Egg yolk environment differentially influences physiological and morphological development of broiler and layer chicken embryos

Journal of Experimental Biology

Volumn 214, Issue 4, 2011, Pages 619-628

  Ho, Dao H ^a   Reed, Wendy L ^b   Burggren, Warren W ^a  

^a UNIVERSITY OF NORTH TEXAS   (United States)

^b NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

Chicken breed; Epigenetics; Maternal effect; Yolk hormone

Indexed keywords

LIOTHYRONINE; TESTOSTERONE;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; BODY WEIGHT; CHEMISTRY; CHICK EMBRYO; COMPARATIVE STUDY; CULTURE MEDIUM; EGG YOLK; EMBRYO DEVELOPMENT; EPIGENETICS; GENETICS; GENOTYPE; HEART RATE; OXYGEN CONSUMPTION; PHYSIOLOGY; PRENATAL DEVELOPMENT; RADIOIMMUNOASSAY; SPECIES DIFFERENCE;

ANALYSIS OF VARIANCE; ANIMALS; BODY WEIGHT; CHICK EMBRYO; CULTURE MEDIA; EGG YOLK; EMBRYONIC DEVELOPMENT; EPIGENOMICS; GENOTYPE; HEART RATE; OXYGEN CONSUMPTION; RADIOIMMUNOASSAY; SPECIES SPECIFICITY; TESTOSTERONE; TRIIODOTHYRONINE;

GALLUS GALLUS; SPONDIAS PURPUREA;

EID: 79951497215     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.046714     Document Type: Article

References (77)

