Abstract
North American river sturgeons of the genus Scaphirhynchus include three species: S. platorynchus, S. albus and S. suttkusi that live in the Missouri, Mississippi, and Mobile basin. All species of Scaphirhynchus are threatened, endangered or critically endangered due to a combination of factors including of habitat loss and over-harvesting. Genetic tools have been applied for conservation studies in this group, however, the tetrapolyploid nature of the genome of these species have brought a huge challenge to development of nuclear markers for these species and limited knowledge that could be obtained, such as the phylogenetic intrarelationships and population genetics of this genus. Moreover, unintentional hybridization arose from two species of Scaphirhynchus (S. platorynchus and S. albus) that share the same spawning space. To address the problem of species identification and provide genetic markers for population genetic studies on Scaphirhynchus, we developed a bioinformatics pipeline to find SNP markers, based on comparison between single-copy loci of diploid gar and two released autotetraploid genomes of Acipenseriformes. We found 77 SNPs at single-copy loci and 642 SNPs at double-copy loci after filtering. Both the single-copy and double-copy loci supported the same phylogenetic relationship among the three species, in which S. albus and S. platorynchus were more closely related to each other than either of them to S. suttkusi. The principal component analysis using these SNPs also showed that S. albus and S. platorynchus were close to each other. The SNP markers developed in this study should facilitate further researches on population genetics and conservation of the Scaphirhynchus sturgeons.
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REFERENCES
Birstein, V.J. and Bemis, W.E., How many species are there within the genus Acipenser?, Environ. Biol. Fishes, 1997, vol. 48, no. 1−4, pp. 157−163. https://doi.org/10.1023/A:1007354827093
Birstein, V.J., Desalle, R., Doukakis, P., et al., Testing taxonomic boundaries and the limit of DNA barcoding in the Siberian sturgeon, Acipenser baerii, Mitochondrial DNA, 2009, vol. 20, no. 5−6, pp. 110−118. https://doi.org/10.3109/19401730903168182
Chassaing O., Hänni C., and Berrebi P., Distinguishing species of European sturgeons Acipenser spp. using microsatellite allele sequences, J. Fish Biol., 2011, vol. 78, no. 1, pp. 208−226. https://doi.org/10.1111/j.1095-8649.2010.02852.x
Cheng, P.L., Huang, Y., Lv, Y.Y., et al., The American Paddlefish Genome Provides Novel lnsignts into Chromosomal Evolution and Bone Mineralization in Early Vertebrates, Mol. Biol. Evol., 2021, vol. 38, no. 4, pp. 1595−1607. https://doi.org/10.1093/molbev/msaa326
Comincini, S., Lanfredi, M., Rossi, R., and Fontana, F., Use of RAPD markers to determine the genetic relationships among sturgeons (Acipenseridae, Pisces), Fish. Sci., 1998, vol. 64, no. 1, pp. 35−38. https://doi.org/10.2331/fishsci.64.35
Du, K., Stock, M., Kneitz, S., et al., The sterlet sturgeon genome sequence and the mechanisms of segmental rediploidization, Nat. Ecol. Evol., 2020, vol. 4, no. 6, pp. 841−852. https://doi.org/10.1038/s41559-020-1166-x
Eichelberger, J.S., Braaten, P.J., Fuller, D.B., et al., Novel Single-Nucleotide Polymorphism Markers Confirm Successful Spawning of Endangered Pallid Sturgeon in the Upper Missouri River Basin, Trans. Am. Fish. Soc., 2014, vol. 143, no. 6, pp. 1373−1385. https://doi.org/10.1080/00028487.2014.935479
Haxton, T.J., Sulak, K., and Hildebrand, L., Status of scientific knowledge of North American sturgeon, J. Appl. Ichthyol., 2016, vol. 32, pp. 5−10. https://doi.org/10.1111/jai.13235
Janosik, A.M., Whitaker, J.M., VanTassel, N.M., and Rider, S.J., Improved environmental DNA sampling scheme for Alabama sturgeon provides new insight into a species once presumed extinct, J. Appl. Ichthyol., 2021, vol. 37, no. 2, pp. 178−185. https://doi.org/10.1111/jai.14183
