Conservation Genetics

, Volume 19, Issue 1, pp 57–69 | Cite as

Introgressive hybridization and species turnover in reservoirs: a case study involving endemic and invasive basses (Centrarchidae: Micropterus) in southeastern North America

  • Max R. BangsEmail author
  • Kenneth J. Oswald
  • Thomas W. Greig
  • Jean K. Leitner
  • Daniel M. Rankin
  • Joseph M. Quattro
Research Article


Invasive species threaten native taxa with extirpation and extinction via several biological mechanisms. One such mechanism, hybridization and subsequent introgression of invasive alleles into native genomes is a serious concern, especially for taxa displaying weak reproductive barriers, as is the case for black basses. Black basses introduced outside of their native ranges thus pose elevated threats to endemic congeners, particularly in the southern United States where restricted ranges preclude refuge from introgression. The recently delineated Bartram’s bass (M. sp. cf M. coosae) is endemic to the upper regions of the Savannah River basin, throughout which anthropogenic modification, including impoundment, has been extensive. Non-native Alabama bass (M. henshalli) and smallmouth bass (M. dolomieu) have been introduced into this system on multiple occasions and now threaten Bartram’s bass via introgression. In this study we sampled four reservoirs (Jocassee, Keowee, Hartwell, and Russell) in the upper Savannah River during 2004 and 2010. Results from three codominant nuclear loci and one mitochondrial locus revealed extensive introgression between Alabama and Bartram’s bass. Results show that Alabama bass have replaced Bartram’s bass in lakes Keowee and Russell, where they were first introduced, while the frequencies of hybrids in lakes Jocassee and Hartwell are increasing. Hybridization involving Bartram’s bass with native largemouth bass and introduced smallmouth bass was detected in very low frequencies. Results highlight the importance of continual study over geographic and temporal scales to inform management and conservation of rare fishes threatened with extinction via interspecific hybridization.


Hybridization Introgression Micropterus Savannah River Invasive species 



The authors acknowledge Vic Blackwell, Mike Wilson, Terry Bryant, Amy Breedlove, Treye Byars, Drew Robb and Weston Houck of South Carolina Department of Natural Resources for their assistance in fish collections, and Dr. Michael Douglas of the University of Arkansas for his editorial input.


The scientific results and conclusions, as well as any opinions expressed herein, are those of the author(s) and do not necessarily reflect the views of NOAA or the Department of Commerce. The mention of any commercial product is not meant as an endorsement by the Agency or Department.

Supplementary material

10592_2017_1018_MOESM1_ESM.docx (33 kb)
Supplementary Table (DOCX 33 KB)
10592_2017_1018_MOESM2_ESM.pptx (70 kb)
Supplementary Fig. 1 Map of sample sites used in the reference database. (PPTX 70 KB)


