Advertisement

Conservation Genetics

, Volume 6, Issue 4, pp 575–585 | Cite as

Evidence for a recent genetic bottleneck in the endangered Florida Keys silver rice rat (Oryzomys argentatus) revealed by microsatellite DNA analyses

  • Yunqiu WangEmail author
  • Dean A. Williams
  • Michael S. Gaines
Article

Abstract

Low levels of genetic variation are thought to contribute significantly to the higher extinction rates of endemic island populations compared to their mainland counterparts. We used six microsatellite loci to compare the genetic structure of the endangered silver rice rat (Oryzomys argentatus) population in Saddlebunch Key, Florida to the mainland population of the closely related marsh rice rat (Oryzomys palustris natator) in Everglades National Park. Allelic richness and gene diversity are significantly lower in Saddlebunch Key than in the larger mainland population, and the two populations are significantly differentiated as measured by both F-statistics and Bayesian clustering methods. These findings support the classification of the Keys population as a “distinct vertebrate population” by the U.S. Fish and Wildlife Service. Current gene diversity (H E) is higher than expected under mutation-drift equilibrium in Saddlebunch Key, indicating a genetic bottleneck. The Keys population also exhibits a mode shift in its allele frequency distribution which suggests a very recent bottleneck has occurred and is consistent with reports of recent population declines. Although habitat loss and exotic species pose a more immediate and serious threat to silver rice rats, the continued loss of genetic variation may contribute to their long-term extinction risk due to inbreeding or by lowering the population’s ability to adapt to future environmental changes. The protection of habitat and the removal of introduced predators and competitors may help increase the population size of silver rice rats and lower their risk of extinction, both from a demographic and a genetic perspective.

Keywords

bottleneck endangered island population microsatellite rice rats 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

We thank Phil Frank of the Key West National Wildlife Refuge (U.S. Fish and Wildlife Service) for providing the silver rice rat samples. This research received significant support from the Department of Interior’s Critical Ecosystems Studies special funding initiative for Everglades restoration, administered by the National Park Service. Our work has also been supported by the U.S. Geological Service’s Florida Integrated Science Centers and the University of Miami. Rejane Lamazares provided laboratory assistance. Numi Mitchell provided helpful discussions on the manuscript and access to unpublished data on the population size of silver rice rats. Comments by Amanda Hale, Colin Hughes, John Purcell, Carles Vilà, and two anonymous reviewers improved this manuscript.

