Comparative analysis of avian hearts provides little evidence for variation among species with acquired endothermy

Abstract

Mammals and birds acquired high performance hearts and endothermy during their independent evolution from amniotes with many sauropsid features. A literature review shows that the variation in atrial morphology is greater in mammals than in ectothermic sauropsids. We therefore hypothesized that the transition from ectothermy to endothermy was associated with greater variation in cardiac structure. We tested the hypothesis in 14 orders of birds by assessing the variation in 15 cardiac structures by macroscopic inspection and histology, with an emphasis on the atria as they have multiple features that lend themselves to quantification. We found bird hearts to have multiple features in common with ectothermic sauropsids (synapomorphies), such as the presence of three sinus horns. Convergent features were shared with crocodylians and mammals, such as the cranial offset of the left atrioventricular junction. Other convergent features, like the compact organization of the atrial walls, were shared with mammals only. Pacemaker myocardium, identified by Isl1 expression, was anatomically node‐like (Mallard), thickened (Chicken), or indistinct (Lesser redpoll, Jackdaw). Some features were distinctly avian, (autapomorphies) including the presence of a left atrial antechamber and the ventral merger of the left and right atrial auricles, which was found in some species of parrots and passerines. Most features, however, exhibited little variation. For instance, there were always three systemic veins and two pulmonary veins, whereas among mammals there are 2–3 and 1–7, respectively. Our findings suggest that the transition to high cardiac performance does not necessarily lead to a greater variation in cardiac structure.

Smooth Muscle in Cardiac Chambers is Common in Turtles and Extensive in the Emydid Turtle,Trachemys scripta

“…Extensions of left atrial myocardium that partially envelop the pulmonary veins, known as “myocardial sleeves,” have been well described in mammals and birds (Nathan and Gloobe, ; Roux et al ., ; Kroneman et al ., ), but were not seen in corn snakes or anole lizards (Jensen et al ., ). Where we could clearly observe the pulmonary veins in T. scripta (Fig.…”

Reptiles as a Model System to Study Heart Development

“…In mammals, the embryo develops an SV, which later becomes the caval vein myocardium that activates together with the atrial myocardium (Spach et al 1972;Opthof 1988;Steding et al 1990;Faber et al 2019). The walls of the atrial and ventricular chambers of reptiles are readily distinguishable from the chamber walls of mammals and birds by their very extensive layer of fine trabecular muscle (Jensen et al 2016aBoukens et al 2019;Kroneman et al 2019). Because the chamber walls are largely trabecular, much of the myocardium can be nourished by the blood of the chamber lumens (Ostadal et al 1999; Sedmera and Ostadal 2012).…”

“…There is little or no myocardium in the pulmonary venous walls (Joyce et al 2019). Most mammals and all birds have myocardium in the intrapericardial part of the pulmonary veins (Nathan and Gloobe 1970;Rowlatt 1990;Kroneman et al 2019). In reptiles, there are three caval veins connected to the right atrium as is the case in most tetrapods (Benninghoff 1933;Farrell et al 1998).…”

“…This conjecture is based on four observations. First, the sinuatrial valve is found in amphibians, reptiles, birds, and monotremes (Benninghoff 1933;Jensen et al 2017b;Kroneman et al 2019). Second, amphibians, reptiles, birds, monotremes, and marsupials develop their atrial septum from the primary septum only (Röse 1889(Röse , 1890Runciman et al 1995;Jensen et al 2019).…”

“…1; Kardong 2006;Zhang et al 2014). Birds, however, are endothermic, or warm-blooded, as they have much higher metabolic rates than reptiles (Geiser et al 2017) and their hearts have multiple anatomical and physiological specializations (Smith et al 2000;Kroneman et al 2019). Herein, "reptiles" will be used to mean ectothermic sauropsids.…”