How do suboptimal temperatures affect polyploid sterlet Acipenser ruthenus during early development?
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
18-09323S
Grantová Agentura České Republiky
Ministerstvo Školství, Mládeže a Tělovýchovy
Czech Science Foundation
CZ.02.1.01/0.0 /0.0/16_025/0007370
the Ministry of Education, Youth and Sports of the Czech Republic
LM2018099
the Ministry of Education, Youth and Sports of the Czech Republic
PubMed
35475498
DOI
10.1111/jfb.15072
Knihovny.cz E-zdroje
- Klíčová slova
- hexaploidy, mosaicism, polyploidy, sturgeon, tetraploidy, triploidy,
- MeSH
- diploidie MeSH
- genom MeSH
- polyploidie * MeSH
- ryby * genetika MeSH
- teplota * MeSH
- triploidie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Sturgeons are ancient fish exhibiting unique genome plasticity and a high tendency to produce spontaneously autopolyploid genome states. The temperature profiles of the rivers in which sturgeon live and reproduce have been severely altered by human intervention, and the effect of global warming is expected to cause further temperature shifts, which may be detrimental for early developmental stages with narrow windows of thermal tolerance. The comparison of the performance of diploid and autopolyploid sturgeon kept at unfavourable temperatures contributes to scientific knowledge of the effects of polyploid genome states on organisms and can shed light on the ability of polyploids to cope with human-induced alterations to natural conditions. Using the sterlet Acipenser ruthenus as a model species, we carried out conventional artificial fertilization, as well as the induction of the second polar body retention (SPBR), of the first mitotic division suppression (FMDS) and of the second polar body retention followed by the first mitotic division suppression (SPBR+FMDS). Two experiments were conducted to evaluate the effect of polyploidy on two basic performance parameters, survival and growth. In Experiment 1, fish belonging to untreated, SPBR-, FMDS- and SPBR+FMDS-induced groups were kept at 10, 16 and 20°C from the neurula stage until the end of endogenous feeding. In Experiment 2, larvae from the untreated and SPBR-induced groups were reared at 10, 16 and 20°C after their endogenous feeding transition for 3 weeks. Based on our findings, we report that the embryos, prelarvae and larvae of triploid A. ruthenus do not differ from diploids in their ability to survive, grow and develop under suboptimal temperature conditions, while the survival of tetraploids was significantly reduced even at the optimal temperature and even more so at temperatures far from the optimum. This was also the case in the 2n/4n mosaics observed in FMDS-induced group. Thus, we assume that in tetraploid and 2n/4n individuals, the limits of thermal tolerance are closer to the optimum than in diploids. We also conclude that the hexaploid genome state is probably lethal in A. ruthenus since none of the hexaploids or 3n/6n mosaics arising from the SPBR+FMDS induction survived the prelarval period.
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Adams, K. L. (2007). Evolution of duplicate gene expression in polyploid and hybrid plants. Journal of Heredity, 98(2), 136-141.
Andrei, R. C., Cristea, V., Creţu, M., Dediu, L., & Mogodan, A. (2018). The effect of temperature on the standard and routine metabolic rates of young of the year sterlet sturgeon (Acipenser ruthenus). Aquaculture, Aquarium, Conservation & Legislation, 11(5), 1467-1475.
Beyea, M. M., Benfey, T. J., & Kieffer, J. D. (2005). Hematology and stress physiology of juvenile diploid and triploid shortnose sturgeon (Acipenser brevirostrum). Fish Physiology and Biochemistry, 31(4), 303-313.
Birstein, V. J., Bemis, W. E., & Waldman, J. R. (1997). The threatened status of acipenseriform species: A summary. In Sturgeon biodiversity and conservation (pp. 427-435). Dordrecht: Springer.
Blaxter, J. H. S. (1992). The effect of temperature on larval fishes. Netherlands Journal of Zoology, 42(2-3), 336-357.
