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Genetic swamping and possible species collapse: tracking introgression between the native Candy Darter and introduced Variegate Darter

  • Isaac Gibson
  • Amy B. Welsh
  • Stuart A. Welsh
  • Daniel A. Cincotta
Research Article

Abstract

Candy Darters (Etheostoma osburni) and Variegate Darters (E. variatum) are both native to West Virginia and Virginia. The geographic ranges of these two species were historically separated by Kanawha Falls, a natural barrier to fish dispersal located at Glen Ferris, WV. In the early 1980s, Variegate Darters or putative hybrids (E. osburni × E. variatum) were first collected at locations upstream of Kanawha Falls, and have since undergone range expansion. Hybridization with the Variegate Darter was one of the threats that led to the Candy Darter being listed as Endangered under the U.S. Endangered Species Act in 2018. Genetic and morphologic data were examined for individuals from the New, Gauley, and Greenbrier river drainages. Individuals were genotyped using a suite of 5 diagnostic microsatellite loci to investigate potential hybridization. Widespread hybridization was found throughout populations of Candy Darters, with the geographic range of hybridization expanding from 2004 to 2014. A hybrid zone was observed, with the highest levels of Variegate Darter introgression representing the kernel within this zone and the locations of first-generation (F1) hybrids at the periphery. F1 hybrids were morphologically intermediate within and across characters for parental species. Introgressive hybridization threatens the genetic integrity of the Candy Darter, and may lead to population extirpation or extinction.

Keywords

Hybridization Genetic swamping Introgression Etheostoma osburni variatum 

Notes

Acknowledgements

This manuscript is dedicated to the memory of Isaac Gibson. The legacy of Isaac’s dedication and tireless commitment to the conservation of this special species will endure. The late Tim King deserves special recognition for his participation and guidance in the early stages of this research as well as his contributions to the field of conservation genetics; John Switzer for the collection of preliminary data; Angie Burns, Lara Hedrick, Jim Hedrick, Heather Hildebrand, Tim Hodge, Dustin Kimble, David Okernick, Nathaniel Owens, Ken Sheehan, David Thorne, and David Wellman for assistance with specimen collection; and Barbara Douglas for review of the manuscript. Funding for this research was provided by West Virginia Division of Natural Resources, State Wildlife Grant, the National Institute of Food and Agriculture, U.S. Department of Agriculture, Hatch Project WVA00690, and the West Virginia Agricultural and Forestry Experiment Station. This study was performed under the auspices of West Virginia University IACUC protocol 01-0510. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

