{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,20]],"date-time":"2026-03-20T18:53:13Z","timestamp":1774032793882,"version":"3.50.1"},"reference-count":75,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2022,11,22]],"date-time":"2022-11-22T00:00:00Z","timestamp":1669075200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100005416","name":"The Research Council of Norway","doi-asserted-by":"publisher","award":["286597"],"award-info":[{"award-number":["286597"]}],"id":[{"id":"10.13039\/501100005416","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005416","name":"The Research Council of Norway","doi-asserted-by":"publisher","award":["309288"],"award-info":[{"award-number":["309288"]}],"id":[{"id":"10.13039\/501100005416","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005416","name":"The Research Council of Norway","doi-asserted-by":"publisher","award":["280782"],"award-info":[{"award-number":["280782"]}],"id":[{"id":"10.13039\/501100005416","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005416","name":"FREMAD","doi-asserted-by":"publisher","award":["286597"],"award-info":[{"award-number":["286597"]}],"id":[{"id":"10.13039\/501100005416","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005416","name":"FREMAD","doi-asserted-by":"publisher","award":["309288"],"award-info":[{"award-number":["309288"]}],"id":[{"id":"10.13039\/501100005416","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005416","name":"FREMAD","doi-asserted-by":"publisher","award":["280782"],"award-info":[{"award-number":["280782"]}],"id":[{"id":"10.13039\/501100005416","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005416","name":"KABIS","doi-asserted-by":"publisher","award":["286597"],"award-info":[{"award-number":["286597"]}],"id":[{"id":"10.13039\/501100005416","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005416","name":"KABIS","doi-asserted-by":"publisher","award":["309288"],"award-info":[{"award-number":["309288"]}],"id":[{"id":"10.13039\/501100005416","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005416","name":"KABIS","doi-asserted-by":"publisher","award":["280782"],"award-info":[{"award-number":["280782"]}],"id":[{"id":"10.13039\/501100005416","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Fishes"],"abstract":"<jats:p>Sexual maturation of post-smolts is a concern for Atlantic salmon producers, and its occurrence is dependent upon factors such as water temperature and energy availability, among others. The present study was designed to investigate the effect of different temperatures and feeding regimes on testis development and local regulation of spermatogenesis in salmon post-smolts. A 3 \u00d7 2 factorial design was used, with three temperatures (8 \u00b0C, 12.5 \u00b0C, and 18 \u00b0C) and two feed regimes (100% and 67% ration). Salmon (1800 parr, initial mean weight 23.1 \u00b1 7.2 g) were reared from 28 October 2018 to 30 May 2019 in a freshwater flow-through system under continuous light (LD24:0), except for a 5-week winter signal (LD12:12) introduced on 4 February 2019. Testis histology, transcription of follicle-stimulating hormone receptor (fshr) and luteinizing hormone receptor (lhr), and transcription of testis proteins involved in spermatogenesis regulation such as gonadal-soma-derived factors 1 (gsdf1) and 2 (gsdf2), anti-M\u00fcllerian hormone (amh), and insulin-like growth factor-3 (igf3), were analyzed. Results showed that high temperature alone (18 \u00b0C), irrespective of the feed regime, promoted early presence of type B spermatogonia and reduced transcript levels of the proliferation-inhibitory factor amh in males still considered immature, of groups 18\u2013100% and 18\u201367% that later matured in high proportion (~100%). This effect was also present to some degree in the group 12.5\u2013100% (40% maturation), and absent in 12.5\u201367%, 8\u2013100%, and 8\u201367% (groups with little or no maturation). Later, at onset of rapid testis growth, high temperature was linked to a pronounced downregulation of amh and of the self-renewal factors gsdf1 and gsdf2, as well as to a pronounced upregulation of the proliferation-stimulating factor igf3. Overall, the present findings demonstrate that rearing salmon at high temperatures can stimulate an early activation of the brain\u2013pituitary\u2013gonad axis before actual onset of rapid testis growth, enhancing and accelerating the mechanisms that control initiation and progression of maturation, while the feed regime has a minor impact. This poses a challenge for current salmon aquaculture practices that use sustained high temperature to maximize growth, since these practices increase the risk of early post-smolt maturation.