As a new article in Nature (title below) notes, there are five major groups of animals that arose early in animal evolution and persist today: ctenophores (comb jellies), sponges (Porifera), placozoans (small, simple multicellular organisms), cnidarians (jellyfish, corals, sea anemones), and bilaterians (all other animals ranging rom molluscs to vertebrates). We have a pretty good notion of when their ancestors branched off from each other in evolution (this is in effect their relatedness, expressed in their phylogeny, or family tree), except for one question: which group’s ancestors branched off first? That group would be called the “sister group” of all living animals. (It could also be called “the outgroup among all groups of animals”.)
DNA sequencing has shown that it’s either the ctenophores or the sponges (the most common candidate), but it’s been very difficult to decide between the two because there’s been so much time since the ancestors of modern sponges and ctenophores branched off from the other groups—700-800 million years—that too many DNA changes have accumulated to allow a firm DNA-based resolution. (DNA is now the best way to go to resolve these trees.) Every few years then, someone attempts another DNA-based phylogeny of animals, and the outgroup keeps changing between sponges and ctenophores.
Why is this an important question? Not just curiosity alone, for its resolution bears on understanding an important fact: like all other animals except sponges, ctenophores have nerves and muscles. This would seem to show that ctenophores are grouped with the other animals, while sponges branches off early, and then nerves and muscles evolved in the ancestor of all other animals. This convinced many that sponges were the outgroup. If ctenophores, on the other hand, were the sister outgroup that branched off first, that would leave us with a puzzle: why are sponges the one exception, lacking nerves and muscles, among all other animals? Here are the two possibilities for the outgroups, with “N&M” showing where nerves and muscles evolved. (I’ve put the dots and “N&M” stuff in myself.)
A. Ctenophore outgroup: The ancestor of ALL animals did have nerves and muscles, but sponges lost them.
or
B. Sponge outgroup: Nerves and muscles evolved after the ancestor of sponges had branched off from the ancestor of all other animals. (No loss of already-evolved characters required.)
The left side shows “A”, with the common ancestor of all animals having nerves and muscles, but then they were lost in the ancestor of living sponges. The right side shows possibility “B,” with the ancestor of all living animals (red dot) lacking nerves and muscles, which appeared later in the common ancestor of all living animals after that ancestor had branched off from the ancestor of sponges.
As you can see, “A” posits two evolutionary events: the evolution of nerves and muscles in the ancestor of all living animals, and then their loss in the sponge lineage, while “B” posits nerves and muscles evolving evolving just once: in the ancestor of all non-sponge animals.
However, if “A” is the case, you could posit another scenario in which ctenophores independently evolved nerves and muscles from other groups of animals, while the ancestor of all animals lacked them.
The diagram below shows a common ancestor of all animals (red dot) lacking nerves and muscles, and then they evolved twice independently: in ctenophores, and then also in the other groups that branched off later from the common ancestor with sponges. Thus, if A is correct and ctenophores are the outgroup, there are still two explanations for the nerve/muscle presence in animals: either they were in the ancestor of all living animals and then lost in the ancestor of sponges, or they didn’t occur in the animal ancestor but then evolved twice independently (N&M shown where the evolution happened). As you can see, if the red-dot ancestor lacked nerves and muscles, but all modern animals save sponges have them, AND ctenophores were the sister group, then nerves and muscles must have evolved twice OR (as you see above), all early animals had them but the ancestor of sponges lost them. So the left side of the diagram above OR the diagram below show the two evolutionary possibilities for where muscles and nerves occur.
This is why resolving the outgroup is important: it leads to different hypotheses about how evolution worked. Again, the alternatives are A with the ctenophore outgroup, in which cases nerves and muscles were either lost in sponges or evolved twice independently; or B, with the sponge outgroup, in which case nerves and muscles evolved just once—in the common ancestor of all other animals. Because “B” seems more parsimonious to many, that has been the consensus scenario.
But now the consensus seems wrong: new data show pretty convincingly that ctenophores do appear to be the outgroup, and sponges are more closely related to all other living animals than are ctenophores. You can read about this by clicking on the screenshot below, or going to the pdf here (reference at bottom).