1. Altimiras, J. and Phu, L. (2000). Lack of physiological plasticity in the early chicken embryo exposed to acute hypoxia. J. Exp. Zool. 286, 450-456. (Pubitemid 30146916)
2. Bennett, A. F. (1987). The accomplishments of ecological physiology. In New directions in ecological physiology (ed. M. E. Feder, A. F. Bennett, W. W. Burggren and R. B. Huey), pp. 1-8. Cambridge: Cambridge University Press.
3. Bernardo, J. (1996). Maternal effects in animal ecology. Amer. Zool. 36, 83-105. (Pubitemid 27004112)
4. Biard, C., Surai, P. F. and Møller, A. P. (2007). An analysis of pre-and post-hatching maternal effects mediated by carotenoids in the blue tit. J. Evol. Biol. 20, 326-339. (Pubitemid 44968183)
5. Boerjan, M. (2004). Genetic progress inspires changes in incubator technology. World Poultry 20, 16-17.
6. Boonstra, T. A. M. E., Clark. and Reed, W. L. (2009). Allocation of maternal resources across the laying sequence in Canada geese. J. Avian Biol. 40, 520-528.
7. Burggren, W. W. and Warburton, S. (2005). Comparative developmental physiology: an interdisciplinary convergence. Annu. Rev. Physiol. 67, 203-223. (Pubitemid 40404491)
8. Burggren, W. W., Warburton, S. J. and Slivkoff, M. D. (2000). Interruption of cardiac output does not affect short-term growth and metabolic rate in day 3 and 4 chick embryos. J. Exp. Biol. 203, 3831-3838. (Pubitemid 32097366)
9. Burggren, W., Khorrami, S., Pinder, A. and Sun, T. (2004). Body, eye, and chorioallantoic vessel growth are not dependent on cardiac output level in day 3-4 chicken embryos. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, R1399-R1406. (Pubitemid 39532224)
10. Chan, T. and Burggren, W. (2005). Hypoxic incubation creates differential morphological effects during specific developmental critical windows in the embryo of the chicken (Gallus gallus). Respir. Physiol. Neurobiol. 15, 251-263. (Pubitemid 40215657)
11. Chapman, S. C., Collignon, J., Schoenwolf, G. C. and Lumsden, A. (2001). Improved method for chick whole-embryo culture using a filter paper carrier. Dev. Dyn. 220, 284-289. (Pubitemid 32173384)
12. Christensen, V. L., Bagley, L. G., Olson, T., Grimes, J. L. and Ort, D. G. (2006). Eggshell conductance of turkey eggs affects cardiac physiology and subsequent embryo survival. Inter. J. Poult. Sci. 5, 1096-1101. (Pubitemid 46422912)
13. Clum, N. J., McClearn, D. K. and Barbato, G. F. (1995). Comparative embryonic development in chickens with different patterns of postnatal growth. Growth Dev. Aging 59, 129-138.
14. Cucco, M., Guasco, B., Malacarne, G., Ottonelli, R. and Tanvez, A. (2008). Yolk testosterone levels and dietary carotenoids influence growth and immunity of grey partridge chicks. Gen. Comp. Endocrinol. 156, 418-425.
15. Dunnington, E. A., Stallard, L. C., Hillel, J. and Siegel, P. B. (1994). Genetic diversity among commercial chicken populations estimated from DNA fingerprints. Poult. Sci. 73, 1218-1225.
16. Dzialowski, E. M. and Sotherland, P. R. (2004). Maternal effects of egg size on emu, Dromaius novaehollandiae, egg composition and hatchling phenotype. J. Exp. Biol. 207, 597-606. (Pubitemid 38231173)
17. Eising, C. M., Eikenaar, C., Schwabl, H. and Groothuis, T. G. G. (2001). Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc. Biol. Sci. 269, 2249-2255.
18. Everaert, N., Willemsen, H., De Smit, L., Witters, A., De Baerdemaeker, J., Decuypere, E. and Bruggeman, V. (2008). Comparison of a modern broiler and layer strain during embryonic development and the hatching process. Br. Poult. Sci. 49, 574-582.
19. Flamant, F. and Samarut, J. (1998). Involvement of thyroid hormone and its α receptor in avian neurulation. Dev. Biol. 197, 1-11. (Pubitemid 28224223)
20. Gibbs, A. G. (1999). Laboratory selection for the comparative physiologist. J. Exp. Biol. 202, 2709-2718.
21. Gill, D. (2008). Hormones in avian eggs: physiology, ecology and behavior. Adv. Stud. Behav. 38, 337-398.
22. Gill, D., Biard, C., Lacroix, A., Spottiswoode, C. N., Saino, N., Peurta, M. and Moller, A. P. (2007). Evolution of yolk androgens in birds: development, coloniality, and sexual dichromatism. Am. Nat. 169, 802-819. (Pubitemid 46847335)
23. Gimeno, M. A., Roberts, C. M. and Webb, J. L. (1967). Acceleration of rate of the early chick embryo heart by visible light. Nature 214, 1014-1016.
24. Goldman-Johnson, D. R., de Kretser, D. M. and Morrison, J. R. (2008). Evidence that androgens regulate early developmental events, prior to sexual differentiation. Endocrinology 149, 5-14.
25. Groothuis, T. G. G. and Schwabl, H. (2008). Hormone-mediated maternal effects in birds. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 1581-1588.
26. Groothuis, T. G. G., Müller, W., von Engelhardt, N., Carere, C. and Eising, C. (2005). Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. & Biobehav. Rev. 29, 329-352. (Pubitemid 40461749)
27. Hamburger, V. and Hamilton, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Morph. 88, 49-92.
