholar
  36. McLean JE, Hay DE, Taylor EB (1999) Marine population structure in an anadromous fish: life-history influences patterns of mitochondrial DNA variation in the eulachon, Thaleichthys pacificus. Mol. Ecol. 8: S143–S158CrossRefPubMedGoogle Scholar
  37. Mossman CA, Waser PM (2001) Effects of habitat fragmentation on population genetic structure in the white-footed mouse (Peromyscus leucopus). Can. J. Zool. 79: 285–295CrossRefGoogle Scholar
  38. Nagylaki T (1976) The decay of genetic variability in geographically structured populations. II. Theor. Popul. Biol. 10: 70–82CrossRefPubMedGoogle Scholar
  39. Olsen JB, Miller SJ, Spearman WJ, Wenburg JK (2003) Patterns of intra- and inter-population genetic diversity in Alaskan coho salmon: implications for conservation. Conserv. Genet. 4: 557–569CrossRefGoogle Scholar
  40. Ogden R, Thorpe RS (2002) Molecular evidence for ecological speciation in tropical habitats. Proc. Natl. Acad. Sci. USA 99: 13612–13615CrossRefPubMedGoogle Scholar
  41. Patton JL, Da Silva MNF, Malcolm JR (1996) Hierarchical genetic structure and gene flow in three sympatric species of Amazonian rodents. Mol. Ecol. 5: 229–238CrossRefPubMedGoogle Scholar
  42. Peterson MA, Denno RF (1998) The influence of dispersal and diet breadth on patterns of genetic isolation by distance in phytophagous insects. Am. Nat. 152: 429–446CrossRefGoogle Scholar
  43. Pfau RS, van Den Bussche RA, McBee K (2001) Population genetics of the hispid cotton rat (Sigmodon hispidus): patterns of genetic diversity at the major histocompatibility complex. Mol. Ecol. 10: 1939–1945CrossRefPubMedGoogle Scholar
  44. Piertney SB, MacColl ADC, Bacon PJ, Dallas JF (1998) Local genetic structure in red grouse (Lagopus lagopus scoticus): evidence from microsatellite DNA markers. Mol. Ecol. 7: 1645–1654CrossRefPubMedGoogle Scholar
  45. Planes S, Galzin R, Bonhomme F (1996) A genetic metapopulation model for reef fishes in oceanic islands: the case of the surgeonfish, Acanthurus triostegus. J. Evol. Biol. 9: 103–117CrossRefGoogle Scholar
  46. Quinn GP, Keough MJ (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, CambridgeGoogle Scholar
  47. Rafiński J, Babik W (2000) Genetic differentiation among northern and southern populations of the moor frog Rana arvalis Nilsson in central Europe. Heredity 84: 610–618CrossRefPubMedGoogle Scholar
  48. Rosenberg MS, Adams DC, Gurevitch J (2000) MetaWin: Statistical Software for Meta-Analysis. Version 2. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  49. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145: 1219–1228PubMedGoogle Scholar
  50. Rowe KC, Heske EJ, Brown PW, Paige KN (2004) Surviving the ice: northern refugia and postglacial colonization. Proc. Nat. Acad. Sci. USA 101: 10355–10359CrossRefPubMedGoogle Scholar
  51. Seppä P, Laurila A (1999) Genetic structure of island populations of the anurans Rana temporaria and Bufo bufo. Heredity 82: 309–317CrossRefPubMedGoogle Scholar
  52. Shaffer HB, Fellers GM, Magee A, Voss SR (2000) The genetics of amphibian declines: population substructure and molecular differentiation in the Yosemite toad, Bufo canorus (Anura, Bufonidae) based on single-strand conformation polymorphism analysis (SSCP) and mitochondrial DNA sequence data. Mol. Ecol. 9: 245–257CrossRefPubMedGoogle Scholar
  53. Slatkin M (1991) Inbreeding coefficients and coalescence times. Genet. Res. 58: 167–175PubMedCrossRefGoogle Scholar
  54. Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47: 264–279CrossRefGoogle Scholar
  55. Slatkin M, Maddison WP (1990) Detecting isolation by distance using phylogenies of genes. Genetics 126: 249–260PubMedGoogle Scholar
  56. Smith TB, Wayne RK, Girman DJ, Bruford MW (1997) A role for ecotones in generating rainforest biodiversity. Science 276: 1855–1857CrossRefGoogle Scholar
  57. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W.H. Freeman & Company, New YorkGoogle Scholar
  58. Taylor EB, Stamford MD, Baxter JS (2003) Population subdivision in westslope cutthroat trout (Oncorhynchus clarki lewisi) at the northern periphery of its range: evolutionary inferences and conservation implications. Mol. Ecol. 12: 2609–2622CrossRefPubMedGoogle Scholar
  59. Turgeon J, Bernatchez L (2001) Clinal variation at microsatellite loci reveals historical secondary intergradation between glacial races of Coregonus artedi (Teleostei: Coregoninae). Evolution 55: 2274–2286PubMedGoogle Scholar
  60. van Hooft WF, Groen AF, Prins HHT (2000) Microsatellite analysis of genetic diversity in African buffalo (Syncerus caffer) populations throughout Africa. Mol. Ecol. 9: 2017–2025CrossRefPubMedGoogle Scholar
  61. Wright S (1943) Isolation by distance. Genetics 28: 114–138PubMedGoogle Scholar
  62. Wright S (1946) Isolation by distance under diverse systems of mating. Genetics 31: 39–59PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  1. 1.Redpath Museum and Department of BiologyMcGill UniversityMontréalCanada

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