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Type: Article
Published: 2023-03-09
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Molecular Systematics of Redband Trout from Genome-Wide DNA Sequencing Substantiates the Description of a New Taxon (Salmonidae: Oncorhynchus mykiss calisulat) from the McCloud River

Genomic Variation Laboratory, 2403 Meyer Hall, Department of Animal Science, University of California, Davis, 1 Shields Avenue, Davis, CA 95616. Phone: 530-752-6351
Genomic Variation Laboratory, 2403 Meyer Hall, Department of Animal Science, University of California, Davis, 1 Shields Avenue, Davis, CA 95616. Phone: 530-752-6351
Genomic Variation Laboratory, 2403 Meyer Hall, Department of Animal Science, University of California, Davis, 1 Shields Avenue, Davis, CA 95616. Phone: 530-752-6351
2Natural Reserve System, University of California Merced, Merced, CA 95343
3California Department of Fish and Wildlife, Genetics Research Laboratory, 1415 N Market Blvd, Suite 9, Sacramento, CA 95834. Phone: 916-616-3970.
4Department of Ecology and Conservation Biology and Biodiversity Research and Teaching Collections, Texas A&M University, College Station, TX 77843.
Genomic Variation Laboratory, 2403 Meyer Hall, Department of Animal Science, University of California, Davis, 1 Shields Avenue, Davis, CA 95616.
Pisces Molecular Phylogenetics Native Trout Pacific Trouts Rainbow Trout Sheepheaven Creek Taxonomy

Abstract

Rainbow Trout, Oncorhynchus mykiss, exhibit high levels of phenotypic diversity leading to the recognition of numerous subspecies. A major distinction among Rainbow Trout subspecies exists between Coastal Rainbow Trout (O. m. irideus), which occurs west of the Cascade and Sierra Nevada mountain ranges, and interior Redband Trout (O. mykiss sspp.), largely distributed to the east. Interior Redband Trout are composed of three primary lineages and can share various outward, anatomical or physiological characteristics that are often symplesiomorphies or examples of convergence. We examine high-throughput DNA sequence data from Sacramento Redband Trout O. m. stonei from the Upper Pit and Upper McCloud Rivers along with representatives of Rainbow Trout and Golden Trout lineages to clarify the composition and relationships of the Sacramento Redband Trout. We find O. m. stonei to be polyphyletic, divided between populations in the Pit River and the Upper McCloud River. Redband Trout obtained from the Pit River are most-closely related to Great Basin Redband Trout O. m. newberrii and to fish of the Warner Lakes Basin and Surprise Valley within the O. m. newberrii lineage. The type specimen of O. m. stonei, collected from the Lower McCloud River, is phenotypically similar to Great Basin Redband Trout. We find as well that the isolated populations of trout in the Upper McCloud River Basin represent a lineage of Rainbow Trout now restricted to that region, are monophyletic and are not most closely related to the interior Redband Trout lineages of O. m. newberrii or O. m. gairdnerii. Furthermore, they are not represented by the type specimens of O. m. stonei or O. m. shasta. Consequently, we formally describe the McCloud River Redband Trout O. mykiss calisulat, new subspecies.

 

References

  1. Abadía-Cardoso, A., Brodsky, A., Cavallo, B., Arciniega, M., Garza, J.C., Hannon, J. & Pearse, D.E. (2019) Anadromy Redux? Genetic analysis to inform development of an indigenous American River steelhead broodstock. Journal of Fish and Wildlife Management, 10 (1), 137–147. https://doi.org/10.3996/072018-JFWM-063
    Aho, A.V., Kernighan, B.W. & Weinberger, P.J. (1988) The AWK programming language. Addison Wesley, Reading, Massachusetts, 210 pp.
