Conservation Genetics

, Volume 16, Issue 1, pp 113–123 | Cite as

Recognition of a highly restricted freshwater snail lineage (Physidae: Physella) in southeastern Oregon: convergent evolution, historical context, and conservation considerations

  • Alexandria C. Moore
  • John B. Burch
  • Thomas F. DudaJr.
Research Article

Abstract

Non-marine mollusks have the highest number of documented extinctions of any major taxonomic group. Given their conservation status and the numerous cases of taxonomic uncertainty concerning freshwater mollusks in particular, the recognition of potentially endangered species is critically important. Here, we evaluate the genetic distinctiveness and phylogenetic position of a freshwater snail restricted to a series of geothermal springs within the Owyhee River drainage in Oregon (the ‘Owyhee wet-rock physa’). Because these snails closely resemble Physella (Petrophysa) zionis, a wet-rock physa that occurs in a small area in Zion National Park (Utah), the Owyhee wet-rock physa is presumably either closely related to or represents a disjunct population of P. zionis. However, phylogenetic analyses of sequences of mitochondrial cytochrome oxidase I and nuclear first and second internal transcribed spacer gene regions indicate that the Owyhee wet-rock physa is genetically distinct from other physid species. Despite exhibiting similar morphologies, the Owyhee wet-rock physa and P. zionis are distantly related physids; instead, the Owyhee wet-rock physa is most closely related to a population of physids from central California. These results suggest that convergent evolution may be responsible for the similar shell morphologies of the Owyhee wet-rock physa and P. zionis. Furthermore, the close relationship between physid populations in southeastern Oregon and central California suggests a historical connection between the Owyhee River and river drainages to the south. Finally, we recommend that the Owyhee wet-rock physa be considered critically endangered based on its extremely limited distribution.

