Bizarre, Bizarrer, Bizarrest…

20 Jun, 2014

Recent research has shown that Ctenophores have a unique genome and nervous system structure, not related to those seen in any other animals.

Once again one of my favorite weird animal groups has risen to the surface in the boiling, bubbling, babbling, cauldron of phylogenomic research.

Phylogenomics is the science of using an organism’s genetic code as a major part of determining the relationships within an animal group, specifically within the evolutionary linkages in the group. Over the last 30 years, this field has developed as one of the major thrusts of recent biological research. It is nothing less than the attempt to put all of the leaves on all of the branches of the family tree of all organisms. A huge and daunting task, to be sure, but a more interesting one I would hard pressed to find.

It was a pipe dream of most biologists of my generation and before: to discover the true relationships among organisms. When I was but a mere and inconsequential young student of invertebrates, as opposed to my present status as a mere and inconsequential moldy and oldie student of invertebrates, when a group of us got together and sat down for an evening of biological chit chat, over pizza and beer, and more beer, and more beer… We would often brainstorm relationships of our favorite groups using the most recent published literature that we thought was pertinent. We knew we couldn’t do much more than deplete the oxygen in the room by our talking, though; as at that time, there were no real ways to attack the problems of who was descendent from whom and when. Oh, we all had ideas, and we were vocal at defending them, and through these discussions we even on occasion came up with some sort of new idea or new way to attack an old idea, but practically speaking we knew that our efforts were useless. There was simply no way to test any idea.

And that was really a problem.

Science is all about hypothesis testing, and that is what separates it from all other methodologies of problem solving. Of all methods humankind has developed for solving problems, the scientific method is the only one that relies on testing hypotheses using empirical evidence as part of the process. Each time we proposed a relationship of species “A” evolving from some other species “B”, we knew that it was not testable. We were discussing science fiction rather than science.

Unless you have been in a closet for the last 25 or 30 years, you know that we now can determine an organism’s genetic code. And even better, by the use of sophisticated and rather esoteric, but perfectly explicable statistical analyses, the genetic codes of any organisms can be compared one to another. If this is done properly and over enough species to provide a reasonable data set, it is possible to relate organisms by their similarity of genetic codes. From this, it is but a hop, skip, and leap, to construct a tree of relatedness… or a family tree. And one based in fact, at that.

If this wasn’t exciting enough, techniques were developed over the same time span allowing the comparison of organisms using virtually any morphological or physiological character. If a large enough number of characters is used in such a comparison, and the comparison is done using the right methods, one can also construct a tree of relatedness using non-genetic characters. And this comparison, like the one using the genome is also based in fact, objective and replicable.

And, Presto! Change-Oh!

And quick like a bunny, all of sudden researchers cound rigorously construct family trees as the hypotheses they always were, test them and discard the losers. Then do it again, and better, and refine the winners and repeat until we have a reasonable idea for an evolutionary pathway. At least, that is the idea. And for many groups it works really well. For example, within vertebrate lineages, it is now reasonably clear that dinosaurs are not extinct, but remain with us, in the form of their avian descendants. This of course, does away with chordate taxonomic group referred to as the Class Aves, as it is clear that there are a good many fossils that are undoubtedly not something that could be called a bird, but are related to, and within the lineage of, birds.

Within the invertebrates, many of the changes were nothing short of paradigm changing. For example, it used to be thought that flatworms, as a group, called the Phylum Platyhelminthes, were primitive animals, pretty much at the base of the animal family tree, just above things like ctenophores, and just below things like the ribbon worms. This was such an obvious straight-forward relationship, that nobody ever gave it a second thought.

Oops… WRONG!!!

Some of the first good phylogenomic investigations showed that first off, there was no valid natural group that could be called the “flatworms.” Instead there was a group of separate lineages, all looking flat and wormy, that were not terribly closely related. Additionally, many of these were animals with simple structure that were clearly descended from more complex animals. In other words, some of the flatworm lineages were not intermediates in structure, but were the result of simplifications for their specific habitats and ecological roles. Finally, in amongst all of these worms that were small and flat, was one lineage, the Acoels, or Acoelomorpha if you like the long term, that were probably as close as possible today to being like some of the ancestral worms that did lead the way to the rest of bilateral animal kingdom. A lot of biology and invertebrate zoology text books found their way into the recycle box or trash bins with the publication of papers elucidating these relationships.

