Abstract
Assessments of genetic diversity for imperiled species can provide a baseline for determining the relative impacts of contemporary anthropogenic threats (e.g., habitat fragmentation) on population connectivity and identify historical factors contributing to population structure. We conducted a population genetics and phylogeographic assessment of the imperiled Pristine Crayfish (Cambarus pristinus) sampled throughout its range encompassing two morphologically distinct forms. Pristine Crayfish exhibit a disjunct distribution throughout lower order tributaries suggesting they are headwater-adapted species. The two morphologically distinct forms of the Pristine Crayfish are found in the upper Caney Fork (nominal Caney Fork form) and the Big Brush Creek and Cane Creek systems (Sequatchie form). We used 19 microsatellite loci and the cytochrome oxidase subunit I (COI) gene to assess population connectivity and genetic diversity of the Pristine Crayfish. Haplotypes recovered from the COI gene revealed that historic connectivity was maintained within each form of the Pristine Crayfish. However, the divergence between forms was higher (2.3%) than within forms (< 2.0%), suggesting each form is on an independent evolutionary trajectory, supporting recognition of the Sequatchie form as a distinct taxon. Microsatellite analyses for the Caney Fork form recovered a high degree of population isolation and support for six genetically isolated population. In addition, genetic diversity metrics per population and for the Caney Fork form were low suggesting that the Caney Fork form is at an increased risk of extinction under anthropogenic disturbances. We suggest that each form receive continued listing protection and conservation resources and that the Sequatchie form be treated as a unique taxon.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All mtDNA COI haplotypes are available on GenBank. Ascensions numbers for all haplotypes used in this study are found in Supplementary Table S1. Microsatellite primers tested and used for this study are listed in Supplementary Table S2.
References
Abdul-Muneer PM (2014) Application of microsatellite markers in conservation genetics and fisheries management: recent advances in population structure analysis and conservation strategies. Genet Res Int. https://doi.org/10.1155/2014/691759
Adamack AT, Gruber B (2014) PopGenReport: simplifying basic population genetic analyses in R. Methods Ecol Evol 5:384–387. https://doi.org/10.1111/2041-210X.12158
Allendorf FW (2017) Genetics and the conservation of natural populations: allozymes to genomes. Mol Ecol 26:420–430. https://doi.org/10.1111/mec.13948
Allendorf FW, Phelps SR (1981) Use of allelic frequencies to describe population structure. Can J Fish Aquat Sci 38:1507–1514. https://doi.org/10.1139/f81-203
Allert AL, Distefano RJ, Schmitt C et al (2012) Effects of mining-derived metals on riffle-dwelling crayfish in southwestern Missouri and southeastern Kansas, USA. Arch Environ Contam Toxicol 63:563–573. https://doi.org/10.1007/s00244-012-9797-9
Allert AL, Distefano RJ, Fairchild JF et al (2013) Effects of historical lead-zinc mining on riffle-dwelling benthic fish and crayfish in the Big River of southeastern Missouri, USA. Ecotoxicol 22:506–521. https://doi.org/10.1007/s10646-013-1043-3
Alp M, Keller I, Westram AM, Robinson C (2012) How river structure and biological traits influence gene flow: a population genetic study of two stream invertebrates with differing dispersal abilities. Freshw Biol 57:969–981. https://doi.org/10.1111/j.1365-2427.2012.02758.x