Keywords

Freshwater gastropods Physidae Convergent evolution COI ITS1 ITS2 

References

  1. Albrecht C, Wilke T, Kuhn K, Streit B (2004) Convergent evolution of shell shape in freshwater limpets: the African genus Burnupia. Zool J Linn Soc 140(4):577–586CrossRefGoogle Scholar
  2. Albrecht C, Wolff C, Gloer P, Wilke T (2008) Concurrent evolution of ancient sister lakes and sister species: the freshwater gastropod genus Radix in lakes Ohrid and Prespa. Hydrobiologia 615(1):157–167CrossRefGoogle Scholar
  3. Albrecht C, Kroll O, Moreno Terrazas E, Wilke T (2009) Invasion of ancient Lake Titicaca by the globally invasive Physa acuta (Gastropoda: Pulmonata: Hygrophila). Biol Invasions 11(8):1821–1826CrossRefGoogle Scholar
  4. Britton DK, McMahon RF (2004) Effects of temperature on physiological energetics in the common pond snail, Physella virgata. Physiol Biochem Zool 77:187–196PubMedCrossRefGoogle Scholar
  5. Burch JB, Tottenham J (1980) North American freshwater snails: species list, ranges, and illustrations. Walkerana 1(3):1–215Google Scholar
  6. Dayrat B, Conrad M, Balayan S, White TR, Albrecht C, Golding R, Gomes SR, Harasewych MG, de Frias Martins AM (2011) Phylogenetic relationships and evolution of pulmonate gastropods (Mollusca): new insights from increased taxon sampling. Mol Phylog Evol 59(2):425–437CrossRefGoogle Scholar
  7. DeJong RJ, Morgan JAT, Paraense WL, Pointier JP, Amarista M, Ayeh-Kumi PFK, Babiker A, Barbosa CS, Bremond P, Canese AP, de Souza CP, Dominguez C, File S, Gutierrez A, Incani RN, Kawano T, Kazibwe F, Kpikpi J, Lwambo NJS, Mimpfoundi R, Njiokou F, Poda JN, Sene M, Velasquez LE, Yong M, Adema CM, Hofkin BV, Mkoji GM, Loker ES (2001) Evolutionary relationships and biogeography of Biomphalaria (Gastropoda: Planorbidae) with implications regarding its role as host of the human bloodfluke, Schistosoma mansoni. Mol Biol Evol 18(12):2225–2239Google Scholar
  8. DeWitt TJ (1995) Functional tradeoffs and phenotypic plasticity in the freshwater snail Physa. PhD Thesis, Boston UniversityGoogle Scholar
  9. DeWitt TJ, Scheiner SM (2004) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, Cary, pp 126–150Google Scholar
  10. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–297PubMedGoogle Scholar
  11. Frest TJ, Johannes EJ (1995) Interior Columbia Basin mollusk species of special concern: Final report. Interior Columbia Basin ecosystem management project. www.icbemp.gov/science/frest_1.pdf. Accessed 1 August 2012
  12. Gates K, Kerans B, Keebaugh J, Kalinowski S, Vu N (2012) Taxonomic identity of the endangered Snake River physa, Physa natricina (Pulmonata: Physidae) combining traditional and molecular techniques. Con Gen 14:159–169Google Scholar
  13. Hershler R, Madsen DB, Currey DR (2002) Great Basin aquatic systems history. Smithsonian Institution Press, Washington DC, pp 145–387Google Scholar
  14. International Union for Conservation of Nature (2010) IUCN guidelines for using the IUCN red list categories and criteria. Version 8.1. Prepared by the standards and petitions subcommittee in March 2010. Downloadable from http://intranet.iucn.org/webfiles/doc/SSC/RedList/RedListGuidelines.pdf. Accessed 1 August 2012
  15. International Union for Conservation of Nature (2012) IUCN red list categories and criteria: version 3.1. Second edition. Gland, Switzerland and Cambridge, UK: IUCN. iv +, pp 32. http://www.iucnredlist.org/technical-documents/categories-and-criteria. Accessed 1 August 2012
  16. Johnson PD, Bogan AE, Brown KM, Burkhead NM, Cordeiro JR, Garner JT, Hartfield PD, Lepitzki DW, Mackie GL, Pip E, Tarpley TA, Tiemann JS, Whelan NV, Strong EE (2013) Conservation status of freshwater gastropods of canada and the united states. Fisheries 38(6):247–282CrossRefGoogle Scholar
  17. Jorgensen A, Kristensen TK, Stothard JR (2007) Phylogeny and biogeography of African Biomphalaria (Gastropoda: Planorbidae), with emphasis on endemic species of the great East African lakes. Zool J Linn Soc 151(2):337–349CrossRefGoogle Scholar
  18. Lydeard C, Cowie RH, Ponder WF, Bogan AE, Bouchet P, Clark SA, Cummings KS, Frest TJ, Gargominy O, Herbert DG, Hershler R, Perez KE, Roth C, Seddon M, Strong EE, Thompson FG (2004) The global decline of nonmarine mollusks. Bio Sci 54(4):321–330Google Scholar
  19. Lysne SJ, Perez KE, Brown KM, Minton RL, Sides JD (2008) A review of freshwater gastropod conservation: challenges and opportunities. J N Am Benthol Soc 27(2):463–470CrossRefGoogle Scholar
  20. Miller RR (1965) Quaternary freshwater fishes of North America. In: Wright HE Jr, Frey DG (eds) The quaternary of the United States. Princeton University Press, Princeton, pp 569–581Google Scholar
  21. Miller RR and Smith GR (1967) New fossil fishes from Plio-Pleistocene Lake Idaho, vol 654. Occasional papers of the Museum of Zoology, University of Michigan, pp 1–24Google Scholar
