The effects of embryonic hypoxic programming on cardiovascular function and autonomic regulation in the American alligator (Alligator mississippiensis) at rest and during swimming
Reptilian embryos naturally experience fluctuating oxygen levels in ovo, and developmental hypoxia has been established to have long-term impacts on cardiovascular function in vertebrates. In the present study, we investigated the impact of developmental 21% (normoxia) and 10% O2 (hypoxia) on juvenile (4-year-old) American alligator cardiovascular function in animals at rest and during swimming. In both experimental groups, combined right aortic and right subclavian blood flow approximately doubled during swimming. Carotid blood flow increased during swimming in the hypoxia-programmed animals only, and both carotid and left aortic blood flow reached higher values in swimming hypoxic-programmed animals compared to the normoxic group. However, pulmonary blood flow, which increased two to threefold during swimming (in both groups), was higher in normoxic-programmed animals at both rest and swimming. The differences between programming groups were preserved after cholinergic blockade (atropine), but reduced by adrenergic receptor antagonists (propranolol and phentolamine). Propranolol and phentolamine also blunted the incremental increases in blood flows during swimming, which was especially clear in the hypoxia-programmed animals. Alteration in adrenergic control and relative cardiac size (which was increased in hypoxic-programmed alligators) may account for the differences between the experimental groups.
KeywordsDevelopmental programming Exercise Alligator Cardiac function Cardiac shunting
This work was supported by NSF CAREER award IBN IOS-0845741 to D.A.C.II. W.J. and T.W. were supported by an EliteForsk travel grant from the Danish Ministry of Higher Education and Science and The Danish Council for Independent Research/Natural Sciences. We are sincerely grateful to Brandt Smith for assistance during the post-mortem dissections. We also thank Jamie Adenuga for suggestions that aided flow probe maintenance.
- Eme J, Rhen T, Tate KB, Gruchalla K, Kohl ZF, Slay CE, Dane A, Crossley II (2013) Plasticity of cardiovascular function in snapping turtle embryos (Chelydra serpentina): chronic hypoxia alters autonomic regulation and gene expression. Am J Physiol Regul Integr Comp Physiol 304:R966–R979CrossRefPubMedGoogle Scholar
- Jones DR, Shelton G (1993) The physiology of the alligator heart: left aortic flow patterns and right-to-left shunts. J Exp Biol 176:247–270Google Scholar
- Joyce W, Elsey R, Wang T, Crossley DA (2018) Maximum heart rate does not limit cardiac output at rest or during exercise in the American alligator (Alligator mississippiensis). Am J Physiol (regulatory, integrative and comparative physiology) (in press)Google Scholar
- Kelly SA, Panhuis TM, Stoehr AM (2011) Phenotypic plasticity: molecular mechanisms and adaptive significance. Wiley, HobokenGoogle Scholar
- Rouwet EV, Tintu AN, Schellings MWM, van Bilsen M, Lutgens E, Hofstra L, Slaaf DW, Ramsay G, le Noble FAC (2002) Hypoxia induces aortic hypertrophic growth, left ventricular dysfunction, and sympathetic hyperinnervation of peripheral arteries in the chick embryo. Circulation 105:2791–2796CrossRefPubMedGoogle Scholar
- Shelton G, Jones D (1991) The physiology of the alligator heart: the cardiac cycle. J Exp Biol 158:539–564Google Scholar
- West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar