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Modeling Temperature-Dependent Sex Determination in Oviparous Species Using a Dynamical Systems Approach

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Abstract

In many oviparous species, the incubation temperature of the egg determines the sex of the offspring. This is known as temperature-dependent sex determination (TSD). The probability of the hatched offspring being male or female varies across the incubation temperature range. This leads to the appearance of different TSD patterns in species such as FM pattern where females are predominately born at lower temperature and males at higher temperature, FMF pattern where the probability of female being born is higher at extreme temperatures and of the male being born is high at intermediate temperatures. We analyze an enzymatic reaction system proposed in the literature involving sex hormones with positive feedback effect to understand the emergence of different TSD patterns. The nonlinearity in the model is accounted through temperature sensitivity of the reaction rates affecting the catalytic mechanism in the reaction system. We employ a dynamical systems approach of singularity theory and bifurcation analysis to divide the parameter plane of temperature sensitivities into different regions where different TSD patterns are observed. Bifurcation analysis in association with the delineation of the parameter space for different TSD pattern has led to the identification of a subspace where all the TSD patterns observed in nature can be realized. We also show how modulation of the sex hormone in the species can be used to change the probability of occurrence of a specific sex, thereby preventing the extinction of endangered species.

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References

  • Abucay JS, Mair GC, Skibinski DOF, Beardmore JA (1999) Environmental sex determination: the effect of temperature and salinity on sex ratio in Oreochromis niloticus L. Aquaculture 173:219–234

    Article  Google Scholar 

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

    Google Scholar 

  • Charnov E, Bull J (1977) When is sex environmentally determined? Nature 266:828–832

    Article  Google Scholar 

  • Chen H, Liu N (2010) Application of non-Arrhenius equations in interpreting calcium carbonate decomposition kinetics: revisited. J Am Ceram Soc 93:548–553

    Article  Google Scholar 

  • Crews D (1996) Temperature-dependent sex determination: the interplay of steroid. Zool Sci 13:1–13

    Article  Google Scholar 

  • Crews D, Bergeron JM, Bull JJ et al (1994) Temperature-dependent sex determination in reptiles: proximate mechanisms, ultimate outcome and practical applications. Dev Genet 15:297–312

    Article  Google Scholar 

  • Crews D, Bergeron JM, McLachlan JA (1995) The role of estrogen in turtle sex determination and the effect of PCBs. Environ Health Perspect 103:73–77

    Google Scholar 

  • Deeming DC, Ferguson MW (1988) Environmental regulation of sex determination in reptiles. Philos Trans R Soc Lond B Biol Sci 322:19–39

    Article  Google Scholar 

  • Eivazi F, Tabatabai MA (1988) Glucosidases and galactosidases in soils. Soil Biol Biochem 20:601–606

    Article  Google Scholar 

  • Ewert MA, Nelson CE (1996) Sex determination in turtles: diverse patterns and some possible adaptive values. Copeia 1:50–69

    Google Scholar 

  • Galwey AK, Brown ME (1995) A theoretical justification for the application of the Arrhenius equation to kinetics of solid state reactions (mainly ionic crystals). Math Phys Sci 450:501–512

    Google Scholar 

  • Guiguen Y, Fostier A, Piferrer F, Chang CF (2010) Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol 165:352–366

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Johnston CM, Barnett M, Sharpe PT (1995) The molecular biology of temperature-dependent sex determination. Philos Trans R Soc Lond B Biol Sci 350:297–304

    Article  Google Scholar 

  • Lang JW, Andrews HV (1994) Temperature-dependent sex determination in crocodilians. J Exp Zool 270:28–44

    Article  Google Scholar 

  • Leach MD, Brown AJP (2012) Posttranslational modifications of proteins in the pathobiology of medically relevant fungi. Am Soc Microbiol 11:98–108

    Google Scholar 

  • Li M, Sun L, Wang D (2019) Roles of estrogens in fish sexual plasticity and sex differentiation. Gen Comp Endocrinol 277:9–16

