Chordate origins: Progress since Romer 1971

Added a few days after posting:
There was a spirited discussion in the comments section (below) regarding the origin of the mouth and anus in the proposed ancestor of chordates: a round worm (Fig. 2). The most recent progress on this subject can be found in the following citations:

https://en.wikipedia.org/wiki/Embryological_origins_of_the_mouth_and_anus
It includes a third possibility, ‘amphistomy” which is a new word for me, and the pertinent comment: “An alternative way to develop two openings from the blastopore during gastrulation, called amphistomy, appears to exist in some animals, such as nematodes.”

And here is a citation for a 2019 paper that seems to sum things up to date: https://onlinelibrary.wiley.com/doi/abs/10.1002/9780470015902.a0027481


When the great paleontologist of the ’30s to early ’70s,
Alfred S. Romer, wrote his widely disseminated abridged textbook, The Vertebrate Body – Shorter Version (1971) he proposed the following scenario (Fig. 1) for the origin of chordates (animals with a notochord).

Figure 1. From Romer 1971 the origin of chordates.

Figure 1. From Romer 1971 the origin of chordates. Note the impossibly complex basal taxon, the sessile arm-feeder at bottom. Here wriggling is highly derived. Compare to figure 2.

Unfortunately
Romer 1971 started with a notoriously complex stalked ‘sessile arm feeder’ (Fig. 1), way more derived than the simple and tiny flat worms, ribbon worms and round worms that were the most evolved animals at the time. Since these worms were soft-bodied they left few to no fossils in pre-Cambrian and pre-Ediacaran strata.

Figure 3. Chordate evolution, changes to Romer 1971 from Peters 1991. Here echinoderms have lost the tail and gills of the free-swimming tunicate larva.

Figure 2. Chordate evolution, changes to Romer 1971 from Peters 1991. Here echinoderms have lost the tail and gills of the free-swimming tunicate larva.

Things changed with Peters 1991
who traced the human lineage from molecules to cells to worms and vertebrates. The round worm, a deuterostomate (mouth arising anew opposite the existing anus, Fig. 4), was put forth in that lineage as a placeholder taxon arising from more primitive flatworms and microscopic organisms. Then this wriggling “intestine wrapped in a layer of skin” (Fig. 2), developed a mesoderm and a notochord to restrict telescoping and so became a primitive chordate. This served as the first step toward swimming in the laterally undulating manner of lancelets and fish.

Added the day of publication when reader CB and Wikipedia both note nematodes are protostomates, not deuterostomates: That’s important to document and perhaps the reason why extant nematodes (roundworms) were never considered before. Given that only chordates, hemichordates and echinoderms are currently considered deuterostomes, we have to ask, which roundworm-like and ribbonworm-like taxa preceded these three derived clades? None, according to current thinking. None. That can’t be possible based on the need to get from a flatworm (mouth and anus are the same) to a lancelet. At this stage the roundworm (mouth on one end, anus on the other) serves as a model ancestor for all higher taxa. The solution to this problem: Either deuterostomate roundworm-types all became extinct, or one kind of protostomate roundworm became a deuterostomate, or deuterostomate roundworms are still around, but remain untested regarding their embryology. Thanks for bringing this fact to the surface. Here’s a problem that needs a better solution than we have now.

By contrast,
in Romer’s chart (Fig. 1), wriggling comes last.

In Peters 1991
sessile and free-floating forms, including those without an undulating tail, evolved far and away from simple notochord worm and lancelet bauplans. Some emphasized developing the cilia and mouth parts (echinoderms), while others emphasized developing the atrium (tunicates). These retained a primitive mobile wriggling bauplan as juveniles (betraying their ancestry, not their future), then metamorphosed into sessile adults.

Figure 2. Chordated evolution from Rychel et al. 2005.

Figure 3. Chordated evolution from Rychel et al. 2005.

Back to Academia… Rychel et al. 2005
likewise started with a benthic worm “with gill slits and acellular gill cartilages” (see Fig. 2 from Peters 1991), but were less clear in showing how complex and distinct starfish, tunicates, etc. evolved directly from that simple form. More to their focus, Rychel et al. 2005 write: “Chordates evolved a unique body plan within deuterostomes and are considered to share five morphological characters,

  1. a muscular postanal tail,
  2. a notochord,
  3. a dorsal neural tube,
  4. an endostyle,
  5. and pharyngeal gill slits.

