Abstract
Both the ability to generate DNA data and the variety of analytical methods for conservation genetics are expanding at an ever-increasing pace. Analytical approaches are now possible that were unthinkable even five years ago due to limitations in computational power or the availability of DNA data, and this has vastly expanded the accuracy and types of information that may be gained from population genetic data. Here we provide a guide to recently developed methods for population genetic analysis, including identification of population structure, quantification of gene flow, and inference of demographic history. We cover both allele-frequency and sequence-based approaches, with a special focus on methods relevant to conservation genetic applications. Although classical population genetic approaches such as F st (and its derivatives) have carried the field thus far, newer, more powerful, methods can infer much more from the data, rely on fewer assumptions, and are appropriate for conservation genetic management when precise estimates are needed.
Similar content being viewed by others
References
Abdo Z, Crandall KA, Joyce P (2004) Evaluating the performance of likelihood methods for detecting population structure and migration. Mol. Ecol., 13, 837–852.
Anderson EC, Williamson EG, Thompson EA (2000) Monte Carlo evaluation of the likelihood for Ne from temporally spaced samples. Genetics, 156, 2109–2118.
Anderson EC, Thompson EA (2002) A model-based method for identifiying species hybrids using multilocus genetic data. Genetics 160, 1217–1229.
Arbogast BS, Edwards SV, Wakely J, Beerli P, Slowinski JB (2002) Estimating divergence times from molecular data on phylogenetic and population genetic timescales. Annu. Rev. Ecol. Syst., 33, 707–740.
Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: The mitochondrial DNA bridge between population genetics and systematics. Annu. Rev. Ecol. Syst. 18, 489–522.
Avise JC (2000) Phylogeography: The history and formation of species. Harvard University Press, Cambridge, Mass.
Bahlo M, Griffiths RC (2000) Inference from gene trees in a subdivided population. Theor. Pop. Biol., 57, 79–95.
Balloux F, Goudet J (2002) Statistical properties of population differentiation estimators under stepwise mutation in a finite island model. Mol. Ecol. 11, 771–783.
Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol. Ecol., 11, 155–165.
Banks, MA, Eichert W (2000) WHICHRUN (Version 3. 2) a computer program for population assignment of individuals based on multilocus genotype data. J. Hered., 91, 87–89.
Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics, 153, 2013–2029.
Beaumont MA, Rannala B (2004) The Bayesian revolution in genetics. Nature Rev. Genet 5, 251–261.
Beebee T, Rowe G (2001) Application of genetic bottleneck testing to the investigation of amphibian declines: a case study with natterjack toads. Cons. Biol. 15, 266–270.
Beerli P (1998) Estimation of migration rates and population sizes in geographically structured populations. In: Advances in Molecular Ecology (ed, Carvalho GR), pp. 39–54. IOS Press, Amsterdam.
Beerli P, Felsenstein J (1999) Maximum likelihood estimation of migration rates and effective population umbers in two populations using a coalescent approach. Genetics, 152, 763–773.
Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc. Natl. Acad. Sci. USA, 98, 4563–4568.
Berry O, Tocher MD, Sarrre SD (2004) Can assignment tests measure dispersal?Mol. Ecol., 13, 551–561.
Bossart JL, Prowell DP (1998) Genetic estimates of population structure and gene flow: limitations, lessons, and new directions. TREE, 13, 202–206.
Brumffeld RT, Beerli P, Nickerson DA, Edwards SV (2003) The utility of single nucleotide polymorphisms in inferences of population history. TREE, 18, 249–256.
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol. Ecol., 9, 1657–1659.
Colson I, Goldstein DB (1999) Evidence for complex mutations at microsatellie loci in Drosophila. Genetics, 152, 617–627.
Corander J, Waldmann P, Sillanpa ¨a ¨ MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics, 163, 367–374.
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144, 2001–14.
Cornuet J-M, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude population as origins of individuals. Genetics, 153, 1989–2000.
Courtois R, Bernatchez L, Ouellet J-P, Breton L (2003) Significance of caribou (Rangifer tarandus) ecotypes from a molecular genetics viewpoint. Conserv. Genet., 4, 393–404.
Crandall KA, Posada D and Vasco D (1999) Effective population sizes: missing measures and missing concepts. Animal Conserv., 2, 317–319.
Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. TREE, 15, 290–295.
Davies N, Villablanca FX, Roderick GK (1999) Determining the source of individuals: multilocus genotyping in non-equilibrium population genetics. TREE, 14, 17–21.
