Temperature-dependent sex determination modulates cardiovascular maturation in embryonic snapping turtles Chelydra serpentina

Journal of Experimental Biology

Volumn 216, Issue 5, 2013, Pages 751-758

  Alvine, Travis ^a   Rhen, Turk ^a   Crossley, Dane A ^b  

^a UNIVERSITY OF NORTH DAKOTA   (United States)

^b UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

Adrenergic; Cardiovascular; Cholinergic; Development; Sexual differentiation; Snapping turtle

Indexed keywords

ALPHA ADRENERGIC RECEPTOR BLOCKING AGENT; ATROPINE; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; MUSCARINIC RECEPTOR BLOCKING AGENT; PHENTOLAMINE; PROPRANOLOL;

ANIMAL; ARTICLE; AUTONOMIC NERVOUS SYSTEM; BLOOD PRESSURE; CARDIOVASCULAR SYSTEM; FEMALE; HEART RATE; HEAT; MALE; PRENATAL DEVELOPMENT; RANDOMIZATION; SEX DETERMINATION PROCESS; SEXUAL DEVELOPMENT; TIME; TURTLE;

ADRENERGIC ALPHA-ANTAGONISTS; ADRENERGIC BETA-ANTAGONISTS; ANIMALS; ATROPINE; AUTONOMIC NERVOUS SYSTEM; BLOOD PRESSURE; CARDIOVASCULAR SYSTEM; FEMALE; HEART RATE; HOT TEMPERATURE; MALE; MUSCARINIC ANTAGONISTS; PHENTOLAMINE; PROPRANOLOL; RANDOM ALLOCATION; SEX CHARACTERISTICS; SEX DETERMINATION PROCESSES; TIME FACTORS; TURTLES;

EID: 84874169318     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.074609     Document Type: Article

References (58)

