Advertisement

Conservation Genetics

, Volume 8, Issue 6, pp 1441–1452 | Cite as

Population genetics and conservation of the threatened southeastern beach mouse (Peromyscus polionotus niveiventris): subspecies and evolutionary units

  • Jacob F. Degner
  • I. Jack Stout
  • James D. Roth
  • Christopher L. Parkinson
Original Article

Abstract

We investigated genetic diversity within the southeastern beach mouse (SEBM-Peromyscus polionotus niveiventris) and also tested the hypothesis that the subspecies recognition of P.p. niveiventris, based on size and color differences, is congruent with this taxon representing a discrete evolutionary lineage. We used ten polymorphic microsatellite loci and mitochondrial cytochrome-b gene DNA sequences to investigate genetic diversity and population structure within the SEBM, and to determine the level of divergence between the SEBM and the nearest known inland subspecies of the oldfield mouse (Peromyscus polionotus rhoadsi). Moderate genetic distances were observed between the SEBM and the inland oldfield mouse based on microsatellite data, with F ST values ranging from 0.11 to 0.22 between these taxa. Additionally, mitochondrial DNA haplotypes of the SEBM formed a distinct monophyletic group relative to haplotypes sampled from P. p. rhoadsi. Based on previous estimates of rates of mitochondrial DNA evolution in rodents, we inferred that Pleistocene sea-level fluctuations are likely responsible for the historical isolation of the SEBM lineage from mainland P. polionotus. Our data demonstrate the genetic distinctiveness of the SEBM, justifying the current subspecies designation for the SEBM and its continued protection under the United States Endangered Species Act. We classify the Cape Canaveral and Smyrna Dunes Park populations of SEBM as a single evolutionary significant unit. The two known extant allopatric populations of the SEBM showed some differentiation in microsatellite frequencies and were moderately reciprocally distinguishable based on assignment to distinct genetic clusters by a Bayesian admixture procedure. These results justify the classification of these two extant SEBM populations as distinct management units that should be independent targets of management and conservation attention.

Keywords

Biogeography Endangered species Evolutionarily significant units Management units Microsatellites Peromyscus polionotus niveiventris 

Notes

Acknowledgements

Funding for this study was provided by Patrick Air Force Base, Florida. We thank the personnel of the 45th CES/CEVR wing and especially Mr. Donald George for support during these studies. We would like to thank Hopi Hoekstra, Alice Bard, Jane Provancha, Alex Suazo, Angie DeLong, Megan Keserauskis, and Donna Oddy, along with field assistants Shannon Letcher, Kasey Gillespie, Meryl Green, David Gunderson, April Verpoorton, Daniel Smith, Weldon Lavigne, and Angie Ashcraft-Cryder, for collecting the tissue samples used in this study. We thank Todd Castoe, Jeff Van Zant, Haakon Kalkvik and Eric Hoffman for comments that greatly improved this manuscript and Lisa McCauley for help with Fig. 1. This work was conducted under permit 12-09-04-01 issued by Florida Department of Environmental Protection Division of Recreation and Parks, WV04065 issued by the Florida Fish and Wildlife Conservation Commission, TE105642-0 issued by USFWS, and Animal Project # 03-13W from the IACUC, University of Central Florida.

