Fertility and Sterility
Volume 81, Issue 4 , Pages 954-964 , April 2004

Environmental versus genetic sex determination: a possible factor in dinosaur extinction?

  • David Miller, Ph.D.

      Affiliations

    • Reproduction and Early Development Group, Department of Paediatrics, Obstetrics and Gynaecology, University of Leeds, Leeds, United Kingdom
    • Corresponding Author InformationReprint requests: David Miller, Ph.D., University of Leeds, Department of Paediatrics, Obstetrics and Gynaecology, Reproduction and Early Development Group, Level D, Clarendon Wing, Leeds General Infirmary, Leeds LS2 9NS, United Kingdom (FAX: 44-113-392-6021).
  • ,
  • Jonathan Summers, Ph.D.

      Affiliations

    • School of Mechanical Engineering, University of Leeds, Leeds, United Kingdom
  • ,
  • Sherman Silber, M.D.

      Affiliations

    • The Infertility Center of St. Louis, St. Luke's Hospital, St. Louis, Missouri, USA

Received 6 May 2003 ,Revised 26 September 2003 ,Accepted 26 September 2003.

References 

  1. Lovell Badge R, Hacker A. The molecular genetics of Sry and its role in mammalian sex determination. Philos Trans R Soc Lond B Biol Sci. 1995;350:205–214
  2. Daneau I, Houde A, Ethier JF, Lussier JG, Silversides DW. Sry gene in bull and boar show greater similarity to human than to mouse gene. Biol Reprod. 1994;50:157
  3. Hacker A, Capel B, Goodfellow P, Lovellbadge R. Expression of Sry, the mouse sex-determining gene. Development. 1995;121:1603–1614
  4. Graves JA. The evolution of mammalian sex chromosomes and the origin of sex determining genes. Philos Trans R Soc Lond B Biol Sci. 1995;350:305–311 ; discussion 311–2
  5. Delbridge ML, Graves JA. Mammalian Y chromosome evolution and the male-specific functions of Y chromosome-borne genes. Rev Reprod. 1999;4:101–109
  6. Marshall Graves JA. The rise and fall of SRY. Trends Genet. 2002;18:259–264
  7. Marshall Graves JA, Shetty S. Sex from W to Z (evolution of vertebrate sex chromosomes and sex determining genes). J Exp Zool. 2001;290:449–462
  8. Shan Z, Nanda I, Wang Y, Schmid M, Vortkamp A, Haaf T. Sex-specific expression of an evolutionarily conserved male regulatory gene, DMRT1, in birds. Cytogenet Cell Genet. 2000;89:252–257
  9. Nanda I, Zend-Ajusch E, Shan Z, Grutzner F, Schartl M, Burt DW, et al.  Conserved synteny between the chicken Z sex chromosome and human chromosome 9 includes the male regulatory gene DMRT1 (a comparative (re)view on avian sex determination). Cytogenet Cell Genet. 2000;89:67–78
  10. Johnston CM, Barnett M, Sharpe PT. The molecular biology of temperature-dependent sex determination. Philos Trans R Soc Lond B Biol Sci. 1995;350:297–303
  11. Pieau C. Sex ratio in the embryos of 2 chelonians (Testudo graeca L. and Emys orbicularis L. born of artificially incubated ova). C R Acad Sci Hebd Seances Acad Sci D. 1971;272:3071–3074
  12. Pieau C. Temperature effects on the development of genital glands in the embryos of 2 chelonians, Emys orbicularis L. and Testudo graeca L. C R Acad Sci Hebd Seances Acad Sci D. 1972;274:719–722
  13. Yntema CL. Effects of incubation temperature on sexual differentiation in the turtle Chelydra serpentine. J Morphol. 1976;150:453–462
  14. Head G, May RM, Pendleton L. Environmental determination of sex in the reptiles. Nature. 1987;329:198–199
  15. Bull JJ, Moon RG, Legler JM. Male heterogamety in kinosternid turtles (genus staurotypus). Cytogenet Cell Genet. 1974;13:419–425
  16. Bull JJ, Vogt RC. Temperature-dependent sex determination in turtles. Science. 1979;206:1186–1188
  17. Bull JJ. Sex determining mechanisms (an evolutionary perspective). Experientia. 1985;41:1285–1296
  18. Bull JJ, Hillis DM, O'Steen S. Mammalian ZFY sequences exist in reptiles regardless of sex-determining mechanism. Science. 1988;242:567–569
