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Conservation Genetics

, Volume 10, Issue 1, pp 177–189 | Cite as

Avoidance of extinction through nonexistence: the use of museum specimens and molecular genetics to determine the taxonomic status of an endangered freshwater crayfish

  • Keith A. Crandall
  • Henry W. Robison
  • Jennifer E. Buhay
Research Article

Abstract

We investigated the endangered status and taxonomic status of the freshwater crayfish Procambarus ferrugineus, a crayfish species considered for the candidate list of the Endangered Species Act. This species has a narrow distribution from central Arkansas, USA and is codistributed with its presumed sister species, Procambarus liberorum. We sampled extensively throughout the ranges of both primary burrowing species and collected mitochondrial DNA from a hypervariable fragment of the 16S gene from 109 individuals across 22 sites. We also collected data from a variable region of the 12S gene from a subset of the resulting 16S haplotypes. Due to our inability to sample what we considered P. ferrugineus in the field, we included museum specimens from the United States Natural History Museum of both P. ferrugineus and P. liberorum. Analyses of the resulting data suggested that these two species are indeed the same and we therefore synonymize them under the name of priority—P. liberorum. Additionally, our sampling discovered three new cryptic species from southwestern Arkansas all from the genus Procambarus. Nested clade phylogeographic analysis coupled with population genetic analyses suggested that P. liberorum has had three rounds of range expansion throughout the inferred evolutionary history. Using IUCN Red List criteria for conservation assessment, we conclude that the species P. liberorum should be considered stable, but with special concern because of habitat fragmentation and urbanization, small restricted range, and a moderate level of genetic diversity. Procambarus reimeri should be considered endangered due to its limited geographic range and the potential for a decline in suitable habitat. The three potentially newly discovered species should be considered data deficient until more information is obtained on their distributional limits and habitat requirements. Our study highlights the importance of thorough geographic and taxonomic sampling coupled with the utility of collecting data from museum specimens to reach robust taxonomic and conservation conclusions for endangered species.

Keywords

Endangered Species Act Nested clade phylogeographic analysis Crayfish Arkansas Population genetics Conservation Species diagnosis 

Notes

Acknowledgements

We thank two anonymous reviewers for helpful comments in improving this manuscript. We gratefully acknowledge the travel and field support from the Arkansas Game & Fish Commission and the mentoring grant provided by the Roger and Victoria Sant Endowment for Conservation at Brigham Young University. We thank Savel Daniels, James Finlay, Betty Crump (USDA Forest Service), Brian Wagner (Arkansas Game and Fish Commission), Michael D. Warriner (Arkansas Natural Heritage Commission), Ron Goddard and students at Waldron High School, Michelle McGee and students at Acorn High School, Gene Leeds, Louie Leeds, and Joe Kremers (Clarksville) for their excellent assistance in collecting crayfish for this study. We thank Karen Reed and Rafael Lemaitre for allowing us access to the crayfish collection at the US Natural History Museum and for their assistance during our visits to the Smithsonian. KAC was partially supported by NSF grant EF-0531762.