References

  1. Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol. Ecol. 5:453–455CrossRefPubMedGoogle Scholar
  2. Caughley G (1994) Directions in conservation biology. J. Anim. Ecol. 63:215–244CrossRefGoogle Scholar
  3. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  4. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol. Evol. 15:290–295PubMedCrossRefGoogle Scholar
  5. Degen B, Petit R, Kremer A (2001) SGS – Spatial genetic software: a computer program for analysis of spatial genetic and phenotypic structures of individuals and populations. J. Heredity 92:447–448CrossRefPubMedGoogle Scholar
  6. Di Renzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc. Nat. Acad. Sci. USA 91:3166–3170PubMedCrossRefGoogle Scholar
  7. El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree (Argania spinosa (L.) Skeels) endemic of Morocco. Theor. App. Gen. 92:832–839CrossRefGoogle Scholar
  8. Esher RJ, Wolfe JL, Layne JN (1978) Swimming behavior of rice rats and cotton rats. J. Mamm. 59:551–558CrossRefGoogle Scholar
  9. Fairbridge RW (1974) The Holocene sea-level record in South Florida. In: Environments of South Florida: Past and Present. Miami Geol. Soc., Memoir 2 (ed. Gleason PJ), pp. 223–232Google Scholar
  10. Forys EA, Dueser RD (1993) Inter-island movements of rice rats (Oryzomys palustris). Am. Midl. Nat. 130:408–412CrossRefGoogle Scholar
  11. Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327CrossRefPubMedGoogle Scholar
  12. Frankham R (1998) Inbreeding and extinction: island populations. Conserv. Biol. 12:665–675CrossRefGoogle Scholar
  13. Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol. Ecol. 10:2741–2752PubMedGoogle Scholar
  14. Gaggiotti OE, Lange O, Rassmann K, Gliddons C (1999) A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Mol. Ecol. 8:1513–1520CrossRefPubMedGoogle Scholar
  15. Gaines MS, Diffendorfer JE, Tamarin RH, Whittam TS (1997) The effects of habitat fragmentation on the genetic structure of small mammal populations. Heredity 88:294–304Google Scholar
  16. Goodyear NC (1991) The taxonomic status of the silver rice rat, Oryzomys argentatus. J. Mamm. 72:723–730CrossRefGoogle Scholar
  17. Goodyear NC, Lazell., Jr. JD (1986) Relationships of the silver rice rat Oryzomys argentatus (Rodentia: Muridae). Postilla 198:1–7Google Scholar
  18. Goodyear NC (1987) Distribution and habitat of the silver rice rat, Oryzomys argentatus. J. Mamm. 68:692–695CrossRefGoogle Scholar
  19. Goudet J (2001) FSTAT: A Program to Estimate and Test Gene Diversities and Fixation Indices (version 2.9.3). Available at http://www.unil.ch/izea/softwares/fstat.htmlGoogle Scholar
  20. Hanski I (1999) Metapopulation Ecology. Oxford University Press, Oxford UKGoogle Scholar
  21. Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol. Ecol. 11:2467–2474CrossRefPubMedGoogle Scholar
  22. Humphrey SR (1992) Lower Keys population of rice rat, Oryzomys palustris natator (in part). In: Humphrey SR, (ed), Rare and endangered biota of Florida, Volume I Mammals. University Press of Florida, Gainesville Florida, pp. 300–309Google Scholar
  23. Humphrey SR, Setzer HW (1989) Geographic variation and taxonomic revision of rice rats (Oryzomys palustris and O. argentatus) of the United States. J. Mamm. 70:557–570CrossRefGoogle Scholar
  24. Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1459PubMedCrossRefGoogle Scholar
  25. Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv. Biol. 12:228–237CrossRefGoogle Scholar
  26. Madsen T, Still B, Shine R (1996) Inbreeding depression in an isolated population of adders Vipera berus. Biol. Conserv. 75:113–118CrossRefGoogle Scholar
  27. Moritz C (1994) Defining “evolutionarily significant units” for conservation. Trends Ecol. Evol. 9:373–375CrossRefGoogle Scholar
  28. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  29. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: Software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes, doi: 10.1111/j.1471–8286.2004.00684.x (online early)Google Scholar
  30. Pimm SL, Jones, HL, Diamond J (1988) On the risk of extinction. Am. Nat. 132:757–785CrossRefGoogle Scholar
  31. Pimm SL, Gittleman JL, McCracken GF, Gilpin M (1989) Plausible alternatives to bottlenecks to explain reduced genetic diversity. Trends Ecol. Evol. 4:176–177CrossRefGoogle Scholar
  32. 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. Hered., 90, 502–503. Available at: http://www.ensam.inra.fr/URLB/bottleneck/bottleneck.htmlGoogle Scholar
  33. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  34. Pritchard JK, Wen W (2003) Documentation for Structure Software: Version 2. Available at: http://pritch.bsd.uchicago. eduGoogle Scholar
  35. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv. Biol. 17:230–237CrossRefGoogle Scholar
  36. Rousset F (2003) Effective size in simple metapopulation models. Heredity 91:107–111CrossRefPubMedGoogle Scholar
  37. Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortellius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature Lond. 392:491–494CrossRefGoogle Scholar
  38. Schluter D (2001) Ecology and the origin of species. Trends Ecol. Evol. 16:372–380CrossRefPubMedGoogle Scholar
  39. Schmitt T, Hewitt GM (2004) The genetic case of population threat and loss: a case study of butterflies. Mol. Ecol. 13:21–31CrossRefPubMedGoogle Scholar
  40. Singh PB, Brown RE, Roser B (1987) MHC antigens in urine as olfactory recognition cues. Nature Lond. 327:161–164CrossRefGoogle Scholar
  41. Smith AT, Vrieze JM (1979) Population structure of Everglades rodents: responses to a patchy environment. J. Mamm. 60:778–794CrossRefGoogle Scholar
  42. Soulé ME (1986) Conservation Biology: The Science of Scarcity and Diversity. Sinauer Associates, Sunderland MassachusettsGoogle Scholar
  43. Spitzer AT, Lazell JD (1978) A new rice rat (genus Oryzomys) from Florida’s Lower Keys. J. Mamm. 59:787–792CrossRefGoogle Scholar
  44. U.S. Fish and Wildlife Service [FWS] (1999) Rice Rat Oryzomys palustris natator. In: Multi-Species Recovery Plan for South Florida. pp. 173–186Google Scholar
  45. Wang DY, Hughes CR, Gines-Candelaria EA, Gaines MS (2000) Polymorphic microsatellite loci of Oryzomys palustris, the marsh rice rat, in South Florida detected by silver staining. Mol. Ecol. 9:1931–1932CrossRefPubMedGoogle Scholar
  46. Wattier R, Engel CR, Saumitou-Laprade P, Valero M (1998) Short allele dominance as a source of heterozygote deficiency at microsatellite loci: experimental evidence at the dinucleotide locus Gv1CT in Gracilaria gracilis (Rhodophyta). Mol. Ecol. 7:1569–1573CrossRefGoogle Scholar
  47. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  48. Wilson AC, Cann RL, Carr SM, George M, Gyllensten UB, Helm-Bychowski KM, Higuchi RG, Palumbi SR, Prager EM, Sage RD, Stoneking M (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biol. J. Linn. Soc. 26:375–400Google Scholar
  49. Wolfe JL (1982) Oryzomys palustris. Mammalian Species 176:1–5Google Scholar
  50. Yamaguchi M, Yamazaki K, Beauchamp GK, Bard J, Thomas L, Boyse EA (1981) Distinctive urinary odors governed by the major histocompatibility locus of the mouse. Proc. Nat. Acad. Sci. U.S.A. 78:5817PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Yunqiu Wang
    • 1
    Email author
  • Dean A. Williams
    • 1
  • Michael S. Gaines
    • 1
  1. 1.Department of BiologyUniversity of MiamiCoral GablesUSA

Personalised recommendations