Sex ratio; Sex determination; Animal behavior; Fish physiology; Sexual differentiation; Freshwater fish; fertilization
Abstract :
[en] Nile tilapia (Oreochromis niloticus) is an African freshwater fish that displays a genetic sex determination system (XX|XY) where high temperatures (above 32°C to 36.5°C) induce masculinization. In Nile tilapia, the thermosensitive period was reported from 10 to 30 days post fertilization. In their natural environment, juveniles may encounter high temperatures that are above the optimal temperature for growth (27–30°C). The relevance of the thermal sex reversal mechanism in a natural context remains unclear. The main objective of our study is to determine whether sexually undifferentiated juveniles spontaneously prefer higher, unfavorable temperatures and whether this choice skews the sex ratio toward males. Five full-sib progenies (from 100% XX crosses) were subjected to (1) a horizontal three-compartment thermal step gradient (thermal continuum 28°C– 32°C– 36.5°C) during the thermosensitive period, (2) a control continuum (28°C– 28°C– 28°C) and (3) a thermal control tank (36.5°C). During the first days of the treatment, up to an average of 20% of the population preferred the masculinizing compartment of the thermal continuum (36.5°C) compared to the control continuum. During the second part of the treatment, juveniles preferred the lower, nonmasculinizing 32°C temperature. This short exposure to higher temperatures was sufficient to significantly skew the sex ratio toward males, compared to congeners raised at 28°C (from 5.0 ± 6.7% to 15.6 ± 16.5% of males). The proportion of males was significantly different in the thermal continuum, thermal control tank and control continuum, and it was positively correlated among populations. Our study shows for the first time that Nile tilapia juveniles can choose a masculinizing temperature during a short period of time. This preference is sufficient to induce sex reversal to males within a population. For the first time, behavior is reported as a potential player in the sex determination mechanism of this species.
Research Center/Unit :
GIGA-I3 - Giga-Infection, Immunity and Inflammation - ULiège Centre de Formation et de Recherche en Aquaculture
Disciplines :
Zoology Aquatic sciences & oceanology
Author, co-author :
Nivelle, Renaud ; Université de Liège - ULiège > I3-Laboratory for Organogenesis and Regeneration
Gennotte, Vincent ; Université de Liège - ULiège > Centre de formation et de recherche en aquaculture (CEFRA)
Muller, Marc ; Université de Liège - ULiège > Département des sciences de la vie > I3-Laboratory for Organogenesis and Regeneration
Mélard, Charles ; Université de Liège - ULiège > Centre de formation et de recherche en aquaculture (CEFRA)
Rougeot, Carole ; Université de Liège - ULiège > Centre de formation et de recherche en aquaculture (CEFRA)
Other collaborator :
Kembolo Kalala, Jules; Université de Liège - ULiège > Research and Education Center in Aquaculture (CEFRA) > 2017
Nguyen, Bich Ngoc ; Université de Liège - ULiège > Département ArGEnCo > LEMA (Local environment management and analysis)
Language :
English
Title :
Temperature preference of Nile tilapia (Oreochromis niloticus) juveniles induces spontaneous sex reversal
Publication date :
14 February 2019
Journal title :
PLoS ONE
eISSN :
1932-6203
Publisher :
Public Library of Science, United States - California
FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture F.R.S.-FNRS - Fonds de la Recherche Scientifique ULiège - Université de Liège
Funding text :
RN is a Ph.D. grant holder from FRIA-FNRS (Fond pour la Formation et la Recherche dans l’Industrie et dans l’Agriculture); MM is a "Maître de Recherche" at the "Fonds National de Recherche Scientifique"; ULiège-ARC progam (Actions de Recherches Concertées, ARC 15/19-7).
Capel B. Vertebrate sex determination: Evolutionary plasticity of a fundamental switch. Nat Rev Genet. 2017; 18(11):675–89. https://doi.org/10.1038/nrg.2017.60 PMID: 28804140
Ospina-Álvarez N, Piferrer F. Temperature-dependent sex determination in fish revisited: Prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS One. 2008; 3(7).
