Aquatic enoplid nematodes: ancestral to hagfish AND common slugs

Earlier we looked at the many homologies that unite
primitive round worms (= aquatic enoplid nematodes, Fig. 1), with primitive chordates (=  hagfish. Fig. 1).

Now let’s look at overlooked evidence
that unites nematodes and hagfish with… primitive molluscs (= slugs, Figs. 1, 2).

Largely (but not completely) overlooked until now,
nematodes (= amphistomes) could have given rise to both hagfish (chordates, deuterostomes) and slugs (molluscs, protostomes). These three taxa are all long, worm-like, bilaterals with sensory tentacles, rasping retreating mouth parts, and for one reason or another depend on producing slime from their skin.

I say ‘not completely overlooked’
because Clark and Uyeno 2019 portrayed cutaway diagrams of a slug and hagfish to show their ‘convergent’ mouth parts.

Figure 1. Nematodes, hagfish and slugs have so many traits in common, one wonders why they are not related to one another.

With that short list, I could be accused
of “Pulling a Larry Martin” by listing only a few traits. The fact is, these simple, soft-bodied taxa only have a few traits, and they still share these few traits 600 million years after their last common ancestor in the Ediacaran.

Figure 2. A selection of slugs (basal molluscs) to scale. Compare to hagfish in figure 1.

Tiny nematodes wriggle through and eat whatever falls on the sea floor.
Slugs slide over and eat whatever falls on the sea floor. Hagfish swim above and eat whatever falls on the sea floor. In the Ediacaran the only food source was the planktonic seafloor and its tiny burrowing and crawling inhabitants.

Side note: Chaetognaths (arrow worms)
(Fig. 3) document yet another clade of swimming nematode descendants with hard mouth parts and fins that evolved by convergence with those of chordates. Notably, on vertically undulating chaetognaths swimming fins appear on the lateral surfaces, distinct from horizontally undulating chordates with vertical fins. Yes, it’s that simple.

Figure 3. Chaetognath (arrow worm) diagram. Note the lateral fins and lateral caudal fin together with the grasping mouth parts.

One reference
(Barnes 1980) considered arrow worms deuterostomes. Wikipedia labeled them protostomes, but reported, “Chaetognaths are traditionally classed as deuterostomes by embryologists. Molecular phylogenists, however, consider them to be protostomes. Thomas Cavalier-Smith places them in the protostomes in his Six Kingdom classification. The similarities between chaetognaths and nematodes mentioned above may support the protostome thesis.”

We’ve already seen that nematodes are amphistomes and that gene studies too often recover false positives. So let’s consider those gene studies unreliable. As noted above, visual examination shows chaetognaths to be deuterostomes, whether by convergence or homology.

Try Googling ‘hagfish + slugs’
and you won’t find any prior discussions of this interrelationship in the online academic literature. Any mention of worm-like ancestors for hagfish or any mention of nematode ancestors for molluscs are also rare to absent in the online literature.

Distinct from annelids, arthropods and any other segmented animals,
chordates and molluscs have no body segments.

Traditionally the most primitive mollusc
is the chiton (with eight separate plates of armor) or the heliconelid (with a slightly spiral-shaped shell).

However,
if you start with a flatworm (Platyhelminthes), as you must… then a ribbon worm (Nemertea), as you must… then a round worm (Nematoida), as you must… you’re looking for only minor adjustments to the basic worm shape in both descendants: hagfish and slugs. In this scenario hard mollusc shells are derived traits that evolve after the slug morphology was established. Thus, contra academic tradition naked slugs represent the basal condition in molluscs. They didn’t lose their shells. Slugs never had shells. Those evolved later.

Figure 4. From Peters 1991 a diagram splitting deuterostomates from protostomates. Now this has to be updated by putting molluscs closer to chordates and nematodes.

Traditional invertebrate clades:

1. Bilateria (Flatworms, single digestive opening)
2. Amphistomia (aquatic nematodes, anus and mouth at the same time)
   1. Protostomia (anus first, mouth second)
      1. Ecdysozoa (segmented invertebrates, tardigrades, arthropods)
      2. Lophotrochozoa (molluscs, annelid worms)
   2. Deuterostomia (mouth first, anus second)
      1. Chordata (hagfish, lancelets, craniates)
      2. Xenambulacraria (hemichordates, echinoderms)

Comment: Annelids should nest with arthropods. Both are elongate and segmented. Velvet worms (Onychophora) are transitional taxa.

Comment: Molluscs are  not segmented. Basal forms (slugs) have sensory tentacles and rasping eversible radula, as in nematodes and hagfish.

Revised invertebrate clades:

1. Bilateria (Flatworms, single digestive opening)
2. Amphistomia (aquatic nematodes, anus and mouth at the same time)
   1. Protostomia (anus first, mouth second)
      1. Segmented invertebrates (tardigrades, annelid worms, arthropods)
   2. Deuterostomia (mouth first, anus second)
      1. Chordata (hagfish, lancelets, craniates)
      2. Xenambulacraria (hemichordates, echinoderms)
      3. Chaetognatha (arrow worms) or direct from Amphistomia
   3. Lophotrochozoa (molluscs, with protostome embryos convergent with segmented invertebrates)

Chitin vs. keratin
Chordates have keratin teeth. Molluscs have chitin teeth. Wikipedia reports, “The structure of chitin is comparable to another polysaccharide, cellulose, forming crystalline nanofibrils or whiskers. It is functionally comparable to the protein keratin. The only other biological matter known to approximate the toughness of keratinized tissue is chitin.”

Chordates and molluscs had a last common ancestor 600 million years ago. Numerous references discuss nematode ‘teeth’, but do not describe them as either chitinous or keratinous. So I don’t know which is the more primitive substance.

This is not the first time that professional systematists
have left ‘low hanging fruit‘ for amateurs to pluck from a long list of traditionally overlooked, ignored and enigma interrelationships. Putting taxa together that have never been put together before is what we should all do to understand our world better. Every so-called enigma taxon is the result of Darwinian evolution and thus did not and can not stand alone. Relatives are out there for all the oddballs. It’s our job to find them.

The hagfish-nematode-slug relationship seems to be a novel hypothesis
of interrelationships. If not, please send a valid citation so I can promote it.

PostScript:
I found this YouTube video of velvet worms, arthropods, Hallucigenia (shown on the screen shot) and other segmented worm-like members of Protostomia. Seems velvet worms also have sensory tentacles and eversible teeth made of chitin (close to keratiin) and spray mucous slime from glands on the side of their head. There’s a deep connection with nematodes here as well.

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References
Barnes RD 1980. Invertebrate Zoology 4th ed. Saunders College, Philadelphia 1–1089.
Clark AJ and Uyeno TA 2019. Feeding in jawless fishes. In: Bels V., Whishaw I. (eds) Feeding in Vertebrates. Fascinating Life Sciences. Springer, Cham.
https://doi.org/10.1007/978-3-030-13739-7_7
Peters D 1991. From the Beginning – The story of human evolution. Wm Morrow.

For more informationm:
wiki/Nematode
wiki/Mollusca
wiki/Evolution_of_molluscs
wiki/Chordate
wiki/Hagfish
wiki/Bilateria
wiki/Annelid
wiki/Chiton
wiki/Helcionellid
wiki/Onychophora
wiki/Chaetognatha
wiki/Lophotrochozoa