No extant echinoderms share any of the chordate features, so presumably they have lost these structures evolutionarily. Hemichordates and cephalochordates, or lancelets, show strong similarities in their gill bars, suggesting that an acellular cartilage may have preceded cellular cartilage in deuterostomes. Our evidence suggests that the deuterostome ancestor was a benthic worm with gill slits and acellular gill cartilages.”

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

Figure 4. From Peters 1991 a diagram splitting deuterostomates from protostomates.

More recently, Satoh et al, 2014 write:
“Although the origin and evolution of chordates has been studied for more than a century, few authors have intimately discussed taxonomic ranking of the three chordate groups themselves.

“Accumulating evidence shows that echinoderms and hemichordates form a clade (the Ambulacraria), and that within the Chordata, cephalochordates diverged first, with tunicates and vertebrates forming a sister group. Chordates share tadpole-type larvae containing a notochord and hollow nerve cord, whereas ambulacrarians have dipleurula-type larvae containing a hydrocoel.

“We propose that an evolutionary occurrence of tadpole-type larvae is fundamental to understanding mechanisms of chordate origin.”

Satoh et al, 2014 discuss the four hypotheses then circulating. 

(1) “The paedomorphosis scenario: was the ancestor sessile or free-living?”

(2) “The auricular hypothesis – According to this view, the pterobranch-like, sessile animals with dipleurula (auricularia-like) larvae led to the primitive ascidians (as the latest common ancestor of chordates) through morphological changes both in larvae and adults.”

(3) “The inversion hypothesis – Recent debates on the origin of chordate body plans have focused most attention on inversion of the dorsal–ventral (D-V) axis of the chordate body, compared with protostomes”

(4) The aboral-dorsalization hypothesis – “Embryological comparison of cephalochordates with nonchordate deuterostomes suggests that, because of limited space on the oral side of the ancestral embryo, morphogenesis to form the neural tube and notochord occurred on the aboral side of the embryo (the side furthest from the mouth).“Namely, the dorsalization of the aboral side of the ancestral embryo may have been a key developmental event that led to the formation of the basic chordate body plan.”

Some of these recent hypotheses are still stuck in Romer’s world
of 50 years ago, replicating ‘primitive sessile arm feeders’ at the expense of ignoring wriggling round worms.

So, round worm exclusion has been going on for at least that long.
Is it because textbooks rule? New ideas are too expensive to bring to the classroom? Nobody questions the professor? No one else is thinking about this issue?

Funny that no competing hypotheses
consider the extremely simple, primitive, wriggling, telescoping, round worm as a suitable starting point in chordate origins. Evidently in 1991 this was heretical and remains so today. I thought, at the time, it was just being logical.

Next time, in Academia,
let’s start with a simple round worm, then discuss how a mesoderm and notochord developed incrementally over deep time as some roundworms evolved to become chordates and their kin back in the Cambrian or earlier.


References
Peters D 1991. From the Beginning. The story of human evolution. Wm Morrow, Morrow Jr Books, New York. FromTheBeginning book.pdf
Romer AS 1971. The Vertebrate Body – Shorter Version 4th ed. WB Saunders.
Rychel AL, Smith SE, Shimamoto HT and Swalla BJ 2005. Evolution and development of the chordates: collagen and pharyngeal cartilage. Molecular Biology and Evolution 23(3): 541–549. https://academic.oup.com/mbe/article/23/3/541/1110188
Satoh N 2008. An aboral-dorsalization hypothesis for chordate origin. Genesis 46(11):614-22
Satoh N, Rokhsar D and Nishikawa T 2014. Chordate evolution and the three-phylum system. Proceedings of the Royal Society B Biological Sciences. https://doi.org/10.1098/rspb.2014.1729

Origin of chordates webpage

Somites = bilaterally paired blocks of paraxial mesoderm along the head-to-tail axis in segmented animals.

 

12 thoughts on “Chordate origins: Progress since Romer 1971

  1. Assuming by “roundworm” you mean nematode (which is what biologists mean by “roundworm”), you’ve got the fate of the blastopore backward. Nematodes are protostomes – the blastopore becomes the mouth, not the anus (as it does in deuterostomes).