    Ali, O.A., O’Rourke, S.M., Amish, S.J., Meek, M.H., Luikart, G., Jeffres, C. & Miller, M.R. (2016) RAD Capture (Rapture): Flexible and efficient sequence-based genotyping. Genetics, 202 (2), 389–400. https://doi.org/10.1534/genetics.115.183665
    Allendorf, F.W., Bassham, S., Cresko, W.A., Limborg, M.T., Seeb, L.W. & Seeb, J.E. (2015) Effects of crossovers between homeologs on inheritance and population genomics in polyploid-derived salmonid fishes. Journal of Heredity, 106 (3), 217–227. https://doi.org/10.1093/jhered/esv015
    Bagley, M.J. & Gall, G.A.E. (1998) Mitochondrial and nuclear DNA sequence variability among populations of rainbow trout (Oncorhynchus mykiss). Molecular Ecology, 7 (8), 945–961. https://doi.org/10.1046/j.1365-294x.1998.00413.x
    Baumsteiger, J., Moyle, P.B., Aguilar, A., O’Rourke, S.M. & Miller, M.R. (2017) Genomics clarifies taxonomic boundaries in a difficult species complex. PLOS ONE, 12, e0189417. https://doi.org/10.1371/journal.pone.0189417
    Behnke, R.J. (1966) Relationships of the Far Eastern Trout, Salmo mykiss Walbaum. Copeia, 1966 (2), 346–348. https://doi.org/10.2307/1441145
    Behnke, R.J. (1979) The Native Trouts of the Genus Salmo Of Western North America. Report to the US Fish and Wildlife Service, Bureau of Land Management and the US Forest Service. US Fish and Wildlife Service, Bureau of Land Management and the US Forest Service, Denver, Colorado, 163 pp.
    Behnke, R.J. (1992) Native trout of western North America. American Fisheries Society monograph (USA). No. 6. American Fisheries Society, Bethesda, Maryland, 275 pp.
    Behnke, R.J. (2002) Trout and salmon of North America. The Free Press, New York, New York, 359 pp.
    Berg, W.J. (1987) Evolutionary genetics of rainbow trout, Parasalmo gairdnerii (Richardson). Dissertation, University of California, Davis, California. [unknown pagination]
    Blumstein, D.M., Campbell, M.A., Hale, M.C., Sutherland, B.J.G., McKinney, G.J., Stott, W. & Larson, W.A. (2020) Comparative genomic analyses and a novel linkage map for cisco (Coregonus artedi) provides insight into chromosomal evolution and rediploidization across salmonids. G3: Genes|Genomes|Genetics, 10 (8), 2863. https://doi.org/10.1534/g3.120.401497
    Busack, C.A., Thorgaard, G.H., Bannon, M.P. & Gall, G.A.E. (1980) An electrophoretic, karyotypic and meristic characterization of the Eagle Lake Trout, Salmo gairdneri aquilarum. Copeia, 1980 (3), 418–424. https://doi.org/10.2307/1444517
    Campbell, M.A., Anderson, E.C., Garza, J.C. & Pearse, D.E. (2021) Polygenic basis and the role of genome duplication in adaptation to similar selective environments. Journal of Heredity, 112 (7), 614-625. https://doi.org/10.1093/jhered/esab049
    Campbell, M.A., Buser, T.J., Alfaro, M.E. & López, J.A. (2020) Addressing incomplete lineage sorting and paralogy in the inference of uncertain salmonid phylogenetic relationships. PeerJ 8, e9389. https://doi.org/10.7717/peerj.9389
    Campbell, M.A., Hale, M.C., McKinney, G.J., Nichols, K.M. & Pearse, D.E. (2019) Long-term conservation of ohnologs through partial tetrasomy following whole-genome duplication in Salmonidae. G3: Genes|Genomes|Genetics, 9 (6), 2017. https://doi.org/10.1534/g3.119.400070
    Chen, Z., Farrell, A.P., Matala, A., Hoffman, N. & Narum, S.R. (2018) Physiological and genomic signatures of evolutionary thermal adaptation in redband trout from extreme climates. Evolutionary Applications, 11 (9), 1686–1699. https://doi.org/10.1111/eva.12672
    Chifman, J. & Kubatko, L. (2014) Quartet inference from SNP data under the coalescent model. Bioinformatics, 30 (23), 3317–3324. https://doi.org/10.1093/bioinformatics/btu530
    Chifman, J. & Kubatko, L. (2015) Identifiability of the unrooted species tree topology under the coalescent model with time-reversible substitution processes, site-specific rate variation, and invariable sites. Journal of Theoretical Biology, 374, 35–47. https://doi.org/10.1016/j.jtbi.2015.03.006
    Cooper, J.J. (1983) Distributional ecology of native and introduced fishes of the Pit River system, Northeastern California, with notes on the Modoc Sucker. California Fish and Game, 69 (1), 39–53.