  22. Miller RR and Smith GR (1981) Distribution and evolution of Chasmistes (Pisces: Catostomidae) in Western North America, vol 696. Occasional papers of the Museum of Zoology, University of Michigan, pp 1–46Google Scholar
  23. Pilsbury HA (1925) A fresh-water snail, Physella zionis, living under unusual conditions. Proc Acad Nat Sci Philadelphia 77:325–328Google Scholar
  24. Pip E, Franck JPC (2008) Molecular phylogenetics of central Canadian Physidae (Pulmonata: Basommatophora) Can. J Zool 86:10–16Google Scholar
  25. Rambaut A (1996) Se–Al: sequence alignment editor. Retrieved August 12, 2012 from http://iubio.bio.indiana.edu/soft/iubionew/molbio/dna/analysis/Pist/main.html
  26. Rambaut A (2009) FigTree v1.3.1 2006–2009. Retrieved August 12, 2012 from http://tree.bio.ed.ac.uk/software/figtree/
  27. Regnier C, Fontaine D, Bouchet P (2009) Not knowing, not recording, not listing: numerous unnoticed mollusk extinctions. Con Bio 23(5):1214–1221CrossRefGoogle Scholar
  28. Remigio E, Lepitzki D, Lee J, Hebert P (2001) Molecular systematic relationships and evidence for a recent origin of the thermal spring endemic snails Physella johnsoni and Physella wrighti (Pulmonata: Physidae). Can J Zool 79(11):1941–1949CrossRefGoogle Scholar
  29. Rogers D, Wethington A (2007) Physa natricina Taylor 1988, junior synonym of Physa acuta Draparnaud, 1805 (Pulmonata: Physidae). Zootaxa 1662:45–51Google Scholar
  30. Smith GR, Morgan N, and Gustafson E (2000) Fishes of the Mio-Pliocene Ringold Formation, Washington: pliocene capture of the snake river by the Columbia River. University of Michigan, papers on paleontology, No. 32Google Scholar
  31. Strayer D (2006) Challenges for freshwater invertebrate conservation. J N Am Benthol Soc 25(2):271–287CrossRefGoogle Scholar
  32. 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 Bio Evo 28:2731–2739CrossRefGoogle Scholar
  33. Taylor DW (1960) Distribution of the freshwater clam Pisidium ultramontanum; a zoogeographic inquiry. Am J Sci 258-A:325–334Google Scholar
  34. Taylor DW (1985) Evolution of freshwater drainages and molluscs in western North America. In: Smiley CJ (ed) Late cenozoic history of the Pacific Northwest. American Association for the Advancement of Science, San Francisco, pp 265–321Google Scholar
  35. Taylor DW (2003) Introduction to Physidae (Gastropoda: Hygrophila) biogeography, classification, morphology. Revista de Biologia Trop 51:1–287Google Scholar
  36. United States geological survey (2010) Water data report: 09413500 Virgin River near St George, UT. National water information system. U.S. geological survey. Retrieved April 15, 2013 from <http://waterdata.usgs.gov/usa/nwis/uv?09413500>
  37. United States geological survey (2013) Water data report: 13184000 Owyhee River at Owyhee, OR. National Water Information System. U.S. geological survey. Retrieved April 15, 2013 from <http://nwis.waterdata.usgs.gov/nwis/monthly/?referred_module=sw&site_no=13184000&por_13184000_2=545544,00060,2,1890-03,1986-09&format=html_table&date_format=YYYY-MM-DD&rdb_compression=file&submitted_form=parameter_selection_list>
  38. Wagner HM, Hanson CB, Gustafson EP, Gobalet KW, Whistler DP (1997) Biogeography of the pliocene and pleistocene vertebrate faunas of Northeastern California and their temporal significance to the development of the Modoc Plateau and Klamath Mountain Region. San Bernardino County Museum Assoc Quarterly 44(1):13–21Google Scholar
  39. Wethington A, Guralnick R (2004) Are populations of physids from different hot springs distinctive lineages? Am Malacol Bull 19(1–2):135–144Google Scholar
  40. Wethington A, Lydeard C (2007) A molecular phylogeny of physidae (Gastropoda: Basommatophora) based on mitochondrial DNA sequences. J Molluscan Stud 73:241–257CrossRefGoogle Scholar
  41. Wheeler HE, Cook EF (1954) Structural and stratigraphic significance of the snake river capture. Idaho-Oregon J Geol 62(6):525–536CrossRefGoogle Scholar
  42. White LR, McPheron BA, Stauffer JR Jr (1996) Molecular genetic identification tools for the unionids of French Creek, Pennsylvania. Malacologia 38:181–202Google Scholar
  43. Wilke T, Schultheiss R, Albrecht C (2009) As time goes by: a simple fool’s guide to molecular clock approaches in invertebrates. Am Malacol Bull 27:25–45CrossRefGoogle Scholar
  44. Xu Z, Guo X, Gaffney PM, Pierce JC (2001) Chromosomal location of the major ribosomal RNA genes in Crassostrea virginica and Crassostrea gigas. Veliger 44:79–83Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Alexandria C. Moore
    • 1
  • John B. Burch
    • 1
  • Thomas F. DudaJr.
    • 1
    • 2
  1. 1.Department of Ecology and Evolutionary Biology and Museum of ZoologyUniversity of MichiganAnn ArborUSA
  2. 2.Smithsonian Tropical Research InstituteAncόnRepublic of Panama

Personalised recommendations