Bunt, C. M., Cooke, S. J., Katopodis, C., & Mckinley, R. S. (1999). Movement and summer habitat of brown trout (Salmo trutta) below a pulsed discharge hydroelectric generating station. Regulated Rivers: Research & Management: An International Journal Devoted to River Research and Management, 15(5), 395-403.
Bytyutskyy, D., Kholodnyy, V., & Flajšhans, M. (2014). 3-D structure, volume, and DNA content of erythrocyte nuclei of polyploid fish. Cell Biology International, 38(6), 708-715.
Cavalier-Smith, T. (1978). Nuclear volume control by nucleoskeletal DNA, selection for cell volume and cell growth rate, and the solution of the DNA C-value paradox. Journal of Cell Science, 34(1), 247-278.
Chebanov, M. S., & Galich, E. V. (2011). Sturgeon hatchery manual. Ankara: FAO.
Chebanov, M. S., & Savelyeva, E. A. (1999). New strategies for brood stock management of sturgeon in the sea of Azov basin in response to changes in patterns of spawning migration. Journal of Applied Ichthyology, 15(4-5), 183-190.
Cheng, F., Wu, J., Cai, X., Liang, J., Freeling, M., & Wang, X. (2018). Gene retention, fractionation and subgenome differences in polyploid plants. Nature Plants, 4(5), 258-268.
Chourrout, D., & Nakayama, I. (1987). Chromosome studies of progenies of tetraploid female rainbow trout. Theoretical and Applied Genetics, 74(6), 687-692.
Comai, L. (2005). The advantages and disadvantages of being polyploid. Nature Reviews Genetics, 6(11), 836-846.
Dahlke, F. T., Wohlrab, S., Butzin, M., & Pörtner, H. O. (2020). Thermal bottlenecks in the life cycle define climate vulnerability of fish. Science, 369, 65-70.
Deguo, Y., Qiwei, W., Xihua, C., Jianyi, L., Yongjiu, Z., & Kai, W. (2007). Hydrological status of the spawning ground of Acipenser sinensis underneath the Gezhouba dam and its relationship with the spawning runs. Acta Ecologica Sinica, 27(3), 862-868.
Duncan, M. S., Isely, J. J., & Cooke, D. W. (2004). Evaluation of shortnose sturgeon spawning in the Pinopolis dam tailrace, South Carolina. North American Journal of Fisheries Management, 24(3), 932-938.
Edinger, J. E., Duttweiler, D. W., & Geyer, J. C. (1968). The response of water temperatures to meteorological conditions. Water Resources Research, 4(5), 1137-1143.
Flajšhans, M., Havelka, M., Lebeda, I., Rodina, M., Gela, D., & Hubálek, M. (2020). Application of hydrostatic pressure shock for retention of the second polar body in sterlet (Acipenser ruthenus). Aquaculture, 520, 734947.
Flajšhans, M., Ráb, P., & Linhart, O. (2013). Polyploidie a genomové manipulace u ryb. In M. Flajšhans (Ed.), Genetika a šlechtění ryb (2nd ed., pp. 151-195). FROV JU: Vodňany.
Flynn, S. R., Matsuoka, M., Reith, M., Martin-Robichaud, D. J., & Benfey, T. J. (2006). Gynogenesis and sex determination in shortnose sturgeon, Acipenser brevirostrum Lesuere. Aquaculture, 253(1-4), 721-727.
Fontana, F., Zane, L., Pepe, A., & Congiu, L. (2007). Polyploidy in Acipenseriformes: Cytogenetic and molecular approaches. In E. Pisano, C. Ozof-Costaz, F. Foresti, & B. G. Kapoor (Eds.), Fish cytogenetic (pp. 385-403). New Hampshire, NH: Science Publisher Inc.
Fopp-Bayat, D., Jankun, M., Woznicki, P., & Kolman, R. (2007a). Viability of diploid and triploid larvae of Siberian sturgeon and bester hybrids. Aquaculture Research, 38(12), 1301-1304.