    Cordes, J.F., Stephens, M.R., Blumberg, M.A. & May, B. (2006) Identifying introgressive hybridization in native populations of California Golden Trout based on molecular markers. Transactions of the American Fisheries Society, 135 (1), 110–128. https://doi.org/10.1577/T05-120.1
    Currens, K.P., Schreck, C.B. & Li, H.W. (2009) Evolutionary ecology of redband trout. Transactions of the American Fisheries Society, 138 (4), 797–817. https://doi.org/10.1577/T08-120.1
    Degnan, J.H. & Rosenberg, N.A. (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends in Ecology & Evolution, 24 (6), 332–340. https://doi.org/10.1016/j.tree.2009.01.009
    Erickson, P.B. (2013) The search for the Kern River Rainbow: Conservation genetics of a native trout. Dissertation, University of California, Davis, California. [unknown pagination]
    Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Molecular Ecology, 14 (8), 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
    Fraik, A.K., McMillan, J.R., Liermann, M., Bennett, T., McHenry, M.L., McKinney, G.J., Wells, A.H., Winans, G., Kelley, J.L., Pess, G.R. & Nichols, K.M. (2021) The impacts of dam construction and removal on the genetics of recovering steelhead (Oncorhynchus mykiss) populations across the Elwha River watershed. Genes, 12 (1), 89. https://doi.org/10.3390/genes12010089
    Fricke, R., Eschmeyer, W.N. & van der Laan, R. (Eds.) (2022) Eschmeyer’s Catalog of Fishes: Genera, Species, References. Available from: http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp (accessed 7 June 2022)
    Gibbons, W.P. (1855) Description of a new trout. The Pacific, 4 (17), 6.
    Gold, J.R. (1977) Systematics of western North American trout (Salmo), with notes on the redband trout of Sheepheaven Creek, California. Canadian Journal of Zoology, 55 (11), 1858–1873. https://doi.org/10.1139/z77-239
    Goose Lake Fishes Working Group (1996) Goose Lake Fishes Conservation Strategy. Goose Lake Fishes Working Group, Lakeview, Oregon, 56 pp.
    Grayson, D. (2011) The Great Basin: A Natural Prehistory. University of California Press, Berkeley, California, 432 pp.
    Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate Maximum-Likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology, 59 (3), 307–321. https://doi.org/10.1093/sysbio/syq010
    Habibi, E., Miller, M.R., Gille, D., Sanders, L., Rodzen, J., Auringer, G.M., Stephens, M. & Finger, A.J. (2022) Genomics facilitates evaluation and monitoring of McCloud River Redband Trout (Oncorhynchus mykiss stonei). Conservation Genetics, 23, 773–789.
    https://doi.org/10.1007/s10592-022-01453-7
    Harris, P.M. (2000) Systematic studies of the genus Siphateles (Ostariophysi: Cyprinidae) from western North America. Dissertation, Oregon State University, Corvallis, Oregon. [unknown pagination]
    Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2017) UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35 (2), 518–522. https://doi.org/10.1093/molbev/msx281
    Hubbs, C.L. & Lagler, K.F. (1949) Fishes of the Great Lakes Region. Cranbrook Institute of Science Bulletin. No. 26. Bloomfield Hills, Michigan, 213 pp.
    Huson, D.H. & Bryant, D. (2005) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23 (2), 254–267.
    https://doi.org/10.1093/molbev/msj030
    Huson, D.H., Rupp, R. & Scornavacca, R. (2010) Phylogenetic Networks: Concepts, algorithms and apllications. Cambridge University Press, Cambridge, 362 pp.
    Jordan, D.S. (1894a) Description of a new subspecies of trout from the McCloud River, California. Proceedings of the Academy of Natural Sciences of Philadelphia, 46, 60.
    Jordan, D.S. (1894b) Descriptions of new varieties of trout. Biennial Report of the State Board of Fish Commissioners of the State of California (1893–1894), 1894, 142–143.
    Kishino, H., Miyata, T. & Hasegawa, M. (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. Journal of Molecular Evolution, 31 (2), 151–160. https://doi.org/10.1007/BF02109483
    Knowles, L.L. & Kubatko, L.S. (2010) Estimating species trees: practical and theoretical aspects. John Wiley and Sons, Hoboken, New Jersey, 215 pp.