Dawson KJ, Belkhir K (2001) A Bayesian approach to the identification of panmictic populations and the assignment of individuals. Genet. Res., 78, 59–77.
Dieringer D, Schlo ¨tterer C (2003) MICROSATELLITE ANA-LYSER(MSA): a platform independent analysis tool for large microsatellite data sets. Mol. Ecol. Notes, 3, 167–169.
Diniz-Filho JAF, Telles MPC (2002) Spatial autocorrelation analysis and the identi cation of operational units for conservation in continuous populations. Conserv. Biol., 16, 924–935.
Dupanloup I, Schneider S, Excoffer L (2002) A simulated annealing approach to de ne the genetic structure of populations. Mol. Ecol., 11, 2571–2581.
Emerson BC, Paradis E, Thebaud C (2001) Revealing the demographic histories of species using DNA sequences. TREE, 16, 707–716.
Emery AM, Wilson IJ, Craig S, Boyle PR, Noble LR (2001) Assignment of paternity groups without access to parental genotypes: multiple mating and developmental plasticity in squid. Mol. Ecol., 10, 1265–1278.
Estoup A, Clegg SM (2003) Bayesian inferences on the recent island colonization history by the bird Zosterops lateralis lateralis. Mol. Ecol., 12, 657–674.
Estoup A, Wilson IJ, Sullivan C, Cornuet J-M, Moritz C (2001) Inferring population history from microsatellite and enzyme data in serially introduced cane toads, Bufo marinus. Genet., 159, 1671–1687.
Excoffer L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479–491.
Fabiani A, Hoelzel AR, Galimberti F, Muelbert MMC (2003) Long-range paternal gene. ow in the southern elephant seal. Science, 299, 676.
Falush D, Wirth T, Linz B, Pritchard JK, Stephens M, Kidd M, Blaser MJ, Graham DY, Vacher S, Perez-Perez GI, Yamaoka Y, Me ´graud F, Otto K, Reichard U, Katzowitsch E, Wang X, Achtman M, Suerbaum S (2003) Traces of human migrations in Helicobacer pylori populations. Science, 299, 1582–1585.
Fisher RA (1930) The Genetical Theory of Natural Selection. Clarendon Press, Oxford.
Ford MJ (2002) Applications of selective neutrality tests to molecular ecology. Mol. Ecol., 11, 1245–1262.
Friar EA, Boose DL, LaDoux T, Roalson EH, Robichaux RH (2001) Population structure in the engangered Mauna Loa silversword, Argyroxiphium kauenese (Aseracea), and its bearing on reintroduction. Mol. Ecol., 10, 1657–1663.
Gaggiotti OE, Lange O, Rassmann K, and Gliddon C (1999) A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Mol. Ecol., 8, 1513–1520.
Gaggiotti OE, Jones F, Lee WM, Amos W, Harwood J, Nichols RA (2002) Patterns of colonization in a metapopulation of grey seals. Nature, 416, 424–427.
Gardner MG, Bull CM, Cooper SJB, Duffeld GA (2000) Microsatellite mutations in litters of the Australian lizard Egernia stokesii. J. Evol. Biol., 13, 551–560.
Garza C, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol. Ecol., 10, 305–318.
Glaubitz JC (2004) CONVERT: A user-friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Molecular Ecology Notes, 4 (2), 309–310.
Goldstein DB, Linares AR, Cavalli-Sforza LL, Feldman MW (1995) Genetic absolute dating based on microsatellites and the origin of modern humans. Proc. Natl. Acad. Sci. USA, 92, 623–6727.
Griffiths RC, Tavare ´ S (1994) Sampling theory for neutral alleles in a varying environment. Phil. Trans. R. Soc. Lond. B, 344, 403–410.
Harpending H, Rogers AR (2000) Genetic perspectives on human origins and differentiation. Ann. Rev. Hum. Gen., 1, 361–385.
Holsinger KE, Mason-Gamer RJ (1996) Hierarchical analysis of nucleotide diversity in geographically structured populations. Genetics, 142, 629–639.
Holsinger KE, Lewis PO, Dey DK (2002) A Bayesian approach to inferring population structure from dominant markers. Mol. Ecol., 11, 1157–1164.
Hudson RR (1990) In: Oxford Surveys in Evolutionary Biology (eds. Futuyma D, Antonovics J), Oxford University Press, Oxford.