28. Ho, D. H. and Burggren, W. W. (2010). Epigenetics and transgenerational transfer: a physiological perspective. J. Exp. Biol. 213, 3-16.
29. Koenen, M. E., Boonstra-Blom, A. G. and Jeurissen, H. M. (2002). Immunological differences between layer-and broiler-type chickens. Vet. Immun. Immunopath. 89, 47-56.
30. Latimer, B. E. and Brisbin, I. L. (1987). Early growth rates and their relationships to mortalities of five breeds of chickens following exposure to acute gamma radiation stress. Growth 51, 411-424.
31. Lipar, J. L. and Ketterson, E. D. (2000). Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc. R. Soc. Lond. B 267, 2005-2010.
32. Martin, T. E. and Schwabl, H. (2008). Variation in maternal effects and embryonic development rates among passerine birds. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 1581-1588.
33. Martinez-Lemus, L. A., Miller, M. W., Jeffrey, J. S. and Odom, T. W. (1998). Echocardiographic evaluation of cardiac structure and function in broiler and Leghorn chickens. Poult. Sci. 77, 1045-1050. (Pubitemid 128525120)
34. Martinez-Lemus, L. A., Hester, R. K., Becker, E. J., Jeffrey, J. S. and Odom, T. W. (1999). Pulmonary artery endothelium-dependent vasodilation is impaired in a chicken model of pulmonary hypertension. Am. J. Physio. Regul. Integr. Comp. Physiol. 277, 190-197.
35. McAdam, A. G., Boutin, S., Réale, D. and Berteaux, D. (2002). Maternal effects and the potential for evolution in a natural population of animals. Evolution Int. J. Org. Evolution 56, 846-851. (Pubitemid 34519796)
36. McNabb, F. M. (1988). Peripheral thyroid hormone dynamics in precocial and altricial avian development. Amer. Zool. 28, 427-440.
37. McNabb, F. M. (2006). Avian thyroid development and adaptive plasticity. Gen. Comp. Endocrinol. 148, 290-298.
38. McNabb, F. M. and Wilson, C. M. (1997). Thyroid hormone deposition in avian eggs and effects on embryonic development. Amer. Zool. 37, 553-560.
39. McRae, V. E., Mahon, M., Gilpin, S., Sandercook, D. A. and Mitchell, M. A. (2006). Skeletal muscle fibre growth and growth associated myopathy in the domestic chicken (Gallus domesticus). Br. Poult. Sci. 47, 264-272. (Pubitemid 43982327)
40. Moussavi, R., Meisami, E. and Timiras, P. S. (1985). Compensatory cell proliferation and growth in the rat heart after postnatal hypothyroidism. Am. J. Physiol. 248, E381-E387. (Pubitemid 15076602)
41. Mousseau, T. A. and Fox, C. W. (1998). The adaptive significance of maternal effects. TREE 13, 403-407. (Pubitemid 28430680)
42. Müller, W., Groothuis, T. G. G., Eising, C. M. and Dijkstra, C. (2005). An experimental study on the causes of sex-biased mortality in the black-headed gull - possible role of testosterone. J. Anim. Ecol. 74, 735-741. (Pubitemid 41576942)
43. Navara, K. J., Hill, G. E. and Mendonca, M. T. (2006). Yolk testosterone stimulated growth and immunity in house finch chicks. Physiol. Biochem. Zool. 79, 550-555. (Pubitemid 43846270)
44. Newbrey, J. L. and Reed, W. L. (2009). Growth of yellow-headed blackbird Xanthocephalus xanthocephalus nestlings in relation to maternal body condition, egg mass, and yolk carotenoids concentrations. J. Avian Biol. 40, 419-429.
45. Nijhout, H. F. (2003). Development and evolution of adaptive polyphenisms. Evol. Dev. 5, 9-18. (Pubitemid 36174972)
46. Nikinmaa, M. and Waser, W. (2007). Molecular and cellular studies in evolutionary physiology of natural vertebrate populations: influences of individual variation and genetic components on sampling and measurements. J. Exp. Biol. 210, 1847-1857. (Pubitemid 46998730)
47. Odom, T. W., Martinez-Lemus, L. A., Hester, R. K., Becker, E. J., Jeffrey, J. S., Meininger, G. A. and Ramirez, G. A. (2004). In vitro hypoxia differentially affects constriction and relaxation responses of isolated pulmonary arteries from broiler and leghorn chickens. Poult. Sci. 83, 835-841. (Pubitemid 39197216)
48. Okuda, A. and Tazawa, H. (1988). Gas exchange and development of chicken embryos with widely altered shell conductance from the beginning of incubation. Respir. Physiol. 74, 187-198.
49. Olkowski, A. A. (2007). Pathophysiology of heart failure in broiler chickens: structural, biochemical, and molecular characteristics. Poult. Sci. 86, 999-1005. (Pubitemid 47581037)
50. Pal, A. K., Quadri, M. A., Jadhao, S. B., Kumbhakar, J., Kushwah, H. S. and Datta, I. C. (2002). Genotype influences body composition of developing chicken embryo. Pakistan J. Nutrition 1, 82-84.
51. Peterson, C. C., Walton, B. M. and Bennett, A. F. (1998). Intrapopulation variation in ecological energetics of the garter snake Thamnophis sirtalis, with analysis of the precision of doubly labeled water measurements. Physiol. Zool. 71, 333-349.
52. Räsänen, K. and Kruuk, L. E. B. (2007). Maternal effects and evolution at ecological time-scales. Funct. Ecol. 21, 408-421. (Pubitemid 46805016)
53. Reed, W. L. and Vleck, C. M. (2001). Functional significance of variation in egg-yolk androgens in the American coot. Oecologia 128, 164-171. (Pubitemid 32760278)
