Sternal morphology in Synapsida

The earliest-diverging synapsids, the paraphyletic pelycosaurs, do not preserve an ossified sternum in any known taxa23. However, a large, ossified interclavicle is always present. The broad interclavicle tends to be mostly uniform in shape (spoon-shaped asper Romer and Price23, with a cruciate anterior part and an elongate posterior rod). The first appearance of an ossified sternum in Synapsida occurs within the diverse and long-lived subclade Therapsida. Although some uncertainty exists as to the relationships between the major therapsid clades, the earliest-diverging group is generally considered to be Biarmosuchia24,25. Few biarmosuchian postcrania are known, but the sternum is preserved in a few taxa (e.g. Hipposaurus26), where it is unipartite and probably incompletely ossified. In known examples the sternum is relatively small compared to the interclavicle and roughly circular in outline (see Fig.1). No sternum is known in the Dinocephalia2,27. As several nearly complete dinocephalian skeletons are known e.g.28,29, it seems that the sternum, if present, must have been cartilaginous in this group, and the lack of discovered sterna is not simply due to incomplete preservation of the bony elements (likely also the case for pelycosaurs).

Anomodontia is the most diverse Permo-Triassic therapsid clade30, and also exhibits a diversity of sternal morphologies. Although an ossified sternum seems to be lacking in basal (non-dicynodont) anomodonts, as indicated by its absence in the well-preserved and fairly complete skeletons of Suminia31, Galechirus, and Galepus32, an ossified sternum is present in Dicynodontia30. In dicynodonts, it is always unipartite and generally a simple, plate-like element (e.g. in Diictodon20 and Eosimops33). However, the sternum is more complex in the burrowing dicynodont Cistecephalus (wide anteriorly, with a strongly tapering posterior edge and pronounced attachment sites for the ribs)19. In the largest known dicynodonts, the Late Triassic stahleckeriids, the sternum is extremely deep dorsoventrally, with a well-developed ventral keel6. The number of ribs attaching to the sternum varies in the clade, with one (e.g. Dinodontosaurus34), two (e.g. Aulacephalodon35), or three (e.g. Cistecephalus19) attachment sites per side.

Few well-described postcrania are known for Gorgonopsia. Previously-described gorgonopsian sterna consist of one element with up to three articulations for ribs on either side (i.e. in the holotypes of Lycaenops ornatus36, Aelurognathus tigriceps36, Aelurognathus microdon37, and Viatkogorgon ivakhnenkoi38). The discovery of an ossified and segmental abaxial sternal structure in Gorgonops torvus, however, raises the possibility that the apparently unipartite sterna of other species reflect incompleteness rather than the true absence of discrete sternebrae. With the exception of V. ivakhnenkoi, the aforementioned specimens were all collected and prepared in the early twentieth century, with damage to the more delicate parts of the anatomy. Also, although complete, well-preserved, and well-prepared, the skeleton of V. ivakhnenkoi is preserved on its side, and the base of the pectoral complex is poorly exposed, making the morphology of the sternum somewhat uncertain.

Similar to the condition in Gorgonopsia, few skeletons of Therocephalia are complete enough to determine whether a sternum was present. An ossified sternum appears to be absent in basal (non-eutherocephalian) therocephalians, as no trace of this element is present even in well-preserved, articulated skeletons of this grade (i.e. Glanosuchus39, Lycosuchus40). However, an ossified sternum is known in a number of eutherocephalian taxa (e.g. Regisaurus22 and Olivierosuchus21) and likely was present throughout that subclade41. In these taxa, the preserved portion of the sternum consists of a single element and is a remarkably large, plate-like structure dwarfing the interclavicle (Fig.1).

Prior to the discovery of the gorgonopsian specimen described here, the earliest record of an ossified multipartite sternum was in the Middle Triassic cynodont Diademodon tetragonus14. No ossified sternal elements are known in any earlier cynodonts (including taxa known from numerous complete skeletons, such as Thrinaxodon), suggesting that the sternum was cartilaginous in those taxa. Therefore, no conclusions can be drawn about the sternal shape in the earliest cynodonts. However, a multipartite sternum is known in several later-occurring non-mammalian cynodonts (e.g. the Jurassic Kayentatherium wellesi17 and Bienotheroides wansienensis18), in which the anteriormost section of the sternum is paired. Although rare, all the non-mammalian cynodont sterna thus far described consist of multiple elements. The connection between all these elements is assumed to have been cartilaginous18.

