Origin of the unique ventilatory apparatus of turtles

Abstract

The turtle body plan differs markedly from that of other vertebrates and serves as a model system for studying structural and developmental evolution. Incorporation of the ribs into the turtle shell negates the costal movements that effect lung ventilation in other air-breathing amniotes. Instead, turtles have a unique abdominal-muscle-based ventilatory apparatus whose evolutionary origins have remained mysterious. Here we show through broadly comparative anatomical and histological analyses that an early member of the turtle stem lineage has several turtle-specific ventilation characters: rigid ribcage, inferred loss of intercostal muscles and osteological correlates of the primary expiratory muscle. Our results suggest that the ventilation mechanism of turtles evolved through a division of labour between the ribs and muscles of the trunk in which the abdominal muscles took on the primary ventilatory function, whereas the broadened ribs became the primary means of stabilizing the trunk. These changes occurred approximately 50 million years before the evolution of the fully ossified shell.

Revision of the Triassic European turtlesProterochersisandMurrhardtia(Reptilia, Testudinata, Proterochersidae), with the description of new taxa from Poland and Germany

“…nov., and Proganochelys quenstedti, which were personally studied by the first author, was scored based on the literature: Australochelys (Gaffney & Kitching, 1994; Dracochelys (Gaffney & Ye, 1992;Brinkman, 2001); Kayentachelys (Gaffney et al, 1987;Sterli & Joyce, 2007;Gaffney & Jenkins, 2010); Meiolania (Gaffney, 1983(Gaffney, , 1985(Gaffney, , 1996; Odontochelys semitestacea (Li et al, 2008;Lyson et al, 2014); Ordosemys (Brinkman & Wu, 1999;Tong, Ji & Ji, 2004); Palaeochersis (Rougier et al, 1995;; Solnhofia (Gaffney, 1975a;Joyce, 2000); Xinjiangchelys (Kaznyshkin, Nalbandyan & Nesov, 1990;Peng & Brinkman, 1993;Matzke et al, 2004;Brinkman et al, 2013); Platychelys (Wagner, 1853;Br€ am, 1965;Cadena & Joyce, 2015); Ninjemys (Gaffney, 1992); Pleurodira (Gaffney et al, 2006(Gaffney et al, , 2011; Kallokibotion (Nopcsa, 1923b;Gaffney & Meylan, 1992); Otwayemys (Gaffney et al, 1998); Judithemys (Parham & Hutchison, 2003); Chubutemys (Gaffney et al, 2007;Sterli, de la Fuente & Umazano, 2013a); Sinemys (Brinkman, 1993;Tong & Brinkman, 2013); Niolamia (Sterli & de la Fuente, 2011); Mongolochelys (Khosatzky, 1997;…”

Pulmonary anatomy and a case of unilateral aplasia in a common snapping turtle (Chelydra serpentina): developmental perspectives on cryptodiran lungs

“…CT and MR imaging are increasingly being used as diagnostic techniques in the veterinary clinic for non-mammalian taxa (Valente et al 2007;Summa et al 2012;Glodek et al 2016;Nardini et al 2016); however, the use of segmented models is largely absent, despite the growing use of these methods in the biological and paleontological sciences (Schachner et al 2013Bourke et al 2014;van de Kamp et al 2014;Lyson et al 2014;Porter et al 2016). Some research groups are even incorporating 3D digital models with their publications as 3D PDFs, which permits readers to manipulate anatomical structures so that they may be viewed in 3D from any angle (van de Kamp et al 2014;Porter et al 2016).…”

“…Recent advancements in imaging technology and three-dimensional (3D) visualization software permits the creation of in situ digital models of the soft tissues and air spaces within the lung and air sacs of living animals, which facilitates a better understanding of form and function relationships in living pulmonary tissues. These techniques, along with anatomical correlates and mathematical modeling, have been used in several species to infer the morphology of the ancestral amniote lung (Lambertz et al 2015), as well as the origin of ventilatory mechanisms in mammals , turtles (Lyson et al 2014), archosaurs (Farmer & Sanders, 2010;Schachner et al 2013), and dinosaurs (Carrier & Farmer, 2000;Schachner et al 2009Schachner et al , 2011.…”

Recent advances on the functional and evolutionary morphology of the amniote respiratory apparatus

“…In order to avoid any further confusion, either with the mammalian or crocodilian muscles with the corresponding name, "M. diaphragmaticus" in turtles should be replaced by M. transversus thoracis. 77 Theoretically, this unique ventilatory mechanism must have originated before the evolution of the shell. The crucial questions, however, are.…”

“…Potential osteological correlates for muscle attachments were discovered only on the third, sixth, and seventh ribs, while ribs four and five lacked such indications. 77 These putative attachment sites were restricted to the caudal edges of ribs 3, 6, and 7, making them unlikely to represent intercostal muscles. This distribution of muscle attachments, however, corresponds well with the origin of the main expirator in extant turtles, the M. transversus, which is bipartite in nature and composed of a thoracic (M. t. thoracis) and abdominal (M. t. abdominis) portion.…”