The Interplay of Ontogeny and Phylogeny at the Transcriptome Level of the Tetrapod Heart

The tetrapod heart is characterized by three chambers in amphibians and non-avian reptiles, as opposed to four in birds, crocodilians and mammals. We explored this diversity via the most phylogenetically comprehensive comparison of heart transcriptomes undertaken to date. Transcriptomes representing the ontogeny of heart compartmentalization (septation) in alligator, chicken, frog, mouse, lizard and turtle embryos exhibited a clear species-specific signal, which was driven by genes involved in heart contraction. During the stage dominated by septation-related tissue transformations, the most highly expressed genes shared by species originated before the tetrapods diversified and were related to septum morphogenesis, ventricular development, and chamber formation. The expression of septation-related genes did not adhere to phylogeny or heart chamber number, and genes differentially expressed across developmental stages within species varied in their evolutionary ages and predicted functions. We discuss how the acquisition of novel structures in some lineages, convergent evolution of four heart chambers, embryonic metabolism, microstructural variation, and ontogenetic shifts (heterochronies), collectively, provide insight into evolved and conserved patterns of transcriptome-level variation. These data serve as a resource to further stimulate evo-devo research on complex organ systems, such as the heart.