References

  1. Allen RT (1990) Insect endemism in the interior highlands of North America. Fla Entomol 78:539–569Google Scholar
  2. Allen RT (1995) Pedetontus gershneri, a new species of Machilidae from the interior highlands of North America (Insecta: Microcoryphidae). Entomol News 106:195–198Google Scholar
  3. Buhay JE, Crandall KA (2005) Subterranean phylogeography of freshwater crayfishes shows extensive gene flow and surprisingly large population sizes. Mol Ecol 14:4259–4273PubMedCrossRefGoogle Scholar
  4. Buhay JE, Moni G, Mann N, Crandall KA (2007) Molecular taxonomy in the dark: evolutionary history, phylogeography, and diversity of cave crayfish in the subgenus Aviticambarus, genus Cambarus. Mol Phylogenet Evol 42:435–488PubMedCrossRefGoogle Scholar
  5. Clegg M (1995) Science and the Endangered Species Act. National Academy Press, WashingtonGoogle Scholar
  6. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659PubMedCrossRefGoogle Scholar
  7. Conservancy TN (1996) TNC priorities for conservation: 1996 annual report card for US plant and animal species. Nature Conservancy, ArlingtonGoogle Scholar
  8. Crandall KA (1997) The crayfish component to an endangered aquatic ecosystem of the southeast United States. Freshw Crayfish 11:83–86Google Scholar
  9. Crandall KA, Buhay JE (2008) Global diversity of crayfish (Astacidae, Cambaridae, and Parastacidae-Decapoda) in freshwater. Hydrobiologia 595:295–301CrossRefGoogle Scholar
  10. Crandall KA, Fitzpatrick JF Jr (1996) Crayfish molecular systematics: using a combination of procedures to estimate phylogeny. Syst Biol 45:1–26CrossRefGoogle Scholar
  11. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295PubMedCrossRefGoogle Scholar
  12. Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192PubMedCrossRefGoogle Scholar
  13. Drummond AJ, Simon WYH, Matthew JP, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:699–710CrossRefGoogle Scholar
  14. Ernst MR, Poulton BC, Stewart KW (1986) Neoperla (Plecoptera: Perlidae) of the southern Ozark and Ouachita mountain region, and two new species of Neoperla. Ann Entomol Soc Am 79:645–661Google Scholar
  15. Evans BJ, Supriatna J, Andayani N, Melnick DJ (2003) Diversification of Sulawesi macaque monkeys: decoupled evolution of mitochondrial and autosomal DNA. Evolution 57:1931–1946PubMedGoogle Scholar
  16. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376PubMedCrossRefGoogle Scholar
  17. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  18. Fetzner JW Jr, Crandall KA (2001) Genetic variation. In: Holdich DM (ed) Biology of freshwater crayfish. Blackwell Science, Oxford, pp 291–326Google Scholar
  19. Fetzner JW Jr, Crandall KA (2003) Linear habitats and the nested clade analysis: an empirical evaluation of geographic vs. river distances using an Ozark crayfish (Decapoda: Cambaridae. Evolution 57:2101–2118PubMedGoogle Scholar
  20. Fitzpatrick JF Jr (1978) Systematics of the crawfishes of the Hagenianus group of the genus Procambarus, subgenus Girardiella (Decapoda, Cambaridae). Tulane Stud Zool Bot 20:57–97Google Scholar
  21. Frazer KS, Harris SC (1991) Cladistic analysis of the Ochrotrichia shawnee group (Trichoptera: Hydroptilidae) and description of a new species from the interior highlands of northwestern Arkansas. J Kans Entomol Soc 64:363–371Google Scholar
  22. Gilbert MTP, Moore W, Melchior L, Worobey M (2007) DNA extraction from dry museum beetles without conferring external morphological damage. PLoS One 2:e272PubMedCrossRefGoogle Scholar
  23. Graham CH, Ferrier S, Huettman F, Moritz C, Peterson AT (2004) New developments in museum-based informatics and applications to biodiversity analysis. Trends Ecol Evol 19:497–503PubMedCrossRefGoogle Scholar
  24. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phyhlogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  25. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  26. Harpending HC, Batzer MA, Gurven M, Jorde LB, Rogers AR (1998) Genetic traces of ancient demography. Proc Natl Acad Sci USA 95:1961–1967PubMedCrossRefGoogle Scholar
  27. Hebert PDN, Ratnasingham S, deWaard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc London BGoogle Scholar
  28. Hobbs HH Jr, Robison HW (1988) The crayfish subgenus Girardiella (Decapoda: Cambaridae) in Arkansas, with the descriptions of two new species and a key to the members of the Gracilis group in the genus Procambarus. Proc Biol Soc Wash 101:391–413Google Scholar
  29. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310–2314PubMedCrossRefGoogle Scholar
  30. IUCN (2001) IUCN Red List Categories: Version 3.1. IUCN Species Survival Commission. Gland, SwitzerlandGoogle Scholar
  31. Matos JA, Schaal BA (2000) Chloroplast evolution in the pinus montezumae complex: a coalescent approach to hybridization. Evolution Int J Org Evolution 54:1218–1233Google Scholar
  32. Matthews WJ, Robison HW (1998) Influence of drainage connectivity, drainage area and regional species richness on fishes of the interior highlands of Arkansas. Am Midl Nat 139:1–19CrossRefGoogle Scholar
  33. Mayden RL (1985) Biogeography of Ouachita highland fishes. Southw Nat 30:195–211CrossRefGoogle Scholar
  34. Mayden RL (1988) Vicariance biogeography, parsimony, and evolution in North American freshwater fishes. Syst Zool 37:329–355CrossRefGoogle Scholar
  35. Mokady M, Loya Y, Achituv Y, Geffen E, Graur D, Rozenblatt S, Brickner I (1999) Speciation versus phenotypic plasticity in coral inhabiting barnacles: Darwin’s obervations in an ecological context. J Mol Evol 49:367–375PubMedCrossRefGoogle Scholar
  36. Morando M, Avila L, Sites JW Jr (2003) Sampling strategies for delimiting species: genes, individuals, and populations in the Liolaemus elongatus-kriegi complex (Squamata: Liolaemidae) in Andean-Patagonian South America. Syst Biol 52:159–185PubMedCrossRefGoogle Scholar