Acoel flatworm

Acoel flatworm from a coral reef aquarium

However, as more and more work was done with certain groups, some phylogenomic work raised more questions than they answered. Particularly, this was true about the important relationships at the absolute base of the animal family tree. Specifically, these questions involved the relationships between four groups, the Sponges, a very small, very funky group of critters called the Placozoa, the Cnidarians, and, my favorite, the Ctenophores. All sorts of odd schemes were produced, mostly on the order of “A” evolved from “X” which gave rise to “C” every second Thursday in the Primeval month of Sludge, but gave rise to “B” on the alternate weeks, but only if Begonias were blooming in the laboratory of the confounded Alchemist in the next office over in the tesseract.

That is only a slight exaggeration of what occurred when the tests done by several very good groups of researchers were all put together. The base of the family tree in virtually all the “old” hypotheses of linkages, in other words, the ancestor to all animals, was likely a type of colonial protozoan called a choanoflagellate. The cells comprising these creatures are very similar to the feeding cells of sponges, called choanocytes. So, the most primitive of real animals were considered to be sponges. And for good reasons, sponges lack virtually all organization, they have no gut, no nerves, no muscles, no this, and certainly none of that. Effectively, most sponges are living pump-filter modules consisting of multicellular blobs. Then somehow or someway, Placozoans arose. Placozoans are very strange critters that consist of two layers of cells, a top and a bottom, fastened together with some goo that ooze, slowly slithering and sliming their way around on rocks in warm oceans making a living by, apparently, absorbing nutrient from things they crawl over. Placozoans have been considered a dead end, with no known descendants, for a very long time. The next great leap up the ladder of life was from Porifera or sponges to the Cnidaria, possibly by some sort of change in some sponge larvae. And from the Cnidaria, like magic, somehow, the Ctenophora arose, after all ctenophorans had to be close relatives of jellyfish, didn’t they? After all, they are gelatinous structures as are jellyfish, and they both used tentacles to catch their prey.

If you have been able to follow my discussion so far, you may be able to find some of the problems in the “old” hypothesis. The major ones have to do with ctenophores. As has become evident to some people (others of us realized this long ago, but nobody would believe us), ctenophores are by no means simple creatures. Cnidarians ARE simple. They consist of two tissue layers and a third layer that is largely connective fibers that glues the two tissues together. In essence, cnidarians are tissue sacks that digest food. They have only one opening to the gut. They have no circulatory system. Most of them don’t have real muscles, but instead have modified epithelial cells that function as muscles. Their nervous system as about simple as nervous system can be. There are no ganglia, and only a few sense organs found in the entire phylum, mostly in various jellyfish. Ctenophores, on the hand (er, tentacle), have true muscle cells derived from an embryonic germ layer, their nervous system is complex, and has an aggregation of nerve cells, and sensory structures that function as the brain. In contrast to the Cnidarians which function wholly by reflexes ctenophores actually have complicated behaviors. They have a one-way gut that has a mouth and anal pores. The ctenophores have an absolutely unique locomotory structure of huge fused cilia called a “ctene” or “ciliated comb”. And, no matter how hard anyone tries, it seems impossible to relate ctenophores to anything else. They cannot be clearly shown to be descendant from any group, and neither can they be shown to have given rise to any group.

And, genomics, the answer to almost all things regarding relationships, has really been of no help. Any relationships that ctenophores have with any other animal groups occurred so long ago that any genetic information that could be used to test “relatedness” is lost in signal noise.

And if that were not enough…

An article published in the 5 June 2014 issue of journal, Nature, adds yet another level of information about the differences between Ctenophores and the rest of the multicellular animals, the metazoa. In an exceptionally neat set of very complicated experiments, by Ctenophorophiles from all over the world, a major study of the ctenophore genome was conducted. The authors sequenced the entire genome of Pleurobrachia bachei, a ctenophore called by some folks the Pacific Sea Gooseberry. The genome was comprised of 156,146,497 base pairs (bp) with 19,523 predicted protein-coding genes. As a comparison, some estimates for the human genome have the total size at about 3,200,000,000 bp with about 21,000 genes. Consequently even though the human genome contains over twenty times the DNA, it encodes for about the same number of genes. Interestingly, a large number of eukaryotic organisms of all sorts of types contain about the same number of genes. 