Schartl M. Sex chromosome evolution in non-mammalian vertebrates. Vol. 14, Current Opinion in Genetics and Development. 2004. p. 634–41. https://doi.org/10.1016/j.gde.2004.09.005 PMID: 15531158
Devlin RH, Nagahama Y. Sex determination and sex differentiation in fish: An overview of genetic, physiological, and environmental influences. Aquaculture. 2002; 208(3–4):191–364.
Conover DO, Kynard BE. Environmental Sex Determination: Interaction of Temperature and Genotype in a Fish. Science (80-). 1981; 213(4507):577–579.
Ospina-Álvarez N, Piferrer F. Temperature-dependent sex determination in fish revisited: Prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS One. 2008; 3(7):2–4.
Mair GC, Scott AG, Penman DJ, Beardmore JA, Skibinski DOF. Sex determination in the genus Oreochromis—1. Sex reversal, gynogenesis and triploidy in O. niloticus (L.). Theor Appl Genet. 1991; 82 (2):144–52. https://doi.org/10.1007/BF00226205 PMID: 24213058
Wessels S, Krause I, Floren C, Schütz E, Beck J, Knorr C. ddRADseq reveals determinants for temperature-dependent sex reversal in Nile tilapia on LG23. BMC Genomics. 2017 Dec; 18(1).
Kobayashi K. Reproductive and developmental strategies. New York, NY: Springer Berlin Heidelberg; 2018.
Baroiller JF, D’Cotta H, Bezault E, Wessels S, Hoerstgen-Schwark G. Tilapia sex determination: Where temperature and genetics meet. Comp Biochem Physiol—A Mol Integr Physiol. 2009; 153(1):30–8. https://doi.org/10.1016/j.cbpa.2008.11.018 PMID: 19101647
Baroiller, Chourrout D, Fostier A, Jalabert B. Temperature and sex chromosomes govern sex ratios of the mouthbrooding Cichlid fish Oreochromis niloticus. J Exp Zool. 1995; 273(3):216–223.
Bezault E, Clota F, Derivaz M, Chevassus B, Baroiller JF. Sex determination and temperature-induced sex differentiation in three natural populations of Nile tilapia (Oreochromis niloticus) adapted to extreme temperature conditions. Aquaculture. 2007; 272(SUPPL. 1).
Denzer H. Studies on the physiology of young tilapia. FAO Fish Rep. 1967; 44:358–66.
Rougeot C, Prignon C, Ngouana Kengne CV, Mélard C. Effect of high temperature during embryogenesis on the sex differentiation process in the Nile tilapia, Oreochromis niloticus. Aquaculture. 2008; 276 (1–4):205–208.
D’Cotta H, Fostier A, Guiguen Y, Govoroun M, Baroiller JF. Aromatase plays a key role during normal and temperature- induced sex differentiation of Tilapia Oreochromis niloticus. Mol Reprod Dev. 2001; 59(3):265–76. https://doi.org/10.1002/mrd.1031 PMID: 11424212
Trewavas E. Tilapiine fishes of the geneva Sarotherodon, Oreochromis and Danakila. London: British Museum (National History); 1983.
Fry FEJ. The Effect of Environmental Factors on the Physiology of Fish. In: Fish Physiology. Elsevier; 1971. p. 1–98.
Beitinger TL, Fitzpatrick LC. Physiological and ecological correlates of preferred temperature in fish. Integr Comp Biol. 1979 Feb; 19(1):319–29.
Crawshaw LI. Physiological and Behavioral Reactions of Fishes to Temperature Change. J Fish Res Board Canada. 1977; 34(5):730–4.