The analysis was very clever. Instead of just looking at large amounts of DNA in the animals, they looked at the order of DNA sequences (genes) on the chromosomes. Over the last 800 million years, that DNA has been shuffled around as chromosome fuse or bits of chromosomes come loose and stick to other chromosomes (translocations). In either case, chunks of DNA then get shuffled around among chromosomes and on a given chromosome by inversions.
And that’s what the authors did: they not only sequenced or took sequences from entire genomes of all the animal lineages above (including two species of ctenophores), but ordered genes along chromosomes. (This isn’t hard to do: you get the DNA as a sequence, and the DNA sequence on one chromosome will not run on to the DNA sequence on another chromosome.) They not only looked at all animal lineages, but also single-celled groups that are less closely related to animals, like amoebas and choanoflagellates (these aren’t considered “animals” but whose ancestors are considered outgroups to all living animals).
The results were pretty unequivocal: they found several chunks of DNA that were shared by the single-celled relatives and ctenophores, but also four ordered chunks of genes that were shared by all living multicellular animals except for ctenophores. That is, sponges shared gene chunks with vertebrates, cnidarians, and placozoans, but those chunks were in completely different places in the ctenophores.
The conclusion: the chunks found their shared locations in modern animals after they had already branched off from the ancestor of modern ctenophores. Ctenophores are thus the outgroup, and we’re less closely related to them than to sponges. The scenario in A above is the correct one. (The three groups at the top of the diagram below are single-celled non-animal organisms that are distantly related to animals.) As you see, the ctenophores branched off from all other living animals before any other animal group, making them less closely related to modern animals than are sponges.
Now this analysis may be wrong, but given the irreversibility of moving gene chunks around repeatedly, shared gene chunks on chromosomes almost certainly means shared ancestry. I’m pretty confident, then, that this paper has resolved the long-standing controversy about the “outgroup” of all animals.
But this leaves us, of course, with two questions. Did the ancestor of all living animals have muscles and nerves, and sponges simply lost them, or did nerves and muscles evolve twice independently?
Each of these comes with another puzzle. The first one is this: why did sponges have complex and highly evolved set of features to sense the environment and move about, but then lost it? The second one is even more puzzling: how could such complex features evolve twice independently?
UPDATE: I forgot about this but was reminded. Another trait shared by ctenophores and all other animals save sponges is the gut: a digestive channel formed by “gastrulation”—invagination of the embryo. Thus we have to account for the disappearance of three features in sponges or the independent evolution of guts, nerves, AND muscles.
While we know that the best information we have is scenario “A” above, we don’t know whether sponges lost their gear or that gear evolved twice independently. The authors of the paper don’t discuss this, but in a NYT article on the piece by Carl Zimmer, he finds a hint that nerves and muscles may have evolved independently in ctenophores and in all other animals that have them:
Instead, researchers are looking now to comb jellies to see how similar and different their nervous systems are from those of other animals. Recently, Maike Kittelmann, a cell biologist at Oxford Brookes University, and her colleagues froze comb jelly larvae so that they could get a microscopic look at their nervous system. What they saw left them baffled.
Throughout the animal kingdom, neurons are typically separated from one another by tiny gaps called synapses. They can communicate across the gap by releasing chemicals.
But when Dr. Kittelmann and her colleagues started to inspect the comb jelly neurons, they struggled to find a synapse between the neurons. “At that point, we were like, ‘This is curious,’” she said.
In the end, they failed to find any synapses between them. Instead, the comb jelly nervous system forms one continuous web.
When Dr. Kittelmann and her colleagues reported their findings last month, they speculated yet another possibility for the origin of animals. Comb jellies may have evolved their own weird nervous system independently of other animals, using some of the same building blocks.
Dr. Kittelmann and her colleagues are now inspecting other species of comb jellies to see if that idea holds up. But they won’t be surprised to be surprised again. “You have to assume nothing,” she said.
That is, there are differences between the nerves in ctenophores and in all other nerve-bearing animals: the former appear to lack synapses. This suggests that nerves could have evolved independently, and taken two routes, one route lacking a gap (the synapse) between the nerves. As for the muscles, neither the paper nor Zimmer deals with whether there’s some fundamental differences between how muscles are structured or how they work between ctenophores on the one hand and all other muscle-bearing animals on the other.
As usual, we’ve probably settled one evolutionary question but it’s raised several others. People now will be devoting more attention to nerves and muscles in animals.
