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Anatomical and Physiological Peculiarities of the Heart in Jawless and Jawed Fish

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Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

The heart is … an organ that gives motion to circulatory fluid

(Randall, Davie, 1980)

The word heart is used to denote chambered circulatory pumps, but is also applied to any segment of the circulation that pumps fluid

(Simões-Costa et al., 2005)

Abstract

The heart of jawless fish (Cyclostomata; lamprey, hagfish) and jawed fish (Teleostei) is homologous to the heart of higher vertebrates. A study of this organ in archaic Cyclostomata and Teleostei, which are different in their evolutionary “ages”, genetic characteristics and hypoxia tolerance, is of particular interest in the search for the factors that determine myocardial resistance to oxygen deficiency. Cyclostomata and Teleostei share the same branchial type of respiration and the presence of only one circle of blood circulation. The principal contractile organ that provides blood circulation, the branchial heart, consists of two chambers. Hagfish make up the oldest class of extant vertebrates whose circulation is maintained by the non-innervated (aneural) branchial heart and three sets of accessory “hearts”. Lampreys are the first vertebrates whose heart receives innervation from the vagus nerve. In turn, Teleostei are the first to receive sympathetic innervation of the heart from the vagosympathetic trunks. In the heart of Cyclostomata and Teleostei, no signs of the cardiac conduction system similar to that in higher vertebrates were found, which does not negate the existence of a well-coordinated mechanism for the propagation of myocardial excitation–contraction coupling. The mechanism of heart rhythm generation links the electrical processes that arise in the myocardium with the expression of hyperpolarization-activated cyclic nucleotide-gated channels (HCN channels). In the heart of hagfish and teleosts, six isoforms of HCN channels are expressed. The regulated distribution density of HCN channels in the myocardium may be a precursor of the cardiac conduction system which characterizes higher vertebrates. The expression of the three cardiac HCN isoforms (HCN2, HCN3 and HCN4) in such a relict taxon as hagfish suggests their presence in the myocardium of the common ancestor of vertebrates before the divergence with Myxiniformes. This may also suggest a particular significance of HCN2, HCN3 and HCN4 in the formation of cardiac activity at the time of the emergence of a multi-chambered myogenic heart. It is assumed that the evolutionary progress in the archaic groups of primitive vertebrates was aimed at the “creation” of a faster effector system for the regulation of cardiac activity and dual (excitatory/inhibitory) control of myocardial functions.

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Funding

This study was implemented within State assignments to Kovalevsky Institute of Biology of the Southern Seas of the Russian Academy of Sciences (reg. no. АААА-А18-118021490093-4 and АААА-А18-118020790229-7) and supported by the Russian Foundation for Basic Research (projects no. 20-04-00037 and 20-44-920001).

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  1. Kovalevsky Institute of Biology of the Southern Seas, Russian Academy of Sciences, Sevastopol, Russia

    Е. E. Kolesnikova

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  1. Е. E. Kolesnikova
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Correspondence to Е. E. Kolesnikova.

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Russian Text © The Author(s), 2021, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2021, Vol. 57, No. 2, pp. 103–123https://doi.org/10.31857/S0044452921020029.

Translated by A. Polyanovsky

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Kolesnikova, Е.E. Anatomical and Physiological Peculiarities of the Heart in Jawless and Jawed Fish. J Evol Biochem Phys 57, 185–207 (2021). https://doi.org/10.1134/S0022093021020022

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