Conservation Genetics

, Volume 17, Issue 5, pp 1055–1066 | Cite as

Conservation genetics of the endangered San Francisco Bay endemic salt marsh harvest mouse (Reithrodontomys raviventris)

  • M. J. StathamEmail author
  • S. Aamoth
  • L. Barthman-Thompson
  • S. Estrella
  • S. Fresquez
  • L. D. Hernandez
  • R. Tertes
  • B. N. Sacks
Research Article


The salt marsh harvest mouse (SMHM, Reithrodontomys raviventris) is an endangered species endemic to the San Francisco Bay region of California, USA, where habitat loss and fragmentation over the past century have reduced the mouse’s distribution to <25 % of its historical range. To aid in conservation prioritization, we first investigated the possibility of hybridization with the morphologically similar western harvest mouse (WHM, R. megalotis) in areas of sympatry and developed genetic tools to differentiate the two species. We then investigated the phylogeography and genetic structure of the SMHM, including support for currently recognized SMHM subspecies designations. Lastly, we evaluated the morphological criteria currently used for the identification of species in the field. Analyses using mtDNA cytochrome b sequences and 11 microsatellites from 142 mice indicated complete and substantial separation of the SMHM and WHM, with no evidence of hybridization. These genetic markers as well as the mtDNA control region also identified a deep genetic division within the SMHM concordant with the current subspecies designations, R. r. raviventris and R. r. halicoetes. We identified the lowest genetic diversity within the southern subspecies, which inhabits a much reduced and highly fragmented portion of the species range. Morphological field identification of harvest mouse species was more successful at identifying SMHM (92 %) than WHM (44 %), with a large portion of WHM being incorrectly identified as SMHM. Field identification of harvest mouse species in the range of the southern SMHM subspecies was just above 50 %, indicating that current methods for morphological differentiation of species in that area are insufficient. Our confirmation of genetically distinct SMHM subspecies highlights the importance of determining the status and genetic composition of relict populations in the remaining patches of marshland in the central San Francisco Bay where the two subspecies may occur, as well as developing better tools for the discrimination of species, particularly in the range of the southern subspecies


Field identification Management Morphology Population subdivision Species identification Subspecies 



The primary funding for this research came from California Department of Fish and Wildlife Grant (P1282009). Additional funding came from the Veterinary Genetics Laboratory at UC Davis. Thank you for to Bill Burkhard (DWR), Peter Moyle (UC Davis) for provision of student funding. SMHM survey cooperators include Karen Taylor (DFW Napa/Sonoma Wildlife Area), Stacy Martinelli (DFW, Fagen Marsh), John Krause (DFW, Eden Landing Ecological Reserve), USFWS staff Joy Albertson (Don Edwards SFB NWR), Meg Marriott (USFWS, San Pablo Bay NWR), and Isa Woo (USGS, San Pablo Bay). Thank you to Natalie Goddard, Michelle Holtz, and Sini Reponen for their help in the field and laboratory. Thank you to two anonymous reviewers whose comments and suggestions improved the quality of this paper.

Supplementary material

10592_2016_843_MOESM1_ESM.docx (44 kb)
Supplementary material 1 (DOCX 43 kb)