    Korneliussen, T.S., Albrechtsen, A. & Nielsen, R. (2014) ANGSD: Analysis of Next Generation Sequencing Data. BMC Bioinformatics, 15, 356. https://doi.org/10.1186/s12859-014-0356-4
    Leitwein, M., Garza, J.C. & Pearse, D.E. (2017) Ancestry and adaptive evolution of anadromous, resident, and adfluvial rainbow trout (Oncorhynchus mykiss) in the San Francisco bay area: application of adaptive genomic variation to conservation in a highly impacted landscape. Evolutionary Applications, 10 (1), 56–67. https://doi.org/10.1111/eva.12416
    Li, H. & Durbin, R. (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics, 25 (14), 1754–1760. https://doi.org/10.1093/bioinformatics/btp324
    Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics, 25 (16), 2078–2079. https://doi.org/10.1093/bioinformatics/btp352
    Maddison, W.P. (1997) Gene trees in species trees. Systematic Biology, 46 (3), 523–536. https://doi.org/10.1093/sysbio/46.3.523
    Martínez, A., Garza, J.C. & Pearse, D.E. (2011) A microsatellite genome screen identifies chromosomal regions under differential selection in steelhead and rainbow trout. Transactions of the American Fisheries Society, 140 (3), 829–842. https://doi.org/10.1080/00028487.2011.588094
    Meisner, J. & Albrechtsen, A. (2018) Inferring population structure and admixture proportions in low-depth NGS data. Genetics, 210 (2), 719. https://doi.org/10.1534/genetics.118.301336
    Miller, M.R., Brunelli, J.P., Wheeler, P.A., Liu, S., Rexroad, C.E., Palti, Y., Doe, C.Q. & Thorgaard, G.H. (2012) A conserved haplotype controls parallel adaptation in geographically distant salmonid populations. Molecular Ecology, 21 (2), 237–249. https://doi.org/10.1111/j.1365-294X.2011.05305.x
    Miller, R.R. (1972) Classification of the native trouts of Arizona with the description of a new species, Salmo apache. Copeia, 1972 (3), 401–422. https://doi.org/10.2307/1442913
    Moyle, P.B. (2002) Inland Fishes of California. University of California Press, Berkeley, California and Los Angeles, California, 413 pp.
    Moyle, P.B. & Campbell, M.A. (2022) Cryptic species of freshwater sculpin (Cottidae: Cottus) in California. Zootaxa, 5154 (5), 501–527. https://doi.org/10.11646/zootaxa.5154.5.1
    Needham, P.R. & Behnke, R.J. (1962) The origin of hatchery Rainbow Trout. The Progressive Fish-Culturist, 24 (4), 156–158. https://doi.org/10.1577/1548-8659(1962)24[156:TOOHRT]2.0.CO;2
    Nguyen, L.-T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2014) IQ-TREE: A fast and effective stochastic algorithm for estimating Maximum-Likelihood phylogenies. Molecular Biology and Evolution, 32 (1), 268–274. https://doi.org/10.1093/molbev/msu300
    Nielsen, J.L., Crow, K.D. & Fountain, M.C. (1999) Microsatellite diversity and conservation of a relic trout population: McCloud River redband trout. Molecular Ecology, 8, S129–S142. https://doi.org/10.1046/j.1365-294X.1999.00817.x
    Nielsen, J.L., Fountain, M.C. & Wright, J.M. (1997) CHAPTER 5—Biogeographic Analysis of Pacific Trout (Oncorhynchus mykiss) in California and Mexico Based on Mitochondrial DNA and Nuclear Microsatellites. In: Kocher, T. D. and Stepien C. A. (Eds.), Molecular Systematics of Fishes. Academic Press, San Diego, California, pp. 53–73.
    Page, L.M. & Burr, B.M. (2011) Peterson Field Guide to Freshwater Fishes of North America North of Mexico. 2nd Edition. Houghton Mifflin Harcourt, Boston, Massachusetts and New York, New York, 663 pp.