Azaza MS, Dhraïef MN, Kraïem MM. Effects of water temperature on growth and sex ratio of juvenile Nile tilapia Oreochromis niloticus (Linnaeus) reared in geothermal waters in southern Tunisia. J Therm Biol. 2008; 33(2):98–105.
Baroiller J-F, Chaurrout D, Fostier H, Jalabert B. Temperature and sex chromosomes govern sex ratios of mouth brooding cichlid fish Oreochromis nilotocus. J Exp Zool. 1995; 273(3):213–23.
Santi S, Rougeot C, Toguyeni A, Gennotte V, Kebe I, Melard C. Temperature Preference and Sex Differentiation in African Catfish, Clarias gariepinus. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology. 2017 Jan;28–37.
Nakamura M, Iwahashi M. Studies on the practical masculinization in Tilapia nilotica by the oral administrator of androgen [hormone, diets]. Bull Soc Sci Fish. 1982;
Rakus K, Ronsmans M, Forlenza M, Boutier M, Piazzon MC, Jazowiecka-Rakus J, et al. Conserved Fever Pathways across Vertebrates: A Herpesvirus Expressed Decoy TNF-α Receptor Delays Behavioral Fever in Fish. Cell Host Microbe. 2017 Feb; 21(2):244–53. https://doi.org/10.1016/j.chom. 2017.01.010 PMID: 28182952
Lenth R V. Least-Squares Means: The R Package lsmeans. J Stat Softw. 2016; 69(1).
Wilson K, Hardy ICWW. Statistical analysis of sex ratios: an introduction. Sex ratios: concepts and research methods. 2002. 48–92 p.
Guerrero RD, Shelton WL. An Aceto-Carmine Squash Method for Sexing Juvenile Fishes. Progress Fish-Culturist. 1974; 36(January 2015):56–56.
Wickham H. Ggplot2: elegant graphics for data analysis. New York: Springer; 2009. 212 p. (Use R!).
Santi S, Rougeot C, Toguyeni A, Gennotte V, Kebe I, Melard C. Temperature Preference and Sex Differentiation in African Catfish, Clarias gariepinus. J Exp Zool Part A Ecol Integr Physiol. 2017 Jan; 327 (1):28–37.
Boltana S, Rey S, Roher N, Vargas R, Huerta M, Huntingford FA, et al. Behavioural fever is a synergic signal amplifying the innate immune response. Proc R Soc B Biol Sci. 2013 Jul; 280(1766):20131381–20131381.
Rey S, Digka N, MacKenzie S. Animal Personality Relates to Thermal Preference in Wild-Type Zebrafish, Danio rerio. Zebrafish. 2015; 12(3):243–9. https://doi.org/10.1089/zeb.2014.1076 PMID: 25807204
Cerqueira M, Rey S, Silva T, Featherstone Z, Crumlish M, MacKenzie S. Thermal preference predicts animal personality in Nile tilapia Oreochromis niloticus. Jentoft S, editor. J Anim Ecol. 2016 Sep; 85 (5):1389–400. https://doi.org/10.1111/1365-2656.12555 PMID: 27219014
Rey S, Moiche V, Boltaña S, Teles M, MacKenzie S. Behavioural fever in zebrafish larvae. Dev Comp Immunol. 2017 Feb; 67:287–92. https://doi.org/10.1016/j.dci.2016.09.008 PMID: 27670815
Rey S, Huntingford FA, Boltaña S, Vargas R, Knowles TG, Mackenzie S. Fish can show emotional fever: Stress-induced hyperthermia in zebrafish. Proc R Soc B Biol Sci. 2015; 282(1819):0–6.
Rey S, Huntingford FA, Knowles TG, Mackenzie S. Stress induced hyperthermia in zebrafish: A reply to key et al. Proc R Soc B Biol Sci. 2017 Jan; 284(1847):20162124.