References

  1. Bradley RD, Baker RJ (2001) A test of the genetic species concept: cytochrome-b sequences and mammals. J Mammal 84:960–973CrossRefGoogle Scholar
  2. Bradley RD, Baker RJ (2006) Speciation in mammals and the genetic species concept. J Mammal 87:643–662–973CrossRefPubMedGoogle Scholar
  3. Brunhoff C, Galbreath K, Fedorov V, Cook J, Jaarola M. (2003) Holarctic phylogeography of the root vole (Microtus oeconomus): implications for late Quaternary biogeography of high latitudes. Mol Ecol 12:957–968PubMedCrossRefGoogle Scholar
  4. Burbrink FT, Lawson R, Slowinski JB (2000) Mitochondrial DNA phylogeography of the polytypic North American Rat Snake (Elaphe obsoleta): a critique of the subspecies concept. Evolution 54:2101–2118Google Scholar
  5. Chapman FM (1889) Description of two new species of the genus Hesperomys from Florida. Bull Am Mus Nat Hist 2:117Google Scholar
  6. Chirhart SE, Honeycutt RL, Greenbaum IF (2000) Microsatellite markers for the deer mouse Peromyscus maniculatus. Mol Ecol 9:1669PubMedCrossRefGoogle Scholar
  7. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660PubMedCrossRefGoogle Scholar
  8. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295PubMedCrossRefGoogle Scholar
  9. Dimmick W, Ghedotti M, Grose M, Maglia A, Meinhardt D, Pennock D (1999) The importance of systematic biology in defining units of conservation. Conserv Biol 13:653–660CrossRefGoogle Scholar
  10. Ehrhart LM (1978) Pallid Beach Mouse. In: Layne JN (ed) Rare and endangered biota of Florida. University Presses of Florida, Gainsville, FloridaGoogle Scholar
  11. 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 to Morocco. Theor Appl Genet 92:832–839CrossRefGoogle Scholar
  12. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611PubMedCrossRefGoogle Scholar
  13. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge, UKGoogle Scholar
  14. Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752PubMedGoogle Scholar
  15. Fritz U, Siroky P, Kami H, Wink M (2005) Environmentally caused dwarfism or a valid species– is Testudo weissingeri Bour, 1996 a distinct evolutionary lineage? New evidence from mitochondrial and nuclear genomic markers. Mol Phylogenet Evol 37:389–401PubMedCrossRefGoogle Scholar
  16. Gentry J, Smith M (1968) Food habits and burrow associates of Peromyscus polionotus. J Mammal 49:562–565CrossRefGoogle Scholar
  17. Gompert Z, Nice C, Fordyce J, Forister M, Shapiro A (2006) Identifying units for conservation using molecular systematics: the cautionary tale of the Karner blue butterfly. Mol Ecol 15:1759–1768PubMedCrossRefGoogle Scholar
  18. Goudet. J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  19. Hadley NF, Schultz TD, Savill AC (1988) Spectral reflectances of three subspecies of the tiger beetle Neocicindela perhispida: correlations with their respective habitat substrates. N Z J Zool 15:343–346Google Scholar
  20. Hall ER (1981) The mammals of North America, 2nd edn. John Wiley and Sons, New YorkGoogle Scholar
  21. Herron DH, Castoe TA, Parkinson CL (2004) Sciurid phylogeny and the paraphyly of Holarctic ground squirrels (Spermophilus). Mol Phylogenet Evol 31:1015–1030PubMedCrossRefGoogle Scholar
  22. Hoekstra HE, Krenz J (2005) Local adaptation in the rock pocket mouse (Chaetodipus intermedius): natural selection and phylogenetic history of populations. Heredity 94:217–228PubMedCrossRefGoogle Scholar
  23. Hoekstra HE, Hirschmann RJ, Bundey RA, Insel PA, Crossland JP (2006) A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313:101–104PubMedCrossRefGoogle Scholar
  24. Hoffman E, Blouin M (2000) A review of colour and pattern polymorphisms in anurans. Biol J Linn Soc, 70:633–665CrossRefGoogle Scholar
  25. Hoffman E, Schueler F, Jones A, Blouin M (2006) An analysis of selection on a colour polymorphism in the northern leopard frog. Mol Ecol 15:2627–2641PubMedCrossRefGoogle Scholar
  26. Humphrey SR, Barbour DB (1981) Status and habitat of three subspecies of beach mice in Florida. J Mammal 68:297–304Google Scholar
  27. Humphrey SR (1992) Pallid Beach Mouse. In: Humphrey SR (ed) Rare and endangered biota of Florida Vol. 1.: Mammals. University Presses of Florida, Gainsville, FloridaGoogle Scholar
  28. Jaarola M, Searle B (2002) Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences. Mol Ecol 11:2613–2621PubMedCrossRefGoogle Scholar
  29. Jensen JL, Bohonak AJ, Kelly ST (2005) Isolation by distance web service. BMC Genetics. 6:13Google Scholar
  30. Kettlewell H (1955) Selection experiments on industrial melanism in the Lepidoptera. Heredity 9:323–342Google Scholar
