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Genetic Effects of a Persistent Bottleneck on a Natural Population of Ornate Box Turtles (Terrapene ornata)

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Abstract

Human activities in the past few hundred years have caused enormous impacts on many ecosystems, greatly accelerating the rate of population decline and extinction. In addition to habitat alteration and destruction, the loss of genetic diversity due to reduced population size has become a major conservation issue for many imperiled species. However, the genetic effects of persistent population bottlenecks can be very different for long-lived and short-lived species when considering the time scale of centuries. To investigate the genetic effects of persistent population bottlenecks on long-lived species, we use microsatellite markers to assess the level of genetic diversity of a small ornate box turtle population that has experienced a persistent bottleneck in the past century, and compare it to a large relatively undisturbed population. The genetic signature of a recent bottleneck is detected by examining the deviation from mutation-drift equilibrium in the small population, but the bottleneck had little effect on its level of genetic diversity. Computer simulations combined with information on population structure suggest that an effective population size of 300, which results in a census population size of 700, would be required for the small population to maintain 90% of the average number of alleles per locus in the next 200 years. The life history of long-lived species could mask the accelerated rate of genetic drift, making population recovery a relatively slow process. Statistical analysis of genetic data and empirical-based computer simulations can be important tools to facilitate conservation planning.

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References

  • Akst EP, Boersma PD, Fleischer RC (2002) A comparison of genetic diversity between the Galapagos Penguin and the Magellanic Penguin. Conserv. Genet., 3, 375–383.

    Google Scholar 

  • Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol., 5, 181–190.

    Google Scholar 

  • Avise JC (1995) Mitochondrial DNA polymorphism and a connection between genetics and demography of relevance to conservation. Conserv. Biol., 9, 686–690.

    Google Scholar 

  • Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol. Ecol., 11, 155–165.

    Google Scholar 

  • Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics, 153, 2013–2029.

    PubMed  Google Scholar 

  • Beheregaray LB, Cio C, Caccone A, Gibbs JP, Powell JR (2003) Genetic divergence, phylogeography and conservation units of giant tortoises from Santa Cruz and Pinzon, Galapagos Islands. Conserv. Genet., 4, 31–46.

    Google Scholar 

  • Belzer B (2002) A nine year study of eastern box turtle courtship with implications for reproductive success and conservation in a translocated population. Turtle Tortoise Newsletter, 6, 17–26.

    Google Scholar 

  • Blair WF (1976) Some aspects of the biology of the ornate box turtle, Terrapene ornata. Southwest Nat., 21, 89–103.

    Google Scholar 

  • Bouzat JL, Cheng HH, Lewin HA, Westemeier RL, Brawn JD, Paige KN (1998a) Genetic evaluation of a demographic bottleneck in the Greater Prairie Chicken. Conserv. Biol., 12, 836–843.

    Google Scholar 

  • Bouzat JL, Lewin HA, Paige KN (1998b) The ghost of genetic diversity past:historical DNA analysis of the Greater Prairie Chicken. Am. Nat., 152, 1–6.

    Google Scholar 

  • Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol. Ecol., 5, 453–455.

    PubMed  Google Scholar 

  • Ciofi C, Bruford MW (1999) Genetic structure and gene. ow among Komodo dragon populations inferred by microsatellite loci analysis. Mol. Ecol., 8, S17–S30.

    PubMed  Google Scholar 

  • Ciofi C, Milinkovitch MC, Gibbs JP, Caccone A, Powell JR (2002) Microsatellite analysis of genetic divergence among populations of giant Galapagos tortoises. Mol. Ecol., 11, 2265–2283.

    PubMed  Google Scholar 

  • Coltman DW, Bowen WD, Wright JM (1998) Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc. R. Soc. London. B., Biol. Sci., 265, 803–809.

    Google Scholar 

  • Congdon JD, Dunham AE, van Loben Sels RC (1993) Delayed sexual maturity and demographics of Blanding's turtles (Emydoidea blandingii):Implications for conservation and management of long-lived organisms. Conserv. Biol., 7, 826–833.