<\/jats:p>","DOI":"10.3390\/fishes7060341","type":"journal-article","created":{"date-parts":[[2022,11,23]],"date-time":"2022-11-23T02:55:51Z","timestamp":1669172151000},"page":"341","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Constant High Temperature Promotes Early Changes in Testis Development Associated with Sexual Maturation in Male Atlantic Salmon (Salmo salar L.) Post-Smolts"],"prefix":"10.3390","volume":"7","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5202-5144","authenticated-orcid":false,"given":"Enrique","family":"Pino Martinez","sequence":"first","affiliation":[{"name":"Department of Biological Sciences, University of Bergen, High Technology Centre, 5020 Bergen, Norway"}]},{"given":"Markus F\u00f8rde","family":"Braanaas","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, University of Bergen, High Technology Centre, 5020 Bergen, Norway"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9365-6775","authenticated-orcid":false,"given":"Pablo","family":"Balseiro","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, University of Bergen, High Technology Centre, 5020 Bergen, Norway"}]},{"given":"Marianne","family":"Kraugerud","sequence":"additional","affiliation":[{"name":"Pharmaq Analytiq, Harbitzall\u00e9en 2A, 0275 Oslo, Norway"}]},{"given":"Cindy","family":"Pedrosa","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, University of Bergen, High Technology Centre, 5020 Bergen, Norway"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0077-8077","authenticated-orcid":false,"given":"Albert Kjartan Dagbjartarson","family":"Imsland","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, University of Bergen, High Technology Centre, 5020 Bergen, Norway"},{"name":"Akvaplan-Niva Iceland Office, Akralind 4, 201 K\u00f3pavogur, Iceland"}]},{"given":"Sigurd O.","family":"Handeland","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, University of Bergen, High Technology Centre, 5020 Bergen, Norway"}]}],"member":"1968","published-online":{"date-parts":[[2022,11,22]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.cbpa.2019.03.011","article-title":"Termination of puberty in out-of-season male Atlantic salmon smolts","volume":"232","author":"Fraser","year":"2019","journal-title":"Comp. Biochem. Physiol. Part A Mol. Integr. Physiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12863-020-00927-2","article-title":"Development of supermale and all-male Atlantic salmon to research the vgll3 allele\u2014Puberty link","volume":"21","author":"Fjelldal","year":"2020","journal-title":"BMC Genet."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1111\/jwas.12342","article-title":"A Review of Factors Influencing Maturation of Atlantic Salmon, Salmo salar, with Focus on Water Recirculation Aquaculture System Environments","volume":"47","author":"Good","year":"2016","journal-title":"J. World Aquac. Soc."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/S0044-8486(03)00125-X","article-title":"Photoperiodic effects on precocious maturation, growth and smoltification in Atlantic salmon, Salmo salar","volume":"222","author":"Berrill","year":"2003","journal-title":"Aquaculture"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/j.aquaculture.2010.12.004","article-title":"Reduced daylength stimulates size-dependent precocious maturity in 0+ male Atlantic salmon parr","volume":"311","author":"Skilbrei","year":"2011","journal-title":"Aquaculture"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1139\/f91-052","article-title":"Role of Fat Stores in the Maturation of Male Atlantic Salmon (Salmo salar) Parr","volume":"48","author":"Rowe","year":"1991","journal-title":"Can. J. Fish. Aquat. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1016\/j.aquaculture.2007.08.039","article-title":"Risk factors for early sexual maturation in Atlantic salmon in seawater farms in New Brunswick and Nova Scotia, Canada","volume":"272","author":"McClure","year":"2007","journal-title":"Aquaculture"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1","DOI":"10.14814\/phy2.13809","article-title":"Sexual maturation and smoltification in domesticated Atlantic salmon (Salmo salar L.)