The search for sterna

This is step 2 in a search for sterna in the Tetrapoda.
Please consider this a work in progress because several hard-to-find appearances of the single sternum or dual sterna in tetrapods (and one fish, Fig. 9) may have been overlooked. Sterna also tend to come and go. They may be poorly ossified if present. We first and last looked at sternum distribution five years ago here with far fewer taxa. 

The sternum
This second anchor for pectoral muscles may be a single medial element (Fig. 1) or side-by-side elements slightly separated by the posterior process of the medial interclavicle, the first anchor for pectoral muscles. Almost universally the sternum is posterior to the interclavicle (Fig. 1). Sometimes the sternal rim anchors sternal ribs.

Since the sternum seems to be missing
more often than present, the various appearances of this bone in disparate clades appears to be largely convergent—with a genetic underpinning based on anterior gastralia in the most primitive reptiles.

Sometimes, as in birds,
the sternum (breast bone) can be the largest bone in the body.

The most primitive appearance of a sternum is in frogs,
like Rana (st in Fig. 1). Other basal tetrapods lack a sternum, but have a large interclavicle.

Figure 1. Rana the frog. Note the tiny sternum in the upper left inset, posterior to the coracoids.

Figure 1. Rana the frog. Note the tiny sternum in the upper left inset, posterior to the coracoids.

The basalmost reptiles in the LRT,
Gephyrostegus and Silvanerpeton (Fig. 2) have short gastralia in the shape and place of sterna. These are immediately posterior to the coracoids and are precursors that variously evolve into sterna, if they don’t disappear, which happens more often than not.

Immediately following these basalmost reptiles,
the first dichotomy splits the new Lepidosauromorpha and the new Archosauromorpha.

Figure 1. Silvanerpeton and Gephyrostegus to the same scale. Each of the two frames takes five seconds. Novel traits are listed. This transition occurred in the early Viséan, over 340 mya. Gephyrostgeus is more robust and athletic with a larger capacity to carry and lay eggs.

Figure 2. Silvanerpeton and Gephyrostegus to the same scale. Each of the two frames takes five seconds. Novel traits are listed. This transition occurred in the early Viséan, over 340 mya. Gephyrostgeus is more robust and athletic with a larger capacity to carry and lay eggs.

Sterna in basal Lepidosauromorpha:

  1. Thuringothyris has small paired post-coracoid elements not seen in sister taxa.
  2. Stephanospondylus (a pareiasaur ancestor) has an anterior ‘procoracoid’ and a  coracoid apparently not homologous to sterna. No gastralia are present.
  3. Both soft-shell and hard-shell turtles develop a plastron, a set of bones presently considered not homologous with sterna or gastralia.

Figure 3. Saurosternon, the first taxon in the lepidosauromorph lineage with sterna.

Sterna in basal Lepidosauriformes:

  1. Saurosternon (Fig. 3) has paired sterna posterior to the coracoids.
  2. Jesairosaurus has a single, posteriorly indented sternum.

Sterna in Rhynchocephalian Lepidosauria:

  1. Sphenodon has a diamond-shaped sternum, but sister taxa lack one.
Tritosaur pectoral girdles demonstrating the evolution and migration of the sternal elements to produce a sternal complex.

Figure 4. Tritosaur pectoral girdles demonstrating the evolution and migration of the sternal elements to produce a sternal complex.

Sterna in Tritosaurian Lepidosauria:

  1. Almost all tritosaurs (e.g. Huehuecuetzpalli through Cosesaurus, Fig. 4 have a sternum except the hyper-neck taxa, Tanystropheus and Dinocephalosaurus.
  2. All pterosaurs and Longisquama fuse the sternum to the clavicles and interclavicle to form a sternal complex (Fig. 4).

Sterna in Protosquamata and Squamata:

  1. Homoeosaurus has a single sternum.
  2. MFSN 19235 (= ‘Renestosaurus‘) has a single sternum.
  3. Lyriocephalus and Chlamydosaurus have a single sternum.
  4. Moloch and Trioceros have a single sternum.
  5. Eolacerta and Gekko have a single sternum.
  6. Varanus and Tylosaurus have a single sternum.