    Page, L.M., Espinosa-Pérez, H., Findley, L.T., Gilbert, C.R., Lea, R.N., Mandrak, N.E., Mayden, R.L. & Nelson, J.S. (2013) Common and scientific names of fishes from the United States, Canada and Mexico. American Fisheries Society, Bethesda, Maryland, 243 pp. https://doi.org/10.47886/9781934874318
    Pearse, D.E., Barson, N.J., Nome, T., Gao, G., Campbell, M.A., Abadía-Cardoso, A., Anderson, E.C., Rundio, D.E., Williams, T.H., Naish, K.A., Moen, T., Liu, S., Kent, M., Moser, M., Minkley, D.R., Rondeau, E.B., Brieuc, M.S.O., Sandve, S.R., Miller, M.R., Cedillo, L., Baruch, K., Hernandez, A.G., Ben-Zvi, G., Shem-Tov, D., Barad, O., Kuzishchin, K., Garza, J.C., Lindley, S.T., Koop, B.F., Thorgaard, G.H., Palti, Y. & Lien, S. (2019) Sex-dependent dominance maintains migration supergene in rainbow trout. Nature Ecology & Evolution, 3, 1731–7142. https://doi.org/10.1038/s41559-019-1044-6
    Pearse, D.E. & Campbell, M.A. (2018) Ancestry and adaptation of Rainbow Trout in Yosemite National Park. Fisheries, 43 (10), 472–484. https://doi.org/10.1002/fsh.10136
    Pearse, D.E. & Garza, J.C. (2015) You can’t unscramble an egg: Population genetic structure of Oncorhynchus mykiss in the California central valley inferred from combined microsatellite and single nucleotide polymorphism data. San Francisco Estuary and Watershed Science, 13 (4), 1–17. https://doi.org/10.15447/sfews.2015v13iss4art3
    Pearse, D.E., Miller, M.R., Abadía-Cardoso, A. & Garza, J.C. (2014) Rapid parallel evolution of standing variation in a single, complex, genomic region is associated with life history in steelhead/rainbow trout. Proceedings of the Royal Society of London B: Biological Sciences, 281 (1783), 20140012. https://doi.org/10.1098/rspb.2014.0012
    Penaluna, B.E., Abadía-Cardoso, A., Dunham, J.B., García-Dé León, F.J., Gresswell, R.E., Luna, A.R., Taylor, E.B., Shepard, B.B., Al-Chokhachy, R., Muhlfeld, C.C., Bestgen, K.R., Rogers, K., Escalante, M.A., Keeley, E.R., Temple, G.M., Williams, J.E., Matthews, K.R., Pierce, R., Mayden, R.L., Kovach, R.P., Garza, J.C. & Fausch, K.D. (2016) Conservation of native Pacific trout diversity in western North America. Fisheries, 41 (6), 286–300. https://doi.org/10.1080/03632415.2016.1175888
    R Development Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from: http://www.R-project.org/ (accessed 20 December 2022)
    Remple, S.L. (2013) Taxonomy and Systematic Relationships of Tui Chubs (Siphateles: Cyprinidae from Oregon’s Great Basin. Thesis, Oregon State University, Corvallis, Oregon. [unknown pagination]
    Richardson, J. (1836) The Fish. In: Fauna Boreali-Americana; or the zoology of the northern parts of British America: containing descriptions of the objects of natural history collected on the late northern land expeditions, under the command of Sir John Franklin. Part 3. R. N. J. Bentley, London, pp. 1.327.
    Robertson, F.M., Gundappa, M.K., Grammes, F., Hvidsten, T.R., Redmond, A.K., Lien, S., Martin, S.A.M., Holland, P.W.H., Sandve, S.R. & Macqueen, D.J. (2017) Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification. Genome Biology, 18 (1), 111. https://doi.org/10.1186/s13059-017-1241-z
    Rode, M. (1990) Bull trout, Salvelinus confluentus Suckley, in the McCloud River: status and recovery options. Inland Fisheries Administrative Report No. 90-15. State of California, Department of Fish and Game, Sacramento, California. [unknown pagination]
    Rodzen, J. & Ahrens, K. (2019) Genetic analysis and recommendations. Eagle Lake Rainbow Trout, Oncorhynchus mykiss aquilarum. CDFW Genetics Research Laboratory, Sacramento, California, 34 pp.
    Rutter, C. (1908) The fishes of the Sacramento-San Joaquin basin, with a study of their distribution and variation. U.S. Bureau of Fisheries Bulletin, 17, 105–152.
