Abstract
Black basses (genus Micropterus) are apex predators in North American streams, rivers, and lakes and important game fishes. Translocation and introductions for angling, accompanied by intrinsically weak genetic barriers, have led to widespread introgressive hybridization and genetic swamping. Species-diagnostic (fixed allele) SNP markers have been utilized successfully in salmonids to monitor hybridization and genetic integrity. Here, we developed similar resources for black basses through initial genotyping-by-sequencing, followed by validation in additional samples using two panels of 64 SNPs. Results from > 1300 genotyped bass indicated that the developed panels robustly and clearly delineate fifteen species and their hybrids among black basses. The panels represent a flexible, rapid turnaround (~ 1 day), and cost-effective tool that should augment ongoing efforts toward black bass conservation and management.
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References
Amish SJ, Hohenlohe PA, Painter S, Leary RF, Muhlfeld C, Allendorf FW, Luikart G (2012) RAD sequencing yields a high success rate for westslope cutthroat and rainbow trout species-diagnostic SNP assays. Mol Ecol Resour 12:653–660
Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3:e3376
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 3635:379–401
Bangs MR, Oswald KJ, Greig TW, Leitner JK, Rankin DM, Quattro JM (2017) Introgressive hybridization and species turnover in reservoirs: a case study involving endemic and invasive basses (Centrarchidae: Micropterus) in southeastern North America. Conserv Genet. https://doi.org/10.1007/s10592-017-1018-7
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 5:661–668
Bolnick DI, Near TJ (2005) Tempo of hybrid inviability in Centrarchid fishes (Teleostei: Centrarchidae). Evolution 59:1754–1767
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635
Campbell NR, Harmon SA, Narum SR (2015) Genotyping-in-Thousands by sequencing (GT-seq): a cost effective SNP genotyping method based on custom amplicon sequencing. Mole Ecol Resour 15:855–867
Dakin EE, Porter BA, Freeman BJ, Long JM (2015) Hybridization threatens shoal bass populations in the upper Chattahoochee river basin. In: Tringali MD, Long JM, Birdsong TW, Allen MS (eds) Black bass diversity: multidisciplinary science for conservation, vol 82. American Fisheries Society, Symposium, Bethesda, pp 491–501
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379
Flanagan SP, Jones AG (2017) Substantial differences in bias between single-digest and double-digest RAD-seq libraries: a case study. Mol Ecol Resour. https://doi.org/10.1111/1755-0998.12734
Freeman BJ, Taylor AT, Oswald KJ, Wares J, Freeman MC, Quattro JM, Leitner JK (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, vol 82. American Fisheries Society, Symposium, Bethesda, pp 449–466
Hohenlohe PA, Day MD, Amish SJ, Miller MR, Kamps-Hughes N, Boyer MC, Luikart G (2013) Genomic patterns of introgression in rainbow and westslope cutthroat trout illuminated by overlapping paired-end RAD sequencing. Mol Ecol 22:3002–3013
Jackson DA (2002) Ecological effects of Micropterus introductions: the dark side of black bass. In: Phillip DP, Ridgway MS (eds) Black bass ecology conservation and management, vol 31. American Fisheries Society Symposium, Bethesda, pp 221–232
Jackson LJ (2017) Molecular tools provide a range of powerful options for the conservationist’s toolbox. Aquat Conserv: Mar Freshw Ecosyst 27:296–302
Kang J, Ma X, He S (2017) Population genetics analysis of the Nujiang catfish Creteuchiloglanis macropterus through a genome-wide single nucleotide polymorphisms resource generated by RAD-seq. Sci Rep 7:2813. https://doi.org/10.1038/s41598-017-02853-3
Li C, Waldbieser G, Bosworth B, Beck BH, Thongda W, Peatman E (2014) SNP discovery in wild and domesticated populations of blue catfish, Ictalurus furcatus, using GBS and subsequent SNP validation. Mol Ecol Resour 14:1261–1270
Li C, Gowan S, Anil A, Beck BH, Thongda W, Kucuktas H, Kaltenboeck L, Peatman E (2015) Discovery and validation of gene-linked diagnostic SNP markers for assessing hybridization between Largemouth bass (Micropterus salmoides) and Florida bass (M. floridanus). Mol Ecol Resour 15:395–404
Littrell BM, Lutz-Carrillo DJ, Bonner TH, Fries LT (2007) Status of an introgressed Guadalupe bass population in a central Texas stream. North Am J Fish Manag 27:785–791
Lu F, Lipka AE, Glaubitz J, Elshire R, Cherney JH, Casler MD, Buckler ES, Costich DE (2013) Switchgrass genomic diversity, ploidy, and evolution: novel insights from a network-based SNP discovery protocol. PLoS Genet 9:e1003215
Lutz-Carrillo DJ, Nice CC, Bonner TH, Forstner MRJ, Fries LT (2006) Admixture analysis of Florida largemouth bass and northern largemouth bass using microsatellite loci. Trans Am Fish Soc 135:779–791
Magnelia SJ, Linam G, Saunders K, Parker M, Lutz-Carillo D, Williamson J, Ranft R, Bonner T (2019) Repatriation of Guadalupe Bass Micropterus treculii in the Blanco River, Texas: a case study in the opportunistic use of drought as a fisheries management tool. In: Siepker M, Quinn J (eds) Managing centrarchid fisheries in rivers and streams. Am Fisheries Society, Symposium, Bethesda