    • Thanks, Chris. That’s important to document and perhaps the reason why extant nematodes (roundworms) were never considered before. Given that only chordates, hemichordates and echinoderms are currently considered deuterostomes, we have to ask, which roundworm-like and ribbonworm-like taxa preceded these three derived clades? None, according to current thinking. None. That can’t be possible based on the need to get from a flatworm (mouth and anus are the same) to a lancelet. At this stage the roundworm (mouth on one end, anus on the other) serves as a model ancestor for all higher taxa. The solution to this problem: Either deuterostomate roundworm-types all became extinct, or one kind of protostomate roundworm became a deuterostomate, or deuterostomate roundworms are still around, but remain untested regarding their embryology. Thanks for bringing this fact to the surface. Here’s a problem that needs a better solution than we have now.

      • Nematodes are related to other protostome groups – annelids, mollusks, arthropods, and some others. They’re not relevant to deuterostome origins.

      • Understood and agreed for all tested nematodes. And yet how to get from a flatworm to a lancelet? Certainly there is a long list of transitional taxa that are not currently in the catalog of known life forms bridging that gap. As mentioned earlier, a roundworm, not segmented, anus on one end, mouth on the other, skin over intestine, no mesoderm (not a nematode) is only one of many missing transitional taxa/stages between flatworms and lancelets. The roundworm model is, at this point, an invention, a placeholder, just like the internally segmented headless worm with gill slits, until someone finds their fossils in the Early Cambrian. Many paleontologists have invented transitional taxa. Romer and Wild are two that come to mind at present.

  2. Maybe the pathway you describe (from flatworms) isn’t what actually happened. There’s a fairly large body of literature over the past 10 to 15 years on the subject of chordate and deuterostome origins. It draws from developmental biology and genetics as well as the fossil record (e.g. vetulicolians). There have been great advances in overall metazoan phylogeny as well, which is how we know neither nematodes nor platyhelminths (flatworms) are relevant to the subject of chordate origins. Romer hasn’t been a primary source on the subject for decades.

    • Chris, you wrote, “Maybe the pathway you describe (from flatworms) isn’t what actually happened.” It would be better if you had a competing hypothesis or citation. Flatworms are diverse and precede the protostomate – deuterostomate split. If not flatworms, then what?

      re: the ‘great advances’… anything more recent or cogent than Satoh N, Rokhsar D and Nishikawa T 2014 (see post)?

      • Question 1 – every analysis to have included “flatworms” as biologists use the term puts them close to, if not within, Protostomata. That’s on the other side of the metazoan tree. I suppose one could imagine some sort of worm that is flat (thus a “flat worm”), but not a member of Platyhelminthes, but the animals that biologists call flatworms are not closely related to deuterostomes.

        Question 2 – I suppose it depends on what one finds to be “cogent,” but the field has advanced in the six years following that reference. And the 2014 reference you used cites very little of the paleontological work that’s been done during the present millenium. It doesn’t mention the vetulicolians, for example. And to understand chordate origins, one must also understand the origins of other deuterostomes (e.g. graptolites, echinoderms, enteropneusts, etc.).

      • I will look for more deuterostome origin citations. If you find any you prefer, please send the citations, because my first search was not very fruitful.

      • This Wiki page might be interesting to the topic, Chris. https://en.wikipedia.org/wiki/Embryological_origins_of_the_mouth_and_anus
        It includes a third possibility, ‘amphistomy” which is a new word for me, and the pertinent comment: “An alternative way to develop two openings from the blastopore during gastrulation, called amphistomy, appears to exist in some animals, such as nematodes.” And here is a citation for a 2019 paper that seems to sum things up to date: https://onlinelibrary.wiley.com/doi/abs/10.1002/9780470015902.a0027481

      • No, flatworms DO NOT precede the protostome/deuterostome. Flatworms (assuming you mean Platyhelminthes) ARE part of the protostome clade. You cannot precede a group you are part of. Dave, you should check again the current knowledge on metazoan phylogeny.

      • Yes, flatworms do precede the protostome/deuterostome split. Primitive forms have no separate mouth/anus. One central ventral opening does the trick.

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