As one of my friends, who teaches introductory biology in a major university, said, “Well, I guess I’ll have to revise my lecture notes. For years I’ve been telling students that while the outgroup of all animals isn’t known for sure, it is most likely the sponges.”
Here’s a ctenophore shown on Wikipedia. They are really cool animals, and if you want to see a bunch of them, go to the Monterey Aquarium in California, where they have a mesmerizing display:
Trying a “sub” – would work great for this – hoping that feature returns one day.
Never having used it, I hadn’t noticed it had gone. Not that “sub” itself is of any significance. But the “Notify me of new posts via email.” check-box is in the “Post Comment” bits, as it always has been.
Jerry, thank you for this summary and excellent explanation, not only of the science but its significance, and for including the primary literature references. I’ve shared your page with my colleagues who teach this material.
It’s not surprising that having nerves and muscles is so useful that it evolved twice – I mean, how many times did eyes and wings evolve independently? But… why haven’t sponges evolved them yet? Are they so happy in their niche that there’s just no gradual advantage to having them?
Around 40 times, for various meanings of “eye” ranging from the relatively simple photosensitive spots of some molluscs (scallops, for example), past the back-to-front designs of vertebrates, to the pinnacle of optical pseudo-design that is the octopoid eye (another mollusc).
Hmmm, about two (EDIT: four) and a (EDIT: two*)half times. Once in the insects. Once in the dinosaurs (now called “birds”, but still dinosaurs nonetheless). Oh, and the pterosaurs, which are of uncertain relations, but definitely not dinosaurs. And the bats – which are not dinosaurs either. With a half-count for various mammals that are trying to develop flight at the moment – “flying squirrels” etc. Oh and some snakes are trying that evolutionary route too. So that would make it about 4 and two-halves times that flight has evolved. Unless I’ve missed one.
(Remembering the “Notify-not-sub” check-box.)
Fascinating. Thanks!
Thanks Jerry for this very informative and fascinating post. These are the crown jewels of your website, I’m always delighted when I see here a deep analysis of some interesting scientific question. No matter how many or how few comments you get on this post, please know how much it is appreciated by your readers.
Your story raises a surprising problem. Everyone knew that the placement of comb jellies was uncertain, and that one of the scenarios could have been strongly supported if it turned out that the nervous system of comb jellies was fundamentally different from that of the other animals. This could have been examined by any observant scientist without special equipment. It is the sort of thing that even Darwin, with the technology of his time, might have written about if he had known to ask the question.
So why had comb jelly nervous systems not been closely examined until Kittelman’s recent work? And why have their muscles still not been examined????
I think this shows that “if you have a hammer, all you see is nails”. Now that we have DNA, people have lost interest in using ordinary tools to help solve these interesting problems. That’s a shame. It is also an inspiration. There are still fundamental problems that could be solved by sufficiently clever observation.
unfortunately it is nowadays easier to get funding based on the amount of data one promises to produce -not their quality or their link to a meaningful hypohesis
Yes, but you can now bring in evo-devo and see if the neural and muscle tissues involve the same genes in ctenophores and other animals. It’s true that “switch genes” like Pax-6 can be repeatedly involved in independent cases of evolution (eyes), but if a LOT of the same genes wer einvolved in ctenophores and other animals, that would mply a secondary loss in sponges. See this thread for a comment I made on Placozoans, which I unfortunately neglected in the discussion above.
Yes, surely genetic analyses give us much more information and much more confidence. But simple observational evidence (microscopic comparisons of nerves and muscles) could have shifted the (apparently wrong) default hypothesis long before now.
I got this far down the comments list and was thinking “what about the Placozoa” too.
Presumably (I don’t claim to know anything about this stuff, but …) if nerves and muscles had evolved twice independently, then the genes for nerves and muscles would be very different in the two cases, wouldn’t they? And wouldn’t that be relatively easy to check?
Not necessarily. Even when structures are evolved independently, sometimes it’s the same genes that are “utilized”. Jerry mentioned a little while back a recent study showing that mammalian air foils (gliding membranes and bat wing skin) involve modifications of the same complex of genes in the several independent origins of air foils. (We know they are independent because of overwhelming comparative evidence from modern and fossil forms. Some, e.g., are marsupials, while others are squirrels.)
GCM
I was just looking at the paper the other day. The synteny diagrams (diagrams showing alignment of genes on chromosomes across species) were important visuals, but hard for me to parse. A couple comments.