Anthony DM, Granger DE (2007) A new chronology for the age of Appalachian erosional surfaces determined by cosmogenic nuclides in cave sediments. Earth Surf Proc Land 32:874–887. https://doi.org/10.1002/esp.1446
Barnett ZC, Adams SB, Ochs CA et al (2019) Crayfish populations genetically fragmented in streams impounded for 36–104 years. Fresh Bio 65:768–785. https://doi.org/10.1111/fwb.13466
Belkhir K, Borsa P, Chikhi L, et al. (2004) GENETIX 4.05, logiciel sous Windows TM pour la genetique des populations. Montpellier, France: Page Laboratorire Genome, Populations, Interactions, CNRS UMR 5171, Universite de Montpellier II. http://www.Univmontp2.Fr/genetix/genetix/genetix
Berendzen PB, Simons AM, Wood RM (2003) Phylogeography of the northern hogsucker, Hypentelium nigricans (Teleostei: Cypriniorms): genetic evidence for the existence of the ancient Teays River. J Biogeogr 30:1139–1152. https://doi.org/10.1046/j.1365-2699.2003.00888.x
Berendzen PB, Simons AM, Wood RM et al (2008) Recovering cryptic diversity and ancient drainage patterns in eastern North America: historical biogeography of the Notropis rubellus species group (Teleostei: Cypriniorms). Mol Phylogenet Evol 46:721–737. https://doi.org/10.1016/j.ympev.2007.07.008
Blanton RE, Cashner MF, Thomas MR et al (2019) Increased habitat fragmentation leads to isolation among and low genetic diversity within populations of the imperiled Kentucky Arrow Darter (Etheostoma sagitta spilotum). Conserv Genet 20:1009–1022. https://doi.org/10.1007/s10592-019-01188-y
Bloom ET, McCall BL, Schuster GA, Blanton RE (2019) Systematics and description of a new species of Faxonius Ortmann, 1905 (Decapoda: Astacidae: Cambaridae) from the Red River system of Kentucky and Tennessee, USA. J Crustac Biol 39:40–53. https://doi.org/10.1093/jcbiol/ruy100
Bohonak AJ (2002) IBD (Isolation by Distance): a program for analyses of isolation by distance. J Hered 93:153–154. https://doi.org/10.1093/jhered/93.2.15
Bouchard R (1975) Geography and ecology of crayfishes of the Cumberland Plateau and Cumberland Mountains, Kentucky, Virginia, Tennessee, Georgia, and Alabama Part 2, the genera Fallicambarus and Cambarus. Freshw Crayfish 2:585–605. https://doi.org/10.5869/fc.1975.v2.585
Brook BW, Tonkyn DW, O’Grady JJ, Frankham R (2002) Contribution of inbreeding to extinction risk in threatened species. Cons Ecol 6:16
Brown JH, Kodric-Brown A (1977) Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58(2):445–449. https://doi.org/10.2307/1935620
Bucklin A, Wiebe PH (1998) Low mitochondrial diversity and small effective population sizes of the copepods Calanus finmarchicus and Nannocalanus minor: possible impact of climatic variation during recent glaciation. J Her 89(5):383–392. https://doi.org/10.1093/jhered/89.5.383
Buhay JE (2009) “COI-like” sequences are becoming problematic in molecular systematic and DNA barcoding studies. J Crustac Biol 29:96–110. https://doi.org/10.1651/08-3020
Clay M, Brannock PM, Barbour M et al (2020) Strong population structure and differentiation within and among burrowing bog crayfish species of southern Alabama wetlands. Wetl 40:1595–1606. https://doi.org/10.1007/s13157-020-01273-w
Colegrave N, Ruxton GD (2003) Confidence intervals are a more useful complement to nonsignificant tests than are power calculations. Behav Ecol 14:446–447. https://doi.org/10.1093/beheco/14.3.446
Crandall KA, Owen CL, Bracken-Grissom H, Stern D (2015) A synthetic phylogeny of freshwater crayfish: insights for conservation. Phil Trans R Soc B 370:20140009. https://doi.org/10.1098/rstb.2014.0009
Davis DJ, Wieman AC, Berendzen PB (2014) The influence of historical and contemporary landscape variables on the spatial genetic structure of the Rainbow Darter (Etheostoma caeruleum) in tributaries of the upper Mississippi River. Conserv Genet 16:167. https://doi.org/10.1007/s10592-014-0649-1
