Skip to main content

Advertisement

SpringerLink
Log in

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

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allen RT (1990) Insect endemism in the interior highlands of North America. Fla Entomol 78:539–569

    Google Scholar 

  • Allen RT (1995) Pedetontus gershneri, a new species of Machilidae from the interior highlands of North America (Insecta: Microcoryphidae). Entomol News 106:195–198

    Google Scholar 

  • Buhay JE, Crandall KA (2005) Subterranean phylogeography of freshwater crayfishes shows extensive gene flow and surprisingly large population sizes. Mol Ecol 14:4259–4273

    Article  PubMed  CAS  Google Scholar 

  • 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 42:435–488

    Article  PubMed  CAS  Google Scholar 

  • Clegg M (1995) Science and the Endangered Species Act. National Academy Press, Washington

    Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  PubMed  CAS  Google Scholar 

  • Conservancy TN (1996) TNC priorities for conservation: 1996 annual report card for US plant and animal species. Nature Conservancy, Arlington

    Google Scholar 

  • Crandall KA (1997) The crayfish component to an endangered aquatic ecosystem of the southeast United States. Freshw Crayfish 11:83–86

    Google Scholar 

  • Crandall KA, Buhay JE (2008) Global diversity of crayfish (Astacidae, Cambaridae, and Parastacidae-Decapoda) in freshwater. Hydrobiologia 595:295–301

    Article  Google Scholar 

  • Crandall KA, Fitzpatrick JF Jr (1996) Crayfish molecular systematics: using a combination of procedures to estimate phylogeny. Syst Biol 45:1–26

    Article  Google Scholar 

  • Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    Article  PubMed  Google Scholar 

  • Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192

    Article  PubMed  CAS  Google Scholar 

  • Drummond AJ, Simon WYH, Matthew JP, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:699–710

    Article  CAS  Google Scholar 

  • 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 79:645–661

    Google Scholar 

  • Evans BJ, Supriatna J, Andayani N, Melnick DJ (2003) Diversification of Sulawesi macaque monkeys: decoupled evolution of mitochondrial and autosomal DNA. Evolution 57:1931–1946

    PubMed  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fetzner JW Jr, Crandall KA (2001) Genetic variation. In: Holdich DM (ed) Biology of freshwater crayfish. Blackwell Science, Oxford, pp 291–326

    Google Scholar 

  • 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 57:2101–2118

    PubMed  CAS  Google Scholar 

  • Fitzpatrick JF Jr (1978) Systematics of the crawfishes of the Hagenianus group of the genus Procambarus, subgenus Girardiella (Decapoda, Cambaridae). Tulane Stud Zool Bot 20:57–97

    Google Scholar 

  • 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 64:363–371

    Google Scholar 

  • Gilbert MTP, Moore W, Melchior L, Worobey M (2007) DNA extraction from dry museum beetles without conferring external morphological damage. PLoS One 2:e272

    Article  PubMed  CAS  Google Scholar 

  • 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 19:497–503

    Article  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phyhlogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harpending HC, Batzer MA, Gurven M, Jorde LB, Rogers AR (1998) Genetic traces of ancient demography. Proc Natl Acad Sci USA 95:1961–1967

    Article  PubMed  CAS  Google Scholar 

  • Hebert PDN, Ratnasingham S, deWaard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc London B

  • 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 101:391–413

    Google Scholar 

  • Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310–2314

    Article  PubMed  CAS  Google Scholar 

  • IUCN (2001) IUCN Red List Categories: Version 3.1. IUCN Species Survival Commission. Gland, Switzerland

    Google Scholar 

  • Matos JA, Schaal BA (2000) Chloroplast evolution in the pinus montezumae complex: a coalescent approach to hybridization. Evolution Int J Org Evolution 54:1218–1233

    CAS  Google Scholar 

  • 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 139:1–19

    Article  Google Scholar 

  • Mayden RL (1985) Biogeography of Ouachita highland fishes. Southw Nat 30:195–211

    Article  Google Scholar 

  • Mayden RL (1988) Vicariance biogeography, parsimony, and evolution in North American freshwater fishes. Syst Zool 37:329–355

    Article  Google Scholar 

  • 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 49:367–375

    Article  PubMed  CAS  Google Scholar 

  • 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 52:159–185

    Article  PubMed  Google Scholar 

  • Moulton SR, Stewart KW (1996) Caddisflies (Trichoptera) of the interior highlands of North America. Mem Am Entomol Inst 56:1–313

    Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • 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 436:1016–1019

    Article  PubMed  CAS  Google Scholar 

  • 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 13:3239–3255

    Article  PubMed  CAS  Google Scholar 

  • 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 53:793–808

    Article  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: Testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Crandall KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45

    Article  PubMed  Google Scholar 

  • Posada D, Crandall KA, Templeton AR (2000) GeoDis: A program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9:487–488

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Crandall KA, Templeton AR (2006) Nested clade analysis statistics. Mol Ecol Notes 6:590–593

    Article  Google Scholar 

  • Poulton BC, Stewart KW (1987) The stoneflies of the Ozark and Ouachita Mountains (Plecoptera). Mem Am Entomol Inst 38:1–116

    Google Scholar 

  • Rambaut A, Drummond AJ (2003) Tracer: MCMC trace analysis tool. http://www.evolve.zoo.ox.ac.uk. University of Oxford, Oxford

  • 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 267–285

    Google Scholar 

  • Robison HW, Allen RT (1995) Only in Arkansas: a study of the endemic plants and animals of the state. University of Arkansas Press, Fayetteville

    Google Scholar 

  • Robison HW, Smith KL (1982) The endemic flora and fauna of Arkansas. Proc Arkansas Acad Sci 36:52–57

    Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Rowe RJ (2007) Legacies of land use adn recent climatic change: the small mammal fauna in the mountains of Utah. Am Nat 170:242–257

    Article  PubMed  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messegyer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • 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 99:16122–16127

    Article  PubMed  CAS  Google Scholar 

  • Sites JJ, Marshall J (2003) Delimiting species: a Renaissance issue in systematic biology. Trends Ecol Evol 18:462–470

    Article  Google Scholar 

  • Sites JW Jr, Crandall KA (1997) Testing species boundaries in biodiversity studies. Cons Biol 11:1289–1297

    Article  Google Scholar 

  • Stark BP, Stewart KW, Feminella J (1983) New records and descriptions of Alloperla (Plecoptera: Chloroperlidae) from the Ozark-Ouachita region. Entomol News 94:55–59

    Google Scholar 

  • Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460

    PubMed  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Templeton AR (1998a) Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol 7:381–397

    Article  PubMed  CAS  Google Scholar 

  • 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 32–43

    Google Scholar 

  • 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 171–192

    Google Scholar 

  • Templeton AR (2001) Using phylogeographic analyses of gene trees to test species status and processes. Mol Ecol 10:779–791

    Article  PubMed  CAS  Google Scholar 

  • Templeton AR (2004) Statistical phylogeography: methods of evaluating and minimizing inference errors. Mol Ecol 13:789–810

    Article  PubMed  Google Scholar 

  • 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 132:619–633

    PubMed  CAS  Google Scholar 

  • 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 31:101–112

    Article  PubMed  CAS  Google Scholar 

  • 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 50:2023–2036

    Article  Google Scholar 

  • Wandeler P, Hoeck PEA, Keller LF (2007) Back to the future: museum specimens in population genetics. Trends Ecol Evol 22:634–642

    Article  PubMed  Google Scholar 

  • Williams AB (1954) Speciation and distribution of the crayfishes of the Ozark Plateaus and Ouachita Provinces. Univ Kansas Sci Bull 36:803–918

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Biology, Brigham Young University, 675 Widtsoe Building, Provo, UT, 84602-5181, USA

    Keith A. Crandall

  2. Monte L. Bean Life Science Museum, Brigham Young University, Provo, UT, 84602, USA

    Keith A. Crandall

  3. Department of Biological Sciences, Southern Arkansas University, Magnolia, AR, 71754, USA

    Henry W. Robison

  4. Belle W. Baruch Institute for Marine Sciences, University of South Carolina, 607 EWS Building, Columbia, SC, 29208, USA

    Jennifer E. Buhay

Authors
  1. Keith A. Crandall
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Henry W. Robison
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jennifer E. Buhay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Keith A. Crandall.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Crandall, K.A., Robison, H.W. & Buhay, J.E. Avoidance of extinction through nonexistence: the use of museum specimens and molecular genetics to determine the taxonomic status of an endangered freshwater crayfish. Conserv Genet 10, 177–189 (2009). https://doi.org/10.1007/s10592-008-9546-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-008-9546-9

Keywords

Search

Navigation