Summary for those in a hurry
After this comparison, nematodes and hagfish need to be added to the base of the vertebrate/ echinoderm/ deuterostome family tree as outgroup taxa. In other words, hagfish are big nematodes with a notochord. And in turn, so are we.
Figure 1. The hagfish Myxine in vivo patrolling the sea floor. Note the nematode-like tentacles surrounding the mouth end at lower left.
Hagfish (clade: Myxini)
are very low on the vertebrate family tree. According to Wikipedia, “They are the only known living animals that have a skull but no vertebral column, although hagfish do have rudimentary vertebrae.”
With origins in the Cambrian or Ediacaran,
we know of only one fossil hagfish, Gilpichthy greenei (Bardack and Richardson 1977, FMNH PE18703, 5cm; Fig. 2) from the famous Mazon Creek Formation, Late Carboniferous, 307 mya.
Figure 2. Gilpichthys, a Pennsylvanian hagfish, enlarged and full scale.
Without vertebrae,
the Atlantic hagfish (genus Myxine, Linneaus 1758, 50cm, other genera up to 127cm) nest between Vertebrata and more basal taxa. (Not yet added to the LRT).
Outgroup taxa include
lancelets and nematodes (= round worms).
Yesterday
one of those insightful bells rung when I realized nematodes have eversible teeth made of keratin, as in hagfish. Something obvious had, once again, been overlooked. Peters 1991 listed nematodes as vertebrate ancestors based on overall morphology. Hagfish were not included then.
Now
let’s see what other details link nematodes to hagfish, a relationship overlooked by all prior authors, probably due to the great size difference (most nematodes are <2.5mm long), or perhaps due to taxon exclusion. According to Wikipedia, “Taxonomically, they [nematodes] are classified along with insects and other moulting animals in the clade Ecdysozoa,”
Figure 3. Nematodes and hagfish side-by-side, focusing on the eversible mouth parts and keratin teeth.
Classification
According to Wikipedia, “The classification of hagfish had been controversial. The issue was whether the hagfish was a degenerate type of vertebrate-fish that through evolution had lost its vertebrae (the original scheme) and was most closely related to lampreys, or whether hagfish represent a stage that precedes the evolution of the vertebral column (the alternative scheme) as is the case with lancelets. Recent DNA evidence has supported the original scheme.”
We have learned time and again, you can never trust DNA evidence, especially when taxon exclusion is in play. Instead, look at the traits of the taxa under study. And look at lots of taxa to make sure none of them share more traits.
Smithsonian Magazine listed 14 (edited to 7) fun facts about hagfish.
- Hagfishes live in cold waters around the world, from shallow to 1700 m.
- Hagfish can go months without food.
- Hagfish can absorb nutrients straight through their skin.
- Hagfish have two rows of tooth-like structures made of keratin they use to burrow deep into carcasses. They can also bite off chunks of food. While eating carrion or live prey, they tie their tails into knots to generate torque and increase the force of their bites.
- No one is sure whether hagfish belong to their own group of animals, filling the gap between invertebrates and vertebrates, or if they are more closely related to vertebrates.
- The only known fossil hagfish, [Gilphichthys, above] looks modern.
- Hagfish produce slime. When harassed, glands lining their bodies secrete stringy proteins that, upon contact with seawater, expand into the transparent, sticky slime.
Figure 4. Illustration of a nematode with labels from corodon.com. This model has been based on the fresh-water nematode Ethmolaimus. Compare to the hagfish in figure 1.
How does the hagfish compare to an aquatic nematode?
- Tail — The post-anal region forms a tail in both
- Mucus — Moens et al. 2005 report, “Many aquatic nematodes secrete mucus while moving.” The authors did not mention hagfish, which are famous for mucus. Some nematodes also exude adhesive from post-anal, tail tip glands.
- Sensory tentacles — The mouth is in the centre of the anterior tip and may be surrounded by 6 lip-like lobes in primitive marine forms, three on each side. Primitively the lips bear 16 sensory papillae or setae.
- Burrowing into their prey — Both hagfish and nematodes attach their lips to larger prey, make incisions and pump out the prey’s contents with a muscular pharynx.
- Swimming — In water nematodes swim by a graceful eel-like motion as they throw their stiff but elastic bodies into sinusoidal curves by contracting longitudinal muscles (the elasticity of the cuticle and hydrostatic skeleton more or less returns the body to its original straight shape). The notochord in the hagfish gives the same sort of elasticity to the famously wriggly body capable, as in nematodes, to form corkscrews and knots.
- Niche — Nematodes represent 90% of all animals on the ocean floor, not counting hagfish. Both play important roles in dead vertebrate decomposition.
- Embryo development — An alternative way to develop two openings from the blastopore during gastrulation, called amphistomy, appears to exist in some animals, such as nematodes.