Sterna in basal Archosauromorpha:

  1. Eldeceeon and Diplovertebron have paired sterna.

Sternal elements in Synapsida
Following these two, the sternum is absent in basal proto-synapsids and basal synapsids.

Sternal elements in Mammalia
In monotremes a string of one to several articulated sternal elements appear (Fig. 5) where the clavicles are green, the interclavicle is red, the sternal manubrium is blue. The interclavicle disappears in the opossum Didelphis and its descendants, all higher therians. Only the manubrium and sternal elements remain. In many placentals the sternal elements fuse together (Fig. 5 image at right) as they anchor dorsal ribs that wrap all the way around from the back.

Figure 1. The pectoral girdle of basal mammals and their relatives. Note the presence of an interclavicle (red), clavicles (green) and a new bone, the manubrium (deep blue), which develops where the sternum develops in other tetrapods.

Figure 5. The pectoral girdle of basal mammals and their relatives. Note the presence of an interclavicle (red), clavicles (green) and a new bone, the manubrium (deep blue), which develops where the sternum develops in other tetrapods.

Sterna in basal Diapsida

  1. Only in Petrolacosaurus and Araeoscelida is a sternum present.
Figure 1. Tangasaurus, Hovasaurus and Thadeosaurus, three marine younginiformes, apparently have no scapula.

Figure 6. Tangasaurus, Hovasaurus and Thadeosaurus, three marine younginiformes, apparently have no scapula.

Sterna in marine Younginiformes and Enaliosauria

  1. Thadeosaurus, and Hovasaurus have paired sterna (Fig. 6).
  2. Tangasaurus has a single large sternum (Fig. 6). these are all basal taxa in this clade.

Sterna in terrestrial Youngininformes and Protorosauria are not present.

Figure 7. Champsosaurus sternum (yellow).

Figure 7. Champsosaurus sternum (yellow).

Sterna in Archosauriformes

  1. Champsosaurus has a small, narrow sternum (Fig. 6). Due to its size and shape a closer examination of related taxa is warranted, but currently a sternum has not been identified.
  2. Crocodylus appears to have a short, broad ‘sternum’ anchoring elongate coracoids, but this is the inter cruciform interclavicle. Basal archosaurs, including basal dinosaurs lack sterna.
Figure 3. Hummingbird skull for comparison to the stilt in figure 2. Image courtesy of Digimorph.org and used with permission.

Figure 8. Hummingbird skull and skeleton. Note the large sternum at bottom, anchoring flight muscles. Image courtesy of Digimorph.org and used with permission.

Sterna in Dinosauria

  1. Scipionyx. Compsognathus and Struthiomimus have paired sterna.
  2. Zhenyuanlong and Tianyuraptor have paired sterna.
  3. Velociraptor, Balaur, HaplocheirusShuuvia and Mononykus have paired sterna.
  4. Limusaurus and Khaan have paired sterna.
  5. Microraptor and Sinornithosaurus have paired sterna.
  6. Troodontids have paired sterna.
  7. Birds (Fig. 8) have large fused sterna, except the enantiornithine, Sulcavism which lacks sterna, replaced with gastralia, as in basalmost reptiles (Fig. 2). Talk about a reversal!!
  8. Camarasaurus, Brachiosaurus, Apatosaurus, and other sauropods have paired sterna.
  9. Psittacosaurus. and ceratopsians have paired sterna. Hard to find them elsewhere.
Figure 1. Rhombichthys, a tiny Late Cretaceous tarpon with deep scutes creating a sternum.

Figure 9. Rhombichthys, a tiny Late Cretaceous tarpon with deep scutes creating a sternum.

Sternum in fish

  1. Rhombichthys (Fig. 9), is a tiny Cretaceous tarpon that looks like an angelfish. Here the ‘sternum’ is created by fusion of several dozen elongate scales that are not pelvic or anal in origin. This is the only sternum present in a fish taxon in the LRT.

Summary
Paired and median sterna appear and disappear throughout the clade Tetrapoda. Since some sterna are small and/or poorly ossified, their distribution within the Tetrapoda may be greater than currently counted. Primitive gastralia proximal to the coracoids appear to be homologous to derived sternal plates proximal to the coracoids. The sternum fuses to the interclavicle and clavicles in pterosaurs and their allies.

