Development and evolution of the metazoan heart

Abstract

The mechanisms of the evolution and development of the heart in metazoans are highlighted, starting with the evolutionary origin of the contractile cell, supposedly the precursor of cardiomyocytes. The last eukaryotic common ancestor is likely a combination of several cellular organisms containing their specific metabolic pathways and genetic signaling networks. During evolution, these tool kits diversified. Shared parts of these conserved tool kits act in the development and functioning of pumping hearts and open or closed circulations in such diverse species as arthropods, mollusks, and chordates. The genetic tool kits became more complex by gene duplications, addition of epigenetic modifications, influence of environmental factors, incorporation of viral genomes, cardiac changes necessitated by air‐breathing, and many others. We evaluate mechanisms involved in mollusks in the formation of three separate hearts and in arthropods in the formation of a tubular heart. A tubular heart is also present in embryonic stages of chordates, providing the septated four‐chambered heart, in birds and mammals passing through stages with first and second heart fields. The four‐chambered heart permits the formation of high‐pressure systemic and low‐pressure pulmonary circulation in birds and mammals, allowing for high metabolic rates and maintenance of body temperature. Crocodiles also have a (nearly) separated circulation, but their resting temperature conforms with the environment. We argue that endothermic ancestors lost the capacity to elevate their body temperature during evolution, resulting in ectothermic modern crocodilians. Finally, a clinically relevant paragraph reviews the occurrence of congenital cardiac malformations in humans as derailments of signaling pathways during embryonic development.

Key Findings

• The cardiac regulatory toolkit contains many factors including epigenetic, genetic, viral, hemodynamic, and environmental factors, but also transcriptional activators, repressors, duplicated genes, redundancies and dose‐dependancies.

• Numerous toolkits regulate mechanisms including cell‐cell interactions, EMT, mitosis patterns, cell migration and differentiation and left/right sidedness involved in the development of endocardial cushions, looping, septum complexes, pharyngeal arch arteries, chamber and valve formation and conduction system.

• Evolutionary development of the yolk sac circulation likely preceded the advent of endothermy in amniotes.

• Parallel evolutionary traits regulate the development of contractile pumps in various taxa often in conjunction with the gut, lungs and excretory organs.