Development of cardiac form and function in ectothermic sauropsids

Abstract

Evolutionary morphologists and physiologists have long recognized the phylogenetic significance of the ectothermic sauropsids. Sauropids have been classically considered to bridge between early tetrapods, ectotherms, and the evolution of endotherms. This transition has been associated with many modifications in cardiovascular form and function, which have changed dramatically during the course of vertebrate evolution. Most cardiovascular studies have focused upon adults, leaving the development of this critical system largely unexplored. In this essay, we attempt a synthesis of sauropsid cardiovascular development based on the limited literature and indicate fertile regions for future studies. Early morphological cardiovascular development, i.e., the basic formation of the tube heart and the major pulmonary and systemic vessels, is similar across tetrapods. Subsequent cardiac chamber development, however, varies considerably between developing chelonians, squamates, crocodilians, and birds, reflected in the diversity of adult ventricular structure across these taxa. The details of how these differences in morphology develop, including the molecular regulation of cardiac and vascular growth and differentiation, are still poorly understood. In terms of the functional maturation of the cardiovascular system, reflected in physiological mechanisms for regulating heart rate and cardiac output, recent work has illustrated that changes during ontogeny in parameters such as heart rate and arterial blood pressure are somewhat species-dependent. However, there are commonalities, such as a beta-adrenergic receptor tone on the embryonic heart appearing prior to 60% of development. Differential gross morphological responses to environmental stressors (oxygen, hydration, temperature) have been investigated interspecifically, revealing that cardiac development is relatively plastic, especially, with respect to change in heart growth. Collectively, the data assembled here reflects the current limited morphological and physiological understanding of cardiovascular development in sauropsids and identifies key areas for future studies of this diverse vertebrate lineage.

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

“…The decrease in f H for embryonic snapping turtles during this span of incubation is similar to that documented in the emu (Crossley et al, 2003a) and the desert tortoise (Crossley and Burggren, 2009), but it differs from that in the American alligator (Crossley et al, 2003b;Crossley and Altimiras, 2005;Eme et al, 2011a;Eme et al, 2011b), the embryonic chicken Altimiras and Crossley, 2000) and the African brown house snake (Lamprophis fuliginosus) (Crossley and Burggren, 2009). Resting f H differed significantly (~9beatsmin -1 ) in male and female snapping turtles at 90% of incubation.…”

“…However, the snapping turtle is unique in that the P m response is absent at 90% of embryonic development. In contrast, the bradycardic response to β-adrenergic blockade reported here in common snapping turtles has been previously reported in egg-laying amniotes: it either increases in intensity or is constant during the final third of incubation Crossley et al, 2003a;Crossley and Burggren, 2009;Eme et al, 2011a). This suggests that dependence on β-adrenergic tone to maintain cardiovascular function is a common feature of amniotic development.…”

“…These data suggest that central nervous system regulatory capacity in snapping turtles is functional relatively early in development compared with that of other embryonic reptiles (Crossley et al, 2003b;Crossley and Burggren, 2009;Eme et al, 2011a). Cholinergic receptor tone was present in snapping turtles at both time points, but the intensity was sexually dimorphic at 90% of incubation.…”

“…Data are presented as means ± s.e.m. agassizii) (Crossley and Burggren, 2009), the American alligator (Alligator mississippiensis) (Crossley et al, 2003b;Crossley and Altimiras, 2005;Eme et al, 2011a), the emu (Dromiceius novaehollandiae) (Crossley et al, 2003a) and the domestic chicken (Gallus gallus) . These findings suggest that an increase in blood pressure during ontogeny is a fundamental requirement for maintaining convective transport in embryos that are increasing in body mass.…”

The phylogeny and ontogeny of autonomic control of the heart and cardiorespiratory interactions in vertebrates

“…The Journal of Experimental Biology (2014Biology ( ) doi:10.1242 African brown house snake, Lamprophis fuliginosus (Crossley and Burggren, 2009) (Fig. 6).…”