Editor’s Note:
WordPress has recently revised their creative methods, now offering buttons for [EDIT], which delivers a blank page permitting no inputs whatsoever and [CLASSIC EDIT], which permits traditional editing. Unfortunately when you press on the [ADD NEW] button you no longer get a blank format ready to be filled, but another blank page permitting no inputs whatsoever. Let’s hope these ‘bugs’ get fixed soon. I have about a week of posts ready to go, but no more possible afterwards given the present ‘bugs’. 


References
Vickaryous MK and Hall BK 2006. Homology of the reptilian coracoid and a reappraisal of the evolution and development of the amniote pectoral apparatus. J Anat. 2006 Mar; 208(3): 263–285. doi: 10.1111/j.1469-7580.2006.00542.x

wiki/Sternum

 

SVP 2018: Rare sternum(?) found in Tawa

Bradley et al. 2018
provide a very rare appearance of theropod sternal plates in several Late Triassic Tawa specimens (Fig. 1), the oldest yet discovered for dinosaurs. They report, “The morphology of all specimens is surprisingly similar to the sterna in avialans in that they bear a sternocoracoidal process, a space along the lateral margin likely homologous to the coracoid facet, costal processes with nutrient foramina in the spaces between them, and a reinforcing ridge possibly homologous to the Pila coracoidea in extant birds.” So this sounds like a single element, not paired plates.

Figure 1. The theropod Tawa compared to the closely related phytodinosaur, Eodromaeus.

Figure 1. The theropod Tawa compared to the closely related phytodinosaur, Eodromaeus.

No basal dino sister taxa in the large reptile tree preserve sternal plates.
In dinosaurs sternal plates appear in derived sauropods, in the basal ornithischian, Haya and most derived ornithischians and among theropods in most taxa derived from Compsognathus. So the appearance of sternal plate(s) in Tawa is odd.

An outgroup taxon,
Pseudhesperosuchus (Fig. 2) nesting at the base of the crocodylomorpha, preserves a narrow interclavicle articulating to the elongate coracoids. Given the phylogenetic bracketing and description, I wonder what they found in Tawa is instead the last interclavicle found in dinosaurs?

Figue 1. A new reconstruction of the basal bipedal croc, Pseudhesperosuchus based on fossil tracings. Some original drawings pepper this image. Note the interclavicle, missing in dinosaurs and the very small ilium, only wide enough for two sacrals. The posterior dorsals are deeper than the anterior ones.

Figue 2. A new reconstruction of the basal bipedal croc, Pseudhesperosuchus based on fossil tracings. Some original drawings pepper this image. Note the interclavicle, missing in dinosaurs and the very small ilium, only wide enough for two sacrals. The posterior dorsals are deeper than the anterior ones.

Bradley et al. report,
“From this new evidence, it is apparent that the distribution of sternal character states across avemetatarsalians shows unexpected variation rather than a stepwise accrual of traits leading to Aves.” No, “unexpected variation” is not the way evolution works. The evidence may have been misinterpreted, or relevant sister taxa may have not been included.

Avemetatarsalia
This traditional, but invalidated clade, Avemetatarsalia, includes pterosaurs, which have a sternal complex (sternum + clavicles + interclavicle). Earlier co-author Nesbitt 2011 scored the sternal complex as a single sternum. That might be a factor in their study. Most paleontologists omit Pseudhesperosuchus and kin from dino origin analyses. This team may have also done so. So I suspect some mixups are happening here. We’ll see. Alert the authors to this possibility, if you know them.

References
Bradley et al. (6 co-authors) 2018. Sternal elements of the early dinosaur Tawa hallae fill a critical gap in the evolution of the sternum in Avemetatatarsalia (Reptilia: Archosauria). SVP abstracts.

Caseid diaphragms? Bogus, bogus, bogus…

Lambertz et al. 2016 imagine
a diving aquatic niche for caseids like Cotylorhyhnchus (Fig. 1), and in order to breathe upon surfacing, a mammal-like diaphragm must have been present.

