DId Comb Jellies Evolve Nervous Systems Separately?

[lpetrich]

Comb jellies (ctenophores) are very odd animals. They look something like jellyfish, if one does not look very closely. They are rounded, and they have strips of cilia extending across their bodies. These animals' name is from those strips of cilia, because they seem like combs. They often have tentacles, sometimes much longer than their main bodies. Their nervous systems are simple nerve nets, without any well-defined central nervous system.

 Ctenophora, Introduction to the Ctenophora, Comb Jellies | Chesapeake Bay Program, Comb jelly, Open Waters, Invertebrates, Beroe spp at the Monterey Bay Aquarium, Jellyfish and Comb Jellies | Smithsonian Ocean, Comb Jelly (Ctenophore) | the Shape of Life | The Story of the Animal Kingdom

How are these animals related to the rest of the animal kingdom? A traditional hypothesis is Coelenterata, that its closest relatives are cnidarians: jellyfish and sea anemones and coral animals and the like. Their nervous systems are also nerve nets. But molecular phylogeny tells a different story.

I must now introduce the rest of the animal kingdom (Metazoa): sea sponges (Porifera), placozoans (small, blob-like), and bilaterians (all the rest). Sponges and placozoans have no nervous systems, but bilaterians do -- and sometimes very well-developed ones.

Independent origins of neurons and synapses: insights from ctenophores | Philosophical Transactions of the Royal Society B: Biological Sciences

Its starting point is this phylogeny: (ctenophores, (sponges, (placozoans, (cnidarians, bilaterians)))) This is supported by work like Extracting phylogenetic signal and accounting for bias in whole-genome data sets supports the Ctenophora as sister to remaining Metazoa | BMC Genomics | Full Text and The ctenophore lineage is older than sponges? That cannot be right! Or can it? | Journal of Experimental Biology though not Genomic data do not support comb jellies as the sister group to all other animals -- that one finds (ctenophores, (placozoans, (cnidarians, bilaterians))) either side-by side with sponges or emerging from within the sponges. I note that the divergence of these major groups was relatively fast compared to their age, thus making their phylogeny difficult to resolve.

But there is a problem with nervous-system evolution. I'll label organisms with a nervous system N and those without _:
(ctenophores N, (sponges _, (placozoans _, (cnidarians N, bilaterians N))))

So if neurons originated once, then we'd have N (ctenophores, (X sponges, (X placozoans, (cnidarians, bilaterians)))) where X is a loss of a nervous system. But if neurons originated twice, we'd have

(N ctenophores, (sponges, (placozoans, N (cnidarians, bilaterians))))

There is a further problem. Ctenophores' neurotransmitters are different. They don't have most of the small-molecule neurotransmitters that cnidarians and bilaterians do: they have glutamate and gamma-aminobutyric acid (GABA), but not acetylcholine, serotonin, histamine, dopamine, noradrenaline, or octopamine. They also have different "neuropeptides", short protein molecules used as neurotransmitters. So with a single origin, we'd have either this:

N2 (ctenophores, (X sponges, (X placozoans, XN1 (cnidarians, bilaterians))))
or
N1 (XN2 ctenophores, (X sponges, (X placozoans, (cnidarians, bilaterians))))

The XN's are loss and regain of features.

But two origins is simpler:
(N2 ctenophores, (sponges, (placozoans, N1 (cnidarians, bilaterians))))

So we have a remarkable window into the early evolution of animals.

 

[lpetrich]

Molecular-phylogeny techniques have produced a revolution in our understanding of phylogeny, helping to untangle a lot of riddles of evolution. It has done so by supplying an enormous number of new taxonomic characters, even if most of them are rather simple ones. Analyzing protein and gene sequences have had problems of their own, it must be conceded. Problems like long-branch effects and composition biases. But biologists have gradually learned how to overcome them, and they have sometimes done a large amount of number crunching to find phylogenies.

