Tully as a Vertebrate

Reconstruction of Tullimonstrum gregarium by Sean McMahon, from McCoy et al. (2016).

McCoy, V. E., E. E. Saupe, J. C. Lamsdell, L. G. Tarhan, S. McMahon, S. Lidgard, P. Mayer, C. D. Whalen, C. Soriano, L. Finney, S. Vogt, E. G. Clark, R. P. Anderson, H. Petermann, E. R. Locatelli & D. E. G. Briggs (in press, 2016) The ‘Tully monster’ is a vertebrate. Nature.

Several years ago, I included the 'Tully monster' Tullimonstrum gregarium in a list of some of the most phylogenetically mysterious organisms on the planet. Multiple suggestions have been made as to its affinities: mollusc, annelid, nemertean (nemerteans and sea cuumbers both having weird histories of problematic fossils assigned to them for little apparent reason), some sort of de-chitinised arthropod relative by way of Opabinia, the Loch Ness monster... A new publication just out by McCoy et al. (2016) adds a further interpretation to the mix.

Tullimonstrum is represented by literally thousands of specimens from the Carboniferous Mazon Creek deposit of Illinois. The organisms preserved in this deposit are contained within nodules, each individual at the centre of a mineral ball that precipitated around it after its death. It had a somewhat elongate, torpedo-shaped body, at the front of which was an elongate proboscis ending in a pincer-like structure. Towards the front of the main body was a dorsal cross-bar with a dark round body at each end; these bodies have most commonly been seen as eyes on the end of stalks but alternative interpretations include statocysts, solid structures that many aquatic animals possess for sensing balance. A fin-like structure was present at the tail end of the animal. Many specimens also show regularly spaced dark cross-lines suggesting some sort of segmental division of the body.

Another structure commonly visible in the Tullimonstrum fossils is a pale, flattened linear structure running down the length of the animal. Most authors have presumed that this represents the gut but McCoy et al. argue that it does not resemble the gut as preserved in other Mazon Creek fossils. In these other fossils, the gut is dark-coloured and is not flattened. Some authors have tried to explain this difference between the 'gut' of Tullimonstrum and that of its associates by suggesting that the Tully monster fed on soft prey such as jellyfish whose remains did not preserve after death, but the dark colour in most Mazon Creek guts does not represent the actual gut contents themselves but minerals that precipitated around the gut contents during the fossilisation process. Presumably, such minerals would be just as likely to condense around jellyfish remains as any other organic tissue. Even more damning, McCoy et al. identified a handful of Tullimonstrum specimens in which the gut was indeed preserved as in other Mazon Creek fossils, and as a separate structure from the pale line that was also present in these same specimens.

An actual fossil of Tullimonstrum in the Museo di Storia Naturale di Milano, copyright Ghedoghedo.

So what was this structure, if not a gut? McCoy et al. note that at least one other fossil from the Mazon Creek preserves a similar structure: the hagfish-like Gilpichthys, in which it represents the notochord. The structure's preservation is consistent with this interpretation: being a fluid-filled tube, the notochord would flatten readily during fossilisation, and it does not accumulate minerals like the gut because it lacks an external connection. And if Tullimonstrum also possesses a notochord, then that makes it also a chordate. And with that in mind, McCoy et al. interpret other structures as supporting chordate, and specifically vertebrate, affinities: the fin-like structures are indeed fins, paired stains bordering the notochord in a few specimens appear to be gill pouches, tooth-like structures within the 'pincer' at the end of the proboscis are keratinous teeth similar to those of lampreys and hagfish, and the apparent 'segments' in some specimens represent vertebrate myomeres (muscle blocks). Including Tullimonstrum in a phylogenetic analysis of basal vertebrates, coded according to these and other interpretations, places it within the stem-lineage of modern lampreys.