One of the authors, Dr. Steven Perry, has been working on the origin of the diaphragm for many years. Perry et al. 2010 wrote: despite over 400 years of research into respiratory biology, the origin of this exclusively mammalian structure remains elusive.” (But see below)

According to Wikipedia: “Mammals have diaphragms, and other vertebrates such as amphibians and reptiles have diaphragm-like structures, but important details of the anatomy vary, such as the position of the lungs in the abdominal cavity.” 

And Tegu lizards are known to possess a proto-diaphragm, which separates the pulmonary cavity from the visceral cavity. While not actually capable of movement, it does allow for greater lung inflation, by taking the weight of the viscera off the lungs.”

And “Crocodilians have a muscular diaphragm that is analogous to the mammalian diaphragm. The difference is that the muscles for the crocodilian diaphragm pull the pubis (part of the pelvis, which is movable in crocodilians) back, which brings the liver down, thus freeing space for the lungs to expand.” 

And this important and pertinent note to pet lizard owners:
“If you turn them over and stroke their bellies, they zonk out… Cute?.. NO, Stop! Lizards do not have diaphragms to help them breath. Their ribs moving in and out actually cause their lungs to inflate and deflate. When a dragon is held upside down or on its back, its stomach pushes on its lungs making it difficult for it to breath and will eventually result in suffocation.” Other similar cautionary notes are compiled here.

Unfortunately, Lambertz et al. also revert to an old invalid tradition,
that caseids are basal synapsids. For over five years it has been known that caseids are not basal to synapsids. The large reptile tree nests caseids as sisters to Feeserpeton and Australothyris and all are derived from a sister to Milleretta within the Lepidosauromorpha, not the Archosauromorpha, in which the Synapsida nests. Thus if you want to know if caseids had a diaphragm, you need to look at living lizards, all of which lack a working diaphragm.

Cotylorhynchus romeri

Figure 1. Cotylorhynchus romeri. Extant lizards lack a diaphragm, so caseids also lacked a daphragm.

Given that backstory Lambertz et al. report:
“The origin of the diaphragm remains a poorly understood yet crucial step in the evolution of terrestrial vertebrates, as this unique structure serves as the main respiratory motor for mammals. Here, we analyze the paleobiology and the respiratory apparatus of one of the oldest lineages of mammal-like reptiles: the Caseidae. [1] Combining quantitative bone histology and functional morphological and physiological modeling approaches, we deduce a scenario in which an auxiliary ventilatory structure was present in these early synapsids. Crucial to this hypothesis are indications that at least the phylogenetically advanced caseids might not have been primarily terrestrial but rather were bound to a predominantly aquatic life. Such a lifestyle would have resulted in severe constraints on their ventilatory system, which consequently would have had to cope with diving-related problems. [2] Our modeling of breathing parameters revealed that these caseids were capable of only limited costal breathing and, if aquatic, must have employed some auxiliary ventilatory mechanism to quickly meet their oxygen demand upon surfacing. [3] Given caseids’ phylogenetic position at the base of Synapsida [4] and under this aquatic scenario, it would be most parsimonious to assume that a homologue of the mammalian diaphragm had already evolved about 50 Ma earlier than previously assumed.” [5]

  1. Not valid for the last five years. Caseids are derived from millerettids and are related to non-synapsids with a convergent lateral temporal fenestra. Hence the confusion.
  2. No one imagines caseids as divers. Maybe shoulder deep in shallow streams.
  3. Diving turtles have no such problems upon surfacing.
  4. Wrong again. See above.
  5. This is a ‘just-so’ story built on taxon exclusion and a couple of big IFs. See below for a hypothesis built on phylogenetic bracketing and skeletal morphology.

So while we’re on the topic of diaphragms,
let’s take a look at another possibility in stem mammals. Since basalmost mammals, like the platypus, Ornithorhynchus, have a diaphragm we’re looking for the origin of this lung muscle in earlier taxa.

A likely place to look 
is at the transition from lateral undulation to limb rotation during locomotion. Only at that stage, where both lungs can inflate simultaneously during locomotion (see Carrier’s constraint), can the diaphragm develop.