  19. Wibbels T, Bull JJ, Crews D. Chronology and morphology of temperature-dependent sex determination. J Exp Zool. 1991;260:371–381
  20. Wibbels T, Bull JJ, Crews D. Synergism between temperature and estradiol (a common pathway in turtle sex determination?). J Exp Zool. 1991;260:130–134
  21. Wibbels T, Bull JJ, Crews D. Steroid hormone-induced male sex determination in an amniotic vertebrate. J Exp Zool. 1992;262:454–457
  22. Wibbels T, Gideon P, Bull JJ, Crews D. Estrogen- and temperature-induced medullary cord regression during gonadal differentiation in a turtle. Differentiation. 1993;53:149–154
  23. Crews D, Bull JJ, Wibbels T. Estrogen and sex reversal in turtles (a dose-dependent phenomenon). Gen Comp Endocrinol. 1991;81:357–364
  24. Crews D, Bergeron JM. Role of reductase and aromatase in sex determination in the red-eared slider (Trachemys scripta), a turtle with temperature-dependent sex determination. J Endocrinol. 1994;143:279–289
  25. Crews D. Temperature, steroids and sex determination. J Endocrinol. 1994;142:1–8
  26. Crews D, Bergeron JM, Bull JJ, Flores D, Tousignant A, Skipper JK, et al. Temperature-dependent sex determination in reptiles (proximate mechanisms, ultimate outcomes, and practical applications). Dev Genet. 1994;15:297–312
  27. Fergusson MW, Joanen T. Temperature of egg incubation determines sex in Alligator mississippiensis. Nature. 1982;296:850–853
  28. Pieau C, Dorizzi M, Richard-Mercier N. Temperature-dependent sex determination and gonadal differentiation in reptiles. Cell Mol Life Sci. 1999;55:887–900
  29. Janzen FJ, Paukstis GL. Environmental sex determination in reptiles. Nature. 1988;332:790
  30. Rage J-C. Latest Cretaceous extinctions and environmental sex determination in reptiles. Bull Soc Geol France. 1998;169:479–483
  31. Alvarez LW. Mass extinctions caused by large bolide impacts. Phys Today. 1987;40:24–33
  32. Lopez-Martinez N, Ardevol L, Arribas ME, Civis J, Gonzales-Delgado A. The geological record in non-marine environments around the K/T boundary. Bull Soc Geol France. 1998;169:11–20
  33. Lopez-Martinez N, Canudo JI, Ardevol L, Suberbiola XP, Prue-Etxebarrai X, Cuenca-Bescos G, et al.  New dinosaur sites correlated with Upper Maastrictian pelagic deposits in the Spanish Pyrenees (impliactions for the dinosaur extinction pattern in Europe). Cretaceous Res. 2001;22:41–61
  34. Cloudsley-Thompson J. Multiple factors in the reptile extinctions of the Cretaceous period. Biologist (London). 2001;48:177–181
  35. Janzen FJ. Climate change and temperature-dependent sex determination in reptiles. Proc Natl Acad Sci U S A. 1994;91:7487–7490
  36. Serono PC. The evolution of dinosaurs. Science. 1999;284:2137–2147
  37. Norell M, Ji Q, Gao K, Yuan C, Zhao Y, Wang L. Palaeontology (‘modern’ feathers on a non-avian dinosaur). Nature. 2002;416:36–37
  38. Norell MA, Clarke JA. Fossil that fills a critical gap in avian evolution. Nature. 2001;409:181–184
  39. Xu X, Norell MA, Wang XL, Makovicky PJ, Wu XC. A basal troodontid from the Early Cretaceous of China. Nature. 2002;415:780–784
  40. Palmer BD, Guillette LJ. Alligators provide evidence for the evolution of an archosaurian mode of oviparity. Biol Reprod. 1992;46:39–47
  41. Geist NR, Jones TD. Juvenile skeletal structure and the reproductive habits of dinosaurs. Science. 1996;272:712–714
  42. Rogers SW. Allosaurus, crocodiles, and birds (evolutionary clues from spiral computed tomography of an endocast). Anat Rec. 1999;257:162–173
  43. Ruben JA, Jones TD, Geist NR, Hillenius WJ. Lung structure and ventilation in theropod dinosaurs and early birds. Science. 1997;278:1267–1270
  44. 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;59:265–276
  45. Baroiller JF, Guiguen Y. Endocrine and environmental aspects of sex differentiation in gonochoristic fish. EXS. 2001;91:177–201
