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.

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.

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.

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 5. From Peters 1991 a diagram splitting deuterostomates from protostomates.

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.


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

Stylaria, Opabinia and Tullimonstrom side-by-side

Yesterday we took a detour into the realm of invertebrates
comparing large, extant, colorful, free-swimming marine flatworms and trilobites to the giant of the Cambrian, Anomalocaris. Although the three taxa show a gradual accumulation of traits and are overall similar in shape, readers suggested some ‘further reading’ of the academic literature was needed.

That reading has been fascinating
and a defense of that minor thesis is forthcoming. So far that argument looks like it will need several building blocks.

Figure 1. Opabinia in situ, enlarged several times.

Figure 1. Opabinia in situ, enlarged several times.

Meanwhile… today brings one of those building blocks.
Opabinia (Figs. 1, 2) is yet another strange Cambrian taxon often found in the same cladogram as Anomalocaris (Figs. 3, 4). Whittington’s (1975) first interpretation of Opabinia was met with laughter due to the implausible ‘strangeness’ of the fossil.

Perhaps the following
will take some of the strangeness out of Opabinia. It has some overlooked relatives, one still living, Stylaria, a tiny segmented worm with a mobile proboscis (Fig. 2). Note the presence of eyes, a head section, a tail section and precursors to swimming lobes present as needle-like lateral spines, one per segment. Opabinia only stands out as odd (Fig. 3)  until you add a few similar taxa.

Figure 1. Comparing the extant worm, Stylaria to Cambrian Opabinia and Carboniferous Tullimontrom. All three share a similar morphology that has not been fully explored yet.

Figure 2. Comparing the extant worm, Stylaria to Cambrian Opabinia and Carboniferous Tullimontrom. All three share a similar morphology that has not been fully explored yet. The proboscis does not aid in feeding Stylaria and it probably acted as a simple probe and/or holdfast for Opabinia and Tullimonstrom. Note the lack of legs in any of these taxa.

According to Wikipedia,
“When the first thorough examination of Opabinia in 1975 revealed its unusual features, it was thought to be unrelated to any known phylum, although possibly related to a hypothetical ancestor of arthropods and of annelid worms. However other finds, most notably Anomalocaris, suggested that it belonged to a group of animals that were closely related to the ancestors of arthropods and of which the living animals onychophorans (velvet worms) and tardigrades may also be members.”

Given the many shared traits with Stylaria, the proboscis in Opabinia does not appear to be used elephant-like, as Whittington 1975 suggested, for carrying prey items back to the ventral mouth. Rather the proboscis was more likely used as a sand probe and/or a poison delivery system. Feeding would have taken place in a more typical flatworm fashion, by settling over a docile prey item and everting soft ventral mouth parts to haul in food that had stopped struggling.

Smith and Ortega-Hernández 2014
offered a competing hypothesis of interrelationships (Fig. 3). In their study focusing on the terminal claws of another Burgess Shale former enigma, Hallucigenia, the authors included Anomalocaris and two related anomalocarids. Opabinia was the outgroup. Stylaria and Tullimonstrum were excluded taxa.

I have no issues with the presence of walking velvet worms nesting with walking tardigrades and walking Hallucigenia. However, I think legless, swimming Opabinia and Anomalocaris do not belong here. An omitted primitive legless taxon, Stylaria (Fig. 2) needs to be added to the Smith and Ortega-Hernandez taxon list to ascertain or modify relationships. More outgroups are probably needed. Or delete the inappropriate swimmers.

Figure 2. Illustrated cladogram from Smith and Ortega-Hernández 2014 (colors, arrows, gray taxa added here) inserts flat, swimming anomalocardids in a claodogram that otherwise features cylindrical lobe-footed crawling worms.

Figure 3. Illustrated cladogram from Smith and Ortega-Hernández 2014 (colors, arrows, gray taxa added here) inserts flat, swimming anomalocardids in a claodogram that otherwise features cylindrical lobe-footed crawling worms as basal taxa. Note how Opabinia stands out as the oddball here. 

Cong et al. 2014 offer a second competing hypothesis
based on their study of Lyrarapax (Fig. 3), a tiny genus clearly related to Anomalocaris. In the Cong et al. cladogram (Fig. 4) Opabinia nests a few nodes further away from several specimens attributed to Anomalocaris. Stylaria and Tullimonstrum were once again omitted from the Cong et al. taxon list.

Figure 3. Cladogram from Cong et al. 2014 nest Anomalocaris in the clade Radiodonta derived from nematodes and penis worms.

Figure 4. Cladogram from Cong et al. 2014 nest Anomalocaris in the clade Radiodonta derived from nematodes and penis worm in which the mouth and anus are both terminal.

The case is building that 
Anomalocaris and Opabinia never went through an evolutionary phase in which the body was cylindrical with the short clawed feet of velvet worms and tardigrades. Instead these two appear to have evolved directly from free-swimming segmented worms without legs. Let’s keep adding taxa to figure this out.


References
Bergström J 1986. Opabinia and Anomalocaris, unique Cambrian arthropods. Lethaia. 19 (3): 241–246.
Whittington HB 1975. The enigmatic animal Opabinia regalis, Middle Cambrian Burgess Shale, British Columbia. Philosophical Transactions of the Royal Society B. 271 (910): 1–43 271.

wiki/Opabinia

 

Anomalocaris: how flatworms transition to trilobites

According to Wikipedia,
Anomalocaris (“unlike other shrimp”, or “abnormal shrimp”) is an extinct genus of radiodont (anomalocaridid), an order of animals thought to be closely related to ancestral arthropods.”

That is confirmed below (Fig. 1). But where did Anomalocaris come from?

According to Wikipedia,
Stephen Jay Gould cites Anomalocaris as one of the fossilized extinct species he believed to be evidence of a much more diverse set of phyla that existed in the Cambrian Period, discussed in his book Wonderful Life, a conclusion disputed by other paleontologists.”

That is not confirmed below. Based on phylogenetic bracketing, Anomalocaris evolved from flatworms and into trilobites. Thus, these do not increase the diversity of phyla in the Cambrian, but blend one into another.

Figure 1. Possible evolution of Anomalocaris after phylogenetic bracketing between flatworms and trilobites.

Figure 1. Possible evolution of Anomalocaris after phylogenetic bracketing between flatworms and trilobites.

Where else do we find such a mouth?
That’s the first clue to the origin of anomalocarids.

Evidently overlooked until now,
certain flatworms have a similar concentric ventral mouth (Fig. 1).

Anomalocarids apparently had the fluidity of motion
of a large swimming flatworm (see video below), combined with the segmentation of trilobites (= arthropod ancestors).

Distinct from flatworms, but like trilobites,
an anus appears posteriorly.

Like tentacled flatworms and trilobites with antennae,
two armored tentacles appear on anomalocarids,

Unlike flatworms, but like trilobites,
a pair of lateral eyes on short stalks appear.

A YouTube video
featuring Burgess Shale expert Professor Des Collins explains how the bits and pieces of Anomalocaris came together historically over several years as he holds a model of a large specimen.https://www.youtube.com/watch?v=xNbaHOJ7GGk

According to the Des Collins website:
“The fossil Anomalacaris was unlike any living animal and was misidentified over a period of 100 years revealing the false starts that can happen in scientific research. Collins set out to piece together the entire animal by looking at the vast trove of Burgess Shale fossils at the Royal Museum of Ontario where he worked. He discovered more pieces of the puzzle and realized that previous fossils that were described as separate organisms were, in fact, part of the animal Anomalacaris. Once he had assembled the entire animal, he had a model built to show what a fearsome predator it must have been.”

Or not. Anomalocaris was large, but its mouth was not ideally suited to crack open and attack the hard-shelled animals that were evolving in the Cambrian. According to the Wired.com article cited below, “We found that it’s extremely unlikely Anomalocaris could eat most trilobites,” said James Whitey Hagadorn, the research team’s leader and a paleontologist at the Denver Museum of Nature and Science. “It couldn’t close its mouth all of the way, its mouth was too soft to crush trilobite shells.”

Anomalocaris arising from large free-swimming flatworms
appears to be a novel hypothesis of interrelationships. If not, please provide a citation so I can promote it here.

This just in (March 11, 2021):
Tests show Anomalocaris was not a trilobite eater, but preferred mush, like modern flatworms do.
https://phys.org/news/2010-11-ancient-shrimp-monster-fierce.html
https://phys.org/news/2010-11-earth-great-predator-wasnt.html


References
Daley AC, Paterson JR, Edgecombe GD, García-Bellido DC and Jago JB 2013. Donoghue P (ed.). New anatomical information on Anomalocaris from the Cambrian Emu Bay Shale of South Australia and a reassessment of its inferred predatory habits. Palaeontology: n/a. doi:10.1111/pala.12029
Whiteaves JF 1892. Description of a new genus and species of phyllocarid Crustacea from the Middle Cambrian of Mount Stephen, BC. The Canadian Record of Science. 5 (4).
Whittington HB and Briggs DE 1985. The largest Cambrian animal, Anomalocaris, Burgess Shale, British Columbia. Philosophical Transactions of the Royal Society B. 309 (1141): 569–609.

wiki/Anomalocaris
shapeoflife.org/video/des-collins-paleontologist-burgess-shale
wired.com/2010/11/anomalocaris-trilobite-bite/