    Google Scholar 

  • Congdon JD, Dunham AE, van Loben Sels RC (1994) Demographics of common snapping turtles (Chelydra serpentina):Implications for conservation and management of long-lived organisms. Am. Zool., 34, 397–408.

    Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144, 2001–2014.

    PubMed  Google Scholar 

  • Cunningham J, Baard EHW, Harley EH, O'Ryan C (2002) Investigation of genetic diversity in fragmented geometric tortoise (Psammobates geometricus) populations. Conserv. Genet., 3, 215–223.

    Google Scholar 

  • Davis WA (1993) History of Whiteside County. Higginson Book Company, Salem.

    Google Scholar 

  • Dever JA, Strauss RE, Rainwater TR, McMurry ST, Densmore LD (2002) Genetic diversity, population subdivision, and gene. ow in Morelet's crocodile (Crocodylus moreletii) from Belize, Central America. Copeia, 2002, 1078–1091.

    Google Scholar 

  • Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple sequence repeat loci in human populations. Proc. Natl. Acad. Sci. USA, 91, 3166–3170.

    PubMed  Google Scholar 

  • Dodd CK (2001) North American Box Turtles. University of Oklahoma Press, Norman.

    Google Scholar 

  • Dodd CK, Siegel (1991) Relocation, repatriation, and translocation of amphibians and reptiles:Are they conservation strategies that work? Herpetologica, 47, 336–350.

    Google Scholar 

  • Doroff AM, Keith LB (1990) Demography and ecology of an ornate box turtle (Terrapene ornata ) population in southcentral Wisconsin. Copeia, 1990, 387–399.

    Google Scholar 

  • England PR, Osler GH (2001) GENELOSS:A computer program for simulating the effects of population bottlenecks on genetic diversity. Mol. Ecol. Notes, 1, 111–113.

    Google Scholar 

  • England PR, Osler GH, Woodworth LM, Montgomery ME, Briscoe DA, Frankham R (2003) Effects of intense versus di. use population bottlenecks on microsatellite genetic diversity and evolutionary potential. Conserv. Genet., 4, 595–604.

    Google Scholar 

  • Ernst CH, Lovich JE, Barbour RW eds. (1994) Turtles of the United States and Canada. Smithsonian Institution Press, Washington, DC.

    Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes:application to human mitochondrial DNA restriction data. Genetics, 131, 479–491.

    PubMed  Google Scholar 

  • Foose TJ, Boer L, Seal US, Lande R (1995) Conservation management strategies based on viable populations. In: Population Management for Survival and Recovery (eds. Ballou JD, Gilpin M, Foose TJ), pp. 273–294. Columbia University Press, New York.

    Google Scholar 

  • Frankel OH, Soule ME (1981) Conservation and Evolution. Cambridge University Press, Cambridge.

    Google Scholar 

  • Frankham R (1998) Inbreeding and extinction:Island populations. Conserv. Biol., 12, 665–675.

    Google Scholar 

  • Franklin IR (1980) Evolutionary change in small populations. In: Conservation Biology, an Evolutionary-Ecological Perspective (eds. Soule ME, Wilcox BA), pp. 135–149. Sinauer, Sunderland.

    Google Scholar 

  • Friar EA, Ladoux T, Roalson EH, Robichaux RH (2000) Microsatellite analysis of a population crash and bottleneck in the Mauna Kea silversword, Argyroxiphium sandwicense ssp. sandwicense (Asteraceae), and its implications for reintroduction. Mol. Ecol., 9, 2027–2034.

    PubMed  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol. Ecol., 10, 305–318.

    PubMed  Google Scholar 

  • Gautschi B, Widmer A, Joshi J, Koella JC (2002) Increased frequency of scale anomalies and loss of genetic variation in serially bottlenecked populations of the dice snake, Natrix tessellata. Conserv. Genet., 3, 235–245.

    Google Scholar 

  • Gibbs JP, Shriver WG (2002) Estimating the e. ects of road mortality on turtle populations. Conserv. Biol., 16, 1647–1652.