Cerqueira M, Rey S, Silva T, Featherstone Z, Crumlish M, MacKenzie S. Thermal preference predicts animal personality in Nile tilapia Oreochromis niloticus. Jentoft S, editor. J Anim Ecol. 2016 Sep; 85 (5):1389–400. https://doi.org/10.1111/1365-2656.12555 PMID: 27219014
K.B. W. Evaluation of Growth Performance, Feed Utilization Efficiency and Survival Rate of Juvenile Nile tilapia, Oreochromis niloticus (Linnaeus, 1758) Reared at Different Water Temperature. Int J Aquac. 2012;
Britz PJ, Hecht T. Temperature Preferences and Optimum Temperature for Growth of African Sharp-tooth Catfish (Clarias gariepinus) Larvae and Post- larvae. Aquaculture. 1987; 63:205–14.
Jobling M. Temperature tolerance and the final preferendum—rapid methods for the assessment of optimum growth temperatures. J Fish Biol. 1981 Oct; 19(4):439–55.
Baras E. Ontogenetic variations of thermal optimum for growth, and its implication on thermolabile sex determination in blue tilapia. J Fish Biol. 2002 Sep; 61(3):645–60.
Reynolds WW, Casterlin ME, Matthey JK, Millington ST, Ostrowski AC. Diel patterns of preferred temperature and locomotor activity in the goldfish Carassius auratus. Comp Biochem Physiol—Part A Physiol. 1978 Jan; 59(2):225–7.
Reynolds WW, Casterlin ME, Millington ST. Circadian rhythm of preferred temperature in the bowfin Amia calva, a primitive holostean fish. Comp Biochem Physiol—Part A Physiol. 1978; 60(1):107–9.
Reynolds WW, Casterlin ME. Behavioral Thermoregulation and the “Final Preferendum” Paradigm. Am Zool. 1979 Feb; 19(1):211–24.
Muller-Belecke A, Horstgen-Schwark G. Sex determination in tilapia (Oreochromis niloticus) sex ratios in homozygous gynogenetic progeny and their offspring. Aquaculture. 1995; 137(1–4):57–65.
Cnaani A, Lee BY, Zilberman N, Ozouf-Costaz C, Hulata G, Ron M, et al. Genetics of sex determination in tilapiine species. Sex Dev. 2008; 2(1):43–54. https://doi.org/10.1159/000117718 PMID: 18418034
Tessema M, Muller-Belecke A, Horstgen-Schwark G. Effect of rearing temperatures on the sex ratios of Oreochromis niloticus populations. Aquaculture. 2006; 258(1–4):270–277.
Shao C, Li Q, Chen S, Zhang P, Lian J, Hu Q, et al. Epigenetic modification and inheritance in sexual reversal of fish. Genome Res. 2014; 24(4):604–15. https://doi.org/10.1101/gr.162172.113 PMID: 24487721
Piferrer F. Epigenetics of sex determination and gonadogenesis. Dev Dyn. 2013; 242(4):360–70. https://doi.org/10.1002/dvdy.23924 PMID: 23335256
Bruton MN, Boltt RE. Aspects of the biology of Tilapia mossambica Peters (Pisces: Cichlidae) in a natural freshwater lake (Lake Sibaya, South Africa). J Fish Biol. 1975 Jul; 7(4):423–45.
Lodi E. Sex inversion in domesticated strains of the swordtail, Xiphophorus helleri Heckel (Pisces, Osteichthyes). Bolletino di Zool. 1980 Jan; 47(1–2):1–8.
Conover DO. Adaptive Significance of Temperature-Dependent Sex Determination in a Fish. Am Nat. 1984; 123(3):297.
Perrin N. Sex reversal: A fountain of youth for sex chromosomes? Evolution (N Y). 2009; 63(12):3043–9.
Baras E, Prignon C, Gohoungo G, Mélard C. Phenotypic sex differentiation of blue tilapia under constant and fluctuating thermal regimes and its adaptive and evolutionary implications. J Fish Biol. 2000; 57(1):210–23.