A fully-ossified multipartite sternum is known in several extinct mammaliaform taxa (e.g. Sinoconodon42, Maiopatagium43, Microdocodon9) (Fig.1) as well as all modern mammals44. Adult monotremes and non-crown group therians retain a distinct interclavicle, which acts as an anchor for the proximal attachment of the clavicle, and the first rib attaches to the largest anterior sternal element (the manubrium). Marsupials and placentals do not preserve an interclavicle as adults, as this element fuses with the manubrium during development. In these taxa, the clavicles and the first ribs both connect to the anteriormost sternal element on either side45.

The new multipartite sternum of a gorgonopsian presented here appears substantially earlier in geological time and is phylogenetically more stemward than any previous records of a mammalian-type sternum. The partial interclavicle shows some similarities to the interclavicles in other gorgonopsian specimens (see Supplementary Fig. S1) as well as those of Therocephalia (e.g. Olivierosuchus21), but the sternum of Gorgonops torvus is novel in its configuration.

The sternal variation within Synapsida discussed above allows us to distinguish between three morphologically differentiated groups:

Synapsids inferred to have an unossified sternum, such as pelycosaurs, dinocephalians, and basal anomodonts, therocephalians, and cynodonts. The lack of an ossified sternum in the predominantly large-bodied Dinocephalia demonstrates that sternal ossification is not necessarily correlated with body size.

Synapsids with usually large, unipartite (singular), and well-ossified sterna, for instance dicynodonts and eutherocephalians. Although it is possible that additional cartilaginous elements were present in life, the lack of a well-developed articular facet on the posterior margin of the sternum in these groups suggests that is unlikely.

Synapsids with segmental and ossified sterna such as Gorgonops torvus, Diademodon tetragonus, Mesozoic mammaliaforms, and extant mammals. The condition in close relatives of Gorgonops and Diademodon is uncertain, due to limited fossil data.

The discovery of the sternal complex of Gorgonops torvus now presents two equally possible hypotheses for the earliest evolution of the mammalian sternum: 1) the mammal-like condition arose first in gorgonopsians (as represented by Gorgonops torvus) but then was lost in eutheriodonts (therocephalians and cynodonts, in which the sternum ancestrally seems to have been cartilaginous) or 2) the condition in Gorgonops torvus evolved convergently to that of cynodonts, originating from a unipartite ancestral state common to both gorgonopsians and eutheriodonts. Until further discoveries of fossil taxa with different sternal conditions provide more evidence, it is impossible to test either of these hypotheses thoroughly, but functional considerations may provide some insight as to which is more likely (see below).

The sternum of extant mammals has several functions. Notably, it helps to reinforce the rib cage, with a more stable, enclosed rib cage offering better protection of the thoracic organs than one exposed abaxially46. Furthermore, an ossified (and hence stronger) sternum is functionally important for forelimb locomotor function, as the ventral surface of the thorax has major attachment sites for pectoral muscles47. These complementary functions of the sternum reflect its integral part in the entire system of the forelimb, the shoulder girdle, and the thorax. In synapsid evolution, there are two major morphologies of ossified sterna (Fig.1): the single, plate-like sternum present in earlier-diverging synapsids (e.g. dicynodonts) and the relatively narrow, segmental sternum seen in cynodonts such as Diademodon, some tritylodontids and mammaliaforms. The shift between these osteological configurations would have been part of a broader suite of functional changes occurring in this section of the synapsid tree.