Plleurobrachia bachei

Pacific Sea Gooseberry, Pleurobrachia bachei.

Additionally, they also looked at the genomes of several species from all other ctenophore lineages. What they found was nothing short of astounding.

The abstract of their paper is here (and the emphases are mine):

“The origins of neural systems remain unresolved. In contrast to other basal metazoans, ctenophores (comb jellies) have both complex nervous and mesoderm-derived muscular systems. These holoplanktonic predators also have sophisticated ciliated locomotion, behaviour and distinct development. Here we present the draft genome of Pleurobrachia bachei, Pacific sea gooseberry, together with ten other ctenophore transcriptomes, and show that they are remarkably distinct from other animal genomes in their content of neurogenic, immune and developmental genes. Our integrative analyses place Ctenophora as the earliest lineage within Metazoa. This hypothesis is supported by comparative analysis of multiple gene families, including the apparent absence of HOX genes, canonical microRNA machinery, and reduced immune complement in ctenophores. Although two distinct nervous systems are well recognized in ctenophores, many bilaterian neuron-specific genes and genes of ‘classical’ neurotransmitter pathways either are absent or, if present, are not expressed in neurons. Our metabolomic and physiological data are consistent with the hypothesis that ctenophore neural systems, and possibly muscle specification, evolved independently from those in other animals.”

When all was well and done, their results showed that ctenophores are absolutely unlike any other multicellular animals. They appear to have independently derived nervous and muscular systems. Their nervous systems by and large use only two of the many neurotransmitters found in the rest of the animals, but just to be different, do use a relative large number of neurotransmitters that are not found or used by any other animals.

Their data showed that the ancestral animal lineage started from Choanoflagellate ancestors and the Ctenophora branched off first, followed by Porifera (sponges), then Placozoa (Trichoplax), then the Cnidaria and finally the bilaterally symmetric animals or Bilateria. There are only two possible ways to explain the data and relationships.

In the first alternative, the Ctenophora branched off the main animal lineage and subsequently developed a nervous system, a digestive system, and muscles. Subsequent organisms that evolved from the main animal lineage lacked a gut, as well as both nerves and muscles, and from this gutless and nerveless ancestral lineage first the sponges and then the placozoans arose. Organisms in these phyla lack nerves and muscles. Subsequently, the organisms in the main ancestral lineage developed a rudimentary nervous system and gut and gave rise to the ancestral Cnidaria. Subsequent to that the ancestral lineage developed muscles and from this lineage all other animals arose. Thus, in this hypothetical alternative the gut, the nerves and nervous systems, and muscles evolved twice.

In the second alternative, the animals in ancestral lineage developed a gut, nerves, and muscles, and then gave rise to the Ctenophores, which had a gut, nerves, and muscles. The animals in the ancestral lineage give rise to the lineage leading to sponges, which then lost nerves and muscles and the gut, so that today’s sponges lack nerves, gut, and muscles. That lineage may have given rise to the placozoans which also lack nerves and muscles, or a second lineage branched off the ancestral lineage containing nerves and muscles which subsequently were lost along the way to the placozoans. After both the nerveless, muscle-less and gutless sponges and placozoans had developed from the ancestral lineage having muscles, nerves, and a gut, that lineage gave rise to the Cnidarians, which lost the complete gut, but retained the mouth and digestive region. Subsequently, all other animals arose from the ancestral line, which had a complete gut, muscles and nerves. In this alternative, the ancestral critters first developed nerves, muscles and a gut. From this ancestor, the Ctenophores arose. The ancestral lineage then gives rise to an offshoot which will develop into the Sponges, and this lineage loses all traces of muscles, nerves and a gut. Subsequently from the ancestral lineage a second lineage arises to give rise to the Placozoans which also loses the gut, muscles and nerves. The ancestral line then gives rise to Cnidarians, which lose the ability to have a complete gut, and true muscles, but retain nerves. Finally the ancestral lineage develops into an ancestor of the rest of the animals, which finally has a complete gut, muscles, and a nervous system.