Huelsenbeck JP, Larget B, Miller RE, Ronquist F (2002) Potential applications and pitfalls of Bayesian inference of phylogeny. Syst. Biol., 51, 673–688.
Jones AG, Ardren WR (2003) Methods of parentage analysis in natural populations. Mol. Ecol., 12, 2511–2523.
Kimmel M, Chakraborty R, King JP, Bamshad M, Watkins WS et al. (1998) Signatures of population expansion in microsatellite repeat data. Genetics, 148, 1921–1930.
Kingman JFC (1982) The coalescent. Stoc. Proc. App., 13, 235–248.
Kinnison MT, Bentzen P, Unwin MJ, Quinn TP (2002) Reconstructing recent divergence: evaluating nonequilibrium population structure in New Zealand chinook salmon. Mol. Ecol., 11, 739–754.
Knowles LL, Maddison WP (2002) Statistical phylogeography. Mol. Ecol., 11, 2623–2635.
Kuhner MK, Yamato J, Felsenstein J (1995) Estimating effective population size and mutation rate from sequence data using Metropolis-Hastings sampling. Genetics, 140, 1421–1430.
Kuhner MK, Yamato J, Felsenstein J (1998) Maximum likeli-hood estimation of population growth rates based on the coalescent. Genetics, 149, 429–434.
Larson S, Jameson R, Etnier M, Fleming M, Bentzen P. (2002) Loss of genetic diversity in sea otters (Enhydra lutris) associated with the fur trade of the 18 th and 19 th centuries. Mol. Ecol., 11, 1899–1903.
Lewis PO (2001) Phylogenetic systematics turns over a new leaf. TREE, 16, 30–37.
Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv. Biol., 12, 28–233.
Lynch M, Crease TJ (1990) The analysis of population survey data on DNA sequence variation. Mol. Biol. Evol., 7, 377–394.
Malone CL, Knapp CR, Taylor JF, Davis SK (2003) Genetic consequences of Pleistocene fragmentation: Isolation, drift, and loss of diversity in rock iguanas (Cyclura). Conserv. Genet., 4, 1–15.
Manel S, Berthier P, Luikart (2002) Detecting wildlife poaching: identifying the origin of individuals with bayesian assignment tests and multilocus genotypes. Conserv. Biol., 16, 650–659.
Manel, S, Schwartz MK, Luikart P, Taberlet P (2003) Landscapge genetics: combining landscape ecology and popula-tion genetics. TREE, 18, 189–197.
Masta SE, Laurent NM, Routman EJ (2003) Population genetic structure of the toad Bufo woodhousii: an empirical assesment of the effects of haplotype extinction on nested cladistic analysis. Mol. Ecol., 12, 1541–1554.
Michalakis Y, Excoffer L (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics, 142, 1061–1064.
Milligan BG (2003) Maximum-likelihood estimation of relatedness. Genetics, 163, 1153–1167.
Mills LS, Citta JJ, Lair KP, Schwarz MK, Tallmon DA (2000) Estimating animal abundance using noninvasive DNA sampling: promise and pitfalls. Ecol. Apps., 10, 283–294.
Moazami-Goudarzi K Laloe D (2002) Is a multivariate consensus representation of genetic relationships among popu-lations always meaningful?Genetics, 162, 473–484.
Moritz C (1994) Defining ''evolutionary signi cant units ''for conservation. TREE, 9, 373–375.
Nee S, Holmes EC, Rambaut A, Harvey PH (1995) Inferring population history from molecular phylogenies. Phil. Trans. Roy. Soc. Lond., 349, 25–31.
Nei M (1973) Analysis of gene diversity in subdivided populations. Proc. Nat. Acad. Sci. USA, 70, 3321–3323.
Neigel JE (1997) A comparison of alternative strategies for estimating gene flow from genetic markers. Annu. Rev. Ecol. Syst., 28, 105–128.
Neigel JE (2002) Is FST ST obsolete?Conserv. Genet., 3, 167–173.
Nielsen R (2001) Statistical tests of selective neutrality in the age of genomics. Heredity, 86, 641–647.
Nielsen R, Slatkin M (2000) Analysis of population subdivision using diallelic models. Evolution, 54, 44–50.
Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: A markov chain monte carlo approach. Genetics, 158, 885–896.
Nordborg M (2001) Coalescent theory. In: Handbook of Sta-tistical Genetics (eds. Balding, DJ, Bishop M, Cannings C), Wiley, England.