Fopp-Bayat, D., Kolman, R., & Woznicki, P. (2007b). Induction of meiotic gynogenesis in sterlet (Acipenser ruthenus) using UV-irradiated bester sperm. Aquaculture, 264(1-4), 54-58.
Fopp-Bayat, D., Ocalewicz, K., Kucinski, M., Jankun, M., & Laczynska, B. (2017). Disturbances in the ploidy level in the gynogenetic sterlet Acipenser ruthenus. Journal of Applied Genetics, 58(3), 373-380.
Fry, F. E. J. (1971). The effect of environmental factors on the physiology of fish. In W. S. Hoar & D. J. Randall (Eds.), Fish physiology, environmental relations and behavior (Vol. 6, pp. 1-98). New York, NY: Academic Press.
Gela, D., Kahanec, M., & Rodina, M. (2012). Metodika odchovu raných stadií jeseterovitých ryb. Vodňany: VÚRH JU.
Gela, D., Rodina, M., & Linhart, O. (2008). Řízená reprodukce jeseterů (Acipenser). VÚRH JU: Vodňany.
Hansen, T. J., Olsen, R. E., Stien, L., Oppedal, F., Torgersen, T., Breck, O., … Fjelldal, P. G. (2015). Effect of water oxygen level on performance of diploid and triploid Atlantic salmon post-smolts reared at high temperature. Aquaculture, 435, 354-360.
Hanson, K. C., & Ostrand, K. G. (2011). Potential effects of global climate change on National Fish Hatchery operations in the Pacific northwest, USA. Aquaculture Environment Interactions, 1(3), 175-186.
Hassan, A., Okomoda, V. T., & Nurhayati, M. N. (2018). Embryonic development of diploid and triploid eggs of Clarias gariepinus (Burchell, 1822). Caryologia, 71(4), 372-379.
Havelka, M., & Arai, K. (2019). Hybridization and polyploidization in sturgeon. In H. P. Wang, F. Piferrer, & S. L. Chen (Eds.), Sex control in aquaculture (Vol. 2, 1st ed., pp. 669-687). Hoboken, NJ: John Wiley & Sons.
Havelka, M., Bytyutskyy, D., Symonová, R., Ráb, P., & Flajšhans, M. (2016). The second highest chromosome count among vertebrates is observed in cultured sturgeon and is associated with genome plasticity. Genetics Selection Evolution, 48(1), 1-9.
Hegarty, M. J., & Hiscock, S. J. (2008). Genomic clues to the evolutionary success of polyploid plants. Current Biology, 18(10), R435-R444.
Hochleithner, M., & Gessner, J. (1999). The sturgeons and paddlefishes of the world. Kitzbuehel: AquaTech Publications.
Huang, Z., & Wang, L. (2018). Yangtze dams increasingly threaten the survival of the Chinese sturgeon. Current Biology, 28(22), 3640-3647.
Hubálek, M., & Flajšhans, M. (2020). Simple field storage of fish samples for measurement of DNA content by flow cytometry. Cytometry Part A, 99(7), 743-752.
Hyndman, C. A., Kieffer, J. D., & Benfey, T. J. (2003). The physiological response of diploid and triploid brook trout to exhaustive exercise. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 134(1), 167-179.
Iegorova, V., Pšenička, M., Lebeda, I., Rodina, M., & Saito, T. (2018). Polyspermy produces viable haploid/diploid mosaics in sturgeon. Biology of Reproduction, 99(4), 695-706.
IPCC (2021). Summary for policymakers. In V. Masson-Delmotte, P. Zhai, A. Pirani, S. L. Connors, C. Péan, S. Berger, et al. (Eds.), Climate change 2021: The physical science basis. Contribution of working group I to the sixth assessment report of the intergovernmental panel on climate change. Cambridge, UK: Cambridge University Press In press.
Kalmykov, V. A., Ruban, G. I., & Pavlov, D. S. (2010). Migrations and resources of sterlet Acipenser ruthenus (Acipenseridae) from the lower reaches of the Volga River. Journal of Ichthyology, 50(1), 44-51.