So how strong is this re-assignment? The problem with the structural analysis of any problematic fossil is that it is ultimately dependent on finding the right comparative framework, and the more distinct the problematicum is from any living organism the harder it is to be sure you're making the right comparison. That's not a criticism of this particular paper; that's simply the limitation its authors have to work with. In this case, I kind of suspect that the identification of Tullimonstrum as a vertebrate all hinges on whether they've correctly identified that notochord. None of the other 'vertebrate' features identified is sufficiently distinct to clinch the deal on their own. A tail-fin could indicate a vertebrate, or it could indicate a mollusc like a squid. The famous Tullimonstrum proboscis (which, offhand, McCoy et al. interpret as a cartilage-supported structure rigidly bending at set points like an arm rather than curling like a tentacle, based on the regular aspect of its preservation) is unlike anything known from any other vertebrate, but nor does it strongly resemble anything found in any other animal (the aforementioned Opabinia suggestion is right out: as I mentioned in an earlier post on Nectocaris, the Opabinia proboscis contains no direct part of the digestive tract itself). Certainly the placement of Tullimonstrum as a stem-lamprey is the weakest part of the whole deal, as the specific features cited as synapomorphies are either convergently present in other vertebrates (e.g. keratinous teeth) and/or dependent on some admittedly more tentative structural interpretations (e.g. tectal cartilages). There may be a certain element here of Tullimonstrum's intractable weirdness conflicting with the phylogenetic analysis' need to put it somewhere. I also wonder if I should be criticising Sean McMahon's reconstruction (reproduced at the top of this post) for presenting Tullimonstrum as somewhat laterally flattened: the majority of Tullimonstrum specimens are preserved dorsoventrally rather than laterally, which I would suspect indicates that they were probably flatter top-to-bottom than side-to-side.

Those criticisms aside, McCoy et al. have certainly presented one of the more robust reconstructions of Tullimonstrum to date. Most of what I've said comes under the heading of intrigued enquiries rather than actual disagreements, and if they're right about that notochord then they're on pretty firm ground. After all, even if the Tully monster is not specifically a stem-lamprey doesn't exclude it from being any sort of chordate. There are few (if any) problematica as well represented in the fossil record as Tullimonstrum, and we have not heard the last word on it yet.

Hagfish: Probably the World's Most Disgusting Vertebrates

South African hagfish Myxine capensis, copyright Andy Murch.

I say "probably" not the title not because there's any question about whether hagfish are disgusting–they are, they really are–but because there's been some debate in the past about whether hagfish are vertebrates. Hagfish, as you may already know, are superficially eel-like marine animals that, together with the lampreys, are one of the two living lineages of 'jawless fish'. Their skeleton is both completely cartilaginous decidedly rudimentary: they even lack a developed spine, instead retaining the fluid-filled notochord throughout their life. They do possess a brain-case, as well as some appendicular cartilages that provide support for the fins. Around the mouth are a set of muscularly-controlled tooth-plates together with short sensory tentacles. Hagfish have no eyes; instead, they find their way about primarily through the use of a single large nostril in the middle of the head. Along the underside of the body run a series of glands capable of producing a truly mind-bending amount of mucus. As noted by Martini & Flescher (2002), "A single live individual hagfish can turn a 2 gallon pail of water into a gelatinous mass within a few minutes". Most hagfish seem to be in the one or two feet range size-wise, but the New Zealand species Eptatretus goliath was described from a single monster specimen a bit over 1.25 metres long (Mincarone & Stewart 2006). In contrast, the hydrothermal vent inhabitant Eptatretus strickrotti is only just over a foot long and built like a swimming shoelace (Møller & Jones 2007).

A demonstration of a hagfish's slime-producing capabilities, copyright Andra Zommers.

Martini & Flescher (2002) summarised the lifestyle of the Atlantic hagfish Myxine glutinosa (or probably the western Atlantic hagfish M. limosa which they regarded as synonymous with the eastern Atlantic M. glutinosa), which I'm guessing is fairly typical of the group. Atlantic hagfish spend most of their lives buried in burrows in muddy sea-bottoms (the technical term for the type of sediment they prefer is 'flocculent', which is a wonderful word to say), emerging primarily to feed. A large part of their diet is obtained by predating small animals such as crustaceans. They are most notorious, though, as scavengers. Hagfish will emerge in large numbers to feed on any animal corpses that sink within their range. Though they are capable of tearing off external chunks of flesh (more on that in a moment), they are not able to do so efficiently so they prefer to focus on the softer internal organs when they can. This they do by worming their way into the carcasse through a convenient orifice such as the mouth or anus and enjoying the laid-on buffet within. The reproduction of hagfish is poorly known. The Royal Academy of Copenhagen offered an award in 1864 to the first person to describe the details of hagfish nooky; the offer was withdrawn in the 1980s, still unclaimed. Female hagfish have been caught with developing eggs, up to 30 at a time, connected in a string by velcro-like hooks. The absence of any sort of obvious intromittent organ in the male suggests that fertilisation is external, but anything beyond that is a mystery.

Their lack of a rigid skeleton makes hagfish capable of some behaviours that would be beyond other vertebrates. One of these is referred to as 'knotting' and it is exactly what it sounds like. The hagfish makes a loop with its body through with it sticks its tail, quite literally tying itself in a knot. By pulling itself through itself, it can move the knot up the body until the head pops out at the other end. One reason it may do this is to clean itself; for instance, a hagfish may drown in its own mucus if not given the opportunity to remove it (so that single live individual in the two-gallon bucket is probably not live any more). Another reason is that the knot can be used to push against something, such as when the hagfish wants to escape from an enclosed space. When feeding on something large and solid (such as the aforementioned external scavenging), the hagfish will latch on with its tooth-plates and then form a knot to push against it until eventually it tears away with a mouthful of food.