- Size –– some species of hagfish and nematode reach 1m in length, though most nematodes are <2.5mm
- Eyes — A few aquatic nematodes possess what appear to be pigmented eye-spots, but most are blind. So are hagfish.
- Reproduction — Usually male and female, sometimes hermaphroditic
- Tough skin and subcutaneous sinus — largely separated from underlying tissue
Evolution from nematode to hagfish
- Head — radially symmetrical evolves to bilaterally symmetrical
- Mouth — three or six lips with teeth on inner edges reduced to two
- Skin and skeleton — Hydroskeleton and cuticle evolve to notochord and ‘eelskin’
- Nerve chord —Dorsal, ventral and lateral in nematodes, reduced to just dorsal in hagfish
- Brain – circular nerve ring in nematodes, dorsal concentration in hagfish
Pikaia gracilens
(Walcott 1911, Middle Cambrian, Fig. Z) has been compared to lancelets and hagfish. Like hagfish, Pikaia retained twin tentacles, but also had cirri instead of rasping eversible teeth.
Figure z. Pikaia gracilens from Mallatt and Holland 2013 showing hagfish and lancelet affinities.
Added 24 hours later
as the question of mouth and anus origin from the original blastopore (Fig. zz) arises again in the comments section.
Figure zz. Blastopre evolution to produce an anus and mouth at the same time in a marine nematode. This is the transitional taxon from protostome nematodes to deuterostomes. This is how it happened. This is how it was ignored in many Western textbooks.
Malakov 1997 writes,
“The blastopore initially has a spherical Caenorhabtitis sp. (Ehrenstein & Schierenberg, shape, but then stretches to become an elongated 1980). oval-shape (Fig. 2). Subsequent development results Embryogenesis in enoplids appears to have several in the lateral edges ofthe blastopore approaching and u.nusual features. Firstly, variability occurs in the eventually connecting with the centre. Two openblastomere arrangement in the stages of early cleavings, one at the anterior end the other at tl1e posterior age. At the four-cells stage various configurations end of the embryo, are persistent remnants of the have been observed, viZ., tetrahedral, rhombic, Tblastopore. The anterior opening provides the beginshaped. These configurations have been variously ning of the definitive mouth, and the posterior one, encountered in the development of nematodes bethe definitive anus.”
See figure z (above). Hagflish and vertebrates arose form marine nematodes exhibiting this form of early cell division. This is how deuterostomes arose.
Malakov 1997 reports, “From these results it may be concluded that enoplids represent an early evolutionary branch, which seperated (sic) from the ancestral nematode stem prior to all other groups of nematodes.”
Figure 5. Medial section of Acipenser (sturgeon) larva with temporary teeth from Sewertzoff 1928. Note this specimen has marginal teeth and deeper teeth.
Getting back to baby sturgeon teeth…
Several months ago I cited Sewertzoff 1928 (Fig. 5) who found tiny teeth in the tiny lava of the large sturgeon, Acipenser. Those tiny teeth disappear during maturity, as you might recall. The question is: are those teeth homologs of keratinous hagfish + nematode teeth? Or homologs of enamel + dentine shark and bony fish teeth? McCollum and Sharpe 2001 in their review of the evolution of teeth reported, “The aim of this review is to see what this developmental information can reveal about evolution of the dentition.”
Unfortunately McCollum and Sharpe 2001 delivered the usual history of citations that indicate teeth started with sharks, overlooking sturgeon, nematode, lamprey and hagfish teeth. Phylogenetic bracketing indicates that baby sturgeon teeth are keratinous, not homologous with dentine + enamel shark teeth, which phylogenetically evolve later, first in sharks and later retained by bony fish. Let me know if this is incorrect.
Figure 6. Ventral view of the GLAHM V830 specimen of Thelodus. This appears to have fang-like teeth, but teeth are too soon. These are barbels = cirri.
Sturgeon barbels:
Are they homologs of hagfish + nematode barbels? Soft tissues, like barbels, are unlikely to fossilize, but one intervening bottom-dwelling taxon, Thelodus (Fig. 6), preserves barbels anterior to the ventral oral opening. Open water thelodonts do not preserve barbels. Catfish barbels appear to be a reversal because a long line of more primitive taxa do not have barbels. The same can be said of the catfish-mimic eel ancestor, the cave fish Kryptoglanis.
The relationship between hagfish and nematodes
should have been known for decades, but apparently this hypothesis of interrelationships has been overlooked, ignored or set to the side until now. If someone else recovered this hypothesis of interrelations previously, let me know so I can promote that citation.
References
Bardack D and Richardson ES Jr 1977. New aganathous fishes from the Pennsylvanian of Illinois. Fieldiana Geology 33(26):489–510.
Linnaeus C 1758. Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata.
Malakov VV 1998. Embryological and histological peculiarities of the order Enoplida, a primitive group of nematodes. Russian Journal of Nematology 6(1):41–46.
