Periods of cardiovascular susceptibility to hypoxia in embryonic american alligators (Alligator mississippiensis)

Abstract

During embryonic development, environmental perturbations can affect organisms' developing phenotype, a process known as developmental plasticity. Resulting phenotypic changes can occur during discrete, critical windows of development. Critical windows are periods when developing embryos are most susceptible to these perturbations. We have previously documented that hypoxia reduces embryo size and increases relative heart mass in American alligator, and this study identified critical windows when hypoxia altered morphological, cardiovascular function and cardiac gene expression of alligator embryos. We hypothesized that incubation in hypoxia (10% O2) would increase relative cardiac size due to cardiac enlargement rather than suppression of somatic growth. We exposed alligator embryos to hypoxia during discrete incubation periods to target windows where the embryonic phenotype is altered. Hypoxia affected heart growth between 20 and 40% of embryonic incubation, whereas somatic growth was affected between 70 and 90% of incubation. Arterial pressure was depressed by hypoxic exposure during 50-70% of incubation, whereas heart rate was depressed in embryos exposed to hypoxia during a period spanning 70-90% of incubation. Expression of Vegf and PdgfB was increased in certain hypoxia-exposed embryo treatment groups, and hypoxia toward the end of incubation altered β-adrenergic tone for arterial pressure and heart rate. It is well known that hypoxia exposure can alter embryonic development, and in the present study, we have identified brief, discrete windows that alter the morphology, cardiovascular physiology, and gene expression in embryonic American alligator.

Developmental plasticity of mitochondrial function in American alligators,Alligator mississippiensis

“…The relative increase in heart mass may be due to a suppression of somatic growth, a response of the cardiac tissue to hypoxia directly, or to a secondary response due to endocrine or hemodynamic changes in the embryonic system. Although our study cannot distinguish between these possibilities, recent work has identified discrete windows in alligator development where embryonic and cardiac growth are affected by hypoxia differentially (67). Cardiac enlargement results after hypoxic exposure between 20% and 40% of incubation, whereas embryonic growth is suppressed when hypoxia occurs from 70% to 90% of incubation (67).…”

“…Although our study cannot distinguish between these possibilities, recent work has identified discrete windows in alligator development where embryonic and cardiac growth are affected by hypoxia differentially (67). Cardiac enlargement results after hypoxic exposure between 20% and 40% of incubation, whereas embryonic growth is suppressed when hypoxia occurs from 70% to 90% of incubation (67). These results suggest developmental hypoxia increases relative cardiac mass in alligators due to cardiac enlargement and not suppression of somatic growth.…”

Embryonic hypoxia programmes postprandial cardiovascular function in adult common snapping turtles (Chelydra serpentina)

“…Organ masses were also calculated in terms of percentage animal mass {organ mass (g)×[animal mass (g)] −1 ×100}. These proportional data were then arcsine square transformed before performing t-tests, which were also used for absolute organ masses, to compare between the two turtle groups (Crossley et al, 2003;Eme et al, 2011;Tate et al, 2016). Cardiovascular responses to feeding in N21 and H10 turtles were assessed using a one-way repeated-measures (RM) ANOVA, with incubation oxygen (i.e.…”

“…Chronic hypoxia during embryonic development has a profound effect on reptiles, changing the trajectory of phenotype maturation of multiple systems, with a pronounced impact on the cardiovascular system (Kam, 1993;Crossley et al, 2003;Crossley and Altimiras, 2005;Owerkowicz et al, 2009;Eme et al, 2011Eme et al, , 2013Eme et al, , 2014Enok et al, 2013;Tate et al, 2015Tate et al, , 2016Wearing et al, 2016). Over the past decade, our understanding of embryonic cardiovascular development in these species has improved markedly.…”

“…However, very few studies have determined lasting impacts of morphological and physiological phenotypic modifications on juveniles and adults (Owerkowicz et al, 2009;Galli et al, 2016;Wearing et al, 2016). Much of the work that has been conducted so far has illustrated that embryonic reductions in oxygen availability restrict body mass at hatching (Kam, 1993;Crossley and Altimiras, 2005;Owerkowicz et al, 2009;Eme et al, 2011Eme et al, , 2013Eme et al, , 2014Marks et al, 2013;Tate et al, 2015Tate et al, , 2016Crossley et al, 2017b), and this persists into the first years of posthatching life (Owerkowicz et al, 2009;Galli et al, 2016;Wearing et al, 2016). In addition, heart mass is relatively enlarged in embryonic reptiles chronically exposed to low oxygen (Kam, 1993;Crossley and Altimiras, 2005;Eme et al, 2013Eme et al, , 2014Marks et al, 2013;Tate et al, 2015Tate et al, , 2016, which again persists at least into the first years after hatching in American alligators (Owerkowicz et al, 2009;Galli et al, 2016), indicating that developmental hypoxia has a lasting impact on the cardiovascular phenotype of this species.…”