  1. Avise J (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
  2. Avise J, Pearce P, Van Den Avyle M, Smith M, Nelson W, Asmussen M (1997) Cytonuclear introgressive swamping and species turnover of bass following an introduction. J Heredity 84:14–20CrossRefGoogle Scholar
  3. Baker WH, Blanton RE, Johnston CE (2013) Diversity within the Redeye Bass, Micropterus coosae (Perciformes: Centrarchidae) species group, with descriptions of four new species. Zootaxa 3635:379–401CrossRefPubMedGoogle Scholar
  4. Bangs M (2011) Decline of the Savannah River Redeye Bass (Micropterus coosae) due to introgressive hybridization with invasive Alabama Spotted Bass (Micropterus punctulatus henshalli) Master’s Thesis, University of South Carolina Press, Columbia, SCGoogle Scholar
  5. Bangs MR, Quattro JM, Oswald KJ, Leitner J (2008) Creating a molecular database for identifying two subspecies of largemouth bass (Micropterus salmoides). MarSci 1:1–5Google Scholar
  6. Barwick D, Moore P (1983) Abundance and growth of redeye bass in two South Carolina reservoirs. Trans Am Fish Soc 112:216–219CrossRefGoogle Scholar
  7. Barwick HK, Oswald K, Quattro J, Barwick R (2006) Redeye bass (Micropterus coosae) and Alabama spotted bass (M. punctulatus henshalli) hybridization in Keowee reservoir. Southeast Nat 5:661–668CrossRefGoogle Scholar
  8. Bean PT, Lutz-Carrillo DJ, Bonner TH (2013) Rangewide survey of the introgressive status of Guadalupe bass: implications for conservation and management. Trans Am Fish Soc 142:681–689CrossRefGoogle Scholar
  9. Boecklen WJ, Howard DJ (1997) Genetic analysis of hybrid zones: number of markers and power of resolution. Ecology 78:2611–2616CrossRefGoogle Scholar
  10. Bolnick DI, Near TJ (2005) Tempo of post-zygotic reproductive isolation in sunfishes (Teleostei: Centrarchidae). Evol Int J Org Evol 59:1754–1767CrossRefGoogle Scholar
  11. Breden F, Ptacek MB, Rahed M, Taphorn D, Fiqueiredo CA (1999) Molecular phylogeny of the live-bearing fish genus Poecilia (Cyprinodontiformes: Poeciliidae). Mol Phylogenet Evol 12:95–104CrossRefPubMedGoogle Scholar
  12. Campton DE (1987) Natural hybridization and introgression in fishes: methods of detection and genetic interpretations. In: Ryman N, Utter F (eds) Population genetics and fishery management. University of Washington Press, Seattle, pp 161–192Google Scholar
  13. Clement M, Posada DCKA, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefPubMedGoogle Scholar
  14. Coleman RR, Gaither MR, Kimokeo B, Stanton FG, Bowen BW, Toonen RJ (2014) Large-scale introduction of the Indo-Pacific damselfish Abudefduf vaigiensis into Hawai’i promotes genetic swamping of the endemic congener A. abdominalis. Mol Ecol 23:5552–5565CrossRefPubMedGoogle Scholar
  15. Crossman EJ, Cudmore BC (2000) Summary of fishes intentionally introduced in North America. In: Claudi R, Leach JH (eds) Nonindigenous freshwater organisms: vectors, biology, and impacts. CRC Press, Boca Raton, pp 99–111Google Scholar
  16. Dextrase AJ, Coscarelli MA (2000) Intentional introductions of nonindigenous freshwater organisms in North America. In: Claudi R, Leach JH (eds) Nonindigenous freshwater organisms: vectors, biology, and impacts. CRC Press, Boca Raton, pp 61–98Google Scholar
  17. Douglas MR, Douglas ME (2010) Molecular approaches to stream fish ecology. Am Fish Soc Symp 73:157–195Google Scholar
  18. Echelle AA, Connor PJ (1989) Rapid, geographically extensive genetic introgression after secondary contact between two pupfish species (Cyprinodon, Cyprinodontidae). Evol Int J Org Evol 43:717–727CrossRefGoogle Scholar
  19. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  20. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50CrossRefGoogle Scholar
  21. Fitzpatrick BM, Johnson JR, Kump DK, Smith JJ, Voss SR, Shaffer HB (2010) Rapid spread of invasive genes into a threatened native species. Proc Natl Acad Sci USA 107:3606–3610CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fitzpatrick BM, Fordyce JA, Niemiller ML, Reynolds RG (2012) What can DNA tell us about biological invasions? Biol Invasions 14:245–253CrossRefGoogle Scholar