Mallatt J and Holland ND 2013. Pikaia gracilens Walcott: stem chordate, or already specialized in the Cambrian? Journal of Experimental Zoology, Part B, Molecular and Developmental Evolution 320B: 247-271.
McCollum M and Sharpe PT 2001. Evolution and development of teeth. Journal of Anatomy 199:153–159.
Moens T et al. (6 co-authors) 2005. Do nematode mucus secretions affect bacterial growth? Aquatic Microbial Ecology 40:77–83.
Morris CS, Caron JB 2012. Pikaia gracilens Walcott, a stem-group chordate from the Middle Cambrian of British Columbia. Biological Reviews 87: 480-512.
Nielsen C, Brunet T and Arendt D 2018. Evolution of the bilaterian mouth and anus. Nature Ecology & Evolution 2:1358–1376.
Nielsen C 2019. Blastopore fate: Amphistomy, Protostomy or Dueterostome. In eLS (eds) John Wiley & Sons Ltd. DOI: 10.1002/9780470015902.a0027481
Peters D 1991. From the Beginning – The story of human evolution. Wm Morrow.
Sewertzoff AN 1928. The head skeleton and muscles of Acipenser ruthensus. Acta Zoologica 13:193–320.
wiki/Hagfish
wiki/Nematode
wiki/Pikaia
cronodon.com/BioTech/Nematode.html
pterosaurheresies.wordpress.com/2020/08/07/chordate-origins-progress-since-romer-1971/
Hagfish Day, occurs every year on the third Wednesday of October:
smithsonianmag.com/science-nature/14-fun-facts-about-hagfish-77165589/
The Pterosaur Heresies 
Nematodes are protostomes – not deuterostomes. They are unrelated to chordates.
This is based on developmental evidence as well as molecular – it’s been understood for well over a century.
Please do some research on the differences between protostomes and deuterostomes.
That’s old information, Chris. We talked about this before. Please check these citations also listed above.
Nielsen C 2019. Blastopore fate: Amphistomy, Protostomy or Dueterostome. In eLS (eds) John Wiley & Sons Ltd. DOI: 10.1002/9780470015902.a0027481
and
Nielsen C, Brunet T and Arendt D 2018. Evolution of the bilaterian mouth and anus. Nature Ecology & Evolution 2:1358–1376.
These references do not support anything you’ve said about nematodes. Nor do they contradict anything I’ve said. My point remains.
Then I’ll provide a picture from Malakov 1998 showing the original blastopore stretching to form a slit, then pinching off in the middle to form a mouth and anus at the same time prior to curling of the embryo, as is typical of all vertebrates. See above.
I did see above. I wasn’t referring to gastrulation in my original comment. There are other developmental similarities shared across protostomes, such as the origin of the mesoderm and various aspects of cleavage in a very early (pre-gastrulation) embryo.
Seriously – that nematodes are not deuterostomes is not controversial.
Your reply is unprofessional and short-sighted, Chris. NO ONE ever said nematodes are deuterosomes. What do they call they call that? A red herring? A straw man? You are better than that! Nematodes develop a mouth and anus at the same time. That makes them neither deuterostomes nor protostomes (at least the aquatic forms). After that hurdle, let this aquatic lineage evolve into a hagfish, a tunicate, a lancelet, or remain a nematode. There are too many traits (listed above) to ignore. Let’s also take note that the nematode embryo shown above curled its tail ventrally, like all vertebrates do. Here’s the opposite example, a protostome annelid that just keeps adding segments posteriorly: https://www.researchgate.net/publication/281031251_Annelida/figures?lo=1
Deuterostomia is a recognized clade, regardless of how we currently assess the fate of the blastopore. Hagfish are vertebrates, which are chordates, which are deuterostomes. If nematodes are closely related to hagfish, then nematodes are deuterostomes in your scheme. I thus stand by my statement.
Likewise, Protostomia is a recognized clade, and again, the blastopore isn’t really central to the group’s monophyly. And every analysis in the peer-reviewed literature puts nematodes within this group.
Chris, you seem to be missing or inverting the concept of nested clades. If birds arise from theropods, that doesn’t make theropods birds. Ask a friend you trust to review the statements you stand by. I am concerned for your logic processor.
Deuterostomia is a clade. It includes echinoderms, hemichordates, chordates, and some bizarre Cambrian oddballs we’re still sorting out.
Hagfishes are vertebrates. Vertebrates are chordates. Chordates are deuterostomes. This makes hagfish deuterostomes.
There is another clade called Protostomia. It includes arthropods, mollusks, annelids, and many other living and extinct groups.
Based on pretty much every analysis in the literature, nematodes belong to Protostomia. This makes them protostomes.