  31. Kettlewell H (1956) Further selection experiments on industrial melansim in the Lepidoptera. Heredity 10:287–301Google Scholar
  32. Kizirian D, Donnelly M (2004) The criterion of reciprocal monophyly and classification of nested diversity at the species level. Mol Phylogenet Evol 32:1072–1076PubMedCrossRefGoogle Scholar
  33. Lessa E, Cook J (1998) The molecular phylogenetics of Tuco-Tucos (genus Ctenomys, Rodentia:Octodontidae) suggests an early burst of speciation. Mol Phylogenet Evol 9:88–99PubMedCrossRefGoogle Scholar
  34. Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375CrossRefGoogle Scholar
  35. Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254PubMedCrossRefGoogle Scholar
  36. O’Hara R (2005) Comparing the effects of genetic drift and fluctuating selection on genotype frequency changes in the scarlet tiger moth. P Roy Soc Lond Bio 272:211–217CrossRefGoogle Scholar
  37. Olendorf R, Rodd F, Punzalan D, Houde A, Hurt C, Reznick D, Hughes K (2006) Frequency dependent survival in natural guppy populations. Nature 441:633–636PubMedCrossRefGoogle Scholar
  38. Osgood WH (1909) A revision of the mice of the American genus Peromyscus. N Am Fauna 28:1–28CrossRefGoogle Scholar
  39. Paetkau D (1999) Using genetics to identify intraspecific conservation units: a critique of current methods. Conserv Biol 13:1507CrossRefGoogle Scholar
  40. Pennock D, Dimmick W (1997) Critique of the evolutionarily significany unit as a definition for “distinct population segment” under the U.S. Endangered Species Act. Conserv Biol 11:611–619CrossRefGoogle Scholar
  41. Prince KL, Glenn TC, Dewey MJ. (2002) Cross-species amplification among peromyscines of new microsatellite DNA loci from the oldfield mouse (Peromyscus polionotus subgriseus). Mol Ecol 2:133–136CrossRefGoogle Scholar
  42. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  43. Posada D, Crandall KA, 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  44. Posada D, Crandall KA, 2001. Selecting the best-Wt model of nucleotide substitution. Syst Biol 50:580–601PubMedCrossRefGoogle Scholar
  45. Rader RB, Belk MC, Shiozawa DK, Crandall KA (2005) Empirical tests for ecological exchangeability. Anim Conserv 8:239–247CrossRefGoogle Scholar
  46. Raymond M, Rousset F (1995) genepop (Web version, 2005) Population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  47. Ronquist F, Huelsenbeck JP, 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  48. Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10CrossRefGoogle Scholar
  49. Schneider S, Roessli D, Excoffier L (2005) arlequin v. 3.0: Documentation and program. Genetics and biometry laboratory, Univerersity of Geneva, Geneva, SwitzerlandGoogle Scholar
  50. Smith M, Patton J (1993) The diversification of South American murid rodents: evidence from mitochondrial sequence data for the akodontine tribe. Biol J Linn Soc 50:149–177CrossRefGoogle Scholar
  51. Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Nat Acad Sci USA 101:15261–15264PubMedCrossRefGoogle Scholar
  52. Stout IJ (1992) Peromyscus polionotus niveiventris. In: Humphrey SR (eds) Rare and endangered biota of Florida. 2nd edn. University Presses of Florida, Gainesville, FloridaGoogle Scholar
  53. Swilling W, Wooten M (2002) Subadult dispersal in a monogamous species: the Alabama Beach Mouse (Peromyscus polionotus ammobates). J Mammal 83:252–259CrossRefGoogle Scholar
  54. Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (and other methods). Version 4.0b10 Sinauer, Sunderland, MAGoogle Scholar
  55. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III Cladogram estimation. Genetics 132:619–633PubMedGoogle Scholar
  56. US Fish and Wildlife Service (1993) Recovery plan for the Anastasia Island and Southeastern Beach Mouse. USFWS, Atlanta, Georgia, p. 30Google Scholar
  57. Van Zant JL (2006) Molecular ecology of Peromyscus polionotus. Dissertation, Auburn UniversityGoogle Scholar
  58. Webb SD (1990) Historical biogeography. In: Myers RL Ewel JJ (eds) Ecosystems of Florida. University of Central Florida Press, Orlando, FloridaGoogle Scholar
  59. Weir BS, Cockerham CC (1984) 1984 Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  60. Wooten MC, Scribner KT, Krehling JT (1999) Isolation and characterization of microsatellite loci from the endangered beach mouse Peromyscus polionotus. Mol Ecol 8:157–168PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  • Jacob F. Degner
    • 1
  • I. Jack Stout
    • 1
  • James D. Roth
    • 1
  • Christopher L. Parkinson
    • 1
  1. 1.Department of BiologyUniversity of Central FloridaOrlandoUSA

Personalised recommendations