  1. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell publishing, HobokenGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  3. Arbogast BS (1999) Mitochondrial DNA phylogeography of the new world flying squirrels (Glaucomys): implications for pleistocene biogeography. J Mammal 80:142–155CrossRefGoogle Scholar
  4. Arellano E, Gonzalez-Cozatl FX, Rogers DS (2005) Molecular systematics of Middle American harvest mice Reithrodontomys (Muridae), estimated from mitochondrial cytochrome b gene sequences. Mol Phylogenet Evol 37:529–540CrossRefPubMedGoogle Scholar
  5. Atwater BF (1979) Ancient processes at the site of Southern San Francisco Bay: movement of the crust and changes in Sea Level. In: Conomos TJ (ed) San Francisco Bay: The urbanized estuary., San Francisco, Pacific Division, American Association for the Advancement of Science, pp 31–45Google Scholar
  6. Bandelt HJ, Forester P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
  7. Bell DM, Hamilton MJ, Edwards CW, Wiggins LE, Martinez RM, Strauss RE, Bradley RD, Baker RJ (2001) Patterns of karyotypic megaevolution in Reithrodontomys: evidence from a cytochrome-b phylogenetic hypothesis. J Mammal 82:81–91CrossRefGoogle Scholar
  8. Brown SK (2003) Conservation genetics of salt marsh harvest mice (Reinthrodontomys raviventris) in Suisun Marsh, CA. Master Thesis, San Luis Obispo, Calif. California Polytechnic State UniversityGoogle Scholar
  9. Castro-Campillo A, Roberts HR, Schmidly DJ, Bradley RD (1999) Systematic status of Peromyscus boylii ambiguus based on morphologic and molecular data. J Mammal 80:1214–1231CrossRefGoogle Scholar
  10. Chan Y, Arcese P (2002) Subspecific differentiation and conservation of song Sparrows (Melospiza melodia) in the San Francisco Bay region inferred by microsatellite loci analysis. Auk 119:641–657CrossRefGoogle Scholar
  11. Chan YL, Hill CE, Maldonado JE, Fleischer RC (2006) Evolution and conservation of tidal-marsh vertebrates: molecular approaches. Stud Avian Biol 32:54–75Google Scholar
  12. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefPubMedGoogle Scholar
  13. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedPubMedCentralGoogle Scholar
  14. Fisler GF (1963) Effects of salt water on food and water consumption and weight of harvest mice. Ecology 44:604–608CrossRefGoogle Scholar
  15. Fisler GF (1965) Adaptations and speciation in harvest mice of the marshes of San Francisco Bay. Univ Calif Publ Zool 77:1–108. doi: 10.2307/1932549 Google Scholar
  16. Goals Project (2000) Baylands ecosystem species and community profiles: Life histories and environmental requirements of key plants, fish and wildlife. Prepared by the San Francisco Bay Area Ecosystems Goals Project. In : P.R. Olofson (ed) San Francisco Bay Regional Water Quality Control Board, Oakland, California, USAGoogle Scholar
  17. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  18. Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913CrossRefPubMedGoogle Scholar
  19. Hey J (2010) Isolation with migration models for more than two populations. Mol Biol Evol 27:905–920CrossRefPubMedGoogle Scholar
  20. Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci USA 104:2785–2790CrossRefPubMedPubMedCentralGoogle Scholar
  21. Ichiyanagi M (2010) The adaptive context of ultraviolet induced reflectance and fluorescence patterns within the order Rodentia. Master of Science Thesis, California State University, SacramentoGoogle Scholar
  22. Maley JM, Brumfield RT (2013) Mitochondrial and next-generation sequence data used to infer phylogenetic relationships and species limits in the Clapper/King Rail complex. Condor 115:316–329CrossRefGoogle Scholar
  23. Méndez-Harclerode FM, Hanson JD, Fulhorst CF, Milazzo ML, Ruthven DC 3rd, Bradley RD (2005) Genetic diversity within the southern plains woodrat (Neotoma micropus) in southern Texas. J Mammal 86:180–190CrossRefPubMedPubMedCentralGoogle Scholar
  24. Moritz C (1994) Defining ‘evolutionary significant units’ for conservation. Trends Ecol Evol 9:373–375CrossRefPubMedGoogle Scholar
  25. Nabholz B, Glémin S, Galtier N (2008) Strong variations of mitochondrial mutation rate across mammals—the longevity hypothesis. Mol Biol Evol 25:120–130. doi: 10.1093/molbev/msm248 CrossRefPubMedGoogle Scholar
  26. National Research Council (2010) Sea level rise and the coastal environment. Advancing the science of climate change. The National Academies Press, Washington, DC, p 245Google Scholar
  27. Paetkau D (1999) Using genetics to identify intraspecific conservation units: a critique of current methods. Conserv Biol 13:1507–1509CrossRefGoogle Scholar
  28. Park SDE (2001) The Excel microsatellite toolkit. Trypanotolerance in West African cattle and the population genetic effects of selection. PhD Thesis, University College DublinGoogle Scholar
  29. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefPubMedGoogle Scholar
  30. Pritchard JK, Wen W (2002) Documentation for structure software version 2.
  31. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  32. Reponen SEM, Statham MJ, Barthman-Thompson L, Sacks BN (2014) Microsatellite primer development for the salt marsh harvest mouse (Reithrodontomys raviventris) and cross-amplification in the western harvest mouse (R. megalotis). Conserv Genet Resour 6:285–287. doi: 10.1007/s12686-013-0120-5 CrossRefGoogle Scholar
  33. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  34. Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  35. Shellhammer HS (1982) Reithrodontomys raviventris, vol 169., Mammalian speciesAmerican Society of Mammalogists, Washington, DC, pp 1–3Google Scholar
  36. Shellhammer HS (1984) Identification of salt marsh harvest mice Reithrodontomys raviventris, in the field and with cranial characteristics. Calif Fish Game 70:113–120Google Scholar
  37. Shellhammer HS (1989) Salt marsh harvest mice, urban development, and rising sea levels. Conserv Biol 3:59–65CrossRefGoogle Scholar
  38. Smith MF, Patton JL (1993) The Diversification of South American Murid Rodents: evidence from mitochondrial DNA sequence data for the Akodontine Tribe. Biol J Linn Soc Lond 50:149–177CrossRefGoogle Scholar
  39. Takekawa JY, Casazza ML, Overton CT, Bui TD, Vandergast A, Wood D, Estrella S (2014) Applied Studies on California Clapper Rail Population Dynamics in support of Comprehensive Multispecies Tidal Marsh Recovery. Unpublished Data Summary Report, U.S. Geological Survey, Western Ecological Research Center, Vallejo, Dixon, and San Diego, CAGoogle Scholar
  40. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  41. U.S. Fish and Wildlife Service (2013) Recovery Plan for Tidal Marsh Ecosystems of Northern and Central California. U.S. Fish and Wildlife Service, SacramentoGoogle Scholar
  42. Vázquez-Domínguez E, Espindola S (2013) Characterization of ten new microsatellite loci from the endangered endemic rodent, Reithrodontomys spectabilis. Conserv Genet Resour 5:251–253CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • M. J. Statham
    • 1
    Email author
  • S. Aamoth
    • 1
  • L. Barthman-Thompson
    • 2
  • S. Estrella
    • 2
  • S. Fresquez
    • 1
    • 2
  • L. D. Hernandez
    • 1
    • 2
  • R. Tertes
    • 3
  • B. N. Sacks
    • 1
    • 4
  1. 1.Mammalian Ecology and Conservation Unit, Veterinary Genetics LaboratoryUniversity of CaliforniaDavisUSA
  2. 2.Suisun Marsh Unit, Bay Delta RegionCalifornia Department of Fish and WildlifeStocktonUSA
  3. 3.Don Edwards San Francisco Bay National Wildlife RefugeUnited State Fish and Wildlife ServiceFremontUSA
  4. 4.Department of Population Health and Reproduction, School of Veterinary MedicineUniversity of CaliforniaDavisUSA

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