1. Abdel-Rahman, A. A. (1999). Gender difference in baroreflex-mediated bradycardia in young rats: role of cardiac sympathetic and parasympathetic components. Can. J. Physiol. Pharmacol. 77, 358-366.
2. Altimiras, J. and Crossley, D. A., II (2000). Control of blood pressure mediated by baroreflex changes of heart rate in the chicken embryo (Gallus gallus). Am. J. Physiol. 278, R980-R986.
3. Altimiras, J., Johnstone, A. D. F., Lucas, M. C. and Prieda, I. G. (1996). Sex differences in the heart rate variability spectrum of free-swimming atlantic salmon (Salmo salar L.) during the spawning season. Physiol. Zool. 69, 770-784.
4. Birchard, G. F. (2000). An ontogenetic shift in the response of heart rates to temperature in the developing snapping turtle (Chelydra serpentina). J. Therm. Biol. 25, 287-291.
5. Birchard, G. F. and Reiber, C. L. (1995). Growth, metabolism, and chorioallantoic vascular density of developing snapping turtles (Chelydra serpentina): influence of temperature. Physiol. Zool. 68, 799-811.
6. Birchard, G. F. and Reiber, C. L. (1996). Heart rate during development in the turtle embryo: effect of temperature. J. Comp. Physiol. B 166, 461-466.
7. Bubb, K. J., Khambata, R. S. and Ahluwalia, A. (2012). Sexual dimorphism in rodent models of hypertension and atherosclerosis. Br. J. Pharmacol. 167, 298-312.
8. Bull, J. J. (1980). Sex determination in reptiles. Q. Rev. Biol. 55, 3-21.
9. Carey, M. A., Card, J. W., Bradbury, J. A., Moorman, M. P., Haykal-Coates, N., Gavett, S. H., Graves, J. P., Walker, V. R., Flake, G. P., Voltz, J. W. et al. (2007). Spontaneous airway hyperresponsiveness in estrogen receptor-alpha-deficient mice. Am. J. Respir. Crit. Care Med. 175, 126-135.
10. Charnier, M. (1966). Action de la température sur la sex-ratio chez lembryon dAgama agama (Agamidae, Lacertilien). C. R. Seances Soc. Biol. Fil. 160, 620-622.
11. Conover, D. O. and Heins, S. W. (1987). Adaptive variation in environmental and genetic sex determination in a fish. Nature 326, 496-498.
12. Crews, D. and Bull, J. J. (2008). Sex determination: some like it hot (and some dont). Nature 451, 527-528.
13. Crews, D., Sakata, J. and Rhen, T. (1998). Developmental effects on intersexual and intrasexual variation in growth and reproduction in a lizard with temperaturedependent sex determination. Comp. Biochem. Physiol. 119C, 229-241.
14. Crossley, D. A., II and Altimiras, J. (2000). Ontogeny of cholinergic and adrenergic cardiovascular regulation in the domestic chicken (Gallus gallus). Am. J. Physiol. 279, R1091-R1098.
15. Crossley, D. A., II and Altimiras, J. (2005). Cardiovascular development in embryos of the American alligator Alligator mississippiensis: effects of chronic and acute hypoxia. J. Exp. Biol. 208, 31-39.
16. Crossley, D. A., II and Burggren, W. W. (2009). Development of cardiac form and function in ectothermic sauropsids. J. Morphol. 270, 1400-1412.
17. Crossley, D. A., II, Bagatto, B. P., Dzialowski, E. M. and Burggren, W. W. (2003a). Maturation of cardiovascular control mechanisms in the embryonic emu (Dromiceius novaehollandiae). J. Exp. Biol. 206, 2703-2710.
18. Crossley, D. A., II, Hicks, J. W. and Altimiras, J. (2003b). Ontogeny of baroreflex control in the American alligator Alligator mississippiensis. J. Exp. Biol. 206, 2895-2902.
19. Daniel, J. M., Hulst, J. L. and Lee, C. D. (2005). Role of hippocampal M2 muscarinic receptors in the estrogen-induced enhancement of working memory. Neuroscience 132, 57-64.
20. Dart, A. M., Du, X. J. and Kingwell, B. A. (2002). Gender, sex hormones and autonomic nervous control of the cardiovascular system. Cardiovasc. Res. 53, 678-687.
21. Dragon, S., Glombitza, S., Götz, R. and Baumann, R. (1996). Norepinephrinemediated hypoxic stimulation of embryonic red cell carbonic anhydrase and 2,3-DPG synthesis. Am. J. Physiol. 271, R928-R989.
22. Du, X. J., Dart, A. M. and Riemersma, R. A. (1994). Sex differences in the parasympathetic nerve control of rat heart. Clin. Exp. Pharmacol. Physiol. 21, 485-493.
23. Du, W. G., Ye, H., Zhao, B., Warner, D. A. and Shine, R. (2010). Thermal acclimation of heart rates in reptilian embryos. PLoS ONE 5, e15308.
24. El-Mas, M. M., Afify, E. A., Mohy El-Din, M. M., Omar, A. G. and Sharabi, F. M. (2001). Testosterone facilitates the baroreceptor control of reflex bradycardia: role of cardiac sympathetic and parasympathetic components. J. Cardiovasc. Pharmacol. 38, 754-763.
25. Eme, J., Altimiras, J., Hicks, J. W. and Crossley, D. A., II (2011a). Hypoxic alligator embryos: chronic hypoxia, catecholamine levels and autonomic responses of in ovo alligators. Comp. Biochem. Physiol. 160A, 412-420.
26. Eme, J., Hicks, J. W. and Crossley, D. A., II (2011b). Chronic hypoxic incubation blunts a cardiovascular reflex loop in embryonic American alligator (Alligator mississippiensis). J. Comp. Physiol. B 181, 981-990.
27. Evans, J. M., Ziegler, M. G., Patwardhan, A. R., Ott, J. B., Kim, C. S., Leonelli, F. M. and Knapp, C. F. (2001). Gender differences in autonomic cardiovascular regulation: spectral, hormonal, and hemodynamic indexes. J. Appl. Physiol. 91, 2611-2618.
28. Ewert, M. A., Lang, J. W. and Nelson, C. E. (2005). Geographic variation in the pattern of temperature-dependent sex determination in the American snapping turtle (Chelydra serpentina). J. Zool. 265, 81-95.
29. Gagnon, R. (2003). Placental insufficiency and its consequences. Eur. J. Obstet. Gynecol. Reprod. Biol. 110, S99-S107.