    Article  Google Scholar 

  • Lolavar A, Wyneken J (2017) Experimental assessment of the effects of moisture on loggerhead sea turtle hatchling sex ratios. Zoology 123:64–70

    Article  Google Scholar 

  • Luckenbach JA, Borski RJ, Daniels HV, Godwin J (2009) Sex determination in flatfishes: mechanisms and environmental influences. Semin Cell Dev Biol 20:256–263

    Article  Google Scholar 

  • Menzinger M, Wolfgang R (1969) The meaning and use of the Arrhenius activation energy. Angew Chemie Int Ed Engl 8:438–444

    Article  Google Scholar 

  • Miller JL, Ligon DB (2014) Sex ratios in naturally incubating Macrochelys temminckii nests, a species with type II temperature-dependent sex determination. J Therm Biol 39:6–11

    Article  Google Scholar 

  • Mitchell NJ, Janzen FJ (2010) Temperature-dependent sex determination and contemporary climate change. Sex Dev 4:129–140

    Article  Google Scholar 

  • Mitchell NJ, Nelson NJ, Cree A et al (2006) Support for a rare pattern of temperature-dependent sex determination in archaic reptiles: evidence from two species of tuatara (Sphenodon). Front Zool 3:1–12

    Article  Google Scholar 

  • Miura S, Komatsu T, Higa M et al (2003) Gonadal sex differentiation in protandrous anemone fish, Amphiprion clarkii. Fish Physiol Biochem 28:165–166

    Article  Google Scholar 

  • Schroeder AL, Metzger KJ, Miller A, Rhen T (2016) A novel candidate gene for temperature-dependent sex determination in the common snapping turtle. Genetics 203:557–571

    Article  Google Scholar 

  • Seydel R (2010) Practical bifurcation and stability analysis, 3rd edn. Springer, Berlin

    Book  Google Scholar 

  • Shoemaker CM, Crews D (2009) Analyzing the coordinated gene network underlying temperature-dependent sex determination in reptiles. Semin Cell Dev Biol 20:293–303

    Article  Google Scholar 

  • Sifuentes-Romero I, Tezak BM, Milton SL, Wyneken J (2018) Hydric environmental effects on turtle development and sex ratio. Zoology 126:89–97

    Article  Google Scholar 

  • Slon Campos JL, Marchese S, Rana J et al (2017) Temperature-dependent folding allows stable dimerization of secretory and virus-associated e proteins of Dengue and Zika viruses in mammalian cells. Sci Rep 7:1–14

    Article  Google Scholar 

  • Vitt LJ, Caldwell JP (2013) Herpetology: an introductory biology of amphibians and reptiles, 4th edn. Academic Press, Cambridge

    Google Scholar 

  • Warner DA, Shine R (2008) The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451:566–568

    Article  Google Scholar 

  • Wartmann T, Stephan UW, Bube I et al (2002) Post-translational modifications of the AFET3 gene product: a component of the iron transport system in budding cells and mycelia of the yeast Arxula adeninivorans. Yeast 19:849–862

    Article  Google Scholar 

  • Waters PD, Mattick JS, Marshall Graves JA et al (2017) Differential intron retention in Jumonji chromatin modifier genes is implicated in reptile temperature-dependent sex determination. Sci Adv 3:e1700731

    Article  Google Scholar 

  • Wibbels T, Bull JJ, Crews D (1991) Synergism between temperature and estradiol: a common pathway in turtle sex determination? J Exp Zool 260:130–134

    Article  Google Scholar 

  • Yamaguchi S, Iwasa Y (2018) Temperature-dependent sex determination, realized by hormonal dynamics with enzymatic reactions sensitive to ambient temperature. J Theor Biol 453:146–155

    Article  Google Scholar 

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Correspondence to S. Pushpavanam.

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Verma, N., Verma, B.K. & Pushpavanam, S. Modeling Temperature-Dependent Sex Determination in Oviparous Species Using a Dynamical Systems Approach. Bull Math Biol 82, 89 (2020). https://doi.org/10.1007/s11538-020-00763-6

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