Kieffer, M., & Kynard, B. (2012). Spawning and non-spawning migrations, spawning, and the effect of river regulation on spawning success of Connecticut River Shortnose sturgeon. In B. Kynard, P. Bronzi, & H. Rosenthal (Eds.), Life history and behaviour of Connecticut River shortnose and other sturgeons (pp. 73-114). Norderstedt: WSCS, Demand GmbH..
Kijima, K., Arai, K., & Suzuki, R. (1996). Induction of allotriploids and allopentaploids in interfamilial hybrids, female spinous loach × male carp and female loach × male carp. Journal of the Faculty of Applied Biological Science-Hiroshima University, 35, 13-26.
Kim, D. S., Nam, Y. K., Noh, J. K., Park, C. H., & Chapman, F. A. (2005). Karyotype of north American shortnose sturgeon Acipenser brevirostrum with the highest chromosome number in the Acipenseriformes. Ichthyological Research, 52(1), 94-97.
King, R. C., & Stansfield, W. D. (1990). A dictionary of genetics (4th ed.). New York, NY: Oxford University Press.
Kirpichnikov, V. S. (1987). Genetics and selection of fishes. Leningrad: Nauka.
Kocour, M. (2013). Testování užitkovosti u ryb a odhad plemenné hodnoty. In M. Flajšhans (Ed.), Genetika a šlechtění ryb (2nd ed., pp. 151-195). FROV JU: Vodňany.
Komen, H., & Thorgaard, G. H. (2007). Androgenesis, gynogenesis and the production of clones in fishes: A review. Aquaculture, 269(1-4), 150-173.
Kubala, M., Farský, M., & Pekárik, L. (2019). Migration patterns of sterlet (Acipenser ruthenus, Linnaeus 1758) in the middle Danube assessed by 1 year acoustic telemetry study. Journal of Applied Ichthyology, 35(1), 54-60.
Lassalle, G., Crouzet, P., Gessner, J., & Rochard, E. (2010). Global warming impacts and conservation responses for the critically endangered European Atlantic sturgeon. Biological Conservation, 143(11), 2441-2452.
Leal, M. J., Van Eenennaam, J. P., Schreier, A. D., & Todgham, A. E. (2019). Triploidy in white sturgeon (Acipenser transmontanus): Effects of acute stress and warm acclimation on physiological performance. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 229, 10-17.
Leal, M. J., Van Eenennaam, J. P., Schreier, A. D., & Todgham, A. E. (2020). Diploid and triploid white sturgeon (Acipenser transmontanus) differ in magnitude but not kinetics of physiological responses to exhaustive exercise at ambient and elevated temperatures. Canadian Journal of Fisheries and Aquatic Sciences, 77(4), 666-673.
Leal, M. J., Van Eenennaam, J. P., Schreier, A. D., & Todgham, A. E. (2021). Reduced growth may be linked to lower aerobic scope in juvenile triploid white sturgeon (Acipenser transmontanus). Aquaculture, 534, 736157.
Lebeda, I., & Flajšhans, M. (2015). Production of tetraploid sturgeons. Journal of Animal Science, 93(8), 3759-3764.
Lebeda, I., Flajšhans, M., Rodina, M., & Gela, D. (2015). Produkce gynogenetických populací jesetera malého. VÚRH JU.: Vodňany.
Lebeda, I., Ráb, P., Majtánová, Z., & Flajšhans, M. (2020). Artificial whole genome duplication in paleopolyploid sturgeons yields highest documented chromosome number in vertebrates. Scientific Reports, 10(1), 1-10.
Lebeda, I., Steinbach, C. H., & Flajšhans, M. (2018). Flow cytometry for assessing the efficacy of interspecific gynogenesis induction in sturgeon. Journal of Fish Biology, 92(6), 1819-1831.