Figure 2. Chiniquodon had erect hind limbs and sprawling forelimbs, the first stage in parasagittal locomotion, a requirement for the invention of the diaphragm.

Figure 2. Procynochus, Thrinaxoon, Chiniquodon transition to erect hind limbs while keeping sprawling forelimbs. This was the first stage in parasagittal locomotion, a requirement for the invention of the diaphragm and the most likely stage for its origin.

That transition began with the hind limbs on
derived cynodonts (Fig. 2) which slowly evolved parasagittally rotating hind limbs while retaining sprawling fore limbs. Monotreme mammals continue to retain sprawling forelimbs. Parasagittal forelimbs first appear with Juramaia and the later Therians.

Coincidentally (#1)
The lumbar ribs began to shrink in derived cynodons (Fig. 2) disappearing completely in basalmost mammals.

Coincidentally (#2)
The dorsal rib cage becomes pear-shaped in dorsal view (Fig. 3), with narrower ribs anteriorly and wider ribs posteriorly, near the developing diaphragm.

Coincidentaly (#3)
The dorsal vertebrae become differentiated into dorsal and lumbar vertebrae with neural spines angled posteriorly and anteriorly respectively and shorter and longer vertebral lengths respectively.

Coincidentally (#4)
Sternal ribs, sternebrae, a manubrium and xiphoid process all appear in basalmost mammals, likely signaling the completion of the evolution of the diaphragm.

Coincidentally (#5)
the vertebral column in vivo develop an arch in lateral view (Fig. 3) with a rise to the base of the rib cage followed by a lumbar decent to the sacrals.

Coincidentally (#6)
The external nares become anteriorly oriented, confluent and the premaxillary ascending process disappears, facilitating greater volumes and velocities with every breath.

Figure 1. Megazostrodon, an early mammal, along with Hadrocodium, a Jurassic tiny mammal.

Figure 3 Megazostrodon, an a Jurassic mammal, along with Hadrocodium, a Jurassic tiny mammal.

In summary
in the transition from Cynodontia to Mammalia many changes occurred in the rib cage. Such changes are the most likely skeletal markers for the origin of the soft tissue diaphragm. Such changes are not seen in caseids, which, in any case, are related to lizards not mammals.

I have not read the Lambertz paper,
only the abstract, but with caseids unrelated to mammals, they are sadly barking up the wrong tree. Based on a false premise, that paper was a complete waste of time to produce. Build your papers on a solid phylogenetic foundation and everything will into place naturally.

References
Lambertz M, Shelton CD, Spindler F & Perry SF 2016. A caseian point for the evolution of a diaphragm homologue among the earliest synapsids. Annals of the New York Academy of Sciences (advance online publication) DOI: 10.1111/nyas.13264. http://onlinelibrary.wiley.com/doi/10.1111/nyas.13264/full
Merrell AJ and Kardon G 2013. Development of the diaphragm – a skeletal muscle essential for mammalian respiration. FEBS Journal 280(17): 4026-4035.
Perry SF, Similowski T, Klein W and Codd JR 2010. The evolutionary origin of the mammalian diaphragm. Repiratory Physiology & Nuerobiology 171(1):1-16.
Zimmer C. 2015. Behind Each Breath, an Underappreciated Muscle. The New York Times 04/07/2015.

Let’s look at the sternum!

Everyone thinks they have a sternum.
But it’s not the same sternum that lizards have, or birds have or frogs have. Let’s take a closer look.

In the large reptile tree an ossified sternum appears about seven times:

  1. Rana the frog
  2. Palaeagama, Jesairosaurus and the rib gliders + Megachirella and Pleurosaurus + Tritosauria + Squamata (sans Eichstaettisaurussnakes) (sans ShinisaurusOphisaurus)
  3. Sphenodon and Kallimodon
  4. Petrolacosaurus + Araeoscelis
  5. Hovasaurus + Tangasaurus + Thadeosaurus
  6. LImusaurus through birds
  7. Haya and Heterodontosaurus

Note there are no synapsids
(including mammals) on this list. Note also the sternum is not present in basal tetrapods and basal amniotes. The sternum in fenestrasaurs, including pterosaurs is actually the sternal complex (clavicles + interclavicle + sternum). And finally, there does not appear to be a sternum in the mesosaur, Stereosternum.