  23. Fleming BP, Garrett GP, Smith NG (2015) Reducing hybridization and introgression in wild populations of Guadalupe bass through supplemental stocking. In: Tringali MD, Long JM, Birdsong TW, Allen MS (eds) Black bass diversity: multidisciplinary science for conservation. American Fisheries Society, Symposium 82, Bethesda, Maryland, pp 537–547Google Scholar
  24. Freeman BJ, Taylor A, Oswald KJ, Wares J, Freeman MC, Quattro J, Leitner J (2015) Shoal basses, a clade of cryptic identity. In: Tringali MD, Long JM, Birdsong TW, Allen MS (eds) Black bass diversity: multidisciplinary science for conservation. American Fisheries Society, Symposium 82, Bethesda, Maryland, pp 449–466Google Scholar
  25. Fuller P, Nico L, Williams J (1999) Nonindigenous fishes introduced into inland waters of the United States. American Fisheries Society, Special Publication 27, BethesdaGoogle Scholar
  26. Godbout JD, Aday DD, Rice JA, Bangs MR, Quattro JM (2009) Morphological models for identifying largemouth bass, spotted Bass, and largemouth bass × spotted bass hybrids. N Am J Fish Manag 29:1425–1437CrossRefGoogle Scholar
  27. Gompert Z, Buerkle CA (2010) INTROGRESS: a software package for mapping components of isolation in hybrids. Mol Ecol Resour 10:378–384CrossRefPubMedGoogle Scholar
  28. Hasselman DJ, Argo EE, McBride MC, Bentzen P, Schultz TF, Perez-Umphrey AA, Palkovacs EP (2014) Human disturbance causes the formation of a hybrid swarm between two naturally sympatric fish species. Mol Ecol 23:1137–1152CrossRefPubMedGoogle Scholar
  29. Hohenlohe PA, Day MD, Amish SJ, Miller MR, Kamps-Hughes N, Boyer MC, Muhlfeld CC, Allendorf FW, Johnson EA, Luikart G (2013) Genomic patterns of introgression in rainbow and westslope cutthroat trout illuminated by overlapping paired-end RAD sequencing. Mol Ecol 22:3002–3013CrossRefPubMedPubMedCentralGoogle Scholar
  30. Holden PB, Stalnaker CB (1975) Distribution and abundance of mainstream fishes of the middle and upper Colorado River basins, 1967–1973. Trans Am Fish Soc 104:217–231CrossRefGoogle Scholar
  31. Hubbs CL (1955) Hybridization between fish species in nature. Syst Zool 4:1–20CrossRefGoogle Scholar
  32. Hubbs CL, Lagler KF (2004) Fishes of the Great Lakes Region, revised edition. University of Michigan Press, Ann ArborCrossRefGoogle Scholar
  33. Jackson DA (2002) Ecological effects of Micropterus introduction: the dark side of black bass. In: Philipp DP, Ridgway MS (eds) Black bass diversity: ecology, conservation, and management. American Fisheries Society, Symposium 31, Bethesda, pp 221–232Google Scholar
  34. Koppelman J, Garrett G (2002) Distribution, biology and conservation of the rare black bass species. In: Philipp DP, Ridgway MS (eds) Black bass diversity: ecology, conservation, and management. American Fisheries Society, Symposium 31, Bethesda, Maryland, pp 333–342Google Scholar
  35. Lamer JT, Dolan CR, Petersen JL, Chick JH, Epifanio JM (2010) Introgressive hybridization between bighead carp and silver carp in the Mississippi and Illinois rivers. N Am J Fish Manag 30:1452–1461CrossRefGoogle Scholar
  36. Leary RF, Allendorf FW, Phelps RS, Knudsen KL (1984) Introgression between west-slope cutthroat and rainbow trout in Clark Fork River drainage, Montana. Proc Montana Acad Sci 43:1–18Google Scholar
  37. Leitner J, Oswald KJ, Bangs M, Rankin D, Quattro J (2015) A consideration of the conservation impacts of hybridization between native Bartram’s bass Micropterus sp. cf. M. coosae and two introduced species in the Savannah basin. In: Tringali MD, Long JM, Birdsong TW, Allen MS (eds) Black bass diversity: multidisciplinary science for conservation. American Fisheries Society, Symposium 82, Bethesda, Maryland, pp 481–490Google Scholar
  38. Littrell BM, Lutz-Carrillo DJ, Bonner TH, Fries LT (2007) Status of an introgressed Guadalupe bass population in a central Texas stream. N Am J Fish Manag 27:785–791CrossRefGoogle Scholar
  39. Marcy BC, Fletcher DE, Martin FD, Paller MH, Reichert MJM (2005) Fishes of the Middle Savannah River Basin with emphasis on the Savannah River site. University of Georgia Press, AthensGoogle Scholar