  46. Janzen FJ, Paukstis GL. Environmental sex determination in reptiles (ecology, evolution, and experimental design). Q Rev Biol. 1991;66:149–179
  47. Scherer G, Schmid M. Genes and mechanisms in vertebrate sex determination. Introduction. Exs. 2001;91:xi–xii
  48. Koopman P. Sry and Sox9 (mammalian testis-determining genes). Cell Mol Life Sci. 1999;55:839–856
  49. Rice WR. Degeneration of a nonrecombining chromosome. Science. 1994;263:230–232
  50. Rice WR. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature. 1996;381:232–234
  51. Dournon C, Houillon C, Pieau C. Temperature sex-reversal in amphibians and reptiles. Int J Dev Biol. 1990;34:81–92
  52. Toder R, Wakefield MJ, Graves JA. The minimal mammalian Y chromosome—the marsupial Y as a model system. Cytogenet Cell Genet. 2000;91:285–292
  53. Just W, Rau W, Vogel W, Akhverdian M, Fredga K, Graves JA, et al. Absence of Sry in species of the vole Ellobius. Nat Genet. 1995;11:117–118
  54. Jegalian K, Page DC. A proposed path by which genes common to mammalian X and Y chromosomes evolve to become X inactivated. Nature. 1998;394:776–780
  55. Ohno S. Sex chromosomes and sex-linked genes. Berlin: Springer-Verlag; 1967;
  56. Lahn BT, Page DC. Functional coherence of the human Y chromosome. Science. 1997;278:675–679
  57. Lahn BT, Page DC. Retroposition of autosomal mRNA yielded testis-specific gene family on human Y chromosome. Nat Genet. 1999;21:429–433
  58. Lahn BT, Page DC. Four evolutionary strata on the human X chromosome. Science. 1999;286:964–967
  59. Saxena R, Brown LG, Hawkins T, Alagappan RK, Skaletsky H, Reeve MP, et al.  The DAZ gene cluster on the human Y chromosome arose from an autosomal gene that was transposed, repeatedly amplified and pruned. Nat Genet. 1996;14:292–299
  60. Kuroda-Kawaguchi T, Skaletsky H, Brown LG, Minx PJ, Cordum HS, Waterston RH, et al.  The AZFc region of the Y chromosome features massive palindromes and uniform recurrent deletions in infertile men. Nat Genet. 2001;29:279–286
  61. Repping S, Skaletsky H, Lange J, Silber S, Van Der Veen F, Oates RD, et al.  Recombination between palindromes P5 and P1 on the human Y chromosome causes massive deletions and spermatogenic failure. Am J Hum Genet. 2002;71:906–922
  62. Silber SJ, Alagappan R, Brown LG, Page DC. Y chromosome deletions in azoospermic and severely oligozoospermic men undergoing intracytoplasmic sperm injection after testicular sperm extraction. Hum Reprod. 1998;13:3332–3337
  63. Silber SJ, Repping S. Transmission of male infertility to future generations (lessons from the Y chromosome). Hum Reprod Update. 2002;8:217–229
  64. Silber S. The disappearing male. In:  Jansen R,  Mortimer D editor. Towards reproductive certainty—fertility and genetics beyond 1999. New York, London: The Parthenon Publishing Group; 1999;p. 499–505
  65. Rozen S, Skaletsky H, Marszalek JD, Minx PJ, Cordum HS, Waterston RH, et al.  Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature. 2003;423:873–876
  66. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, et al.  The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature. 2003;423:825–837
  67. Shetty S, Griffin DK, Graves JA. Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosome Res. 1999;7:289–295
  68. Short RV. The evolution of human reproduction. Proc R Soc Lond B Biol Sci. 1976;195:3–24
  69. Shine R. Why is sex determined by nest temperature in may reptiles?. Trends Ecol Evol. 1999;14:186–189
  70. Robert KA, Thompson MB. Sex determination. Viviparous lizard selects sex of embryos. Nature. 2001;412:698–699
  71. Western PS, Sinclair AH. Sex, genes, and heat (triggers of diversity). J Exp Zool. 2001;290:624–631
  72. Vidal VP, Chaboissier MC, de Rooij DG, Schedl A. Sox9 induces testis development in XX transgenic mice. Nat Genet. 2001;28:216–217