\u2014Is there a developmental conflict?","volume":"6","author":"Fjelldal","year":"2018","journal-title":"Physiol. Rep."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.aquaculture.2011.08.017","article-title":"Continuous light and elevated temperature can trigger maturation both during and immediately after smoltification in male Atlantic salmon (Salmo salar)","volume":"321","author":"Fjelldal","year":"2011","journal-title":"Aquaculture"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1331","DOI":"10.1007\/s10499-014-9750-1","article-title":"Photoperiod and temperature effects on growth and maturation of pre- and post-smolt Atlantic salmon","volume":"22","author":"Imsland","year":"2014","journal-title":"Aquac. Int."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"738877","DOI":"10.1016\/j.aquaculture.2022.738877","article-title":"Interaction of temperature and feed ration on male postsmolt maturation of Atlantic salmon (Salmo salar L.)","volume":"562","author":"Balseiro","year":"2023","journal-title":"Aquaculture"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"285","DOI":"10.3354\/meps335285","article-title":"Maturation responses of salmonids to changing developmental opportunities","volume":"335","author":"Thorpe","year":"2007","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1016\/j.ygcen.2009.05.004","article-title":"Control of puberty in farmed fish","volume":"165","author":"Taranger","year":"2010","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"844","DOI":"10.2331\/fishsci.65.844","article-title":"Changes in Immunoglobulin Producing Cells in Response to Gonadal Maturation in Rainbow Trout","volume":"65","author":"Hou","year":"1999","journal-title":"Fish. Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/S0165-2427(00)00235-X","article-title":"Modulation of the fish immune system by hormones","volume":"77","author":"Harris","year":"2000","journal-title":"Veter Immunol. Immunopathol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1733","DOI":"10.1139\/z89-248","article-title":"Androgens impair seawater adaptability in smolting Baltic salmon (Salmo salar)","volume":"67","author":"Lundqvist","year":"1989","journal-title":"Can. J. Zool."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1016\/j.ygcen.2005.01.015","article-title":"Endocrine disruption of parr-smolt transformation and seawater tolerance of Atlantic salmon by 4-nonylphenol and 17\u03b2-estradiol","volume":"142","author":"McCormick","year":"2005","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_18","first-page":"121","article-title":"Photoperiod manipulation can stimulate or inhibit pubertal testis maturation in Atlantic salmon (Salmo salar)","volume":"31","author":"Schulz","year":"2006","journal-title":"Anim. Reprod."},{"key":"ref_19","unstructured":"Shrimpton, J.M. (2013). Seawater to Freshwater Transitions in Diadromous Fishes. Fish Physiology, Elsevier."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"260","DOI":"10.4172\/2155-9546.1000260","article-title":"The Impact of Water Exchange Rate and Treatment Processes on Water-Borne Hormones in Recirculation Aquaculture Systems Containing Sexually Maturing Atlantic Salmon Salmo salar","volume":"05","author":"Good","year":"2014","journal-title":"J. Aquac. Res. Dev."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/S0044-8486(01)00583-X","article-title":"The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin","volume":"197","author":"Bromage","year":"2001","journal-title":"Aquaculture"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1111\/j.1095-8649.2009.02484.x","article-title":"Temperature and salmonid reproduction: Implications for aquaculture","volume":"76","author":"Pankhurst","year":"2010","journal-title":"J. Fish Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.aquaculture.2008.06.042","article-title":"The effect of temperature and fish size on growth, feed intake, food conversion efficiency and stomach evacuation rate of Atlantic salmon post-smolts","volume":"283","author":"Handeland","year":"2008","journal-title":"Aquaculture"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1111\/j.1365-2656.2012.02022.x","article-title":"Effects of temperature and food quality on age and size at maturity in ectotherms: An experimental test with Atlantic salmon","volume":"82","author":"Jonsson","year":"2012","journal-title":"J. Anim. Ecol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/0044-8486(89)90483-3","article-title":"Photoperiod