Ortý ´G, Pearse DE, Avise JC (1997) Phylogenetic assessment of length variation at a microsatellite locus. Proc. Natl. Acad. Sci. USA, 94, 10745–10749.
Paetkau D, Calvert W, Sterling I, Strobeck C (1995) Micro-satellite analysis of population structure in Canadian polar bears. Mol. Ecol., 4, 347–354.
Palsbøll PJ, Allen J, Be ´rube ´ M, Clapham PJ, Feddersen TP, Hammond P, Hudson RR, Jørgensen J, Katona S, Larsen AH, Larsen F, Lien J, Mattila DK, Sigurjo ´nsson J, Sears R, Smith T, Sponer R, Stevick P, Øien N (1997) Genetic tagging of humpback whales. Nature, 388, 767–769.
Pearse DE, Eckerman CM, Janzen FJ, Avise JC (2001) A genetic analogue of 'mark-recapture 'methods for estimating population size: an approach based on molecular parentage assessments. Mol. Ecol., 10, 2711–2718.
Pella JJ, Milner GB (1987) Use of genetic marks in stock composition analysis. In: Population genetics and shery management (eds. Ryman N, Utter F), pp. 247–276. University of Washington.
Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. J. Heredity, 90, 502–503.
Posada D, Crandall KA, Templeton AR (2000) GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol. Ecol., 9, 487–488.
Primmer CR, Koskinen MT, Piironen J (2000) The one that did not get away: individual assignment using microsatellite data detects a case of shing competition fraud. Proc. Roy. Soc. Lond., 267, 1699–1704.
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.
Pybus OG, Rambaut A, Harvey PH (2000) An integrated framework for the inference of viral population history from reconstructed genealogies. Genetics, 155, 1429–1437.
Pybus OG, Rambaut A (2002) GENIE: estimating demographic history from molecular phylogenies. Bioinformatics, 18, 1404–1405.
Randi E, Lucchini V (2002) Detecting rare introgression of domestic dog genes into wild wolf (Canis lupus) populations by Bayesian admixture analyses of microsatellite variation. Conserv. Genet., 3, 31–45.
Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc. Natl. Acad. Sci. USA, 94, 9197–9201.
Ray, N, Currat M, Excoffer L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol. Biol. Evol., 20, 76–86.
Raymond M and Rousset F (1995) An exact test for population differentiation. Evolution, 49, 1280–1283.
Rogers AR and Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol., 9, 552–569.
Roman J, Palumbi SR (2003) Whales before whaling in the north atlantic. Science, 301, 508–510.
Rooney AP, Honeycutt RL, Derr JN (2001) Historical population size change of bowhead whales inferred from DNA sequence polymorphism data. Evolution, 55, 1678–1685.
Rousset F (1996) Equilibrium values of measures of population subdivision for stepwise mutation processes. Genetics, 142, 1357–1362.
Saint-Laurent R, Legault M, Bernatchez L (2003) Divergent selection maintains adaptive di. erentiation despite high gene flow between sympatric rainbow smelt ecotypes (Osmerus mordax Mitchill). Mol. Ecol., 12, 315–330.
Schnabel A, Beerli P, Estoup A, Hillis D. (1998) A guide to software packages for data analysis in molecular ecology. In: Advances in Molecular Ecology (ed. Carvalho GR), pp. 291–303. IOS Press, Amsterdam.
Schneider S, Excoffer L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics, 152, 1079–1089.
Shoemaker JS, Painter IS, Weir BS (1999) Bayesian statistics in genetics. TIG, 15, 354–358.
Sites JW Jr., FitzSimmons NN, DA Silva NJ Jr., Cantarelli VH (1999) Conservation genetics of the giant amazon river turtle (Podocnemis expansa; Pelomedusidae)-inferences from two classes of molecular markers. Chelonian Conserv. Biol., 3, 454–463.
Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution, 47, 264–279.
Slatkin M(1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139, 457–462.
Slatkin M, Barton NH (1989) Methods for estimating gene flow. Evolution, 43, 1349–1368.
Smouse PE, Waples RS, Tworek JA (1990) A mixed shery model for use with incomplete source population data. Can. J. Fish. Aquat. Sci., 47, 620–634.
Spencer CC, Neigel JE, Leberg PL (2000) Experimental evaluation of the usefulness of microsatellite DNA for detecting demographic bottlenecks. Mol. Ecol., 9, 1517–1528.