  73. Foster JW, Dominguez-Steglich MA, Guioli S, Kowk G, Weller PA, Stevanovic M, et al.  Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature. 1994;372:525–530
  74. Wagner T, Wirth J, Meyer J, Zabel B, Held M, Zimmer J, et al.  Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell. 1994;79:1111–1120
  75. Western PS, Harry JL, Graves JA, Sinclair AH. Temperature-dependent sex determination in the American alligator (AMH precedes SOX9 expression). Dev Dyn. 1999;216:411–419
  76. Richard-Mercier N, Dorizzi M, Desvages G, Girondot M, Pieau C. Endocrine sex reversal of gonads by the aromatase inhibitor Letrozole (CGS 20267) in Emys orbicularis, a turtle with temperature-dependent sex determination. Gen Comp Endocrinol. 1995;100:314–326
  77. Vaillant S, Dorizzi M, Pieau C, Richard-Mercier N. Sex reversal and aromatase in chicken. J Exp Zool. 2001;290:727–740
  78. Rashedi PM, Maraud R. Secretion of the anti-mullerian hormone by the gonads of experimentally sex reversed female chick embryos. Gen Comp Endocrinol. 1987;65:87–91
  79. Bruggeman V, Van As P, Decuypere E. Developmental endocrinology of the reproductive axis in the chicken embryo. Comp Biochem Physiol A Mol Integr Physiol. 2002;131:839–846
  80. Carlsen E, Giwercman A, Keiding N, Skakkebaek NE. Evidence for decreasing quality of semen during past 50 years. Br Med J. 1992;305:609–613
  81. Olsen J. Is human fecundity declining—and does occupational exposures play a role in such a decline if it exists?. Scand J Work Environ Health. 1994;20:72–77
  82. Giwercman A, Bonde JP. Declining male fertility and environmental factors. Endocrinol Metab Clin North Am. 1998;27:807–830 , viii
  83. Vanderschueren D. Is male fertility declining?. Verh K Acad Geneeskd Belg. 1999;61:433–440
  84. Jouannet P, Wang C, Eustache F, Kold-Jensen T, Auger J. Semen quality and male reproductive health (the controversy about human sperm concentration decline). APMIS. 2001;109:333–344
  85. Allen E, Cooper JE. Sex reversal in birds. Vet Rec. 1997;140:636
  86. Clinton M. Sex determination and gonadal development (a bird's eye view). J Exp Zool. 1998;281:457–465
  87. Gray LE Jr. Xenoendocrine disrupters: laboratory studies on male reproductive effects. Toxicol Lett 1998;102–3; 331–5
  88. St Mary CM. Sex allocation in a simultaneous hermaphrodite, the blue banded Goby (Lythypnus dalli). Behav Ecol. 1994;5:304–312
  89. Gabriel WN, Blumberg B, Sutton S, Place AR, Lance VA. Alligator aromatase cDNA sequence and its expression in embryos at male and female incubation temperatures. J Exp Zool. 2001;290:439–448
  90. Belaid B, Richard-Mercier N, Pieau C, Dorizzi M. Sex reversal and aromatase in the European pond turtle (treatment with letrozole after the thermosensitive period for sex determination). J Exp Zool. 2001;290:490–497
  91. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, et al.  Emerging marine diseases—climate links and anthropogenic factors. Science. 1999;285:1505–1510
  92. Archie JW, Cole CJ, Vilella OF. A review of phylogenetic hypotheses for lizards: implications for ecological and evolutionary studies. Bull Am Museum Natural History 1992:1–110
  93. Reis PM, Zeigler AM, Valdes PJ. Jurassic phytogeography and climate: new data and model comparisons. In:  Huber BT,  McLeod KG,  Wing SL editor. Warm climates in earth history. Cambridge, United Kingdom: Cambridge University Press; 2000;
  94. Deconto RM, Brady EC, Bergengren J, Hay WW. Late Cretaceous climate, vegetation and ocean interactions. In:  Huber BT,  McLeod KG,  Wing SL editor. Warm climates in earth history. Cambridge, United Kingdom: Cambridge University Press; 2000;p. 275–297
  95. Crain DA, Guillette LJ. Reptiles as models of contaminant-induced endocrine disruption. Anim Reprod Sci. 1998;53:77–86

PII: S0015-0282(03)03206-0

doi: 10.1016/j.fertnstert.2003.09.051

Fertility and Sterility
Volume 81, Issue 4 , Pages 954-964 , April 2004