and temperature effects on early development and reproductive investment in Atlantic salmon (Salmo salar L.)","volume":"79","author":"Adams","year":"1989","journal-title":"Aquaculture"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1530\/JOE-13-0240","article-title":"Salinity and photoperiod modulate pubertal development in Atlantic salmon (Salmo salar)","volume":"220","author":"Melo","year":"2013","journal-title":"J. Endocrinol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"738772","DOI":"10.1016\/j.aquaculture.2022.738772","article-title":"Atlantic salmon male post-smolt maturation can be reduced by using a 3-hour scotophase to induce smoltification","volume":"562","author":"Fraser","year":"2022","journal-title":"Aquaculture"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1111\/j.1365-2109.1994.tb00668.x","article-title":"Reproductive strategies in Atlantic salmon, Salmo salar L.","volume":"25","author":"Thorpe","year":"1994","journal-title":"Aquac. Res."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"McCormick, S.D. (2012). Smolt Physiology and Endocrinology, Fish Physiology, Elsevier.","DOI":"10.1016\/B978-0-12-396951-4.00005-0"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1007\/BF00367308","article-title":"Increased daylength stimulates plasma growth hormone and gill Na+, K+-ATPase in Atlantic salmon (Salmo salar)","volume":"165","author":"McCormick","year":"1995","journal-title":"J. Comp. Physiol. B"},{"key":"ref_31","unstructured":"Finn, R.N., and Kapoor, B.G. (2008). Smoltification. Fish Larval Physiology, Science Publishers."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Zydlewski, J., and Wilkie, M.P. (2013). Freshwater to Seawater Transitions in Migratory Fishes, Fish Physiology, Elsevier.","DOI":"10.1016\/B978-0-12-396951-4.00006-2"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Yaron, Z., Levavi-Sivan, B., Yaron, Z., and Levavi-Sivan, B. (2011). Hormonal control of reproduction and growth | Endocrine Regulation of Fish Reproduction, Encyclopedia of Fish Physiology, Elsevier.","DOI":"10.1016\/B978-0-12-374553-8.00058-7"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1016\/j.ygcen.2009.04.017","article-title":"Neuroendocrinology of reproduction in teleost fish","volume":"165","author":"Zohar","year":"2010","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1002\/mrd.20767","article-title":"Expression of gonadotropin and gonadotropin receptor genes during early sexual maturation in male Atlantic salmon parr","volume":"75","author":"Maugars","year":"2008","journal-title":"Mol. Reprod. Dev."},{"key":"ref_36","first-page":"1","article-title":"Entry into puberty is reflected in changes in hormone production but not in testicular receptor expression in Atlantic salmon (Salmo salar)","volume":"17","author":"Schulz","year":"2019","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1016\/j.ygcen.2009.02.013","article-title":"Spermatogenesis in fish","volume":"165","author":"Schulz","year":"2010","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1095\/biolreprod.105.039891","article-title":"Sertoli Cell Proliferation in the Adult Testis\u2014Evidence from Two Fish Species Belonging to Different Orders1","volume":"73","author":"Schulz","year":"2005","journal-title":"Biol. Reprod."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Crespo, D., Bogerd, J., Sambroni, E., LeGac, F., Andersson, E., Edvardsen, R.B., Bergman, E.J., Bj\u00f6rnsson, B.T., Taranger, G.L., and Schulz, R.W. (2019). The initiation of puberty in Atlantic salmon brings about large changes in testicular gene expression that are modulated by the energy status. BMC Genom., 20.","DOI":"10.1186\/s12864-019-5869-9"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"3804","DOI":"10.1210\/en.2015-1157","article-title":"Fsh Stimulates Spermatogonial Proliferation and Differentiation in Zebrafish via Igf3","volume":"156","author":"Morais","year":"2015","journal-title":"Endocrinology"},{"key":"ref_41","unstructured":"Schulz, R.W., and Nobrega, R.H. (2011). Anatomy and Histology of Fish Testis. Encyclopedia of Fish Physiology: From Genome to Environment, Elsevier."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1530\/JME-12-0197","article-title":"Fsh and Lh have common and distinct effects on gene expression in rainbow trout testis","volume":"50","author":"Sambroni","year":"2013","journal-title":"J. Mol. Endocrinol."