54. Reinhold, K. (2002). Maternal effects and the evolution of behavioral and morphological characters: a literature review indicates the importance of extended maternal care. J. Hered. 93, 400-405. (Pubitemid 36268514)
55. Romanoff, L. L. (1960). The Avian Embryo: Structural and Functional Development. New York, USA: Macmillan.
56. Royle, N. J., Surai, P. F. and Hartley, I. R. (2001). Maternally-derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav. Ecol. 12, 381-385. (Pubitemid 32632074)
57. Saino, N., Martinelli, R., Biard, C., Gil, D., Spottiswoode, C. N., Rubolini, D., Surai, P. F. and Møller, A. P. (2007). Maternal immune factors and the evolution of secondary sexual characters. Behav. Ecol. 18, 513-520. (Pubitemid 47364555)
58. Sato, M., Tachibana, T. and Furuse, M. (2006). Heat production and lipid metabolism in broiler and layer chickens during embryonic development. Comp. Biochem. Physiol. 143 A, 382-388. (Pubitemid 43288135)
59. Schjeide, O. A., Prahlad, K. V., Molsen, D., Smith, S. and Hanzely, L. (1989). Morphological and metabolic responses of embryonic hearts to administration of exogenous L-thyroxine. Cytobios 60, 71-95. (Pubitemid 20101207)
60. Schreurs, F. J., van der Heide, D., Leenstra, F. R. and de Wit, W. (1995). Endogenous proteolytic enzymes in chicken muscles. Differences among strains with different growth rates and protein efficiencies. Poult. Sci. 74, 523-537.
61. Schwabl, H. (1993). Yolk is a source of maternal testosterone for developing birds. Proc. Natl. Acad. Sci. USA 90, 11446-11450. (Pubitemid 24008655)
62. Schwabl, H. (1996). Maternal testosterone in the avian egg enhances postnatal growth. Comp. Biochem. Physiol. 114 A, 271-276. (Pubitemid 26234068)
63. Schwabl, H., Palacios, M. G. and Martin, T. E. (2007). Selection for rapid embryo development correlates with embryo exposure to maternal androgens among passerine birds. Am. Nat. 170, 196-206. (Pubitemid 47221679)
64. Sharma, S. K., Lucitti, J. L., Nordman, C., Tinney, J. P., Tobita, K. and Keller, B. B. (2006). Impact of hypoxia on early chick embryo growth and cardiovascular function. Pediatr. Res. 59, 116-120.
65. Sinervo, B. and Huey, R. B. (1990). Allometric engineering: an experimental test of the causes of interpopulational differences in performance. Science 248, 1106-1110.
66. Slotkin, T. A., Seidler, F. J., Kavlock, R. J. and Bartolome, J. V. (1992). Thyroid hormone differentially regulates cellular development in neonatal rat heart and kidney. Teratology 45, 303-312.
67. Sotherland, P. R. and Rahn, H. (1987). On the composition of bird eggs. Condor 89, 48-65.
68. Spicer, J. I. and Burggren, W. W. (2003). Development of physiological regulatory systems: altering the timing of crucial events. Zoology 106, 91-99. (Pubitemid 36933039)
69. Spicer, J. I. and Rundle, S. D. (2007). Plasticity in the timing of physiological development: physiological heterokairy - what is it, how frequent is it, and does it matter? Comp. Biochem. Physiol. A Mol. Integr. Physiol. 148, 712-719. (Pubitemid 350101293)
70. Tazawa, H. and Nakagawa, S. (1985). Response of egg temperature, heart rate and blood pressure in the chick embryo to hypothermal stress. J. Comp. Physiol B: Biochem. Syst. Environ. Physiol. 155, 195-200. (Pubitemid 15229515)
71. Tazawa, H., Nakazawa, S., Okuda, A. and Whittow, G. C. (1988). Short-term effects of altered shell conductance on oxygen uptake and hematological variables of late chicken embryos. Respir. Physiol. 74, 199-210.
72. Williams, T. D. (2008). Individual variation in endocrine systems: moving beyond the 'tyranny of the Golden Mean'. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 1687-1698. (Pubitemid 351441047)
73. Wilson, C. M. and McNabb, F. M. (1997). Maternal thyroid hormones in Japanese quail eggs and their influence on embryonic development. Gen. Comp. Endocrinol. 107, 153-165. (Pubitemid 27323570)
74. Wingfield, J. C., Matt, K. S. and Farner, D. S. (1984). Physiologic properties of steroid hormone-binding proteins in avian blood. Gen. Comp. Endocrinol. 53, 281-292.
75. Wong, G. K., Liu, B., Wang, J., Zhang, Y., Yang, X., Zhang, Z., Meng, Q., Zhou, J., Li, D., Zhang, J. et al. (2004). A genetic variation map for chicken with 2.8 million single-nucleotide polymorphisms. Nature 432, 717-722.
76. Yoneta, H., Fukuoka, S., Akiyama, R. and Tazawa, H. (2006). Early development of cholinergic heart rate control in embryos of broiler and White Leghorn chicken. In New Insights into Fundamental Physiology and Peri-natal Adaptation of Domestic Fowl (ed. S. Yahav and B. Tzschentke), pp. 1-14. Nottingham: Nottingham University Press.
77. Yoneta, H., Dzialowski, E. M., Burggren, W. W. and Tazawa, H. (2007). Endothermic heart response in broiler and White Leghorn chicks (Gallus gallus domesticus) during the first two days of post-hatch life. Comp. Biochem. Physiol. 147 A, 529-535. (Pubitemid 46618011)