So, the first alternative has a simple form giving rise, on two separate occasions, to different derivations of animals with guts, muscles and nerves. The second alternative has a simple form developing a complete gut, muscles, and nerves. This form gives rise to one derivation with a gut, muscles, and nerves, additionally it gives rise to two separate derivations which lose the gut, nerves and muscles, and finally it gives rise to one derivation that has nerves and an incomplete gut, but not true muscles, and one final derivation that loses the complete gut, but has muscles and nerves. Eventually this animal develops a complete gut and becomes ancestral to all other animals.

The authors conclude the first alternative is more likely.

One of the unifying tenets of modern biology is that the evolution of life has only occurred once, and that virtually all cellular microstructures as well as most cellular functions are identical no matter where they are found. So, that cilia are cilia are cilia are the structurally same in all animals and plants and fungi. Muscles are formed the same way in all organisms that have them, so smooth muscles in a mollusk’s foot have the same basic properties as smooth muscles in the human stomach lining. By and large, sperm look like sperm anywhere in the animals. The two types of photoreceptors are basically the same in all animals. The same metabolic pathways work the same way in all animals, and are used for the same functions. The nervous system components appear identical and function identically using the chemical pathways in all animals that have nerves (sponges and placozoans lack a nervous system), and so on…

Uh… Oh… Well, until a few days ago, that was true.

Now, we can scratch the nervous and muscular systems off that list. And the last sentence must be corrected to read as follows: The nervous system components in all animals except Ctenophores appear identical and function identically using the chemical pathways in all animals that have nerves (sponges and placozoans lack a nervous system). Ctenophores appear to have a uniquely derived nervous system, and possibly a muscular system derived differently from all other animals. Furthermore, their means of locomotion using huge fused cilia is unique as is their method of capturing prey using colloblasts.

Finally, ctenophores actually have a fossil record that dates back over 500 million years to the Burgess Shales and the Chengjiang Fauna. These fossils have a somewhat different structure from modern forms, but can reasonably interpreted as being Ctenophores. Additionally, Ctenophores have been proposed to remnants of a type of life called the Vendian fauna, which arose prior to the Cambrian “Explosion” of life that appeared to spawn almost all modern groups. Perhaps that hypothesis has gotten some supportive evidence in the study reported upon here.

References:

Dzik, J. 2002. Possible ctenophoran affinities of the Precambrian ‘‘sea-pen’’ Rangea. Journal of Morpholology. 252: 315–334.

Moroz, L., K. Kocot, M. Citarella, S. Dosung, T. Norekian, I. Povolotskaya, A. Grigorenko, C. Dailey, E. Berezikov, K. Buckley, A. Ptitsyn, D. Reshetov, K. Mukherjee, T. Moroz, Y. Bobkova, F. Yu, V. Kapitonov, J. Jurka, Y. Bobkov, J. Swore, D. Girardo, A. Fodor, F. Gusev, R. Sanford, R. Bruders, E. Kittler, C. Mills, J. Rast, R. Derelle, V. Solovyev, F. Kondrashov, B. Swalla, J. Sweedler, E. Rogaev, K. Halanych, and A. Kohn. 2014. The ctenophore genome and the evolutionary origins of neural systems. Nature 510: 109-114.

Tang, F., Bengtson, S., Wang, Y., Wang, X. L. & C. Y. Yin. 2011. Eoandromeda and the origin of Ctenophora. Evolution and. Development. 13: 408–414 (2011).

 

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About the author

Ronald L. Shimek, PhD
Ronald L. Shimek, PhD

I am a marine biologist/invertebrate zoologist who got captivated by - or sucked into - the reef aquarium hobby late in the last millennium, I have written widely in the hobby press and elsewhere, mostly about invertebrates (in the context of the hobby, anything but fishes) and how to keep them alive. I reside in Wilsall, Montana, about as far from the ocean as one can get and still live in the contiguous 48 states, go figure... What can I say, it is home. :-)

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