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Zheng, S., Long, J., Liu, Z., Tao, W., and Wang, D. (2018). Identification and Evolution of TGF-\u03b2 Signaling Pathway Members in Twenty-Four Animal Species and Expression in Tilapia. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19041154"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2689","DOI":"10.1242\/dev.129.11.2689","article-title":"Spermatogenesis-preventing substance in Japanese eel","volume":"129","author":"Miura","year":"2002","journal-title":"Development"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/j.mce.2016.08.033","article-title":"Expression profiling identifies Sertoli and Leydig cell genes as Fsh targets in adult zebrafish testis","volume":"437","author":"Crespo","year":"2016","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.ygcen.2015.09.025","article-title":"The role of Amh signaling in teleost fish\u2014Multiple functions not restricted to the gonads","volume":"223","author":"Pfennig","year":"2015","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"3527","DOI":"10.1210\/en.2010-1469","article-title":"Proteolytically Activated, Recombinant Anti-M\u00fcllerian Hormone Inhibits Androgen Secretion, Proliferation, and Differentiation of Spermatogonia in Adult Zebrafish Testis Organ Cultures","volume":"152","author":"Skaar","year":"2011","journal-title":"Endocrinology"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.ygcen.2013.06.010","article-title":"Isolation and characterization of Ff1 and Gsdf family genes in European sea bass and identification of early gonadal markers of precocious puberty in males","volume":"191","author":"Crespo","year":"2013","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Kleppe, L., Edvardsen, R.B., Furmanek, T., Andersson, E., Skaftnesmo, K.O., Segafredo, F.T., and Wargelius, A. (2020). Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon. BMC Genom., 21.","DOI":"10.1186\/s12864-020-6513-4"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1016\/j.ydbio.2006.10.001","article-title":"A novel transforming growth factor-\u03b2 superfamily member expressed in gonadal somatic cells enhances primordial germ cell and spermatogonial proliferation in rainbow trout (Oncorhynchus mykiss)","volume":"301","author":"Sawatari","year":"2007","journal-title":"Dev. Biol."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Sambroni, E., Lareyre, J.-J., and Le Gac, F. (2013). Fsh Controls Gene Expression in Fish both Independently of and through Steroid Mediation. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0076684"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1016\/j.bbrc.2007.12.136","article-title":"Discovery of a gonad-specific IGF subtype in teleost","volume":"367","author":"Wang","year":"2008","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1007\/s10695-008-9252-z","article-title":"An overview of functional and stereological evaluation of spermatogenesis and germ cell transplantation in fish","volume":"35","author":"Batlouni","year":"2009","journal-title":"Fish Physiol. Biochem."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1023\/B:FISH.0000030523.16010.62","article-title":"Spermatogenesis in teleost: Insights from the Nile tilapia (Oreochromis niloticus) model","volume":"28","author":"Vilela","year":"2003","journal-title":"Fish Physiol. Biochem."},{"key":"ref_55","first-page":"747","article-title":"The influence of increased water temperature on the duration of spermatogenesis in a neotropical fish, Astyanax altiparanae (Characiformes, Characidae)","volume":"47","author":"Rodrigues","year":"2020","journal-title":"Fish Physiol. Biochem."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.ygcen.2014.04.033","article-title":"Regulation of the seasonal leptin and leptin receptor expression profile during early sexual maturation and feed restriction in male Atlantic salmon, Salmo salar L., parr","volume":"204","author":"Trombley","year":"2014","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_57","unstructured":"Chomczynski, P. (1993). A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques, 15."