Di Rienzo A, Peterson AC, Garzat JC et al (1994) Mutation processes of simple sequence repeat loci in human populations. Proc Natl Acad Sci USA 91(3166):3170
Do C, Waples RS, Peel D et al (2014) NeEstimator v2: Re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214. https://doi.org/10.1111/1755-0998.12157
Dudgeon D, Arthington AH, Gessner MO et al (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81(2):163–182. https://doi.org/10.1017/S1464793105006950
Duncan SI, Robertson EP, Fletcher RJ et al (2020) Urbanization and population genetic structure of the Panama City crayfish (Procambarus econfinae). J Hered 111:204–215. https://doi.org/10.1093/jhered/esz072
England LE, Rosemond AD (2004) Small reductions in forest cover weaken terrestrial-aquatic linkages in headwater streams. Fresh Bio 49(6):721–734. https://doi.org/10.1111/j.1365-2427.2004.01219.x
Epps CW, Keyghobadi N (2015) Landscape genetics in a changing world: disentangling historical and contemporary influences and inferring change. Mol Ecol 24:6021–6040. https://doi.org/10.1111/mec.13454
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Fagan WF (2002) Connectivity, fragmentation, and extinction risk in dendritic metapopulations. Ecology 83:3243–3249. https://doi.org/10.1890/0012-9658(2002)083[3243:CFAERI]2.0.CO;2
Fetzner JW Jr, Crandall KA (2003) Linear habitats and the nested clade analysis: an empirical evaluation of geographic versus river distances using an Ozark crayfish (Decapoda: Cambaridae). Evolution 57:2101–2118. https://doi.org/10.1111/j.0014-3820.2003.tb00388.x
Finlay JB, Buhay JE, Crandall KA (2006) Surface to subsurface freshwater connections: phylogeographic and habitat analyses of Cambarus tenebrosus, a facultative cave-dwelling crayfish. Anim Conserv 1:375–387. https://doi.org/10.1111/j.1469-1795.2006.00046.x
Fluker BL, Kuhajda BR, Harris PM (2014) The influence of life-history strategy on genetic differentiation and lineage divergence in darters (Percidae: Etheostomatinae). Evolution 68:3199–3216. https://doi.org/10.1111/evo.12505
Fluker BL, Jones KD, Kuhajda BR (2019) Genetic structure and diversity of the blueface darter Etheostoma cyanoprosopum, a microendemic freshwater fish in the southeastern USA. Endang Species Res 40:133–147. https://doi.org/10.3354/esr00986
Folmer O, Black M, Hoeh W et al (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299. https://doi.org/10.1371/journal.pone.0013102
Frankham R (1995a) Conservation genetics. Annu Rev Genet 29:305–327. https://doi.org/10.1146/annurev.genet.29.1.305
Frankham R (1995b) Effective population size/adult population size ratios in wildlife: a review. Genet Res 89:95–107. https://doi.org/10.1017/S0016672308009695
Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140. https://doi.org/10.1016/j.biocon.2005.05.002
Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: Revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63. https://doi.org/10.1016/j.biocon.2013.12.036
Fraser DJ, Gilliam JF, Yip-Hoi T (1995) Predation as an agent of population fragmentation in a tropical watershed. Ecology 76:1461–1472
Frissell CA, Liss WJ, Warren CE, Hurley MD (1986) A hierarchical framework for stream habitat classification: viewing streams in a watershed context. Environ Manage 10:199–214. https://doi.org/10.1007/BF01867358
Gangloff MM, Perkins M, Blum PW, Walker C (2015) Effects of coal mining, forestry, and road construction on southern Appalachian stream invertebrates and habitats. Environ Manage 55:702–714. https://doi.org/10.1007/s00267-014-0429-1