1. I guess I need to revise what I say about this in my next Evolution class. This does seem like a powerful, though novel argument.
2. And those @$%# Placozoa! These are the simplest animals (move over sponges), with just a pancake of epithelium surrounding a loose filling of mesenchyme cells. No nervous tissue or muscles, but apparently they had those things once upon a time but then lost them?
Yeh this is an important point. Placozoa losing *everything* seems unlikely. Perhaps even more unlikely than bilaterans *also* evolving nerves and muscles a 3rd time?
IMO this needs to be considered alongside the Ediacaran biota – we already know that complex “animals” must have evolved severally times at least because of them…
Placozoans apparently have some of the molecular precursors of neurons, but as far as I’ve been able to discover, nothing like muscle cells. The get around by amoeboid or cilliary action.
Weird little things. Their phylogenetic position is still uncertain. These authors did look at them, however, and found that they fall into the sponge-cnidarian-bilaterian group.
I think they go there based on genetic comparisons, in that they have as you say molecular precursors (or molecular remnants?) of neurons.
This approach of using synteny comparisons could be a way to help test many other phylogenetic models (and/or further test this synteny trick), and maybe it can help resolve some difficult problems like where the hell did bats come from?
I think that the authors put placozoans in with the rest of the non-ctenophore using their syntemy criterion. Clearly there’s a lot of finer-scale molecular work to be done.
It would be a real blow if we found that Calvin was right and bats are actually bugs.
Ummm, has there been significant doubt over them coming out from “indeterminate small insectivores”, even if those indeterminate ones don’t map well onto our extant mammal groups by dint of having been extinct for several tens of millions of years?
I”d have to check, but doesn’t the fossil record of the bats go back into the Eocene – some 50 Myr ago?
Mark,
I asked an animal systematist about those damn placozoa, which I’d unfortunately neglected above. Here’s what he/she said:
So that might make another case of secondary losses!
I have a theory, which is mine, and it is that the placozoans came about from a piece of skin that was torn away from a more advanced animal which simply refused to die. And so it has been cloning itself ever since and has even managed to form some new species. I am not entirely serious, btw.
All the same, copyright the idea!
I had to check, but there are reports (Wiki) that Placozoa can indulge in both sexual and asexual reproduction. Possibly (the article is unclear) two different types of asexual reproduction.
Thanks for this! Excellent, informative, and complementary to Zimmer’s piece in the NYT. I was hoping you’d comment.
Letting you know I love the scientific bits of your website!!! As they say in my favorite crowd-sourced game–For Science!
Forgot to say the name of the game–Eyewire.
Non- scientist here. Just wanted to say how interesting this was. I’ll head over to the NYT to read that article you mentioned.
Very interesting work! In the “old days,” ctenophores were thought to be closest to cnidarians (because they are both jellyfish-like), but this work sets them pretty far apart despite their superficial similarities. I look forward to reading more about how the ctenophore nervous system differs from that of the bilaterians. Also it would be interesting to know if sponges universally lack nerve cells or, perhaps, have degenerate remnants of what were once nerve cells. It might be worth another look at sponges with this question in mind.
Many of us are interested in the origins of things: life forms, languages, etc etc
This post is a wonderful addition to our knowledge !
Thanks Jerry, great post!
“…Each of these comes with another puzzle. The first one is this: why did sponges have complex and highly evolved set of features to sense the environment and move about, but then lost it?” – J. Coyne
Ernst Mayr writes that “among the higher organisms there are lineages such as parasites, cave animals, subterranean animals, and other specialists that show many retrogressive and simplifying trends.” So it is a mistake to suppose (as I myself once did) that evolution always results in an increase of complexity.
“Is evolution progressive?
Are phylogenetically later organisms ‘higher’ than their ancestors? Yes, they are higher on the phylogenetic tree. But is it true that they are ‘better’ than their ancestors? Those who make this claim list a number of characteristics of ‘higher’ organisms, purporting to demonstrate advance, such as division of labor among their organs, differentiation, greater complexity, better utilization of the resources of the environment, and in general better adaptation. But are these so-called measures of ‘progress’ truly valid evidence for an advance?