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Pfaffl, M. (2001). Development and Validation of an Externally Standardised Quantitative Insulin-like Growth Factor-1 RT-PCR Using LightCycler SYBR Green I Technology. Rapid Cycle Real-Time PCR, Springer.","DOI":"10.1007\/978-3-642-59524-0_30"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.ygcen.2019.05.010","article-title":"Evaluation of endocrine and transcriptomic markers of male maturation in winter-run steelhead trout (Oncorhynchus mykiss)","volume":"281","author":"Middleton","year":"2019","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2199-6-21","article-title":"Evaluation of potential reference genes in real-time RT-PCR studies of Atlantic salmon","volume":"6","author":"Olsvik","year":"2005","journal-title":"BMC Mol. Biol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"2731","DOI":"10.1093\/molbev\/msr121","article-title":"MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods","volume":"28","author":"Tamura","year":"2011","journal-title":"Mol. Biol. Evol."},{"key":"ref_62","unstructured":"Fox, J., and Weisberg, S. (2019). An R Companion to Applied Regression, Sage Publications. [3rd ed.]."},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis, Springer.","DOI":"10.1007\/978-3-319-24277-4_9"},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Kassambara, A. (2017). ggpubr: \u201cggplot2\u201d based publication ready plots. R Package Version 0.2, CRAN.","DOI":"10.32614\/CRAN.package.ggpubr"},{"key":"ref_65","unstructured":"Hope, R.M. (2013). Rmisc: Ryan miscellaneous. R Package version 1.5, CRAN."},{"key":"ref_66","first-page":"3","article-title":"Emmeans: Estimated marginal means, aka least-squares means","volume":"1","author":"Lenth","year":"2018","journal-title":"R Packag. Version"},{"key":"ref_67","unstructured":"Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., Heisterkamp, S., Van Willigen, B., and Maintainer, R. (Package \u2018nlme.\u2019 Linear nonlinear Mix. Eff. Model, 2017). Package \u2018nlme.\u2019 Linear nonlinear Mix. Eff. Model, Version 3."},{"key":"ref_68","unstructured":"Christensen, R.H.B. (2019). \u201cordinal\u201d\u2014Regression Models for Ordinal Data. R Package Version. Comput. Softw., 10\u201312."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"737086","DOI":"10.1016\/j.aquaculture.2021.737086","article-title":"Sexual maturation in Atlantic salmon male parr may be triggered both in late summer and early spring under standard farming conditions","volume":"544","author":"Ciani","year":"2021","journal-title":"Aquaculture"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.gene.2010.10.014","article-title":"The gsdf gene locus harbors evolutionary conserved and clustered genes preferentially expressed in fish previtellogenic oocytes","volume":"472","author":"Gautier","year":"2011","journal-title":"Gene"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fcell.2021.684352","article-title":"Evolution, Expression, and Function of Gonadal Somatic Cell-Derived Factor","volume":"9","author":"Hsu","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_72","first-page":"202","article-title":"Two new TGF beta members are restricted to the gonad and differentially expressed during sex differentiation and gametogenesis in trout","volume":"32","author":"Lareyre","year":"2008","journal-title":"Cybium"},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Graziano, M., Benito, R., Planas, J.V., and Palstra, A.P. (2018). Swimming exercise to control precocious maturation in male seabass (Dicentrarchus labrax). BMC Dev. Biol., 18.","DOI":"10.1186\/s12861-018-0170-8"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1095\/biolreprod.111.096248","article-title":"Insulin-Like Growth Factor 3 Regulates Expression of Genes Encoding Steroidogenic Enzymes and Key Transcription Factors in the Nile Tilapia Gonad1","volume":"86","author":"Li","year":"2012","journal-title":"Biol. Reprod."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"4921","DOI":"10.1007\/s00018-019-03439-0","article-title":"Regulation of spermatogenesis and reproductive capacity by Igf3 in tilapia","volume":"77","author":"Li","year":"2020","journal-title":"Cell. Mol. Life Sci."}],"container-title":["Fishes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2410-3888\/7\/6\/341\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:24:35Z","timestamp":1760145875000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2410-3888\/7\/6\/341"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,11,22]]},"references-count":75,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["fishes7060341"],"URL":"https:\/\/doi.org\/10.3390\/fishes7060341","relation":{},"ISSN":["2410-3888"],"issn-type":[{"value":"2410-3888","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,11,22]]}}}