References

  1. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:11:613–622CrossRefGoogle Scholar
  2. Almodóvar A, Nicola GG, Leal S, Torralva M, Elvira B (2012) Natural hybridization with invasive bleak Alburnus alburnus threatens the survival of Iberian endemic calandino Squalius alburnoides complex and southern Iberian chub Squalius pyrenaicus. Biol Invasions 14.11:2237–2242CrossRefGoogle Scholar
  3. Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229PubMedPubMedCentralGoogle Scholar
  4. Bangs MR, Oswald KJ, Greig TW, Leitner JK, Rankin DM, Quattro JM (2018) Introgressive hybridization and species turnover in reservoirs: a case study involving endemic and invasive basses (Centrarchidae: Micropterus) in southeastern North America. Cons Gen 19:57–69CrossRefGoogle Scholar
  5. Burns AD (2007) Comparison of two electrofishing gears (backpack and parallel wires) and abundances of fishes of the upper Greenbrier River drainage. MS Thesis, West Virginia University, Morgantown, WVGoogle Scholar
  6. Cincotta DA, Chambers DB, Messinger T (1999) Recent changes in the distribution of fish species in the New River basin in West Virginia and Virginia. In: Proceedings of the new river symposium, Apr 15–16, Boone North Carolina, US National Park Service, Glen Jean, WV, pp 98–106Google Scholar
  7. Eschenroeder JC, Roberts JH (2018) What role has hybridization played in the replacement of native Roanoke bass with invasive Rock bass? T Am Fish Soc 147:497–513CrossRefGoogle Scholar
  8. Fitzpatrick BM, Johnson JR, Kump DK, Shaffer HB, Smith JJ, Voss SR (2009) Rapid fixation of non-native alleles revealed by genome-wide SNP analysis of hybrid tiger salamanders. BMC Evol Biol 9:1:176CrossRefPubMedPubMedCentralGoogle Scholar
  9. Frankham R, Ballou JD, Ralls K, Eldridge MDB, Dudash MR, Fenster CB, Lacy RC, Sunnucks P (2017) Genetic management of fragmented animal and plant populations. Oxford University Press, New YorkCrossRefGoogle Scholar
  10. Halas D, Simons AM (2014) Cryptic speciation reversal in the Etheostoma zonale (Teleostei: Percidae) species group, with an examination of the effect of recombination and introgression on species tree inference. Mol Phylogenet Evol 70:13–28CrossRefPubMedGoogle Scholar
  11. Hitt NP, Frissell CA, Muhlfeld CC, Allendorf FW (2003) Spread of hybridization between native westslope cutthroat trout, Oncorhynchus clarki lewisi, and nonnative rainbow trout, Oncorhynchus mykiss. Can J Fish Aquat Sci 60:12:1440–1451CrossRefGoogle Scholar
  12. Hocutt CH, Wiley EO (1986) The zoogeography of North American freshwater fishes. Wiley, HobokenGoogle Scholar
  13. Hubbs CL, Black JD (1940) Percid fishes related to Poecilichthys variatus, with descriptions of three new forms. Occas Pap Mus of Zool Univ Mich, Number 416Google Scholar
  14. Hubbs CL, Trautman MB (1932) Poecilichthys osburni, a new darter from the upper Kanawha River system in Virginia and West Virginia. Ohio J Sci 32:1:31–38Google Scholar
  15. Jelks HL, Walsh SJ, Burkhead NM, Contreras-Balderas S, Diaz-Pardo E, Hendrickson DA, Lyons J, Mandrak NE, McCormick F, Nelson JS, Platania SP, Porter BA, Renaud CB, Schmitter-Soto JJ, Taylor EB, Warren ML Jr (2008) Conservation status of imperiled North American freshwater and diadromous fishes. Fisheries 33:8:372–407CrossRefGoogle Scholar
  16. Jenkins RE, Burkhead NM (1994) Freshwater fishes of Virginia. Am Fish Soc, BethesdaGoogle Scholar
  17. Kirtland JP (1840) Descriptions of four new species of fishes. Boston J Nat Hist 3:273–277Google Scholar
  18. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:4:199–204CrossRefGoogle Scholar
  19. Lawson LP, Fessl B, Vargas FH, Farrington HL, Cunninghame HF, Mueller JC, Nemeth E, Sevilla PC, Petren K (2017) Slow motion extinction: inbreeding, introgression, and loss in the critically endangered mangrove finch (Camarhynchus heliobates). Cons Gen 18:159–170CrossRefGoogle Scholar
  20. Manaster CJ (2009) ALLELOGRAM v2.2: a program for normalizing and binning microsatellite genotypes. http://code.google.com/p/allelogram/
  21. Matthews WJ, Turner TF, Osborne MJ (2016) Breakdown of a hybrid swarm between two darters (Percidae), Etheostoma radiosum and Etheostoma spectabile, with loss of one parental species. Copeia 104:873–878CrossRefGoogle Scholar
