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Thermosensitive period of sex determination in the coral-reef damselfish Acanthochromis polyacanthus and the implications of projected ocean warming

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Abstract

Higher temperatures associated with climate change have the potential to significantly alter the population sex ratio of species with temperature-dependent sex determination. Whether or not elevated temperature affects sex determination depends on both the absolute temperature experienced and the stage of development at which the thermal conditions occur. We explored the importance of exposure timing during early development in the coral reef fish, Acanthochromis polyacanthus, by increasing water temperature 1.5 or 3 °C above the summer average (28.5 °C) at different stages of development. We also measured the effect of treatment temperature on fish size and condition, in order to gauge how the thermal threshold for sex-ratio bias may compare with other commonly considered physiological metrics. Increasing grow-out temperature from 28.5 to 30 °C had no effect on the sex ratio of offspring, whereas an increase to 31.5 °C (+3 °C) produced a strong male bias (average ~90%). The thermosensitive period for this species lasted between 25 and 60 d post hatching, with the bias in sex ratio greater the earlier that fish experienced warm conditions. Temperatures high enough to bias the sex ratio are likely to be seen first during late summer (January and February) and would affect clutches produced late in the breeding season. There was no change to fish condition in response to temperature; however, the two higher temperature treatments produced significantly smaller fish at sampling. Clutches produced early in the season could buffer the population from a skewed sex ratio, as their development will remain below the thermal threshold; however, continued ocean warming could mean that clutches produced earlier in the breeding season would also be affected in the longer term. A skewed sex ratio could be detrimental to population viability by reducing the number of females in the breeding population.

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References

  • Angelopoulou R, Lavranos G, Manolakou P (2012) Sex determination strategies in 2012: towards a common regulatory model? Reprod Biol Endocrinol 10:13

    Article  PubMed  PubMed Central  Google Scholar 

  • Baroiller JF, Toguyeni A (1996) Comparative effects of a natural steroid, 11αβ-hydroxy- androstenedione (11αβ-OH-D4) and a synthetic androgen, 17αα-methyltestosterone (17αα-MT) on sex-ratio in Oreochromis niloticus. In: Pullin RSV, Lazard J, Legendre M, Amon Kothias JB, Pauly D (eds.), Third International Symposium on Tilapia in Aquaculture. Abidjan, Côte d’Ivoire, pp. 344–351

  • Baroiller JF, D’Cotta H (2001) Environment and sex determination in farmed fish. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 130:399–409

    Article  CAS  Google Scholar 

  • Baroiller JF, Guiguen Y, Fostier A (1999) Endocrine and environmental aspects of sex differentiation in fish. Cell Mol Life Sci 55:910–931

    Article  CAS  Google Scholar 

  • Baroiller JF, Chourrout D, Fostier A, Jalabert B (1995) Temperature and sex chromosomes govern sex ratios of the mouthbrooding cichlid fish Oreochromis niloticus. J Exp Zool A Ecol Genet Physiol 273:216–223

    Google Scholar 

  • Bull JJ, Vogt RC (1981) Temperature-sensitive periods of sex determination in emydid turtles. J Exp Zool A Ecol Genet Physiol 218:435–440

    CAS  Google Scholar 

  • Charnov EL, Bull J (1977) When is sex environmentally determined? Nature 266:828–830

    Article  CAS  PubMed  Google Scholar 

  • Ciofi C, Swingland IR (1997) Environmental sex determination in reptiles. Appl Anim Behav Sci 51:251–265

    Article  Google Scholar 

  • Collins M, Knutti R, Arblaster J, Dufresne J-L, Fichefet T, Friedlingstein P, Gao X, Gutowski WJ, Johns T, Krinner G, Shongwe M, Tebaldi C, Weaver AJ, Wehner M (2013) Long-term climate change: projections, commitments and irreversibility. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds.) Climate Change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, United Kingdom and New York

  • Conover DO (1984) Adaptive significance of temperature-dependent sex determination in a fish. Am Nat 123:297–313

