In recent months
I’ve been applying tetrapod skull bone homologies to cartilaginous shark skulls (Fig. 1). This has never been done before because paleontologists and ichthyologists do not consider cartilage homologous with bone. Only a few fish skull names have tetrapod homologs. That number increases with lungfish and crossopterygians, because these taxa approach the tetrapod grade. Even so, wouldn’t it be better if all craniate skull bones and cartilage had tetrapod names. Is it even possible?
at least in the large reptile tree (LRT, 1775+ taxa), sharks follow sturgeons and paddlefish. Sharks precede bony fish based on the application of tetrapod skull bone homologies to all fish. But is this possible? Some say no.
Sharks, lacking bone, provide a controversy without possible resolution
according to some workers. So, how can we keep sharks in the LRT and score them with the present set of characters? Maybe the divide is not so divisive after all, contra tradition.
Let’s look at
two available lines of evidence (Figs. 1, 2).
Figure 1. Squalus skull in dorsal view. Changing the contrast enables seeing the cartilage sutures that had bone precursors. The pineal opening homolog is between the nasals and frontals here.
The first line of evidence
is a dorsal view photo of the dogfish (Squalus) skull (Fig. 1). It is made of cartilage, but you can’t tell that by looking at this photo. Normally bright white, the skull image above has been multiplied in several layers of Photoshop to bring up the contrast. One more multiplied layer provides colors and labels. This process is called Digital Graphic Segregation or DGS and is being used more and more often in paleontology, especially in µCT scans. I’ve been using DGS since 2003.
In the old days of black and white plus halftone publication in journals
outline tracings were used because color incurred an extra charge. With online publishing, color is not an extra charge. So, why not use it?
Here in the dorsal view of the skull of the dogfish, Squalus,
(Fig. 1) the tetrapod-homolog nasal (pink) is still out front, over the nares. The circumorbital cartilage has sutures that match the prefrontal (brown) and postfrontal (orange). Sutures also mark the intertemporal (yellow-green), supratemporal (green) and tabular (red) rimming the lateral cranium. The parietal (lavender) and post parietal (tan) appear to have switched places here, but that is due to a previous complete splitting and re-melding of the parietal in more primitive taxa.
In sturgeons, paddlefish and sharks the jaws
are often separate from the cranium. The upper jaw (= traditional palatoquadrate) here (Fig. 2 color overlay) consists of the large lacrimal + jugal + preopercular + quadrate all fused together. The tooth-bearing premaxilla and maxilla are thin sheets on the jaw rims. Shark teeth have no roots, so the premaxilla and maxilla need not be deeper. In fish and tetrapods with tooth roots the premaxilla and maxilla are deeper and the lacrimal shrinks.
Figure 2. Online diagrams of a shark skull with all sutures obliterated with an airbrush. Compare to figure 1, a real shark (Squalus) skull.
The alternative view
(Fig. 2, gray layer) comes in the form of an airbrushed diagram of a shark skull that does not show any sutures. Even so, DGS colors can still be added based on the bumps and valleys of skull topography. Figure 2 is a generalized shark skull done freehand. It has labels. That’s good for translating traditional shark nomenclature to tetrapod nomenclature, but such diagrams do not provide the overlooked details present in photography.
If this method and attitude toward sharks skulls is adopted
Squalus (Fig. 1) will no longer have to disqualify itself from tetrapod homologies based on skull sutures and architecture. Actually, Squalus is a great example of the homologies found in shark cartilage and tetrapod bone. Graphically the two cannot be distinguished from one another. Present day diagrams lacking necessary details (Fig. 2) need to be updated to reflect tetrapod homologies. If cartilage or bone sutures are obliterated on certain taxa, then we can use skull topography and phylogenetic bracketing to estimate where the fusion took place, or score the suture for fusion. Some birds likewise fuse skull elements. That doesn’t seem to be a problem for ornithologists.
Some notes from the literature follow.