You appear to be using “deuterostome” and “protostome” merely as descriptors of a developmental condition defined by the fate of the blastopore. This is not how the terms are used by modern biologists.
does that help?
Chris, you wrote: “Based on pretty much every analysis in the literature, nematodes belong to Protostomia. This makes them protostomes.” You wrote it yourself: “pretty much”. That means you know there are exceptions. The exceptions are pertinent to hagfish. They are amphistomes, a clade you seem to reticent to accept despite the literature. They develop a mouth and anus at the same time as shown in the illustration. Nematodes are everywhere. From mountains to deserts to caves. Some estimate they comprise the vast majority of biomass on Earth. From among the aquatic species hagfish and lancelets arise. Please provide a more parsimonious ancestor if this is not so. Since you haven’t yet, and likely would have, evidently you can’t, but I won’t give up hope. Either compete with a better ancestor or accept the amphistome hypothesis, not from me, but from the authors who describe it cited above.
Also – your claim that Gilpicthys is the only known fossil hagfish is not entirely correct. There’s also the more recently described Tethymyxine.
Wonderful! That’s a new one for me. And let’s add PIkaia, lacking keratin teeth, like a lancelet, retaining sensory tentacles, like a hagfish.
Maybe add Myxinikela siroka too.
Ref: Miyashita, Tetsuto (23 November 2020). “A Paleozoic stem hagfish Myxinikela siroka — revised anatomy and implications for evolution of the living jawless vertebrate lineages”. Canadian Journal of Zoology. 98 (12): 850–865. doi:10.1139/cjz-2020-0046. ISSN 0008-4301.
The more the better!
The “amphistome hypothesis” discusses how the blastopore arises. It has nothing to do with phylogeny, and I am unable to find a clade called “Amphistomia” or “Amphistomata” anywhere in the literature. I’m not rejecting the model for blastopore formation in the literature you listed – only pointing out that there doesn’t seem to be a clade by that name, nor does there seem to be a clade (other than maybe Bilateralia) diagnosed by it.
I said “pretty much” as a hedge. In fact, I am unable to find a single phylogeny published in the past few decades in which nematodes are more closely related to vertebrates than they are to other protostomes (phylogenetic sense, not developmental sense). But, because my knowledge of the subject is not exhaustive, I said “pretty much” in case there’s something I’m missing. It’s the verbal equivalent of putting error bars around my claim.
You wrote, “I am unable to find a clade called “Amphistomia” or “Amphistomata” anywhere in the literature.” There need not be such a clade if no one has gone to the trouble of erecting it, yet. It’s a biological process, as you note, that enables one clade of nematodes to be ancestral to deuterostomes. I’m still waiting for your outgroup taxon to the Deuterostomia…
Chris, you seem to be letting the authority of the literature be your guide — and the door you use to close to new ideas and discoveries. You got into this thing we call paleontology to conceive new ideas and make discoveries. So did the rest of us.
Yes, I got into the field to make discoveries. That’s why I’ve devoted so much time and effort to study the group I work on. This meant looking at actual specimens (which is necessary to really build expertise) and reading the literature on the subject comprehensively.
That means I have been unable to become an expert on many other subjects. But other people really have become experts on those subjects, one of which is metazoan phylogeny and the relationship between early embryological development and ingroup relationships.
Those experts have all concluded that nematodes are unrelated to hagfishes. This includes the experts who have put intense effort into the study of early embryological stages among metazoan clades.
I do tend to rely on experts more than non-experts on a given subject. That doesn’t mean the experts are always right, but they’re far more likely to be right than non-experts.
I don’t have an outgroup to Deuterostomia in mind. Like I said, I’m not an expert on the subject, and I know that relying on photographs and literature citations, by themselves, won’t make me one. But have you reached out to any of the real, living experts on this subject for an opinion? Might be informative.
Last things first: Yes! I have reached out to experts. Still waiting to hear back.
Worth noting that no prior papers tested nematodes and hagfish in one study as taxa in phenomic phylogenetic analyses. If so, please let me know and I will promote that citation.
That sort of taxon exclusion happens too often. That’s where the LRT steps in to bring excluded taxa back under study. The challenge is always out there to others to add taxa to their study. Likewise I accept suggestions to add taxa to my study. Too often this turns out to be ‘low hanging fruit’, ignored by others, easy to pluck for anyone looking where others are not.
You should add Myxinikela. It is a stem hagfish that has mixed characters that suggest that the apparently primitive characteristics of hagfish are in reality reversals (which is what molecular evidence says and makes sense considering the temporality of Myxinikela).
I appreciate the suggestion, SechSech. I downloaded and DGS’d images in 2021 from the 2020 paper, but did not add it to the LRT owing to the paucity of data and my lack of knowledge back then. I will reconsider it. No promises, but thank you.
PS molecular evidence? I’m always skeptical about DNA in DEEEEEP time taxa. Perhaps a citation?