Glon MG, Thoma RF, Taylor CA et al (2018) Molecular phylogenetic analysis of the devil crayfish group, with elevation of Lacunicambarus Hobbs, 1969 to generic rank and a redescription of the devil crayfish, Lacunicambarus diogenes (Girard, 1852) comb. Nov. (Decapoda: Astacoidea: Cambaridae). J Crustac Bio 38:600–613. https://doi.org/10.1093/jcbiol/ruy057
Glon MG, Thoma RF, Daly M, Freudenstein JV (2019) Lacunicambarus chimera: a new species of burrowing crayfish (Decapoda: Cambaridae) from Illinois, Indiana, Kentucky, and Tennessee. Zootaxa 4544:451–478. https://doi.org/10.11646/zootaxa.4544.4.1
Gouin N, Grandjean F, Souty-Grosset C (2006) Population genetic structure of the endangered crayfish Austropotamobius pallipes in France based on microsatellite variation: biogeographical inferences and conservation implications. Freshw Biol 81:1369–1387. https://doi.org/10.1111/j.1365-2427.2006.01570.x
Gouin N, Souty-Grosset C, Bórquez J et al (2011) Disentangling the impact of demographic factors on population differentiation of an endangered freshwater crayfish (Austropotamobius pallipes) using population density and microsatellite data. Freshw Biol 56:2105–2118. https://doi.org/10.1111/j.1365-2427.2011.02629.x
Haddad NM, Brudvig LA, Clobert J et al (2015) Habitat fragmentation and its impact on Earth’s ecosystems. Sci Adv 1(2):e1500052. https://doi.org/10.1126/sciadv.1500052En
Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174
Helms BS, Figiel CFJ, Rivera J et al (2013) Life-history observations, environmental associations, and soil preferences of the Piedmont Blue Burrower (Cambarus [Depressicambarus] harti) Hobbs. Southeast Nat 12:143–160. https://doi.org/10.1656/058.012.0112
Hoban S, Gaggiott O, Bertorelle G (2013) The number of markers and samples needed for detecting bottlenecks under realistic scenarios, with and without recovery: a simulation-based study. Mol Ecol 22:3444–3450. https://doi.org/10.1111/mec.12258
Hobbs HH Jr (1965) A new crayfish of the genus Cambarus from Tennessee with an emended definition of the genus (Decapoda, Astacidae). Proc Biol Soc Wash 78:265–274
Hollingsworth PR, Near TJ (2009) Temporal patterns of diversification and microendemism in Eastern Highland endemic barcheek darters (Percidae: Etheostomatinae). Evolution 63:228–243. https://doi.org/10.1111/j.1558-5646.2008.00531.x
Hubisz M, Falush D, Stephens M et al (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332. https://doi.org/10.1111/j.1755-0998.2009.02591.x
Hughes JM, Bunn SE, Kingston DM, Hurwood DA (1995) Genetic differentiation and dispersal among populations of Paratya australiensis (Atyidae) in rainforest streams in southeast Queensland, Australia. J North Am Benthol Soc 14:158–173
Hurry CR, Schmidt DJ, Hughes JM (2015) Phylogeography and limited distribution of the endangered freshwater crayfish, Euastacus urospinosus. Aust J Zool 63:236–244. https://doi.org/10.1071/ZO15006
Ingvarsson PK (2001) Restoration of genetic variation lost—the genetic rescue hypothesis. Trends Ecol Evol 16(2):62. https://doi.org/10.1016/S0169-5347(00)02065-6
Janes JK, Miller JM, Dupuis JR et al (2017) The K = 2 conundrum. Mol Ecol 26:3594–3602. https://doi.org/10.1111/mec.14187
Johansen JW (2018) Using multiscale rarity patterns to inform conservation actions in a diverse and understudied taxonomic group. Tennessee Technological University
Johansen JW, Mattingly HT, Padgett MD (2016) Population densities of two rare crayfishes, Cambarus obeyensis and Cambarus pristinus, on the Cumberland Plateau in Tennessee. Southeast Nat 15:275–290. https://doi.org/10.1656/058.015.0208
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555. https://doi.org/10.1111/j.1755-0998.2009.02787.x
Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026. https://doi.org/10.1111/j.1365-294X.2008.03887.x
Jost L, Archer F, Flanagan S et al (2018) Differentiation measures for conservation genetics. Evol Appl 11:1139–1148. https://doi.org/10.1111/eva.12590
Kanno Y, Vokoun JC, Letcher BH (2011) Fine-scale population structure and riverscape genetics of brook trout (Salvelinus fontinalis) distributed continuously along headwater channel networks. Mol Ecol 20:3711–3729. https://doi.org/10.1111/j.1365-294X.2011.05210.x
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Tre Eco Evol 17(5):230–241. https://doi.org/10.1016/S0169-5347(02)02489-8
Kopelman NM, Mayzel J, Jakobsson M et al (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191. https://doi.org/10.1111/1755-0998.12387
Kozak KH, Blaine RA, Larson A (2006) Gene lineages and eastern North American palaeodrainage basins: phylogeography and speciation in salamanders of the Eurycea bislineata species complex. Mol Ecol 15:191–207. https://doi.org/10.1111/j.1365-294X.2005.02757.x
Kumar S, Stecher G, Tamura K et al (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Kunin WE, Gaston KJ (1993) The biology of rarity: patterns, causes and consequences. Trends Ecol Evol 8(8):298–301. https://doi.org/10.1016/0169-5347(93)90259-R
Lamphere BA, Blum MJ (2011) Genetic estimates of population structure and dispersal in a benthic stream fish. Ecol Freshw Fish 21:75–86. https://doi.org/10.1111/j.1600-0633.2011.00525.x
Li Y, Liu J (2018) StructureSelector: a web-based software to select and visualize the optimal number of clusters using multiple methods. Mol Ecol 18:176–177. https://doi.org/10.1111/1755-0998.12719
Li F, Tonkin JD, Haase P (2018) Dispersal capacity and broad-scale landscape structure shape benthic invertebrate communities along stream networks. Limnol 71:68–74. https://doi.org/10.1016/j.limno.2018.06.003
Loughman ZJ, Welsh SA, Fetzner JW Jr, Thoma RF (2015) Conservation of imperiled crayfish, Cambarus veteranus (Decapoda:Reptantia: Cambaridae). J Crustac Biol 35:850–860. https://doi.org/10.1163/1937240X-00002383
Mace GM, Collar NJ, Gaston KJ et al (2008) Quantification of extinction risk: IUCN’s system for classifying threatened species. Con Bio 22(6):1424–1442. https://doi.org/10.1111/j.1523-1739.2008.01044.x
Manangwa O, De Meeûs T, Grébaut P et al (2019) Detecting Wahlund effects together with amplification problems: cryptic species, null alleles and short allele dominance in Glossina pallidipes populations from Tanzania. Mol Ecol Resour 19:757–772. https://doi.org/10.1111/1755-0998.12989
Matocq MD, Villablanca FX (2001) Low genetic diversity in an endangered species: recent or historic pattern? Biol Conserv 1:61–68. https://doi.org/10.1016/S0006-3207(00)00142-7
McGrath DA, Evans JP, Smith CK et al (2004) Mapping land-use change and monitoring the impacts of hardwood-to-pine conversion on the southern Cumberland Plateau in Tennessee. Earth Interact 8:1–24. https://doi.org/10.1175/1087-3562(2004)008%3c0001:mlcamt%3e2.0.co;2
Meirmans PG, Hedrick PW (2011) Assessing population structure: FST and related measures. Mol Ecol Resour 11:5–18. https://doi.org/10.1111/j.1755-0998.2010.02927.x
Micheletti SJ, Storfer A (2017) An approach for identifying cryptic barriers to gene flow that limit species’ geographic ranges. Mol Ecol 26:490–504. https://doi.org/10.1111/mec.13939
Miller AD, Sweeney OF, Whiterod NS et al (2014) Critically low levels of genetic diversity in fragmented populations of the endangered Glenelg Spiny freshwater crayfish Euastacus bispinosus. Endanger Species Res 25:43–55. https://doi.org/10.3354/esr00609
Moore JL (1985) Geologic map and mineral resources summary of the Pleasant Hill Quadrangle. Tennessee Div. Geol.