The origin of mammals is associated with major changes in skeletal morphology, and the stepwise assembly of these changes in Permo-Triassic synapsids has historically been cited as one of the best bodies of evidence for macroevolution in the fossil record48,49. The inferred functional associations (and evolutionary drivers) of these changes can be roughly broken down into three areas: 1. dental (increasing complexity, both from differentiation in the heterodont tooth series, and from elaboration of individual teeth, particularly the postcanines, with multicusped and expanded crowns capable of occlusion); 2. cranial (formation of a complete secondary palate, loss of the postorbital bar, simplification of the jaw elements, increase in brain size/complexity); and 3. postcranial (increased regionalization of the axial column, changes in limb morphology associated with posture, origin of the segmental sternum). Each of these changes has functional implicationsmore efficient food processing driven by changes to the inferred muscular complement and jaw orientation for the craniodental characters50, and more active locomotion associated with an erect gait for the postcranial characters51. Each of these had downstream effects on portions of the anatomy not immediately subject to selection. For example, the expansion of jaw musculature attachment on the dentary is thought to have contributed to the decrease in size of the post-dentary bones and their eventual detachment to form middle ear bones52.

We offer a similar interpretation for the evolution of a segmental sternum in Permo-Triassic therapsids. On its own, this feature would have had little to do with improved gait in mammalsthe forelimbs themselves, the shoulder girdle, and the thoracic vertebral column all have more immediate influences on locomotion. However, the sternum bridges the girdle to the axial skeleton and it is thereforeconnected with shifts in locomotor evolution. And it is involved in two ways of particular note in the evolution of mammal-like morphologies and function: 1. increased regionalization of the axial skeleton and 2. increased posteriorization of thoracic elements. For the former, mammals are well known to have greater differentiation of the axial column into discrete regions than reptiles, although this transition is now thought to be more complex and to have occurred earlier in synapsid evolution than previously believed53. In the typical mammalian condition, the thorax is a highly discrete unit readily distinguished by vertebral morphology, and it also differs in range of motion from the cervical, lumbar, and caudal regions. By contrast, in many reptiles and even early synapsids, the distinction between the thoracic and lumbar regions is less evident, and the cervical-thoracic transition is also difficult to discern54. The origins of the mammal-like rib cage, a structure surrounding the thoracic organs (the heart, lungs and muscular diaphragm), are intimately associated with changes in gait that took synapsids from the lateral undulation of early amniotes to the primarily dorsoventral flexion of mammals47, in a divergent evolutionary path from the evolution of modern reptiles55. In the context of this paradigm shift in synapsid history, a massive, plate-like sternum broadly overlapping the interclavicle would have been a hindrance, a relic of the pelycosaurian condition with sprawling forelimbs in close association with the substrate. In the evolution of theriodonts (the group containing gorgonopsians, therocephalians, and cynodonts), even as early as gorgonopsians there is a shift towards more cursorial locomotion and more erect gaits, with a focus on dorsoventral rather than side-to-side motion51,55. To facilitate this style of locomotion, it was necessary to reduce the size of the pectoral girdle, thereby enhancing its mobility relative to the axial skeleton.

There are multiple ways to reduce the weight of bony elements, one being simply to not ossify them. This may have been the ancestral condition in eutheriodonts, given that the sternum seems to have been cartilaginous in the earliest therocephalians and cynodonts (although this would imply a reversal to the pre-theriodont condition in eutherocephalians). Another is to transform from a single solid plate to a series of connected elements, which can retain the protective function of the sternum without limiting mobility (similar transitions can be seen in the evolution of armor, with trends towards multipartite structures offering greater flexibility56). This latter approach appears to characterize sternal evolution in Gorgonopsia.

Greater flexibility of the thorax also has importance beyond permitting dorsoventral flexion during locomotion, as shown by Jones et al.53,55 in their studies of the axial skeletal evolution in Synapsida. Increased potential for axial twisting can also aid in behaviors such as grooming and fast locomotory maneuvers, but this requires vertebral specializations for torsion. In earlier non-mammalian synapsids (i.e. most non-cynodont taxa), the functional regions of the vertebral column are not as distinct as in later taxa such as advanced cynodonts (e.g. the Jurassic Kayentatherium55), and there is little evidence of selection for performance under torsion in the anterior vertebrae. However, a general phylogenetic trend towards more regionalization into pre- and post-diaphragmic areas of the vertebrate column can be observed even in more stemward portions of synapsid phylogeny55. A more flexible, segmental sternum, as seen in Gorgonops torvus, may represent a prerequisite for accommodating intervertebral torsion in the thorax.