    Saglam, I.K., Prince, D.J., Meek, M., Ali, O.A., Miller, M.R., Peacock, M., Neville, H., Goodbla, A., Mellison, C., Somer, W., May, B. & Finger, A.J. (2017) Genomic analysis reveals genetic distinctiveness of the Paiute Cutthroat Trout Oncorhynchus clarkii seleniris. Transactions of the American Fisheries Society, 146 (6), 1291–1302. https://doi.org/10.1080/00028487.2017.1356373
    Schreck, C.B. & Behnke, R.J. (1971) Trouts of the Upper Kern River Basin, California, with reference to systematics and evolution of Western North American Salmo. Journal of the Fisheries Research Board of Canada, 28 (7), 987–998. https://doi.org/10.1139/f71-143
    Shimodaira, H. (2002) An approximately unbiased test of phylogenetic tree selection. Systematic Biology, 51 (3), 492–508. https://doi.org/10.1080/10635150290069913
    Simmons, R.E., Lavretsky, P. & May, B. (2010) Introgressive hybridization of redband trout in the upper McCloud River watershed. Transactions of the American Fisheries Society, 139 (1), 201–213. https://doi.org/10.1577/T08-245.1
    Skotte, L., Korneliussen, T.S. & Albrechtsen, A. (2013) Estimating individual admixture proportions from Next Generation Sequencing data. Genetics, 195 (3), 693. https://doi.org/10.1534/genetics.113.154138
    Smith, G.R. & Stearley, R.F. (1989) The classification and scientific names of Rainbow and Cutthroat Trouts. Fisheries, 14 (1), 4–10. https://doi.org/10.1577/1548-8446(1989)014<0004:TCASNO>2.0.CO;2
    Snyder, J.O. (1933) California trout. California Fish and Game, 19 (2), 81–112.
    Solís-Lemus, C. & Ané, C. (2016) Inferring phylogenetic networks with Maximum Pseudolikelihood under Incomplete Lineage Sorting. PLOS Genetics, 12 (3), e1005896. https://doi.org/10.1371/journal.pgen.1005896
    Stephens, M., Erickson, B., Finger, A.J., Simmons, R. & May, B. (2013) Final report: Genetic analysis of Native California Trout (Phase 6). Genomic Variation Laboratory, University of California, Davis, California, 195 pp.
    Stephens, M.R. (2007) Systematics, Genetics and Conservation of Golden Trout. Dissertation, University of California, Davis, California. [unknown pagination]
    Strimmer, K. & Rambaut, A. (2002) Inferring confidence sets of possibly misspecified gene trees. Proceedings of the Royal Society B: Biological Sciences, 269 (1487), 137–142. https://doi.org/10.1098/rspb.2001.1862
    Swofford, D.L. (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Associates, Sunderland, Massachusetts. [program]
    Taylor, W.R. & Van Dyke, G.C. (1985) Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium, 9 (2), 107–120.
    Trifinopoulos, J., Nguyen, L.-T., von Haeseler, A. & Minh, B.Q. (2016) W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research, 44 (W1), W232–W235. https://doi.org/10.1093/nar/gkw256
    Walbaum, J.J. (1792) Petri Artedi sueci genera piscium. In: quibus systema totum ichthyologiae proponitur cum classibus, ordinibus, generum characteribus, specierum differentiis, observationibus plurimis. Redactis speciebus 242 ad genera 52. Part 3. Rose, Grypeswaldiae, 723 pp.
    Wales, J.H. (1939) General report of investigations on the McCloud River drainage in 1938. California Fish and Game, 25 (4), 272–309.
    Wickham, H. (2009) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York, New York, 213 pp.
    Wishard, L.N., Seeb, J.E., Utter, F.M. & Stefan, D. (1984) A genetic investigation of suspected redband trout populations. Copeia, 1984 (1), 120–132. https://doi.org/10.2307/1445042
    Yoshiyama, R.M., Gerstung, E.R., Fisher, F.W. & Moyle, P.B. (2001) Historical and present distribution of Chinook salmon in the Central Valley drainage of California. Fish Bulletin, 179 (1), 71–176.
    Yu, Y., Than, C., Degnan, J.H. & Nakhleh, L. (2011) Coalescent histories on phylogenetic networks and detection of hybridization despite incomplete lineage sorting. Systematic Biology, 60 (2), 138–149. https://doi.org/10.1093/sysbio/syq084

  2.