Muncy L, Price SJ, Bonner SJ, Barton CD (2014) Mountaintop removal mining reduces stream salamander occupancy and richness in southeastern Kentucky (USA). Biol Conserv 180:115–121. https://doi.org/10.1016/j.biocon.2014.09.040
Murias dos Santo AM, Cabezas MP, Tavares AI et al (2016) tcsBU: a tool to extend TCS network layout and visualization. J Bioinform 32:627–628. https://doi.org/10.1093/bioinformatics/btv636
Near TJ, Page LM, Mayden RL (2001) Intraspecific phylogeography of Percina evides (Percidae: Etheostomatinae): an additional test of the Central Highlands pre-Pleistocene vicariance hypothesis. Mol Ecol 10:2235–2240. https://doi.org/10.1046/j.1365-294X.2001.01362.x
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
Nguyen TTT, Austin CM, Meewan MM et al (2004) Phylogeography of the freshwater crayfish Cherax destructor Clark (Parastacidae) in inland Australia: historical fragmentation and recent range expansion. Biol J Linn Soc 83:539–550. https://doi.org/10.1111/j.1095-8312.2004.00410.x
Niemiller ML, Zigler KS (2013) Patterns of cave biodiversity and endemism in the Appalachians and Interior Plateau of Tennessee, USA. PLoS ONE 8:e64177. https://doi.org/10.1371/journal.pone.0064177
Oliveira R, Pedro R, Anastácio M (2015) Factors inducing overland movement of invasive crayfish (Procambarus clarkii) in a ricefield habitat. Hybrobiologia 746:135–146. https://doi.org/10.1007/s10750-014-2052-9
Paz-Vinas I, Loot G, Stevens VM, Blanchet S (2015) Evolutionary processes driving spatial patterns of intraspecific genetic diversity in river ecosystems. Mol Ecol 24:4586–4604. https://doi.org/10.1111/mec.13345
Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539
Petkova D, Novembre J, Stephens M (2016) Visualizing spatial population structure with estimated effective migration surfaces. Nat Genet 25(289–313):1. https://doi.org/10.1016/j.bbi.2017.04.008
Pilger TJ, Gido KB, Propst DL et al (2015) Comparative conservation genetics of protected endemic fishes in an arid land riverscape. Conserv Genet 16(4):875–888. https://doi.org/10.1007/s10592-015-0707-3
Pilger TJ, Gido KB, Propst DL et al (2017) River architecture, genetic effective size and distributional patterns predict differences in genetic structure across species in a dryland fish community. Mol Ecol 26(10):2687–2697. https://doi.org/10.1111/mec.14079
Piry S, Luikart G, Cornuer J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503. https://doi.org/10.1093/jhered/90.4.502
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1093/genetics/155.2.945
Puechmaille SJ (2016) The program STRUCTURE does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Mol Ecol Res 16:608–627. https://doi.org/10.1111/1755-0998.12512
Purvis A, Gittleman JL, Cowlishaw G, Mace GM (2000) Predicting extinction risk in declining species. Proc Roy Soc Bio Sci 267(1456):1947–1952. https://doi.org/10.1098/rspb.2000.1234
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ Accessed August 2019
Rambaut A (2012) FigTree v1.4 http://tree.bio.ed.ac.uk/software/figtree/. Accessed 10 Mar 2018
Rands MRW, Adams WM, Bennun L et al (2010) Biodiversity conservation: challenges beyond 2010. Science 329(5997):1298–1303. https://doi.org/10.1126/science.1189138
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225. https://doi.org/10.2307/2409177
Richardson JS, Danehy RJ (2007) A synthesis of the ecology of headwater streams and their riparian zones in temperate forests. For Sci 53(2):131–147. https://doi.org/10.1093/forestscience/53.2.131
Richman NL, Böhm M, Adams SB et al (2015) Multiple drivers of decline in the global status of freshwater crayfish (Decapoda: Astacidea). Phil Trans R Soc B 370:20140060. https://doi.org/10.1098/rstb.2014.0060
Rohrbach, GM, Withers DI (2006) A status survey of the Caney Fork Crayfish (Cambarus pristinus) and Hardin County Crayfish (Orconectes wrighti) with notes on the Brawley’s Fork Crayfish (Cambarus williami). Tennessee Wildlife Resources Agency, Nashville, TN. pp 81
Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
Sasowsky ID, White WB, Schmidt VA (1995) Determination of stream-incision rate in the Appalachian plateaus by using cave-sediment magnetostratigraphy. Geology 23(5):415–418. https://doi.org/10.1130/0091-7613(1995)023%3c0415:DOSIRI%3e2.3.CO;2