Lecommandeur, D., Haffray, P., & Philippe, L. (1994). Rapid flow cytometry method for ploidy determination in salmonid eggs. Aquaculture Research, 25(3), 345-350.
Lenhardt, M., Jaric, I., Kalauzi, A., & Cvijanovic, G. (2006). Assessment of extinction risk and reasons for decline in sturgeon. Biodiversity and Conservation, 15(6), 1967-1976.
Levin, D. A. (1983). Polyploidy and novelty in flowering plants. The American Naturalist, 122(1), 1-25.
Liu, Z., & Adams, K. L. (2007). Expression partitioning between genes duplicated by polyploidy under abiotic stress and during organ development. Current Biology, 17(19), 1669-1674.
Ludwig, A., Belfiore, N. M., Pitra, C., Svirsky, V., & Jenneckens, I. (2001). Genome duplication events and functional reduction of ploidy levels in sturgeon (Acipenser, Huso and Scaphirhynchus). Genetics, 158(3), 1203-1215.
Mandal, P., Cai, L., Tu, Z., Johnson, D., & Huang, Y. (2016). Effects of acute temperature change on the metabolism and swimming ability of juvenile sterlet sturgeon (Acipenser ruthenus, Linnaeus 1758). Journal of Applied Ichthyology, 32(2), 267-271.
McCombie, H., Lapègue, S., Cornette, F., Ledu, C., & Boudry, P. (2005). Chromosome loss in bi-parental progenies of tetraploid Pacific oyster Crassostrea gigas. Aquaculture, 247(1-4), 97-105.
Moody, M. E., Mueller, L. D., & Soltis, D. E. (1993). Genetic variation and random drift in autotetraploid populations. Genetics, 134(2), 649-657.
Nelson, K. C., & Palmer, M. A. (2007). Stream temperature surges under urbanization and climate change: Data, models, and responses. Journal of the American Water Resources Association, 43(2), 440-452.
Olden, J. D., & Naiman, R. J. (2010). Incorporating thermal regimes into environmental flows assessments: Modifying dam operations to restore freshwater ecosystem integrity. Freshwater Biology, 55(1), 86-107.
Omoto, N., Maebayashi, M., Adachi, S., Arai, K., & Yamauchi, K. (2005). Sex ratios of triploids and gynogenetic diploids induced in the hybrid sturgeon, the bester (Huso huso female× Acipenser ruthenus male). Aquaculture, 245(1-4), 39-47.
Otto, S. P., & Whitton, J. (2000). Polyploid incidence and evolution. Annual Review of Genetics, 34(1), 401-437.
Pankhurst, N. W., & Munday, P. L. (2011). Effects of climate change on fish reproduction and early life history stages. Marine and Freshwater Research, 62(9), 1015-1026.
Piferrer, F., Beaumont, A., Falguière, J. C., Flajšhans, M., Haffray, P., & Colombo, L. (2009). Polyploid fish and shellfish: Production, biology and applications to aquaculture for performance improvement and genetic containment. Aquaculture, 293(3-4), 125-156.
Poff, N. L., Olden, J. D., Merritt, D. M., & Pepin, D. M. (2007). Homogenization of regional river dynamics by dams and global biodiversity implications. Proceedings of the National Academy of Sciences, 104(14), 5732-5737.
Politis, S. N., Mazurais, D., Servili, A., Zambonino-Infante, J. L., Miest, J. J., Sørensen, S. R., … Butts, I. A. (2017). Temperature effects on gene expression and morphological development of European eel, Anguilla anguilla larvae. PLoS One, 12(8), e0182726.
Pörtner, H. (2001). Climate change and temperature-dependent biogeography: Oxygen limitation of thermal tolerance in animals. Naturwissenschaften, 88(4), 137-146.
Pörtner, H. O., & Farrell, A. P. (2008). Physiology and climate change. Science, 322, 690-692.
Pörtner, H. O., & Peck, M. A. (2010). Climate change effects on fishes and fisheries: Towards a cause-and-effect understanding. Journal of Fish Biology, 77(8), 1745-1779.