Hagfish can be abundant in some areas, make them an important part of the local ecosystem. They may be regarded as a nuisance in fisheries, attacking fish caught on lines and traps and reducing their commercial value. However, hagfish are also caught for food in some parts of the world (particularly in east Asia) and their skins are cured to produce a soft textile known somewhat euphemistically as 'eelskin'.

Pacific hagfish Eptatretus stoutii, photographed by Linda Snook.

About sixty species of hagfish are currently recognised around the world, usually classified in a single family Myxinidae. Most are divided between two subfamilies (sometimes recognised as separate families), the Myxininae and Eptatretinae. Myxininae have a single external gill opening whereas Eptatretinae have multiple gill openings. A phylogenetic analysis of the hagfish by Fernhom et al. (2013) found a couple of species previously assigned to Eptatretus to probably sit outside the Myxininae-Eptatretinae clade and transferred them to a new genus Rubicundus in its own small subfamily, differing from other hagfish in having the single nostril on a short tubular snout.

As alluded to above, there has been some debate about the affinities of hagfish. Though superficially similar to the other living group of 'jawless fishes', the lampreys (largely through both being eel-like in form), hagfish are very different in the anatomical details, and at the very least the two lineages have been separate for a very long time. Because of their lack of a number of derived features, hagfish were suggested to be the sister lineage of all other vertebrates, leading to the observation that it was not really appropriate to classify a lineage that did not have and probably never had vertebrae as 'vertebrates'. As such, hagfish became regarded as the closest relatives of vertebrates rather than vertebrates themselves. However, molecular studies of vertebrate phylogeny have pretty much universally identified hagfish as forming a clade with lampreys after all, implying that the 'primitive' features of hagfish probably represent secondary losses. When constrained as a clade in morphological analyses, nevertheless, the hagfish-lamprey group remains basal in vertebrates: most if not all of the fossil groups of 'jawless fish', particularly those with an outer covering of bony plates, are more closely related to the jawed fishes than to hagfish or lampreys.

The most likely fossil hagfish (and even then it's not much), Myxinikela siroka, copyright RCFossils.

Not surprisingly for something without much of a skeleton, the fossil record of hagfish is pretty minimal. A species from the Carboniferous Mazon Creek lagerstätte, Myxinikela siroka, is likely to be a stem-hagfish; a couple of other fossils from the same formation have also been suggested as candidates. Myxinikela was broadly similar to a modern hagfish, the most obvious difference being that it was shorter and more cigar- or banana-shaped than eel-like (I can't really imagine it being able to tie itself in knots). Some authors have also suggested similarities between the braincase of hagfish and that of Palaeospondylus, an unusual eel-like vertebrate from the Middle Devonian of Scotland whose confusing assortment of features has lead to it being seen at one time or another as a jawless fish, a degenerate bony fish that failed to develop bone, or even a larval amphibian (Janvier 2015). The most obvious difference between Palaeospondylus and a hagfish is that Palaeospondylus possessed a complete cartilaginous skeleton, but the molecular phylogenies suggest that may not be the problem it would have previously been assumed to be...

REFERENCES

Fernholm, B., M. Norén, S. O. Kullander, A. M. Quattrini, V. Zintzen, C. D. Roberts, H.-K. Mok & C.-H. Kuo. 2013. Hagfish phylogeny and taxonomy, with description of the new genus Rubicundus (Craniata, Myxinidae). Journal of Zoological Systematics and Evolutionary Research 51 (4): 296–307.

Janvier, P. 2015. Facts and fancies about early fossil chordates and vertebrates. Nature 520: 483–489.

Martini, F. H., & D. Flescher. 2002. Hagfishes. Family Myxinidae. In: Collette, B. B., & G. Klein-MacPhee (eds) Bigelow and Schroeder's Fishes of the Gulf of Maine 3rd ed. pp. 9–16. Smithsonian Institution Press: London.

Mincarone, M. M., & A. L. Stewart. 2006. A new species of giant seven-gilled hagfish (Myxinidae: Eptatretus) from New Zealand. Copeia 2006 (2): 225–229.

Møller, P. R., & W. J. Jones. 2007. Eptatretus strickrotti n. sp. (Myxinidae): first hagfish captured from a hydrothermal vent. Biol. Bull. 212: 55–66.