While describing the origin of the fish skull, Richter and Underwood 2019 report: “The evolutionary origin of the brain and braincase of fishes remains largely elusive.”
Adding taxa to the LRT has improves that situation, revealing a tree topology featuring the gradual accumulation of derived traits among all included taxa that all cladograms are supposed to have, but too often don’t.
“The development of the vertebrate skull is dependent on the presence of an embryonic neural crest whose cells migrate to induce the formation of various elements of the cranial skeleton, dentitions and certain soft tissues. Much progress has been made in the understanding of the vertebrate skull since pioneering anatomical descriptions made last century.”
So, which is it? ‘remains elusive‘ or ‘much progress‘? This is no reason to build up drama. This is science, not Shakespeare. Just start with ‘much progress’ if that is so.
“In the last few decades, studies involving micro-anatomy, ontogenetic development, molecular biology and gene expression have shed light on key developmental processes that seem to be widely shared among vertebrates. However, molecular biology and ontogenetic studies have been restricted to a small number of fish species.”
As readers know, molecular studies (= genomics) recover false positives way to often. Toss out the gene studies. Add fossils. Score traits. See what the software recovers. Phenomics works better than genomic ichthyologists ever imagined.
Figure 3. Pineal body in a primitive jawless fish, like the lamprey.
Richter and Underwood continue:
“There is still much uncertainty about precise homologies between parts of the skull of distinct groups of fishes, due to the fact that the vertebrate skull shows a remarkable morphological and anatomical plasticity.”
As readers know, precise homologies have been offered here between parts of the skull of distinct groups of fishes while maintaining a standard gradual accumulation of derived traits. The Early Carboniferous nurse shark, Tristychius (Fig. 4), is a good example of how DGS can work on a µCT scan.
Figure 1. CT scans of Tristychius skull from Coates et al. 2019.
ScienceDirect.com presented some traditional thinking
on the topic of shark chondrocrania. Several shark experts helped produce this online summary.
Iuliis and Pulera 2011 provide a definition:
“The chondrocranium is the large single element of the head skeleton.. It surrounds and provides support for the brain and sense organs.”
You’ll notice the skull (= chondocranium, Fig. 1) can have several openings and medial fenestra in dorsal view in some sharks. Most of these correspond to narial, optical, spinal and pineal openings (close to the nasals), plus space for various jaw muscles, as in all craniates. On top of the nasal in sharks is a large pre-cerebral cavity typically not found in tetrapods, sturgeons or bony fish. The cavity communicates posteriorly with the cranial cavity by way of the pre-cerebral fenestra. In life this area is filled with gelatinous material. Rostrum cartilage in sharks is spongy and flexible, allowing the shark to absorb considerable impact with its nose.
“This chapter provides the anatomy of the shark. [which] belongs to Chondrichthyes, which first appeared in the Silurian Period and is among the earliest to branch off from the rest of the gnathostomes (jawed vertebrates).
By contrast the LRT recovers sharks derived from paddlefish and bony fish derived from hybodontid sharks. Sharks are not a separate clade. Tetrapods, including mammals are highly derived hybodontid sharks.
“Among the specialized features that unite these groups [Chondrichthyes] are unique perichondral and endochondral mineralization, distinctive placoid scales, an inner ear that opens externally through the endolymphatic duct, pelvic claspers in males, and a cartilaginous skeleton.”
“The perichondrium is a dense layer of fibrous connective tissue that covers cartilage in various parts of the body.”
“Endochondral ossification takes place at the base of the skull, vertebrae, hips, and limbs through the replacement of a cartilaginous rudiment with bone.”
Pelvic claspers also appear, by convergence, in placoderms.
“The tail and caudal fin are generally reduced and often whip–like. Locomotion is accomplished through wave-like flapping of the fins rather than lateral undulations of the trunk and tail.”
This is false. Generally we see rays, skates and chimaera swimming by flapping their pectoral fins. Sharks swim with rhythmic undulations of the torso tipped by a large V-shaped tail.