Among placental mammals, the taxonomic orders fall into four superorders, Euarchontoglires, named after its members, Laurasiatheria, named after its northern-continent origins, Xenarthra, named after its distinctive vertebral joints, and Afrotheria, named after its African origins. Of these, Euarchontoglires and Laurasiatheria are grouped together as Boreoeutheria, named after its northern origins, but it's hard to go further. All three possible additional groupings have been proposed by various biologists working on this issue:

• Afrotheria, Exafroplacentalia: Boreoeutheria + Xenarthra
• Xenarthra, Epitheria: Afrotheria + Boreoeutheria
• Boreoeutheria, Atlantogenata: Afrotheria + Xenarthra

Some biologists have even proposed that the split between Afrotheria, Boreoeutheria, and Xenarthra may not be resolvable.

What is interesting is that most of these groups lack distinctive phenotypic features, meaning that they diverged while retaining ancestral-mammalian phenotypes. They looked rodentlike while having an ancestral sort of teeth: 3 incisors, 1 canine, 3 premolars, and 3 molars in each of the four main jaw positions, with the canines elongated as fangs.

 

[lpetrich]

Turning to birds, we find that they split as follows:

• Paleognaths: ratites: ostrich, etc.
• Neognaths:
  • Galloanserae
    • Galliformes: chicken, turkey, pheasant, peacock
    • Answeriformes: duck, goose, swan
  • Neoaves: all the rest

Neoaves has been *very* hard to resolve beyond its taxonomic orders. The phylogenomic forest of bird trees contains a hard polytomy at the root of Neoaves - Suh - 2016 - Zoologica Scripta - Wiley Online Library argues that Neoaves has an unresolvable nine-way split. This is after such work as Ornithologists Publish Most Comprehensive Avian Tree of Life | Biology | Sci-News.com

Integrated Analyses Resolve Conflicts over Squamate Reptile Phylogeny and Reveal Unexpected Placements for Fossil Taxa -- using both morphological (macroscopic-feature) and molecular features. One only has macroscopic features for fossils, but vertebrate skeletons typically have a lot of detail that one can work with.

Snakes are highly modified lizards, and they and some lizards form the taxon Toxicofera, a taxon that contains all lizards known to have venom, and also many without venom. Did venom evolve once and later get lost several times? Or did it evolve more than once?

A phylogenomic analysis of turtles - ScienceDirect (reprint as PDF) Present-day turtles' earliest split is between the Pleurodira (side-neck turtles) and the Cryptodira (hidden-neck turtles). They are distinguished by how they hide their heads, either by turning sideways or by pulling them in. Most turtles, including the better-known ones, are in Cryptodira.

Then an interesting conundrum about turtle evolution. What are their closest relatives? Their skulls do not have certain extra openings, and that's led biologists to conclude that they are descended from late-Paleozoic reptiles called anapsids, from their lack of those openings. But molecular phylogeny points to a different ancestry: diapsids, a group of reptiles with two pairs of extra skull openings, a group that includes the lepidosaurs (lizards (with snakes)) and archosaurs (crocodilians and dinosaurs (with birds)). In particular, turtles are most closely related to archosaurs.

So if turtles are descended from diapsids, their extra openings must have closed up in their ancestors, and a fossil turtle shows evidence of that: Evolutionary origin of the turtle skull | Nature discusses a Permian fossil reptile that looks like it could be a proto-turtle -- and that has a diapsid skull that is becoming an anapsid one. Thus resolving a conflict between molecular and macroscopic-feature phylogeny.

 

[lpetrich]

Why we still need fossils:

Fossil‐based comparative analyses reveal ancient marine ancestry erased by extinction in ray‐finned fishes - Betancur‐R - 2015 - Ecology Letters - Wiley Online Library ((PDF))

This complicates the issue of which habitat was ancestral, because many freshwater-only groups of fish have extinct marine members. So from present-day ones, one would conclude that ray-finned fish have a freshwater ancestor, while from fossil evidence, one may conclude a marine ancestor. One also finds that marine-to-freshwater is much more common than freshwater-to-marine.