Figure 1. The pectoral girdle of basal mammals and their relatives. Note the presence of an interclavicle (red), clavicles (green) and a new bone, the manubrium (deep blue), which develops where the sternum develops in other tetrapods.

Figure 1. The pectoral girdle of basal mammals and their relatives. Note the presence of an interclavicle (red), clavicles (green) and a new bone, the manubrium (deep blue), which develops where the sternum develops in other tetrapods. Click to enlarge. Image modified from Luo, Ji and Yuan 2007.

In mammals
what we call a sternum is actually a novel set of bones forming a ventral anchor for the ribs (as the sternum does in most tetrapods). The interclavicle is retained in basalmost mammals, but it too disappears in higher forms only to be replaced by these novel rib anchors.

I had no idea about this
until I found the Luo et al. 2007 reference. Thought I’d share it with you, especially if you need to get up to speed, like I did.

References
Luo Z-X,  Ji Q and Yuan C-X 2007. Convergent dental adaptations in pseudo-tribosphenic and tribosphenic mammals. Nature 450, 93-97. doi:10.1038/nature06221

The many and varied origins of the sterna (plural of sternum)

Basal reptiles appear do not have sterna. Neither do they have a sternum. Birds have ’em. We (mammals) have ’em. Lizards have ’em.  Crocs and turtles don’t. So what’s the story?

Figure 1. Saurosternon, the first taxon in the lepidosauromorph lineage with sterna. But don’t they look like posterior extensions to the coracoid?

I can’t find sterna within the new Lepidosauromorpha before Saurosternon (Fig. 1), a skull-less, but otherwise completed taxon with long fingers and large feet. This arboreal taxon nests at the base of the Lepidosauriformes and has twin sterna that look like posterior extensions to the coracoids (convergent with metacoracoids in therapsids and araeoscelids).

Homoeosaurus

Figure 2. Homeosaurus, a sister to Dalinghosaurus

These sterna fuse to become a sternum in Sphenodon and Homoeosaurus (fig. 2 and presumably their last common ancestor, Gephyrosaurus, but it is no preserved), where they create gliding paths for the coracoids to roll upon in most living lizards. The sternum shifts anteriorly in fenestrasaurs then fuses to the interclavicle and clavicles in Longisquama + pterosaurs where this combo becomes known as the sternal complex. Other than here and in the basal lizard, Huehuecuetzpalli, there is no trace of a sternum in other tritosaurs, including drepanosaurs or tanystropheids. Lizards with legs (including the worm-like Bipes) have a sternum. Those that don’t, including snakes, lack a sternum.

Among the new Archosaurmorpha, there are no sterna until one gets to primitive mammals.  The sterna appear as segments growing from the posterior of the very much shortened interclavicle (the anteriormost sternal bone that articulates with the clavicles.)  The manubrium (anteriormost sternal bones) appear paired in Bienotheroides, but fused in all others.

Araeoscelis and the appearance of sternae

Fig 3. Araeoscelis and the appearance of sterna between the metacoracoids.

The next sternum appears in Araeoscelis (Fig. 3), as a central bone or bones above the elongated interclavicle and between the metacoracoids. Altogether these bones create in immobile pectoral girdle. There is no such sternum in Galechirus, a therapsid which includes metacoracoids. Thadeosaurus has paired sterna. Again creating an immobile girdle. No enaliosaurs have a sternum. The giant coracoids do the job.

Prolacertiformes don’t have sterna. Neither do choristoderes. Neither do any of the basal archosauriformes. The sternum reappears in Archaeopteryx and sterna appear in Velociraptor. In more primitive theropods in situ gaps suggest an unossified sternum was present. In both of these birdy taxa the coracoids had transformed into immobile struts, a morphology indicative of flapping.

Alright, so, the sternum, or sternal bones, are not primitive to reptiles, but develop and disappear independently and convergently in several lineages.

As always, I encourage readers to see specimens, make observations and come to your own conclusions. Test. Test. And test again.

Evidence and support in the form of nexus, pdf and jpeg files will be sent to all who request additional data.