30. Kuo, A. Y., Lee, J. C., Siegel, P. B. and Denbow, D. M. (2001). Differential cardiovascular effects of pharmacological agents in chickens selected for high and low body weight. Physiol. Behav. 74, 573-579.
31. Lance, V. A. (2009). Is regulation of aromatase expression in reptiles the key to understanding temperature-dependent sex determination? J. Exp. Zool. 309A, 1-9.
32. Liao, D., Barnes, R. W., Chambless, L. E., Simpson, R. J., Jr., Sorlie, P. and Heiss, G. (1995). Age, race, and sex differences in autonomic cardiac function measured by spectral analysis of heart rate variability -the ARIC study. Atherosclerosis Risk in Communities. Am. J. Cardiol. 76, 906-912.
33. Lindgren, I., Crossley, D. A., II, Villamor, E. and Altimiras, J. (2011). Hypotension in the chronically hypoxic chicken embryo is related to the β-adrenergic response of chorioallantoic and femoral arteries and not to bradycardia. Am. J. Physiol. 301, R1161-R1168.
34. Mahmoud, I. Y. and Licht, P. (1997). Seasonal changes in gonadal activity and the effects of stress on reproductive hormones in the common snapping turtle, Chelydra serpentina. Gen. Comp. Endocrinol. 107, 359-372.
35. Mendelsohn, M. E. and Karas, R. H. (2005). Molecular and cellular basis of cardiovascular gender differences. Science 308, 1583-1587.
36. Mulder, A. L. M., Golde, J. M., Goor, A. A., Giussani, D. A. and Blanco, C. E. (2000). Developmental changes in plasma catecholamine concentrations during normoxia and acute hypoxia in the chick embryo. J. Physiol. 527, 593-599.
37. Orshal, J. M. and Khalil, R. A. (2004). Gender, sex hormones, and vascular tone. Am. J. Physiol. 286, R233-R249.
38. Place, A. R., Lang, J., Gavasso, S. and Jeyasuria, P. (2001). Expression of P450arom in Malaclemys terrapin and Chelydra serpentina: a tale of two sites. J. Exp. Zool. 290, 673-690.
39. Ramsey, M. and Crews, D. (2009). Steroid signaling and temperature-dependent sex determination -reviewing the evidence for early action of estrogen during ovarian determination in turtles. Semin. Cell Dev. Biol. 20, 283-292.
40. Rhen, T. and Lang, J. W. (1994). Temperature-dependent sex determination in the snapping turtle: manipulation of the embryonic sex steroid environment. Gen. Comp. Endocrinol. 96, 243-254.
41. Rhen, T. and Lang, J. W. (1995). Phenotypic plasticity in the common snapping turtle: effects of incubation temperature, clutch, and their interaction. Am. Nat. 146, 726-747.
42. Rhen, T. and Lang, J. W. (1998). Among-family variation for environmental sex determination in reptiles. Evolution 52, 1514-1520.
43. Rhen, T. and Lang, J. W. (1999). Temperature during embryonic and juvenile development influences growth in hatchling snapping turtles (Chelydra serpentina). J. Therm. Biol. 24, 33-41.
44. Rhen, T. and Lang, J. W. (2004). Phenotypic effects of incubation temperature in reptiles. In Temperature-dependent Sex Determination (ed. N. Valenzuela and V. Lance), pp. 90-98. Washington, DC: Smithsonian Institution Press.
45. Rhen, T., Elf, P. K., Fivizzani, A. J. and Lang, J. W. (1996). Sex reversed and normal turtles display similar sex steroid profiles. J. Exp. Zool. 274, 221-226.
46. Rhen, T., Metzger, K., Schroeder, A. and Woodward, R. (2007). Expression of putative sex-determining genes during the thermosensitive period of gonad development in the snapping turtle, Chelydra serpentina. Sex Dev. 1, 255-270.
47. Rhen, T., Jangula, A., Schroeder, A. and Woodward-Bosh, R. (2009). The plateletderived growth factor signaling system in snapping turtle embryos, Chelydra serpentina: potential role in temperature-dependent sex determination and testis development. Gen. Comp. Endocrinol. 161, 335-343.
48. Shechtman, O. and Katovich, M. J. (1993). Sex differences in vascular reactivity to adrenergic agents in the rat. Comp. Biochem. Physiol. 106, 519-524.
49. Semyachkina-Gluchkovskaya, O. V., Anishchenko, T. G., Berdnikova, V. A. and Najdyonova, O. S. (2008). Sex-specific peculiarities of cholinergic regulation of the cardiovascular system in normal and hypertensive rats. Bull. Exp. Biol. Med. 146, 29-32.
50. Spencer, J. L., Waters, E. M., Romeo, R. D., Wood, G. E., Milner, T. A. and McEwen, B. S. (2008). Uncovering the mechanisms of estrogen effects on hippocampal function. Front. Neuroendocrinol. 29, 219-237.
51. Thompson, J. and Khalil, R. A. (2003). Gender differences in the regulation of vascular tone. Clin. Exp. Pharmacol. Physiol. 30, 1-15.
52. Warner, M. J. and Ozanne, S. E. (2010). Mechanisms involved in the developmental programming of adulthood disease. Biochem. J. 427, 333-347.
53. Warner, D. A. and Shine, R. (2008). The adaptive significance of temperaturedependent sex determination in a reptile. Nature 451, 566-568.
54. Wu, G., Bazer, F. W., Cudd, T. A., Meininger, C. J. and Spencer, T. E. (2004). Maternal nutrition and fetal development. J. Nutr. 134, 2169-2172.
55. Yntema, C. L. (1968). A series of stages in the embryonic development of Chelydra serpentina. J. Morphol. 125, 219-251.
56. Yntema, C. L. (1976). Effects of incubation temperatures on sexual differentiation in the turtle Chelydra serpentina. J. Morphol. 150, 453-461.
57. Yntema, C. L. (1978). Incubation times for eggs of the turtle Chelydra serpentina (Testudines: Chelydridae) at various temperatures. Herpetologica 34, 274-277.
58. Yntema, C. L. (1979). Temperature levels and periods of sex determination during incubation of eggs of Chelydra serpentina. J. Morphol. 159, 17-27.