    Google Scholar 

  • Haig SM (1998) Molecular contributions to conservation. Ecology, 79, 413–425.

    Google Scholar 

  • Halley J, Hoelzel AR (1996) Simulation models of bottleneck events in natural populations. In: Molecular Genetic Approaches in Conservation (eds. Smith TB, Wayne RK), pp. 347–364. Oxford University Press, Oxford.

    Google Scholar 

  • Hedrick PW (1999) Perspective:Highly variable loci and their interpretation in evolution and conservation. Evolution, 53, 313–318.

    Google Scholar 

  • Heppell SS (1998) Application of life-history theory and population model analysis to turtle conservation. Copeia, 1998, 367–375.

    Google Scholar 

  • Houlden BA, England PR, Taylor AC, Greville WD, Sherwin WB (1996) Low genetic variability of the Koala Phascolarctos cinereus in South-eastern Australia following a severe population bottleneck. Mol. Ecol., 5, 269–281.

    PubMed  Google Scholar 

  • Hoelzel AR (1999) Impact of population bottlenecks on genetic variation and the importance of life-history;A case study of the northern elephant seal. Biol. J. Linn. Soc., 68, 23–39.

    Google Scholar 

  • Hoelzel AR, Halley J, O'Brien SJ, Campagna C, Arnbom T, Le Boeuf B, Ralls K, Dover GA (1993) Elephant seal genetic variation and the use of simulation models to investigate historical population bottlenecks. J. Hered., 84, 443–449.

    PubMed  Google Scholar 

  • Ingvarsson PK (2002) Lone wolf to the rescue. Nature, 420, 472.

    PubMed  Google Scholar 

  • Kett HF (1993) History of Carroll County. Higginson Book Company, Salem.

    Google Scholar 

  • Kuo C-H, Janzen FJ (2003) BottleSim:a bottleneck simulation program for long-lived species with overlapping generations. Mol. Ecol. Notes, 3, 669–673.

    Google Scholar 

  • Lande R (1988) Demographic models of the northern spotted owl (Strix occidentalis caurina). Oecologia, 75, 601–607.

    Google Scholar 

  • Lande R (1993) Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am. Nat., 142, 911–927.

    Google Scholar 

  • Legler JM (1960) Natural history of the ornate box turtle, Terrapene ornata ornata Agassiz. Univ. Kans. Publ., Mus. Nat. Hist., 11, 527–669.

    Google Scholar 

  • Levell JP (1997) A Field Guide to Reptiles and the Law. Serpent's Tale Books, Lanesboro.

    Google Scholar 

  • Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv. Biol., 12, 228–237.

    Google Scholar 

  • Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998a) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J. Hered., 89, 238–247.

    PubMed  Google Scholar 

  • Luikart G, Sherwin WB, Steele BM, Allendorf FW (1998b) Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol. Ecol., 7, 963–974.

    PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Metcalf AL, Metcalf E (1985) Longevity in some ornate box turtles (Terrapene ornata ornata). J. Herpetol., 19, 157–158.

    Google Scholar 

  • Moore W (1993) 1992 Ornate Box Turtle Project–Results and Recommendations. Bureau of Endangered Resources, Madison.

    Google Scholar 

  • Nei M, Marayuma T, Chakraborty R (1975) The bottleneck e. ect and genetic variability in populations. Evolution, 29, 1–10.

    Google Scholar 

  • Newman D, Pilson D (1997) Increased probability of extinction due to decreased genetic e. ective population size:Experimental populations of Clarkia pulchella. Evolution, 51, 354–362.

    Google Scholar 

  • Nunney L (1991) The in. uence of age structure and fecundity on e. ective population size. Proc. R. Soc. Lond. B, 246, 71–76.

    PubMed  Google Scholar 

  • Nunney L (1993) The in. uence of mating system and overlapping generations on effective population size. Evolution, 47, 1329–1341.

    Google Scholar 

  • Nunney L (1995) Measuring the ratio of e. ective population size to adult numbers using genetic and ecological data. Evolution, 49, 389–392.