Schmidt BV, Schaefer J (2018) Ecological and landscape effects on genetic distance in an assemblage of headwater fishes. Ecol Freshw Fish 27:617–631. https://doi.org/10.1111/eff.12375
Schorr MS, Backer JC, Schorra MS (2006) Localized effects of coal mine drainage on fish assemblages in a Cumberland Plateau stream in Tennessee. J Freshw Ecol 21:17–24. https://doi.org/10.1080/02705060.2006.9664091
Schorr MS, Dyson MC, Nelson CH et al (2013) Effects of stream acidification on lotic salamander assemblages in a coal-mined watershed in the Cumberland Plateau. J Freshw Ecol 28:339–353. https://doi.org/10.1080/02705060.2013.778219
Schrimpf A, Schulz HK, Theissinger K, Pârvulescu L, Schulz R (2011) The first large-scale genetic analysis of the vulnerable noble crayfish Astacus astacus reveals low haplotype diversity in central European populations. Knowl Managt Aquat Ecosyst 401:35. https://doi.org/10.1051/kmae/2011065
Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Eco Let 9:615–620. https://doi.org/10.1111/j.1461-0248.2006.00889.x
Sexton JP, Hangartner SB, Hoffmann AA (2013) Genetic isolation by environment or distance: which pattern of gene flow is most common? Evolution (NY) 68:1–15. https://doi.org/10.1111/evo.12258
Sinclair EA, Fetzner JW Jr, Buhay JE et al (2004) Proposal to complete a phylogenetic taxonomy and systematic revision for freshwater crayfish (Astacidae). Freshw Crayfish 14:21–29
Song H, Buhay JE, Whiting MF et al (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proc Nat Acad Sci USA 105(36):13486–13491. https://doi.org/10.1073/pnas.0803076105
Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101(42):15261–15264. https://doi.org/10.1073/pnas.0403809101
Sterling KA, Reed DH, Noonan BP, Warren ML Jr (2012) Genetic effects of habitat fragmentation and population isolation on Etheostoma raneyi (Percidae). Conserv Genet 13:859–872. https://doi.org/10.1007/s10592-012-0335-0
Strayer DL (2006) Challenges for freshwater invertebrate conservation. J N A Benth Soc 25(2):271–287. https://doi.org/10.1899/0887-3593(2006)25[271:CFFIC]2.0.CO;2
Strayer DL, Dudgeon D (2010) Freshwater biodiversity conservation: recent progress and future challenges. J N A Benth Soc 29(344):358. https://doi.org/10.1899/08-171.1
Taylor CA, Knouft JH (2006) Historical influences on genital morphology among sympatric species: gonopod evolution and reproductive isolation in the crayfish genus Orconectes (Cambaridae). Bio J Linn Soc 89:1–12. https://doi.org/10.1111/j.1095-8312.2006.00637.x
Taylor CA, Schuster GA, Cooper JE et al (2007) A reassessment of the conservation status of crayfishes of the United States and Canada after 10+ years of increased awareness. Fisheries 32(8):372–389. https://doi.org/10.1577/1548-8446(2007)32[372:AROTCS]2.0.CO;2
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 Gen 132:619–633. https://doi.org/10.1093/genetics/132.2.619
Thoma RF, Fetzner Jr. JW (2008) Taxonomic status of Cambarus (jugicambarus) jezerinaci, Spiny Scale Crayfish (Powell River Crayfish). Report submitted to Virginia Department of Game & Inland Fisheries, Richmond, Virginia. Unpaginated
Thomas JR, Fisher J, Cable J et al (2018) Terrestrial dispersal of invasive signal crayfish during vulnerable life stages. Behav Processes. https://doi.org/10.1016/j.beproc.2018.09.014
Thornbury WD (1965) Regional geomorpholgy of the United States. Wiley, New York
Tonkin JD, Altermatt F, Finn DS et al (2018) The role of dispersal in river network metacommunities: patterns, processes, and pathways. Freshw Biol 63:141–163. https://doi.org/10.1111/fwb.13037
Turner TF, Trexler JC (1998) Ecological and historical associations of gene flow in darters. Evol 52(6):1781–17801. https://doi.org/10.1111/j.1558-5646.1998.tb02256.x
Turner TF, Trexler JC, Kuhn DN et al (1996) Life history variation and comparative phylogeograpahy of daters (Pices: Percidae) from the North American central highlands. Evol 50:2023–2036. https://doi.org/10.1111/j.1558-5646.1996.tb03589.x
Vähä JP, Erkinaro J, Niemelä E et al (2007) Life-history and habitat features influence the within-river genetic structure of Atlantic salmon. Mol Ecol 16:2638–2654. https://doi.org/10.1111/j.1365-294X.2007.03329.x