Resolution of ray-finned fish phylogeny and timing of diversification | PNAS - uses fossils for calibration.

Early Gnathostome Phylogeny Revisited: Multiple Method Consensus -- morphological, but uses molecular-phylogeny methods. Present-day jawed vertebrates are descended from mid-Paleozoic armored fish called placoderms.

Hagfish from the Cretaceous Tethys Sea and a reconciliation of the morphological–molecular conflict in early vertebrate phylogeny | PNAS -- morphological: (hagfish, (lamprey, jawed fish)), molecular: ((lamprey, hagfish), jawed fish). This new specimen has only morphological information, for obvious reasons, but it is consistent with the molecular tree.

Hemichordate genomes and deuterostome origins | Nature is about the genomes of some acorn worms (enteropneusts). They have gill slits in the sides of their throats, as chordates do, at least embryonically. But they are more closely related to echioderms (starfish, sea urchins, sea cucumbers, sea lilies) than to chordates, contrary to what one would expect from their appearance. Among the chordates, urochordates (sea squirts) are closer to vertebrates than cephalochordates (amphioxus) are, also contrary to what one would expect from their appearance:

• Chordata
  • Cephalochordata - amphioxus
  • Urochordata (sea squirts), Vertebrata
• Ambulacraria
  • Hemichordata - acorn worms, pterobranchs
  • Echinodermata - starfish, etc.

 

[lpetrich]

Fossil calibrations for the arthropod Tree of Life - ScienceDirect (PDF) - Uniramia (insects and myriapods) is gone. Insects (Hexapoda) branch off from within Crustacea. Their closest relatives is some obscure ones called remipedes.

Overall: (Mandibulata: (crustaceans with insects, myriapods (centipedes, millipedes, ...)), Chelicerata (spiders, scorpions, horseshoe crabs, ...))

Current Understanding of Ecdysozoa and its Internal Phylogenetic Relationships | Integrative and Comparative Biology | Oxford Academic - named after their molting, their shedding of outer skins.

Arthropods' closest relatives are consistently identified as onychophorans (velvet worms), though beyond that, it is less than clear. This group includes tardigrades (water bears), nematodes (roundworms), and some obscure marine worms: kinorhynchs, loriciferans, and priapulids (penis worms).

Loriciferans are tiny worms (< 1 mm long) that became big news when some of them were discovered to not need oxygen (Anaerobic Metazoans: No longer an oxymoron | BMC Biology | Full Text, Anaerobic animals from an ancient, anoxic ecological niche). They were living on the Mediterranean seafloor, and the decomposition of organic detritus there tends to eat up the oxygen there -- decay microbes get it first. Some loriciferans there survived by doing only pre-oxygen parts of their energy metabolism, and some of them lost oxygen use because it was no longer maladaptive. Thus doing what lots of one-celled organisms had done.

Tardigrades have gotten a lot of attention recently because of their ability to survive hostile conditions like outer-space conditions. They do so by going into suspended animations. Like every other organism on our planet, they need liquid water to metabolize and grow and reproduce in. Another interesting curiosity is segment homology. The Compact Body Plan of Tardigrades Evolved by the Loss of a Large Body Region: Current Biology -- they are essentially a head without a body, though they have a genital segment on their rear ends.

 

[lpetrich]

I now turn to the other subdivision of Protostomia, a taxon variously called Lophotrochozoa or Spiralia. Sometimes Spiralia is a subtaxon of Lophotrochozoa, or vice versa.

