Embryonic hypoxia alters cardiac gene expression patterns in American alligators, Alligator mississippiensis.

Abstract

How environmental conditions during embryogenesis shape development, physiology, and phenotype is a key question for understanding the roles of plasticity and environmental factors in determining organismal traits. Answering this question is essential for revealing how early-life environmental variation drives adaptive responses and influences evolutionary processes. Here we examine how hypoxia impacts cardiac gene expression during embryonic development in the American alligator (Alligator mississippiensis). Eggs were incubated in normoxic (21% O₂) or hypoxic (10% O₂) conditions from 20% to 90% of embryogenesis. Embryos were sampled at 70% and 90% of development to measure gene expression, embryo mass, and organ mass. Hypoxia significantly restricted embryonic growth while enlarging hearts and brains relative to body size. Gene expression analyses show that hypoxia led to upregulation of 182 genes and downregulation of 222 genes, which were enriched in pathways related to muscle contraction, oxygen transport, protein catabolism, and metabolism. Developmental changes in 3,544 genes were associated with cell division, extracellular matrix remodeling, and structural organization. Functional and network analyses highlighted hypoxia-induced shifts in cardiomyocyte physiology, suggesting adaptations to enhance cardiac performance under low oxygen availability. Despite hypoxia-related downregulation of sarcomere and metabolic genes, hypertrophic responses were evident, consistent with previous findings of improved cardiac function in hypoxia-exposed juveniles. Collectively, our findings offer new genome-wide insights into the effects of hypoxia on the embryonic alligator heart, uncovering significant adaptive developmental plasticity. These results have broad implications for understanding how environmental factors shape cardiovascular phenotypes and drive evolutionary responses to hypoxia in reptiles.NEW & NOTEWORTHY This study investigated the impact of hypoxia on the cardiac transcriptome in alligator embryos. Exposure to low oxygen levels induced significant changes in gene networks controlling cardiac contraction, protein catabolism, oxygen transport, pyruvate metabolism, and adrenergic signaling. Ontogenetic changes suggest slowing of cell proliferation and remodeling of the extracellular matrix in the heart as embryos approach the end of incubation. This study provides the first characterization of myocardial gene expression patterns in developing alligator hearts.