  22. Morizot DC, Calhoun SW, Clepper LL, Schmidt ME (1991) Multispecies hybridization among native and introduced centrarchid basses in central Texas. T Am Fish Soc 120.3:283–289CrossRefGoogle Scholar
  23. Muhlfeld CC, Kalinowski ST, McMahon TE, Taper ML, Painter S, Leary RF, Allendorf FW (2009) Hybridization rapidly reduces fitness of a native trout in the wild. Biol Lett 5:328–331CrossRefPubMedPubMedCentralGoogle Scholar
  24. Page LM (1983) Handbook of darters. TFH Publications, Neptune CityGoogle Scholar
  25. Page LM, Burr BM (2011) Peterson field guide to freshwater fishes of North America North of Mexico. Houghton Mifflin Harcourt, BostonGoogle Scholar
  26. Peters JL, Sonsthagen SA, Lavretsky P, Rezsutek M, Johnson WP, McCracken KG (2014) Interspecific hybridization contributes to high genetic diversity and apparent effective population size in an endemic population of mottled ducks (Anas fulvigula maculosa). Cons Gen 15:509–520CrossRefGoogle Scholar
  27. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  28. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  29. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109CrossRefGoogle Scholar
  30. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefPubMedGoogle Scholar
  31. Roberts DG, Gray CA, West RJ, Ayre DJ (2010) Marine genetic swamping: hybrids replace an obligately estuarine fish. Mol Ecol 19:508–520CrossRefPubMedGoogle Scholar
  32. Seehausen O, Van Alphen JJ, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:5333:1808–1811CrossRefGoogle Scholar
  33. Stauffer JR, Boltz JM, White LR (1995) Fishes of West Virginia. Proc Acad Natl Sci Phila, PhiladelphiaGoogle Scholar
  34. Switzer JF (2004) Molecular systematics and phylogeography of the Etheostoma variatum species group (Actinopterygii: Percidae). PhD dissertation, Saint Louis University, St Louis, MOGoogle Scholar
  35. Switzer JF, Welsh SA, King TL (2008) Microsatellite DNA primers for the candy darter, Etheostoma osburni and variegate darter, Etheostoma variatum, and cross-species amplification in other darters (Percidae). Mol Ecol Resour 8.2:335–338CrossRefGoogle Scholar
  36. Taylor EB, Boughman JW, Groenenboom M, Sniatynski M, Schluter D, Gow JL (2006) Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol Ecol 15.2:343–355Google Scholar
  37. Todesco M, Pascual MA, Owens GL, Ostevik KL, Moyers BT, Hubner S, Heredia SM, Hahn MA, Caseys C, Bock DG, Rieseberg LH (2016) Hybridization and extinction. Evol App 9:892–908CrossRefGoogle Scholar
  38. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2003) Micro-Checker, version 2.2.3. Department of Biological Sciences and Department of Computer Science, University of Hull, HullGoogle Scholar
  39. Vilà C, Walker C, Sundqvist AK, Flagstad Ø, Andersone Z, Casulli A, Kojola I, Valdmann H, Halverson J, Ellegren H (2003) Combined use of maternal, paternal and bi-parental genetic markers for the identification of wolf–dog hybrids. Heredity 90 1:17–24CrossRefGoogle Scholar
  40. Walters DM, Blum MJ, Rashleigh B, Freeman BJ, Porter BA, Burkhead NM (2008) Red shiner invasion and hybridization with blacktail shiner in the upper Coosa River, USA. Biol Invasions 10.8:1229–1242CrossRefGoogle Scholar
  41. Ward JL, Blum MJ, Walters DM, Porter BA, Burkhead N, Freeman B (2012) Discordant introgression in a rapidly expanding hybrid swarm. Evol Appl 5:4:380–392CrossRefPubMedPubMedCentralGoogle Scholar
  42. Wellman DI (2004) Post-flood recovery and distributions of fishes in the New River Gorge National River and the Gauley River National Recreation Area. MS Thesis, West Virginia University, Morgantown, WVGoogle Scholar
  43. Wilson CC, Bernatchez L (1998) The ghost of hybrids past: fixation of arctic charr (Salvelinus alpinus) mitochondrial DNA in an introgressed population of lake trout (S. namaycush). Mol Ecol 7:1:127–132CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Isaac Gibson
    • 1
  • Amy B. Welsh
    • 2
  • Stuart A. Welsh
    • 3
  • Daniel A. Cincotta
    • 1
  1. 1.West Virginia Division of Natural ResourcesElkinsUSA
  2. 2.Division of Forestry and Natural ResourcesWest Virginia UniversityMorgantownUSA
  3. 3.U.S. Geological SurveyWest Virginia Cooperative Fish and Wildlife Research UnitMorgantownUSA

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