The evolutionary origins of cardiac chambers

XAVIER-NETO, Jose*; SIM�ES-COSTA, Marcos S; Instituto do Coracao HC FMUSP; Instituto do Coracao HC FMUSP: The evolutionary origins of cardiac chambers

We suggest cardiac chambers evolved from anterior-posterior patterning of invertebrate peristaltic pumps, which lack efficient coordination between inflow/outflow. Strong evidence implicates retinoic acid (RA) signaling in this process. In amniotes, a caudorostral wave of the RA-synthetic enzyme RALDH2 patterns the cardiac field into inflow/outflow. The wave forms by a dynamic pattern rather than cell migration and studies in amphibians and fishes indicate it is ancestral in vertebrates. Cephalochordates, utilize 4 smooth muscle-powered vessels to drive their circulation. Urochordates centralized circulatory work in pump powered by striated muscle and encased in pericardium. Likewise, vertebrates concentrated work in the striated muscle-powered, pericardially-enclosed heart. In the traditional phylogeny similarities between urochordate and vertebrate pumps reflect inheritance of characters in the chordate ancestor. Thus, urochordates maintained the striated pump, cephalochordates regressed to a decentralized, smooth muscle system, while vertebrates developed chambers. Alternative phylogenies grouping urochordates with vertebrates provide solutions for pump similarities in these taxa, and suggest the rudimentary design of cephalochordates is primitive rather than regressed. Thus, the urochordate/vertebrate ancestor concentrated circulatory work in a striated, pericardially-enclosed pump. Urochordates further centralized circulatory work eliminating auxiliary pumps. Vertebrates created chambers, while maintaining redundancy in accessory pumps present in many species. While it is premature to decide between scenarios, the study of chordate RALDH2 expression patterns may shed light on how vertebrate hearts evolved from chordate pumps.

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