  40. McDowell JR, Graves JE (2002) Nuclear and mitochondrial DNA markers for specific identification of Istiophorid and Xiphiid billfishes. Fish Bull 100:537–544Google Scholar
  41. Meilink WR, Arntzen JW, van Delft JJ, Wielstra B (2015) Genetic pollution of a threatened native crested newt species through hybridization with an invasive congener in the Netherlands. Biol Conserv 184:145–153CrossRefGoogle Scholar
  42. Meyerson LA, Viola DV, Brown RN (2010) Hybridization of invasive Phragmites australis with a native subspecies in North America. Biol Invasions 12:103–111CrossRefGoogle Scholar
  43. Morizot D, Calhoun S, Clepper L, Schmidt M, Williamson J, Carmichael G (1991) Multispecies hybridization among native and introduced Centrarchid basses in central Texas. Trans Am Fish Soc 120:283–289CrossRefGoogle Scholar
  44. Near TJ, Bolnick DI, Wainwright PC (2005) Fossil calibrations and molecular divergence time estimates in Centrarchid fishes (Teleostei: Centrarchidae). Evol Int J Org Evol 59:1768–1782CrossRefGoogle Scholar
  45. O’Leary SJ, Hice LA, Feldheim KA, Frisk MG, McElroy AE, Fast MD, Chapman DD (2013) Severe inbreeding and small effective numbers of breeders in a formerly abundant marine fish. PLoS ONE 8:e66126CrossRefPubMedPubMedCentralGoogle Scholar
  46. Olden JD, Poff NL (2004) Ecological processes driving biotic homogenization: testing a mechanistic model using fish faunas. Ecology 85:1867–1875CrossRefGoogle Scholar
  47. Oswald KJ (2007) Phylogeography and contemporary history of redeye bass (Micropterus coosae). Ph.D. Dissertation, University of South Carolina Press, Columbia, SCGoogle Scholar
  48. Oswald KJ, Leitner J, Rankin D, Barwick DH, Freeman B, Greig T, Bangs M, Quattro J (2015) Evolutionary genetic diversification, demography, and conservation of Bartram’s bass. In: Tringali MD, Long JM, Birdsong TW, Allen MS (eds) Black bass diversity: multidisciplinary science for conservation. American Fisheries Society, Symposium 82, Bethesda, Maryland, pp 601–614Google Scholar
  49. Page LM, Burr BM (1991) A field guide to freshwater fishes of North America north of Mexico. Houghton Mifflin Company, BostonGoogle Scholar
  50. Perry WL, Lodge DM, Feder JL (2002) Importance of hybridization between indigenous and nonindigenous freshwater species: an overlooked threat to North American biodiversity. Syst Biol 51:255–275CrossRefPubMedGoogle Scholar
  51. Pierce PC, Van Den Avyle MJ (1997) Hybridization between introduced spotted bass and smallmouth bass in reservoirs. Trans Am Fish Soc 126:939–947CrossRefGoogle Scholar
  52. Pipas J, Bulow F (1998) Hybridization between redeye bass and smallmouth bass in Tennessee streams. Trans Am Fish Soc 127:141–146CrossRefGoogle Scholar
  53. Presa P, Pardo B, Martinez P, Bernatchez L (2002) Phylogeographic congruence between mtDNA and rDNA ITS markers in brown trout. Mol Biol Evol 19:2161–2175CrossRefPubMedGoogle Scholar
  54. Quattro JM, Avise JC, Vrijenhoek RC (1991) Molecular evidence for multiple origins of hybridogenetic fish clones (Poeciliidae: Poeciliopsis). Genetics 127:391–398PubMedPubMedCentralGoogle Scholar
  55. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 10 April 2014
  56. Rabern A (2014) Lake Tugaloo Annual Report. Georgia Department of Natural Resources, Wildlife Resources DivisionGoogle Scholar
  57. Rahel FJ (2000) Homogenization of fish faunas across the United States. Science 288:854–856CrossRefPubMedGoogle Scholar
  58. Rahel FJ (2002) Homogenization of freshwater faunas. Annu Rev Ecol Syst 33:291–315CrossRefGoogle Scholar
  59. Rahel FJ (2010) Homogenization, differentiation, and the widespread alteration of fish faunas. In: Gido K, Jackson D (eds) Community ecology of stream fishes: concepts, approaches, and techniques. American Fisheries Society, Symposium 73, Bethesda, Maryland, pp 311–326Google Scholar
  60. Randi E (2008) Detecting hybridization between wild species and their domesticated relatives. Mol Ecol 17:285–293CrossRefPubMedGoogle Scholar