  37. Moulton SR, Stewart KW (1996) Caddisflies (Trichoptera) of the interior highlands of North America. Mem Am Entomol Inst 56:1–313Google Scholar
  38. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858PubMedCrossRefGoogle Scholar
  39. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  40. Orme CD, Davies RG, Burgess M, Eigenbrod F, Pickup N, Olson VA, Webster AJ, Ding TS, Rasmussen PC, Ridgely RS, Stattersfield AJ, Bennett PM, Blackburn TM, Gaston KJ, Owens IP (2005) Global hotspots of species richness are not congruent with endemism or threat. Nature 436:1016–1019PubMedCrossRefGoogle Scholar
  41. Paquin P, Hedin M (2004) The power and perils of ‘molecular taxonomy’: a case study of eyeless and endangered Cicurina (Araneae: Dictynidae) from Texas caves. Mol Ecol 13:3239–3255PubMedCrossRefGoogle Scholar
  42. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: Advantages of Akaike Information Criterion and Bayesian approaches over Likelihood Ratio Tests. Syst Biol 53:793–808PubMedCrossRefGoogle 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) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45PubMedCrossRefGoogle Scholar
  45. Posada D, Crandall KA, Templeton AR (2000) GeoDis: A program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9:487–488PubMedCrossRefGoogle Scholar
  46. Posada D, Crandall KA, Templeton AR (2006) Nested clade analysis statistics. Mol Ecol Notes 6:590–593CrossRefGoogle Scholar
  47. Poulton BC, Stewart KW (1987) The stoneflies of the Ozark and Ouachita Mountains (Plecoptera). Mem Am Entomol Inst 38:1–116Google Scholar
  48. Rambaut A, Drummond AJ (2003) Tracer: MCMC trace analysis tool. http://www.evolve.zoo.ox.ac.uk. University of Oxford, Oxford
  49. Robison HW (1986) Zoogeography of North American freshwater fishes. In: Hocutt CH, Wiley EO (eds) Zoogeography of North American freshwater fishes. Wiley, New York, pp 267–285Google Scholar
  50. Robison HW, Allen RT (1995) Only in Arkansas: a study of the endemic plants and animals of the state. University of Arkansas Press, FayettevilleGoogle Scholar
  51. Robison HW, Smith KL (1982) The endemic flora and fauna of Arkansas. Proc Arkansas Acad Sci 36:52–57Google Scholar
  52. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  53. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  54. Rowe RJ (2007) Legacies of land use adn recent climatic change: the small mammal fauna in the mountains of Utah. Am Nat 170:242–257PubMedCrossRefGoogle Scholar
  55. Rozas J, Sánchez-DelBarrio JC, Messegyer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  56. Shaw KL (2002) Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proc Natl Acad Sci USA 99:16122–16127PubMedCrossRefGoogle Scholar
  57. Sites JJ, Marshall J (2003) Delimiting species: a Renaissance issue in systematic biology. Trends Ecol Evol 18:462–470CrossRefGoogle Scholar
  58. Sites JW Jr, Crandall KA (1997) Testing species boundaries in biodiversity studies. Cons Biol 11:1289–1297CrossRefGoogle Scholar
  59. Stark BP, Stewart KW, Feminella J (1983) New records and descriptions of Alloperla (Plecoptera: Chloroperlidae) from the Ozark-Ouachita region. Entomol News 94:55–59Google Scholar
  60. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460PubMedGoogle Scholar
  61. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  62. Templeton AR (1998a) Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol 7:381–397PubMedCrossRefGoogle Scholar
  63. Templeton AR (1998b) Species and speciation: geography, population structure, ecology, and gene trees. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, Oxford, pp 32–43Google Scholar
  64. Templeton AR (1999) Using gene trees to infer species from testable null hypotheses: cohesion species in the Spalax ehrenbergi complex. In: Wasser SP (ed) Evolutionary theory and processes: modern perspectives, papers in Honour of Eviatar Nevo. Kluwer Academic Publishers, Dordrecht, pp 171–192Google Scholar
  65. Templeton AR (2001) Using phylogeographic analyses of gene trees to test species status and processes. Mol Ecol 10:779–791PubMedCrossRefGoogle Scholar
  66. Templeton AR (2004) Statistical phylogeography: methods of evaluating and minimizing inference errors. Mol Ecol 13:789–810PubMedCrossRefGoogle Scholar
  67. 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
  68. Thomas WK, Paabo S, Villablanca F, Wilson A (1990) Spatial and temporal continuity of kangaroo rat populations shown by sequencing mitochondrial DNA from museum specimens. J Mol Evol 31:101–112PubMedCrossRefGoogle Scholar
  69. Turner TF, Trexler JC, Kuhn DN, Robison HW (1996) Life-history variation and comparative phylogeography of darters (Pisces: Percidae) from the North American central highlands. Evolution 50:2023–2036CrossRefGoogle Scholar
  70. Wandeler P, Hoeck PEA, Keller LF (2007) Back to the future: museum specimens in population genetics. Trends Ecol Evol 22:634–642PubMedCrossRefGoogle Scholar
  71. Williams AB (1954) Speciation and distribution of the crayfishes of the Ozark Plateaus and Ouachita Provinces. Univ Kansas Sci Bull 36:803–918Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Keith A. Crandall
    • 1
    • 2
  • Henry W. Robison
    • 3
  • Jennifer E. Buhay
    • 4
  1. 1.Department of BiologyBrigham Young UniversityProvoUSA
  2. 2.Monte L. Bean Life Science MuseumBrigham Young UniversityProvoUSA
  3. 3.Department of Biological SciencesSouthern Arkansas UniversityMagnoliaUSA
  4. 4.Belle W. Baruch Institute for Marine SciencesUniversity of South CarolinaColumbiaUSA

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