    Article  Google Scholar 

  • Conover DO, Fleisher MH (1986) Temperature-sensitive period of sex determination in the Atlantic silverside Menidia menidia. Can J Fish Aquat Sci 43:514–520

    Article  Google Scholar 

  • Craig JK, Foote CJ, Wood CC (1996) Evidence for temperature-dependent sex determination in sockeye salmon (Oncorhynchus nerka). Can J Fish Aquat Sci 53:141–147

    Article  Google Scholar 

  • Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364

    Article  CAS  Google Scholar 

  • Doherty PJ, Mather P, Planes S (1994) Acanthochromis polyacanthus, a fish lacking larval dispersal, has genetically differentiated populations at local and regional scales on the Great Barrier Reef. Mar Biol 121:11–21

    Article  Google Scholar 

  • Donelson JM, Munday PL (2015) Transgenerational plasticity mitigates the impact of global warming to offspring sex ratios. Glob Chang Biol 21:2954–2962

    Article  PubMed  Google Scholar 

  • Godwin J, Luckenbach JA, Borski RJ (2003) Ecology meets endocrinology: environmental sex determination in fishes. Evol Dev 5:40–49

    Article  PubMed  Google Scholar 

  • Hawkes LA, Broderick AC, Godfrey MH, Godley BJ (2007) Investigating the potential impacts of climate change on a marine turtle population. Glob Chang Biol 13:923–932

    Article  Google Scholar 

  • Hayes TB (1998) Sex determination and primary sex differentiation in amphibians: genetic and developmental mechanisms. J Exp Zool A Ecol Genet Physiol 281:373–399

    CAS  Google Scholar 

  • Janzen FJ (1994) Climate change and temperature-dependent sex determination in reptiles. Proc Natl Acad Sci U S A 91:7487–7490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janzen FJ, Paukstis GL (1991) Environmental sex determination in reptiles: ecology, evolution, and experimental design. Q Rev Biol 66:149–179

    Article  CAS  PubMed  Google Scholar 

  • Kavanagh KD (2000) Larval brooding in the marine damselfish Acanthochromis polyacanthus (Pomacentridae) is correlated with highly divergent morphology, ontogeny and life-history traits. Bull Mar Sci 66:321–337

    Google Scholar 

  • Korpelainen H (1990) Sex ratios and conditions required for environmental sex determination in animals. Biol Rev Camb Philos Soc 65:147–184

    Article  CAS  PubMed  Google Scholar 

  • Koumoundouros G, Pavlidis M, Anezaki L, Kokkari C, Sterioti A, Divanach P, Kentouri M (2002) Temperature sex determination in the European sea bass, Dicentrarchus labrax (L., 1758) (Teleostei, Perciformes, Moronidae): critical sensitive ontogenetic phase. J Exp Zool A Ecol Genet Physiol 292:573–579

    Google Scholar 

  • Laloë J, Cozens J, Renom B, Taxonera A, Hays GC (2014) Effects of rising temperature on the viability of an important sea turtle rookery. Nat Clim Chang 4:513–518

    Article  Google Scholar 

  • Legrand JJ, Legrand-Hamelin E, Juchault P (1987) Sex determination in Crustacea. Biol Rev Camb Philos Soc 62:439–470

    Article  Google Scholar 

  • Milner-Gulland EJ, Bukreeva OM, Coulson T, Lushchekina AA, Kholodova MV, Bekenov AB, Grachev IA (2003) Reproductive collapse in saiga antelope harems. Nature 422: 135–135

  • Munday PL, Kingsford MJ, O’Callaghan M, Donelson JM (2008) Elevated temperature restricts growth potential of the coral reef fish Acanthochromis polyacanthus. Coral Reefs 27:927–931

    Article  Google Scholar 

  • Navarro-Martin L, Viñas J, Ribas L, Díaz N, Gutiérre A, Di Croce L, Piferrer F (2011) DNA methylation of the gonadal aromatase (cyp19a) promoter is involved in temperature- dependent sex ratio shifts in the European sea bass. PLoS Genet 7:e1002447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ospina-Álvarez N, Piferrer F (2008) Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS One 3:e2837