Mesak F, Tatarenkov A, Earley RL, Avise JC (2014) Hundreds of SNPs vs. dozens of SSRs: which dataset better characterizes natural clonal lineages in a self-fertilizing fish? Front Ecol Evolut. https://doi.org/10.3389/fevo.2014.00074
Pierce PC, Van den Avyle MJ (1997) Hybridization between introduced spotted bass and smallmouth bass in reservoirs. Trans Am Fish Soc 126:939–947
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Pritchard, J. K., Wen, X., & Falush, D. (2010). Documentation for structure software: Version 2.3. Software from http://pritch.bsd.uchicago.edu/structure.html
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 Resour 16:608–627
Seyoum S, Barthel BL, Tringali MD, Davis MC, Schmitt SL, Bellotti PS, Porak WF (2013) Isolation and characterization of eighteen microsatellite loci for the largemouth bass, Micropterus salmoides, and cross amplification in congeneric species. Conserv Genet Resour 5:697–701
Shafer AB, Wolf JB, Alves PC, Bergström L, Bruford MW, Brännström I, Zieliński P (2015) Genomics and the challenging translation into conservation practice. Trends Ecol Evol 30:78–87
Shaw SL (2015) Black bass diversity and conservation: an overview. In: Tringali MD, Long JM, Birdsong TW, Allen MS (eds) Black bass diversity multidisciplinary science for conservation. American Fisheries Society, Symposium, Bethesda, pp 3–8
Slaughter JE (2015) Black bass diversity: multidisciplinary science for conservation. In: Tringali MD, Long JM, Birdsong TW, Allen MS (eds) Black bass diversity multidisciplinary science for conservation. American Fisheries Society, Symposium, Bethesda, pp 681–685
Takamura K (2007) Performance as a fish predator of largemouth bass (Micropterus salmoides) (Lacepede) invading Japanese freshwaters: a review. Ecol Res 22:940–946
Taylor AT, Papeş M, Long JM (2017) Incorporating fragmentation and non-native species into distribution models to inform fluvial fish conservation. Conserv Biol. https://doi.org/10.1111/cobi.13024
Taylor AT, Tringali MD, O’Rourke PM, Long JM (2018) Shoal bass hybridization in the Chattahoochee River Basin near Atlanta, Georgia. J Southeast Assoc Fish Wildl Agencies 5:1–9
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, Bethesda, pp 421–448
van der Walt JA, Weyl OLF, Woodford DJ, Radloff FGT (2016) Spatial extent and consequences of black bass (Micropterus spp.) invasion in a Cape Floristic Region river basin. Aquat Conserv: Mar Freshw Ecosyst 26:736–748
Zhan L, Paterson IG, Fraser BA, Watson B, Bradbury IR, Nadukkalam Ravindran P, Bentzen P (2017) Megasat: automated inference of microsatellite genotypes from sequence data. Mol Ecol Resour 17:247–256
Zhao H, Li C, Hargrove JS, Bowen BR, Thongda W, Zhang D, Peatman E (2018) SNP marker panels for parentage assignment and traceability in the Florida bass (Micropterus floridanus). Aquaculture 485:30–38
Acknowledgements
The study was conducted with funding from the Alabama Department of Conservation and Natural Resources (ADCNR) and the Southeastern Fish Genetics Cooperative. We are appreciative of collaborators for their assistance in sample collection, including our coauthors, and particularly Steven Sammons and Carol Johnston at School of Fisheries, Aquaculture, and Aquatic Sciences, Auburn University, Steven Rider and Chris McKee at ADCNR, Bud Freeman at Georgia Museum of Natural History and Odum School of Ecology, University of Georgia, and Patrick Black at the Tennessee Wildlife Resources Agency.
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12686_2019_1109_MOESM1_ESM.tiff
Supplementary material 1 STRUCTURE analyses with K = 10 were unable to differentiate Coosa bass, Cahaba bass (A. yellow bars), or Warrior bass (C. yellow bars) while Tallapoosa bass (B) could be distinguished due to the effect of large sample size. STRUCTURE analyses with K = 12 were unable to differentiate Coosa bass, Cahaba bass, or Tallapoosa bass (D. yellow bars) (TIFF 53061 kb)
12686_2019_1109_MOESM2_ESM.tiff
Supplementary material 2 STRUCTURE analyses with K = 9 using the SNP markers demonstrated genetic assignments of each redeye bass species; (A) Coosa bass, (B) Cahaba bass, (C) Tallapoosa bass, and (D) Warrior bass when analyzed with other non-redeye bass species (TIFF 51511 kb)
12686_2019_1109_MOESM3_ESM.tiff
Supplementary material 3 STRUCTURE analyses with K = 5 using the SNP markers revealed hybridization within the Mobile River drainage redeye bass group and outgroup (Alabama bass) (TIFF 17961 kb)
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Supplementary material 4 STRUCTURE analyses with K = 6 using the SNP markers revealed purity among shoal bass broodstock from GADNR (TIFF 2814 kb)
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Thongda, W., Lewis, M., Zhao, H. et al. Species-diagnostic SNP markers for the black basses (Micropterus spp.): a new tool for black bass conservation and management. Conservation Genet Resour 12, 319–328 (2020). https://doi.org/10.1007/s12686-019-01109-8
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DOI: https://doi.org/10.1007/s12686-019-01109-8
Keywords
- Micropterus spp.
- Genotyping-by-sequencing
- SNP
- Black bass
- Hybridization