    Google Scholar 

  • Nunney L, Elam DR (1994) Estimating the e. ective population size of conserved populations. Conserv. Biol., 8, 175–184.

    Google Scholar 

  • O'Brien SJ (1994) A role for molecular genetics in biological conservation. Proc. Natl. Acad. Sci. USA, 91, 5748–5755.

    PubMed  Google Scholar 

  • Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a nite population. Genet. Res., 22, 201–204.

    PubMed  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK:A program for detecting recent e. ective population size reductions from allele frequency data. J. Hered., 90, 502–503.

    Google Scholar 

  • Pope TR (1996) Socioecology, population fragmentation, and patterns of genetic loss in endangered primates. In: Conservation Genetics: Case Histories from Nature (eds. Avise JC, Hamrick JL), pp. 119–159. Chapman & Hall, New York.

    Google Scholar 

  • Quattro JM, Vrijenhoek RC (1989) Fitness di. erences among remnant populations of the endangered Sonoran topminnow. Science, 245, 976–978.

    PubMed  Google Scholar 

  • Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution, 55, 1095–1103.

    PubMed  Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between tness and genetic diversity. Conserv. Biol., 17, 230–237.

    Google Scholar 

  • Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butter. y metapopulation. Nature, 392, 491–494.

    Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin:A Software for Population Genetics Data Analysis. Ver 2.000. Genetics and Biometry Lab, Department of Anthropology, University of Geneva.

  • Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can. J. Zool., 69, 82–90.

    Google Scholar 

  • Soule M, Gilpin M, Conway W, Foose T (1986) The millennium ark:How long a voyage, how many staterooms, how many passengers? Zoo Biol., 5, 101–114.

    Google Scholar 

  • Spencer CC, Neigel JE, Leberg PL (2000) Experimental evaluation of the usefulness of microsatellite DNA for detecting demographic bottlenecks. Mol. Ecol., 9, 1517–1528.

    PubMed  Google Scholar 

  • Starkey DE, Shaffier HB, Burke RL, Forstner MRJ, Iverson JB, Janzen FJ, Rhodin AGJ, Ultsch GR (2003) Molecular systematics, phylogeography, and the e. ects of Pleistocene glaciation in the painted turtle (Chrysemys picta) complex. Evolution, 57, 119–128.

    PubMed  Google Scholar 

  • Tallmon DA, Draheim HM, Mills LS, Allendorf FW (2002) Insights into recently fragmented vole populations from combined genetic and demographic data. Mol. Ecol., 11, 699–709.

    PubMed  Google Scholar 

  • Taylor BL, Dizon AE (1996) The need to estimate power to link genetics and demography for conservation. Conserv. Biol., 10, 661–664.

    Google Scholar 

  • Vrijenhoek RC (1994) Genetic diversity and tness in small populations. In: Conservation Genetics (eds. Loeschcke V, Tomiuk J, Jain SK), pp. 37–53. Birkhauser, Berlin.

    Google Scholar 

  • Weir BS (1996) Genetic Data Analysis II:Methods for Discrete Population genetic Data. Sinauer, Sunderland.

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.

    Google Scholar 

  • Weisrock DW, Janzen FJ (2000) Comparative molecular phylogeography of North American softshell turtltes (Apalone): implications for regional and wide-scale historical evolutionary forces. Molecular Phylogenetics and Evolution, 14, 152–164.

    PubMed  Google Scholar 

  • Yeh FC, Boyle TJB (1997) Population genetic analysis of codominant and dominant markers and quantitative traits. Belg. J. Bot., 129, 157.

    Google Scholar 

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Authors and Affiliations

  1. Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA, 50011, USA

    Chih-Horng Kuo & Fredric J. Janzen

  2. Department of Genetics, The University of Georgia, Athens, GA, 30602, USA

    Chih-Horng Kuo

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  1. Chih-Horng Kuo
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Kuo, CH., Janzen, F.J. Genetic Effects of a Persistent Bottleneck on a Natural Population of Ornate Box Turtles (Terrapene ornata). Conservation Genetics 5, 425–437 (2004). https://doi.org/10.1023/B:COGE.0000041020.54140.45

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