    Article  PubMed  PubMed Central  Google Scholar 

  • Patiño R, Davis KB, Schoore JE, Uguz C, Strüssmann CA, Parker NC, Simco BA, Goudie CA (1996) Sex differentiation of channel catfish gonads: normal development and effects of temperature. J Exp Zool A Ecol Genet Physiol 276:209–218

    Google Scholar 

  • Ramsey M, Crews D (2009) Steroid signaling and temperature-dependent sex determination – reviewing the evidence for early action of estrogen during ovarian determination in the red-eared slider turtle (Trachemys scripta elegans). Semin Cell Dev Biol 20:283–292

    Article  CAS  PubMed  Google Scholar 

  • Randall JE, Allen RA, Steene RC (1997) Fishes of the Great Barrier Reef and Coral Sea. Crawford House Press, Bathurst

    Google Scholar 

  • Robertson DR (1973) Field observations on the reproductive behaviour of a pomacentrid fish, Acanthochromis polyacanthus. Z Tierpsychol 32:319–324

    Article  CAS  PubMed  Google Scholar 

  • Römer U, Beisenherz W (1996) Environmental determination of sex in Apistogramma (Cichlidae) and two other freshwater fishes (Teleostei). J Fish Biol 48:714–725

    Google Scholar 

  • Schwanz LE, Janzen FJ (2008) Climate change and temperature-dependent sex determination: can individual plasticity in nesting phenology prevent extreme sex ratios? Physiol Biochem Zool 81:826–834

    Article  PubMed  Google Scholar 

  • Strüssmann CA, Saito T, Usui M, Yamada H, Takashima F (1997) Thermal thresholds and critical period of thermolabile sex determination in two atherinid fishes, Odontesthes bonariensis and Patagonina hatcheri. J Exp Zool A Ecol Genet Physiol 278:167–177

    Google Scholar 

  • Thresher RE (1983) Habitat effects on reproductive success in the coral reef fish, Acanthochromis polyacanthus (Pomacentridae). Ecology 64:1184–1199

    Article  Google Scholar 

  • Valenzuela N, Lance V (eds) (2004) Temperature-dependent sex determination in vertebrates. Smithsonian Books, Washington, DC

    Google Scholar 

  • Wang LH, Tsai CL (2000) Effects of temperature on the deformity and sex differentiation of tilapia, Oreochromis mossambicus. J Exp Biol 286:534–537

    CAS  Google Scholar 

  • Wright LI, Stokes KL, Fuller WJ, Godley BJ, McGowan A, Snape R, Tregenza T, Broderick AC (2012) Turtle mating patterns buffer against disruptive effects of climate change. Proc R Soc Lond B Biol Sci 279:2122–2127

    Article  Google Scholar 

  • Yamamoto E (1999) Studies on sex-manipulation and production of cloned populations in hirame, Paralichthys olivaceus (Temminck et Schlegel). Aquaculture 173:235–246

    Article  Google Scholar 

  • Yntema CL, Mrosovsky N (1982) Critical periods and pivotal temperatures for sexual differentiation in loggerhead sea turtles. Can J Zool 60:1012–1016

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by the ARC Centre of Excellence for Coral Reef Studies. Thank you to Shannon McMahon and staff at JCU Research Aquarium Facility for logistical support. We also thank three anonymous reviewers for their valuable feedback during the development of this manuscript. This project was completed under JCU Ethics A2055.

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Correspondence to G. G. Rodgers.

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Communicated by Biology Editor Dr. Line K. Bay

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Rodgers, G.G., Donelson, J.M. & Munday, P.L. Thermosensitive period of sex determination in the coral-reef damselfish Acanthochromis polyacanthus and the implications of projected ocean warming. Coral Reefs 36, 131–138 (2017). https://doi.org/10.1007/s00338-016-1496-y

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