Jiang, J., Yuan, H., Zheng, X., et al., Gene markers for exon capture and phylogenomics in ray-finned fishes, Ecol Evol., 2019, vol. 9, no. 7, pp. 3973–3983. https://doi.org/10.1002/ece3.5026
Katoh, K., Misawa, K., Kuma, K., and Miyata, T., MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform, Nucleic Acids Res., 2002, vol. 30, no. 14, pp. 3059−3066. https://doi.org/10.1093/nar/gkf436
Khlestkina, E. K., and Salina, E. A., SNP markers: Methods of analysis, ways of development, and comparison on an example of common wheat, Russ. J. Genet., 2006, vol. 42, no. 6, pp. 585−594. https://doi.org/10.1134/S1022795406060019
Knaus, B. J., and Grünwald, N. J., VCFR: a package to manipulate and visualize variant call format data in R, Mol. Ecol. Res., 2017, vol. 17, no. 1, pp. 44−53. https://doi.org/10.1111/1755-0998.12549
Krieger, J., Fuerst, P. A. and Cavender, T. M., Phylogenetic relationships of the North American sturgeons (order Acipenseriformes) based on mitochondrial DNA sequences, Mol. Phylogenet. Evol., 2000, vol. 16, no. 1, pp. 64–72. https://doi.org/10.1006/mpev.1999.0743
Krieger, J., Hett, A.K., Fuerst, P.A., et al., The molecular phylogeny of the order Acipenseriformes revisited, J. Appl. Ichthyol., 2008, vol. 24, no. s1, pp. 36−45. https://doi.org/10.1111/j.1439-0426.2008.01088.x
Li, H., Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM, arXiv pre-print server, 2013. https://doi.org/10.48550/arXiv.1303.3997
Li, C. H., Orti, G., Zhang, G., and Lu, G.Q.,A practical approach to phylogenomics: the phylogeny of ray-finned fish (Actinopterygii) as a case study, BMC Evol. Biol., 2007, vol. 7, Article 44. https://doi.org/10.1186/1471-2148-7-44
Li, C.H., Riethoven, J.J.M., and Naylor, G.J.P., EvolMarkers: a database for mining exon and intron markers for evolution, ecology and conservation studies, Mol. Ecol. Res., 2012, vol. 12, no. 5, pp. 967−971. https://doi.org/10.1111/j.1755-0998.2012.03167.x
Li, Z., De La Torre, A. R., Sterck, L., et al., Single-Copy Genes as Molecular Markers for Phylogenomic Studies in Seed Plants, Genome Biol. Evol., 2017, vol. 9, no. 5, pp. 1130−1147. https://doi.org/10.1093/gbe/evx070
Liu, Y., Chen, Y.Y., Gong, Q., et al., Paternity assignment in the polyploid Acipenser dabryanus based on a novel microsatellite marker system, PLoS One, 2017, vol. 12, no. 9, Article e0185280. https://doi.org/10.1371/journal.pone.0185280
Ludwig, A., Identification of Acipenseriformes species in trade, J. Appl. Ichthyol., 2008, vol. 24, pp. 2−19. https://doi.org/10.1111/j.1439-0426.2008.01085.x
Ludwig, A., Belfiore, N.M., Pitra, C., et al., Genome duplication events and functional reduction of ploidy levels in sturgeon (Acipenser, Huso and Scaphirhynchus), Genetics, 2001, vol. 158, no. 3, pp. 1203−1215. https://doi.org/10.1093/genetics/158.3.1203
Luo, D.H., Li, Y.P., Zhao, Q.Y., et al., Highly resolved phylogenetic relationships within order acipenseriformes according to novel nuclear markers, Genes, 2019, vol. 10, no. 1, Article 38. https://doi.org/10.3390/genes10010038
McQuown, E.C., Sloss, B.L., Sheehan, R.J., et al., Microsatellite analysis of genetic variation in sturgeon: New primer sequences for Scaphirhynchus and Acipenser, Trans. Am. Fish. Soc., 2000, vol. 129, pp. 1380–1388. https://doi.org/10.1577/1548-8659(2000)129<1380:MAOGVI>2.0.CO;2
Murphy, C.E., Hoover, J.J., George, S.G., and Killgore, K.J., Morphometric variation among river sturgeons (Scaphirhynchus spp.) of the Middle and Lower Mississippi River, J. Appl. Ichthyol., 2007, vol. 23, no. 4, pp. 313−323. https://doi.org/10.1111/j.1439-0426.2007.00883.x
Nguyen, L.T., Schmidt, H.A., von Haeseler, A., and Minh, B., Q. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies, Mol. Biol. Evol., 2015, vol. 32, no. 1, pp. 268−274. https://doi.org/10.1093/molbev/msu300
Rothfels, C.J., Larsson, A., Li, F.W., et al., Transcriptome-mining for single-copy nuclear markers in ferns, PLoS One, 2013, vol. 8, no. 10, Article e76957. https://doi.org/10.1371/journal.pone.0076957
Schrey, A.W. and Heist, E.J. Stock structure of pallid sturgeon analyzed with microsatellite loci, J. Appl. Ichthyol., 2007, vol. 23, no. 4, pp. 297−303. https://doi.org/10.1111/j.1439-0426.2007.00881.x