Therefore, we hypothesize that the evolution of the ossified segmental sternum in Theriodontia is a part of the broad evolutionary shift towards more mammal-like locomotion, which may have facilitated the rise of this group as the dominant carnivores of the late Permian. Selection for a lighter, more flexible sternum in the context of changing posture, gait, and vertebral mobility can be inferred regardless of the homology of the segmental sternum in Gorgonopseither this morphology evolved convergently in gorgonopsians and eucynodonts, or it would represent an ancestral adoption retained in cynodont evolution (albeit cartilaginous in taxa other than eucynodonts).

However, posture and gait were not the only major changes in thoracic anatomy occurring in Permo-Triassic therapsids. The transition to a mammal-like thoracic morphology is also tied to the way for therapsids to break Carriers constraint: the respiratory limitation driven by dual use of the axial musculature during lateral flexion and costal breathing during rapid locomotion47. Dorsoventral flexion in mammals, and a more rigid thorax centered more anteriorly along the vertebral column, fundamentally altered synapsid ventilation, permitting both lungs to be expanded or compressed simultaneously, a metabolically more efficient method advantageous for active locomotion. For this to work, however, it is necessary that the dorsal and ventral limits (i.e. the vertebral column and sternum) of the bony enclosures of the lungs (i.e. the rib cage) are both strong and pliable, conferring functional advantage over a single stiff interclavicle-sternal plate in managing volume of the thoracic cavity57. A multipartite sternum with cartilaginous tissue between the manubrium and the sternebrae is consistent with this requirement. However, while this on its own would have helped to reduce the impact of Carriers constraint, actually breaking the constraint required an additional innovation: the diaphragm, a muscular sheet at the base of the thoracic cavity capable of pumping air through the lungs independently of locomotion.

Amongst the basic requirements for a diaphragm is that it must functionally be positioned caudad to the sternum, because by contracting during respiration, it creates negative pressure in the chest that is stabilized by the robust yet flexible complex of ribs, costal cartilages, and the segmental sternum. The origins of the diaphragm are obscure, however; it has been proposed to be unique to mammals or to have originated in some of the earliest pelycosaurs (e.g. caseids)58. Recent research taking data from developmental studies suggests that the diaphragm originated from ancestral pharygneal muscles of the cervico-thoracic region by posteriorization of elements associated with it, i.e. the forelimb bud during development and the brachial plexus nerve59. Accordingly, if the diaphragm did indeed originate from cervico-thoracic pharyngeal muscles, then the two requisite changes associated with the diaphragm may have been well underway in gorgonopsians: a) the posteriorization, evidenced by the likely presence of seven cervical vertebrae60 and the herein described elongate segmental sternum. And b) the elongate configuration itself of the sternum of Gorgonops, providing the needed caudad-positioned attachment for the diaphragm. This indicates that a mammalian-style diaphragm should already have been present in this taxon (and possibly, by inference, in theriodonts generally) to support the changes in ventilatory function.

Ontogenetic development of the sternum is well studied in extant mammals, with a particularly robust literature in the realms of human medicine and mouse embryology, demonstrating that formation of the characteristic segmental sternum is mediated by interactions with the developing ribs15,61. Specifically, the rib tips inhibit skeletal maturation, resulting in ossification of the intermediary regions but maintenance of cartilaginous connections between them62. As such, we must consider whether the segmental sternum would even have been selected for at all, or merely is an inherent consequence of developmental formation of a thoracic rib cage between the axial skeleton and sternum. Here, the fossil record is instructive. The plate-like sternum of dicynodonts has a variable number of rib attachments (see above), but a number of taxa clearly show multiple ribs attached to the single sternal element19. Therefore, it is apparently not an inherent developmental feature of Synapsida that rib attachments inhibit sternal growth and cause segments of the sternebrae to form. Rather, we propose that this system evolved through co-opting developmental mechanisms during a period of selection towards lighter and more jointed thoracic structures. Unfortunately, the cartilaginous nature of these elements in many synapsid groups (notably early cynodonts) makes it difficult to establish a precise understanding of the shift between dicynodont- and therocephalian-like structures and those of mammals. However, discoveries like that of the new Gorgonops specimen provide strong support for an early origin of the functional suite of derived mammalian locomotion and ventilation in the Permian antecedents of the clade.

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