Stephens M (2001) Inference under the coalescent. In: Handbook of Statistical Genetics (eds. Balding, DJ, Bishop M, Cannings C), Wiley, England.
Storz JF, Beaumont MA (2002) Testing for genetic evidence of population expantion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56, 154–166.
Storz JF, Beaumont MA, Alberts SC (2002) Genetic evidence for long-term population decline in a savannah-dwelling primate: inferences from a hierarchical Bayesian model. Mol. Biol. Evol., 19, 1981–1990.
Strimmer K and Pybus OG (2001) Exploring the demographic history of DNA sequences using the generalized skyline plot. Mol. Biol. Evol., 18, 2298–2305.
Sunnucks P (2000) Efficient genetic markers for population biology. TREE, 15, 199–203.
Tajima F (1989) Statistical methods for testing the neutral mutation hypothesis by DNA polymorphisms. Genetics, 123, 585–595.
Templeton AR, Routman E, Phillips C (1995) Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum. Genetics, 140, 767–782.
Templeton AR (1998) Nested clade analyses of phylogeo-graphic data: testing hypotheses about gene. ow and population history. Mol. Ecol., 7, 381–397.
Templeton AR (2004) Statistical phylogeography: methods of evaluating and minimizing inference errors. Mol. Ecol., 13, 789–810.
Turner TF, Wares JP, Gold JR (2002) Genetic effective size is three orders of magnitude smaller than adult census size in an abundant, estuarine-dependent marine sh (Sciaenops ocellatus) Genetics, 162, 1329–1339.
Utter F and Ryman N (1993) Genetic markers and mixed stock sheries. Fisheries, 18, 11–21.
Van Oppen MJH, Rico C, Turner GF, Hewitt GM (2000) Extensive homoplasy, nonstepwise mutations, and shared ancestral polymorphism at a complex microsatellite locus in Lake Malawi cichlids. Mol. Biol. Evol., 17, 489–498.
Vila`et al. (2003) Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proc. Roy. Soc. Lond., 270, 91–97.
Wakeley J (1996) Distinguishing migration from isolation using the variance of pairwise dierences. Theor. Pop. Biol., 49, 369–386.
Waldick RC, Kraus S, Brown M, White BN (2002) Evaluating the effects of historic bottleneck events: an assessment of microsatellite variability in the endangered North Atlantic right whale. Mol. Ecol., 11, 2241–2249.
Wall JD (2003) Estimating ancestral population sizes and divergence times. Genetics, 163, 395–404.
Waples RS (1989) A generalized approach for estimating e. ective population size from temporal changes in allele frequency. Genetics, 121, 379–391.
Waples RS (1998) Separating the wheat from the chaff: patterns of genetic di. erentiation in high gene flow species. J. Hered., 89, 438–450.
Waser PM, Strobeck C (1998) Genetic signatures of interpop-ulation dispersal. TREE, 13, 43–44.
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.
Weir BS, Hill WG (2002) Estimating F-statistics. Annu. Rev. Gen., 36, 721–750.
Whitlock M, McCauley DE (1999) Indirect estimation of gene flow and migration: FST≠1/(4Nm+1). Heredity, 82, 117–125.
Williamson EG, Slatkin M (1999) Using maximum likelihood to estimate population size from temporal changes in allele frequencies. Genetics, 152, 755–761.
Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics, 163, 1177–1191.
Wilson IJ, Balding DJ (1998) Genealogical inference from mi-crosatellite data. Genetics, 150, 499–510.
Wilson IJ, Weale, Balding DJ (2003) Inferences from DNAdata: population histories, evolutionary processes and forensic match probabilities. J. Roy. Stat. Soc. A, 166, 155–188.
Wright S (1931) Evolution in Mendelian population. Genetics, 16, 97–159.
Wright S (1951) The genetical structure of populations. Ann. Eugen., 15, 323–354.
Yang Z (2002) Likelihood and Bayes estimation of ancestral population sizes in hominoids using data from multiple loci. Genetics, 162, 1811–1823.
Zhivotovsky LA (1999) A new genetic distance with application to constrained variation at microsatellite loci. Mol. Biol. Evol., 16, 467–471.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Pearse, D.E., Crandall, K.A. Beyond FST: Analysis of population genetic data for conservation. Conservation Genetics 5, 585–602 (2004). https://doi.org/10.1007/s10592-003-1863-4
Issue Date:
DOI: https://doi.org/10.1007/s10592-003-1863-4