Chondrocranium: according to Wikipedia
“In cartilaginous fishes (e.g. sharks and rays) and agnathans (e.g. lampreys and hagfish), the chondrocranium persists throughout life. Embryologically, the chondrocranium represents the basal cranial structure, and lays the base for the formation of the endocranium in higher vertebrates.”
Dermal bone: according to Wikipedia
“In contrast to endochondral bone, dermal bone does not form from cartilage that then calcifies, and it is often ornamented. Dermal bone is formed within the dermis and grows by accretion only – the outer portion of the bone is deposited by osteoblasts.
Endochondral ossification: according to Wikipedia
“Unlike intramembranous ossification, which is the other process by which bone tissue is created, cartilage is present during endochondral ossification. Endochondral ossification is also an essential process during the rudimentary formation of long bones, the growth of the length of long bones, and the natural healing of bone fractures.”
Here’s an invalidated shark skull story:
According to Guardian.com “Fossil upends theory of how shark skeletons evolved, say scientists. The partial skull of an armoured fish that swam in the oceans over 400m years ago could turn the evolutionary history of sharks on its head, researchers have said.”
“The fossil, about 410m years old and reported in the journal Nature Ecology & Evolution, was unearthed in western Mongolia in 2012, and belongs to a placoderm that has been dubbed Minjinia turgenensis and would have been about 20-40cm in length. “This fossil is probably the most surprising thing I have ever worked on in my career. I never expected to find this,” Dr Martin Brazeau of Imperial College London, first author of the research, said.”
Figure 2. Minjina in 4 views, mirror-image and colors added.
We looked at Minjinia earlier
here and here. It is indeed a bottom-dwelling placoderm with reduced jaws and eyes. So it is no surprise that bone was present because placoderms nest with bony fish in the LRT. Contra traditional views, placoderms do not precede sharks in the LRT.
The root word chondro,
as in ‘Chondrichthyes’ indicates cartilage. Immature tetrapods and bony fish have a chondrocranium that gets replaced by a skull made of bone. Sturgeons, paddlefish and sharks had not yet gained the ability to replace cartilage with bone. According to the LRT, hybodontids, with their highly ossified skulls and the bony fish that succeed them regain that ability to replace cartilage with bone while losing the flexibility in the rostrum of sharks.
Kaucka and Adameyko 2019
review the evolution of cartilage in the cranial region and discuss shaping of the chondrocranium in different groups of vertebrates.
Compagnucci et al. 2013
review several then current, now out-of-date hypotheses of jaw development, all without a cladogram.
Finally, let’s not forget
Borrell 2014 found it only took one gene turned off to stop bone production in shark-relative chimaeras. Whenever that gene was turned on it restarted bone production.
Borrell B 2014. Why sharks have no bones. Nature online here
Compagnucci C et al. (11 co-authors) 2013. Pattern and polarity in the development and evolution of the gnathostome jaw: both conservation and heterotopy in the branchial archesof the shark, Scyliorhinus canicula, Dev. Biol. 377(2): 428–448.
De Iuliis G Pulerà D 2011. Chapter 3. The Shark in The Dissection of Vertebrates (Second Edition), Science Direct online
Kaucka M and Adameyko I 2019. Evolution and development of the cartilaginous skull: From a lancelet towards a human face. Seminars in Cell & Developmental Biology 91:2–12. https://doi.org/10.1016/j.semcdb.2017.12.007
Richter M and Underwood C 2019. Chapter 8 – Origin, development and evolution of the fish skull. Pages144–159 in Evolution and development of fishes Eds. Johanson Z, Underwood C and Richter M. Cambridge University Press DOI: https://doi.org/10.1017/9781316832172.009
Venkatesh B et al. 2014. Elephant shark genome provides unique insights into gnathostome evolution. Nature 505:174–179.
Steven E Campana Lab webpage: