Comparative analysis of the cardiac structure and transcriptome of scallop and snail, perspectives on heart chamber evolution.

Unlabelled: The evolution of a two-chambered heart, with an atrium and a ventricle, has improved heart function in both deuterostomes (vertebrates) and some protostomes (invertebrates). Although studies have examined the unique structure and function of these two chambers, molecular comparisons are few and limited to vertebrates. Here, we focus on the two-chambered protostome heart of the mollusks, offering data that may provide a better understanding of heart evolution. Specifically, we asked if the atrium and ventricle differ at the molecular level in the mollusk heart. To do so, we examined two very different species, the giant African land snail () and the relatively small, aquatic yesso scallop (), with the assumption that if they exhibited commonality these similarities would likely reflect those across the phylum. We found that, although the hearts of these two species differed histologically, their cardiac gene function enrichments were similar, as revealed by transcriptomic analysis. Furthermore, the atrium and ventricle in each species had distinct gene function clusters, suggesting an evolutionary differentiation of cardiac chambers in mollusks. Finally, to explore the relationship between vertebrate and invertebrate two-chambered hearts, we compared our transcriptomic data with published data from the zebrafish, a well-studied vertebrate model with a two-chambered heart. Our analysis indicated a functional similarity of ventricular genes between the mollusks and the zebrafish, suggesting that the ventricle was differentiated to achieve the same functions in invertebrates and vertebrates. As the first such study on protostomes, our findings offered initial insights into how the two-chambered heart arose, including a possible understanding of its occurrence in both protostomes and deuterostomes.

Supplementary Information: The online version contains supplementary material available at 10.1007/s42995-023-00202-0.