van Oosterhout C, Hutchinson WF, Wills DPM et al (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
van Strien MJ, Holderegger R, Van Heck HJ (2015) Isolation-by-distance in landscapes: considerations for landscape geneticists. Heredity 114:27–37
Vannote RL, Minshall GW, Cummins KW et al (1980) The river continuum concept. Can J Fish Aqua Sci 37(1):130–137. https://doi.org/10.1139/f80-017
Vrijenhoek RC (1998) Conservation genetics of freshwater fish. Fish Bio 53(SA):394–412. https://doi.org/10.1111/j.1095-8649.1998.tb01039.x
Wang J (2018) Effects of sampling close relatives on some elementary population genetics analyses. Mol Ecol Resour 18:41–54. https://doi.org/10.1111/1755-0998.12708
Wang J, Santiago E, Caballero A (2016) Prediction and estimation of effective population size. Heredity (edinb) 117:193–206. https://doi.org/10.1038/hdy.2016.43
Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184. https://doi.org/10.1007/s10592-005-9100-
Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262. https://doi.org/10.1111/j.1752-4571.2009.00104.x
Ward RD, Woodwark M, Skibinski OF (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J Fish Biol 44:213–232. https://doi.org/10.1111/j.1095-8649.1994.tb01200.x
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Williams CE, Bivens RD, Carter BD (2009) Key to the crayfishes of Tennessee, abstracted from H. H. Hobbs Jr. 1972, H. H. Hobbs Jr. 1981, and Bouchard 1978 and an annotated list of the crayfishes of Tennessee. Tennessee Wildlife Resources Agency, Nashville, TN. pp 78
Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562. https://doi.org/10.1007/s10592-005-9009-5
Withers DI, McCoy RA (2005) Distributional surveys for Cambarus pristinus and Cambarus williami, two endangered crayfish in Tennessee final report contract # ID-05-0828-00 Tennessee Division of Natural Heritage Nashville, Tennessee. pp 57
Wright S (1943) Isolation by distance. Genetics 28:114–138
Wright LL, Tregenza T, Hosken DJ (2008) Inbreeding, inbreeding depression and extinction. Conserv Genet 9:83. https://doi.org/10.1007/s10592-007-9405-0
Zachariah Peery M, Kirby R, Reid BN et al (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418. https://doi.org/10.1111/j.1365-294X.2012.05635.x
Zellmer AJ, Knowles LL (2009) Disentangling the effects of historic vs. contemporary landscape structure on population genetic divergence. Mol Ecol 18:3593–3602. https://doi.org/10.1111/j.1365-294X.2009.04305.x
Acknowledgements
We thank multiple people for aiding in field work and lab protocols: Nastasia Disotell, Jacob Brumley, Ben Wilson, Brooke Washburn, Josh Stonecipher, Allison Kirby, Bailey Harris, Clair Ciafre, Mollie Cashner, Lyranda Thiem, Thomas Murphy, Sandra Bojic, Beau Rapier, Libnis Sanches, Tammy St. James, Chelsea Blumbergs, Mariah Schlis-Elias, Caroline Wilford, Chris Skelton, Carl Williams, and Jeff Simmons. We also thank Matt Brown for aiding us in accessing sample sites within Fall Creek Falls State Park. We collected all tissues under a Tennessee Wildlife Resource Agency scientific collection permit #169 and State of Tennessee Department of Environment and Conservation scientific research and collection permit #2017-040. Funding was provided by the Tennessee Wildlife Resource Agency and Austin Peay’s Center of Excellence for Field Biology.
Funding
This work was supported by the Tennessee Wildlife Resource Agency Grant #3208-00834 (Contract #56872).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study concept and design. Material preparation and data collection were performed by BG, JWJ, and REB. Analyses were performed by BG. Funding was sought by REB and JWJ. The first draft of the manuscript was written by BG and all authors provided comments and approval for the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Grubb, B., Johansen, J.W. & Blanton, R.E. Phylogeography and population genetics of a headwater-stream adapted crayfish, Cambarus pristinus (Decapoda: Cambaridae), from the Cumberland Plateau in Tennessee. Conserv Genet 23, 1115–1132 (2022). https://doi.org/10.1007/s10592-022-01477-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-022-01477-z