Schrey, A.W., Boley, R., and Heist, E.J., Hybridization between pallid sturgeon Scaphirhynchus albus and shovelnose sturgeon Scaphirhynchus platorynchus, J. Fish Biol., 2011, vol. 79, no. 7, pp. 1828−1850. https://doi.org/10.1111/j.1095-8649.2011.03123.x
Shen, W., Le, S., Li, Y., and Hu, F.Q., SeqKit: A cross-platform and ultrafast toolkit for FASTA/Q file manipulation, PLoS One, 2016, vol. 11, no. 10, Article e0163962. https://doi.org/10.1371/journal.pone.0163962
Shen, Y., Yang, N., Liu, Z. et al., Phylogenetic perspective on the relationships and evolutionary history of the Acipenseriformes, Genomics, 2020, vol. 112, no. 5, pp. 3511−3517. https://doi.org/10.1016/j.ygeno.2020.02.017
Sheraliev, B. and Peng, Z.G., Complete mitochondrial genome sequence and phylogenetic position of the Amu Darya sturgeon, Pseudoscaphirhynchus kaufmanni (Acipenseriformes: Acipenseridae), J. Appl. Ichthyol., 2020, vol. 36, no. 4, pp. 389−392. https://doi.org/10.1111/jai.14043
Simpson, J.T., Wong, K., Jackman, S.D., Schein, J.E., Jones, S.J. M., and Birol, I. ABySS: A parallel assembler for short read sequence data, Genome Res., 2009, vol. 19, no. 6, pp. 1117–1123. https://doi.org/10.1101/gr.089532.108
Van De Peer, Y., Mizrachi, E., and Marchal, K., The evolutionary significance of polyploidy, Nat. Rev. Genet., 2017, vol. 18, no. 7, pp. 411−424. https://doi.org/10.1038/nrg.2017.26
Yuan, H., Jiang, J.M., Jimenez, F.A., et al., Target gene enrichment in the cyclophyllidean cestodes, the most diverse group of tapeworms, Mol. Ecol. Resour., 2016, vol. 16, no. 5, pp. 1095−1106. https://doi.org/10.1111/1755-0998.12532
Zeng, L.P., Zhang, N., Zhang, Q.A., et al., Resolution of deep eudicot phylogeny and their temporal diversification using nuclear genes from transcriptomic and genomic datasets, New Phytol., 2017, vol. 214, no. 3, pp. 1338−1354. https://doi.org/10.1111/nph.14503
Zhang, H., Jarić, I., Roberts, D.L., et al., Extinction of one of the world’s largest freshwater fishes: Lessons for conserving the endangered Yangtze fauna, Sci. Total Environ., 2020, vol. 710, Article 136242. https://doi.org/10.1016/j.scitotenv.2019.136242
ACKNOWLEDGMENTS
We are grateful to E.J. Hilton, Virginia Institute of Marine Science, Gloucester Point, VA, USA, R.M. Wood, Saint Louis University, St. Louis, MO, USA, B.R. Kuhajda, University of Alabama, Tuscaloosa, AL, USA and R.L. Mayden, Saint Louis University, St. Louis, MO, USA for tissues of Scaphirhynchus. We thank the anonymous reviewers for their constructive suggestions.
Funding
This work was supported by the Science and Technology Commission of Shanghai Municipality (19050501900). C.B. Dillman was supported by U.S. National Science Foundation (DEB-0841691).
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C. Li and T. Zhou conceived the research. T. Zhou and J. Huang performed experiment and carried the analysis. T. Zhou, J. Huang, C.B. Dillman, Y. He, and C. Li drafted the manuscript. All authors have edited and approved the final version of the manuscript.
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Statement on the welfare of animals. The animal study was reviewed and approved by the Animal Ethics Committee of Shanghai Ocean University, China (no. 22, Aug. 2014).
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Custom scripts used for generating the results are available at GitHub (https://github.com/TaoZhou2021/ SNP_marker). Supplementary file of sequences of conserved loci (fasta) and filtered SNPs (vcf) were available by searching the https://data.mendeley.com/datasets/77z94jv27v/2.
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Zhou, T., Huang, J., Dillman, C.B. et al. Development of Single Nucleotide Polymorphism Markers for the Autotetraploid Scaphirhynchus Sturgeons (Acipenseriformes). J. Ichthyol. 62, 1419–1429 (2022). https://doi.org/10.1134/S0032945222060340
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DOI: https://doi.org/10.1134/S0032945222060340