  61. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249CrossRefGoogle Scholar
  62. Rhymer J, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109CrossRefGoogle Scholar
  63. Rodriguez MS (2013) The pelagic forage fish community of Lake Jocassee, South Carolina relationships to operations at Jocassee and Bad Creek pumped storage stations. Keowee-Toxaway Hydroelectric Project Fish Community Assessment Study. FERC No. 2503, Chapter 2, pp 37–229Google Scholar
  64. Rohde FC, Arndt RG, Foltz JW, Quattro JM (2009) Freshwater fishes of South Carolina. University of South Carolina Press, ColumbiaGoogle Scholar
  65. Ross ST (1991) Mechanisms structuring stream fish assemblies: are there lessons from introduced species? Environ Biol Fishes 30:359–368CrossRefGoogle Scholar
  66. Ryan ME, Johnson JR, Fitzpatrick BM (2009) Invasive hybrid tiger salamander genotypes impact native amphibians. Proc Natl Acad Sci USA 106:11166–11171CrossRefPubMedPubMedCentralGoogle Scholar
  67. Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774CrossRefPubMedGoogle Scholar
  68. Scott MC, Helfman GS (2001) Native invasions, homogenization, and the mismeasure of integrity of fish assemblages. Fisheries 26:6–15CrossRefGoogle Scholar
  69. Scribner KT, Page KS, Bartron ML (2001) Hybridization in freshwater fishes: a review of case studies and cytonuclear methods of biological inference. Rev Fish Biol Fish 10:293–323CrossRefGoogle Scholar
  70. Seehausen O, Van Alphen JJ, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808–1811CrossRefGoogle Scholar
  71. Siepker MJ, Ostrand KG, Cooke SJ, Philipp DP, Wahl DH (2007) A review of the effects of catch-and-release angling on black bass, Micropterus spp.: implications for conservation and management of populations. Fish Manag Ecol 14:91–101CrossRefGoogle Scholar
  72. Southcott L, Nagel L, Hatfield T, Schluter D (2013) Weak habitat isolation in a threespine stickleback (Gasterosteus spp.) species pair. Biol J Linn Soc 110:466–476CrossRefGoogle Scholar
  73. Stamatakis A (2006) RAXML-VI-HPC: maximum likelihood-based phylo-genetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690CrossRefPubMedGoogle Scholar
  74. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989CrossRefPubMedPubMedCentralGoogle Scholar
  75. Tringali MD, Barthel BL, Seyoum S, Knight JR (2015) The Choctaw Bass: an undescribed species of Micropterus in the Gulf Coastal Plain rivers of Florida. In: Tringali MD, Long JM, Birdsong TW, Allen MS (eds) Black bass diversity: multidisciplinary science for conservation. American Fisheries Society, Symposium 82, Bethesda, Maryland, pp 421–448Google Scholar
  76. Webb JF, Reeves WC (1975) Age and growth of Alabama spotted bass and northern largemouth bass. In: Clepper H (ed) Black bass biology and management. Sport Fishing Institute, Washington, DC, pp 204–215Google Scholar
  77. Whitmore D, Hellier T (1988) Natural hybridization between largemouth and smallmouth bass (Micropterus). Copeia 1988:493–496CrossRefGoogle Scholar
  78. Wood R, Macomber RH, Franz RK (1956) Trends in fishing pressure and catch, Allatoona Reservoir, Georgia, 1950–1953. J Tennessee Acad Sci 31:215–223Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Max R. Bangs
    • 1
    • 6
    • 7
    Email author
  • Kenneth J. Oswald
    • 2
  • Thomas W. Greig
    • 3
  • Jean K. Leitner
    • 4
  • Daniel M. Rankin
    • 5
  • Joseph M. Quattro
    • 1
  1. 1.Department of Biological Sciences, Marine Science ProgramUniversity of South CarolinaColumbiaUSA
  2. 2.Department of Biological and Allied Health SciencesOhio Northern UniversityAdaUSA
  3. 3.Center for Coastal Environmental Health and Biomolecular Research at CharlestonCharlestonUSA
  4. 4.South Carolina Department of Natural ResourcesFreshwater Fisheries ResearchEastoverUSA
  5. 5.South Carolina Department of Natural ResourcesFreshwater Fisheries Region OnePendletonUSA
  6. 6.School of Fisheries, Aquaculture and Aquatic SciencesAuburn UniversityAuburnUSA
  7. 7.Department of Biological SciencesUniversity of ArkansasFayettevilleUSA

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