On 20 years of Lophotrochozoa | SpringerLink
Phylogenomics of Lophotrochozoa with Consideration of Systematic Error | Systematic Biology | Oxford Academic
The phylogenetic position of dicyemid mesozoans offers insights into spiralian evolution | Zoological Letters | Full Text
Spiralian Phylogeny Informs the Evolution of Microscopic Lineages - ScienceDirect
A New Spiralian Phylogeny Places the Enigmatic Arrow Worms among Gnathiferans - ScienceDirect

Hard to come to any clear conclusions about subdivisions of them.

Their best-known subgrouping is the molluscs:

Resolving the evolutionary relationships of molluscs with phylogenomic tools | Nature (PDF)
The evolution of molluscs - Wanninger - 2019 - Biological Reviews - Wiley Online Library

Molluscs aplit up into two main groups, Conchifera and Aculifera. Conchifera contains the better-known ones: gastropods (snails), bivalves (clams, oysters, mussels, scallops), and cephalopods (octopus, squid, nautilus), along with the scaphopods (tusk shells). Aculifera contains the chitons, with their body covered by 8 mini-shells, and some obscure wormlike forms.

Annelids include earthworms and leeches, and also lots of marine worms, including some that have lost their segments: Sipuncula (peanut worms), Echiura (spoon worms), and Siboglinidae (beard worms and giant tube worms). I remember a biologist describing the discovery of tube worms at a hydrothermal vent. He described that for much of his career, the largest organisms that he would find on the ocean floor were tiny worms that he'd need a microscope to see. But these tube worms, he said excitedly, one could dissect with a knife and a fork and a spoon.

 

[untermensche]

Maybe.

 

[lpetrich]

Phylogenomic Analyses Support Traditional Relationships within Cnidaria

• Anthozoa -- polyp-only
  • Hexacorallia - most stony corals, sea anemones
  • Octocorallia - soft corals, sea pens
  • Ceriantharia - tube-dwelling sea anemones
• Medusozoa -- polyp-medusa alternation, though some are one or the other
  • Hydrozoa - Portuguese Man O' War is a colony of some of them that acts like some single super jellyfish
  • -
    • Staurozoa - stalked jellyfish
    • Scyphozoa - ordinary jellyfish
    • Cubozoa - box jellyfish

Some anatomy: cnidarians are cylindrical or disk-shaped with the mouth at one end or side, the oral one. The other end or side is the aboral one. Around a cnidarian's mouth is some tentacles, and the tentacles have stingers on them.

A polyp is benthic (ocean-floor), with its aboral end attached to the seafloor. A medusa is the jellyfish form, and is pelagic (open-ocean), with its aboral end upward and its mouth and tentacles downward. From the looks of it, it would seem that cnidarians are ancestrally polyps, with the medusa phase being derived from it.

 

[lpetrich]

Ancient coexistence of norepinephrine, tyramine, and octopamine signaling in bilaterians | BMC Biology | Full Text
Two types of receptors for each kind of monoamine neurotransmitter are found for some species and presumed ancestral in Bilateria.

Ancestry of neuronal monoamine transporters in the Metazoa | Journal of Experimental Biology
The ancestral bilaterian had three kinds of transporters: SERT for serotonin, DAT for dopamine, and MAT for an assortment of monoamine neurotransmitters.

Anatomy and development of the nervous system of Nematostella vectensis, an anthozoan cnidarian - Marlow - 2009 - Developmental Neurobiology - Wiley Online Library N. v. is a common model system.

Cnidarians utilize both classical fast (acetylcholine, glutamate, GABA, and glycine) and slow (catecholamines and serotonin) transmitters and neu-ropeptides (especially of the RFamide and RWamidefamilies) for synaptic neurotransmission (Satterlie, 2002; Kass-Simon and Pierobon, 2007).

Catecholamines include epinephrine (adrenaline), norepinephrine (noradrenaline), and dopamine.

The paper mentioned that N.v. has a gene for a protein much like bilaterian dopamine beta hydroxylase, which converts dopamine into norepinephrine.

So cnidarians and bilaterians have a lot of neurotransmitters in common.