Pörtner, H. O., Van Dijk, P. L. M., Hardewig, I., & Sommer, A. (2000). Levels of metabolic cold adaptation: Tradeoffs in eurythermal and stenothermal ectotherms. In W. Davison & C. Howard Williams (Eds.), Antarctic ecosystems: Models for wider ecological understanding (pp. 109-122). Christchurch: Caxton Press.
Pörtner, H. O., & Zielinski, S. (1998). Environmental constraints and the physiology of performance in squids. South African Journal of Marine Science, 20(1), 207-221.
Rajkov, J., Shao, Z., & Berrebi, P. (2014). Evolution of polyploidy and functional diploidization in sturgeons: Microsatellite analysis in 10 sturgeon species. Journal of Heredity, 105(4), 521-531.
Rivers-Moore, N. A., Dallas, H. F., & Morris, C. (2013). Towards setting environmental water temperature guidelines: A south African example. Journal of Environmental Management, 128, 380-392.
Rochard, E., Castelnaud, G., & Lepage, M. (1990). Sturgeons (Pisces: Acipenseridae); threats and prospects. Journal of Fish Biology, 37, 123-132.
Rombough, P. J. (1997). The effects of temperature on embryonic and larval development. In C. M. Wood & D. G. McDonald (Eds.), Global warming: Implications for freshwater and marine fish (pp. 177-223). New York, NY: Cambridge University Press..
Rożyński, M., Demska-Zakęś, K., & Fopp-Bayat, D. (2015). Hematological and blood gas profiles of triploid Siberian sturgeon (Acipenser baerii Brandt). Fisheries & Aquatic Life, 23(4), 197-203.
Sakao, S., Fujimoto, T., Kimura, S., Yamaha, E., & Arai, K. (2006). Drastic mortality in tetraploid induction results from the elevation of ploidy in masu salmon Oncorhynchus masou. Aquaculture, 252(2-4), 147-160.
Sambraus, F., Olsen, R. E., Remen, M., Hansen, T. J., Torgersen, T., & Fjelldal, P. G. (2017). Water temperature and oxygen: The effect of triploidy on performance and metabolism in farmed Atlantic salmon (Salmo salar L.) post-smolts. Aquaculture, 473, 1-12.
Schreier, A. D., Gille, D., Mahardja, B., & May, B. (2011). Neutral markers confirm the octoploid origin and reveal spontaneous autopolyploidy in white sturgeon, Acipenser transmontanus. Journal of Applied Ichthyology, 27, 24-33.
Schreier, A. D., Van Eenennaam, J. P., Anders, P., Young, S., & Crossman, J. (2021). Spontaneous autopolyploidy in the Acipenseriformes, with recommendations for management. Reviews in Fish Biology and Fisheries, 31, 159-180.
Shivaramu, S., Lebeda, I., Vuong, D. T., Rodina, M., Gela, D., & Flajšhans, M. (2020). Ploidy levels and fitness-related traits in purebreds and hybrids originating from Sterlet (Acipenser ruthenus) and unusual ploidy levels of Siberian sturgeon (A. baerii). Genes, 11(10), 1164.
Sokolov, L. I., & Vasil'ev, V. P. (1989). Acipenser ruthenus Linnaeus, 1758. In J. Holčík (Ed.), The freshwater fishes of Europe. General introduction to fishes-Acipenseriformes (Vol. I/II, pp. 226-262). Wiesbaden: Aula-Verlag..
Sommer, A., Klein, B., & Pörtner, H. O. (1997). Temperature induced anaerobiosis in two populations of the polychaete worm Arenicola marina (L.). Journal of Comparative Physiology B, 167(1), 25-35.
Van Eenennaam, A. L., Van Eenennaam, J. P., Medrano, J. F., & Doroshov, S. I. (1996). Rapid verification of meiotic gynogenesis and polyploidy in white sturgeon (Acipenser transmontanus Richardson). Aquaculture, 147(3-4), 177-189.
Van Eenennaam, J. P., Fiske, A. J., Leal, M. J., Cooley-Rieders, C., Todgham, A. E., Conte, F. S., & Schreier, A. D. (2020). Mechanical shock during egg de-adhesion and post-ovulatory ageing contribute to spontaneous autopolyploidy in white sturgeon culture (Acipenser transmontanus). Aquaculture, 515, 734530.
Van Eenennaam, J. P., Linares-Casenave, J., Deng, X., & Doroshov, S. I. (2005). Effect of incubation temperature on green sturgeon embryos, Acipenser medirostris. Environmental Biology of Fishes, 72(2), 145-154.
Van Vliet, M. T. H., Ludwig, F., Zwolsman, J. J. G., Weedon, G. P., & Kabat, P. (2011). Global river temperatures and sensitivity to atmospheric warming and changes in river flow. Water Resources Research, 47(2), W02544.
Vandeputte, M., Peignon, E., Vallod, D., Haffray, P., Komen, J., & Chevassus, B. (2002). Comparison of growth performances of three French strains of common carp (Cyprinus carpio) using hemi-isogenic scaly carp as internal control. Aquaculture, 205(1-2), 19-36.
Vasil'ev, V. P. (2009). Mechanisms of polyploid evolution in fish: Polyploidy in sturgeons. In R. Carmona, A. Domezian, M. García-Gallego, & J. A. Hernando (Eds.), Biology, conservation, and sustainable development of sturgeons (pp. 97-117). Berlin: Springer.
Vassetzky, S. G. (1967). Changes in the ploidy of sturgeon larvae induced by heat treatment of eggs at different stages of development. Doklady Akademii Nauk SSSR Biological Science Section, 172, 23-26.
Vindelov, L. L., Christensen, I. J., Keiding, N., Spang-Thomsen, M., & Nissen, N. I. (1983). Long-term storage of samples for flow cytometric DNA analysis. Cytometry, 3(5), 317-322.
Wang, Y. L., Buodington, R. K., & Doroshov, S. I. (1987). Influence of temperature on yolk utilization by the white sturgeon, Acipenser transmontanus. Journal of Fish Biology, 30(3), 263-271.
Webb, B. W., & Nobilis, F. (2007). Long-term changes in river temperature and the influence of climatic and hydrological factors. Hydrological Sciences Journal, 52(1), 74-85.
Wertheim, B., Beukeboom, L. W., & Van de Zande, L. (2013). Polyploidy in animals: Effects of gene expression on sex determination, evolution and ecology. Cytogenetic and Genome Research, 140(2-4), 256-269.
Yin, F., Liu, W., Chai, J., Lu, B., Murphy, R. W., & Luo, J. (2018). CRISPR/Cas9 application for gene copy fate survey of polyploid vertebrates. Frontiers in Genetics, 9, 260.
Zhang, H., Kang, M., Wu, J., Wang, C., Li, J., Du, H., … Wei, Q. (2019). Increasing river temperature shifts impact the Yangtze ecosystem: Evidence from the endangered Chinese sturgeon. Animals, 9(8), 583.
Zhang, Y., & Kieffer, J. D. (2017). The effect of temperature on the resting and post-exercise metabolic rates and aerobic metabolic scope in shortnose sturgeon Acipenser brevirostrum. Fish Physiology and Biochemistry, 43(5), 1245-1252.
Zhou, H., Fujimoto, T., Adachi, S., Yamaha, E., & Arai, K. (2011). Genome size variation estimated by flow cytometry in Acipenser mikadoi, Huso dauricus in relation to other species of Acipenseriformes. Journal of Applied Ichthyology, 27(2), 484-491.
Zubair, S. N., Peake, S. J., Hare, J. F., & Anderson, W. G. (2012). The effect of temperature and substrate on the development of the cortisol stress response in the lake sturgeon, Acipenser fulvescens, Rafinesque (1817). Environmental Biology of Fishes, 93(4), 577-587.