It seems that those who deny any signs of evolutionary progress in the advance from bacteria to higher organism give a teleological or deterministic aspect to the idea of progress. Indeed, evolution seems highly progressive when we look at the lineage from bacteria to cellular protists, higher plants and animals, primates, and man. However, the earliest of these organisms, the bacteria, are just about the most successful of all organisms, with a total biomass that may well exceed that of all other organisms combined. Furthermore, among the higher organisms there are lineages such as parasites, cave animals, subterranean animals, and other specialists that show many retrogressive and simplifying trends. They may be higher on the phylogenetic tree, but they lack the characteristics always listed as evidence for evolutionary progress. What cannot be denied, however, is that in every generation of the evolutionary process, a surviving individual is on the average better adapted than the average of the nonsurvivors. To that extent, evolution is clearly progressive. Also, throughout evolutionary history innovations were introduced that made functional processes more efficient.”
(Mayr, Ernst. What Evolution Is. New York: Basic Books, 2001. p. 278)
If one thinks of a multidimensional space representing morphology, physiology, and ways of life, this space has been expanding over time (the past 3.2 billion years). Early on, in the Archaean, this biological space was occupied only by simple life forms—since evolution started simple—whereas over time, more and more complex life forms have appeared. Some of these life forms have evolved extraordinary adaptations, such as giant brains, wings, incredible eyes, and all the rest. One can call this path toward complexity “progress” but one can also regard the pattern as one of expansion into previously unoccupied areas of the multidimensional space—expansion outward from simple beginnings.
I tend to avoid the word “progress” since it may be taken to imply betterment. Has there been betterment? In certain ways, yes. In human evolution, brains have gotten smarter, and in plant evolution, wood has give trees amazing strength. But it’s debatable whether there has been *overall* progress in evolution. My take is that much of what we think of as progress is better understood as the evolution of complexity from simple beginnings. As humans, we tend to put ourselves at the top of the evolutionary heap and interpret evolutionary history as leading toward us—as progress. An ant might interpret the same history differently.
Love, love, love the science!
Thank you for this post! I have been interested in this controversy for a long time, and have periodically checked the ever-shifting trees of life. I’ll be glad if a lasting consensus has finally been reached, though personally, I’d prefer the sponges to be the sister group. At our Department, we have circumvented the tricky topic by omitting ctenophorans altogether (we haven’t enough time for them anyway, and our students are unhappy whenever we try to entertain them with organisms without medical importance).
Given that ctenophorans have a sort of bilateral symmetry, I ask myself, was this another trait that was either primitive and lost by some, or acquired multiple times?
[Mission Impossible theme] “Your mission, should you choose to accept it,” is to find cases of ctenophore-caused diseases in humans. Given that I can remember “sea goosberries” stinging my lips through the skin, then their nematocysts (I think they use that name, by analogy with Cnidarians ; but that’s a bit “hairy” now.), they’ve got some good anti-mammalian neurotoxins cooking up somewhere.
And if ever I saw an organism designed to star in a repulsive-looking skin infection, it’s Trichoplax and it’s placozoan kith and kin.
“Your mission, should you choose to accept it, may be a short one. This tape will self destruct in 5 seconds.”
Not having actually watched any of the M.I. films, how do they explain to the youth of today what a tape recorder is?
It seems to have been overlooked that there are some reasonable arguments to support the idea that the origin of the higher animals (Metazoa) might lie among the fungi, or fungal-like organisms.
I refer to a paper published many years ago entitled:
“Biochemical Keys to the Emergence Of Complex Life.”
by Kenneth M. Towe
An excerpt…
“Implausible as it may sound, it is instructive to examine the potential of the fungi (fungus-like protists) in this regard. Considered as a broad group, fungi have the ability to synthesize hydroxyproline, chitin, cellulose, and even ferritin. They have already replaced phototrophy with heterotrophic absorption. And fungi were surely not derived from protozoa, simply because to do so would require that the protozoan ancestor, already having lost the ability to synthesize Iysine, rederived it later – a peculiar step indeed. Whittaker (1977) has already noted that “metazoans with digestive tracts have probably evolved from absorptive flagellates and, in this evolution, internalized the process of food absorption and added it to the process of ingestion.” Could some lower fungal type have given rise to a protometazoan by some neotenous or paedomorphic transformation during a flagellate stage? And if it were one of the fungi that had utilized the aminoadipic acid pathway for Iysine synthesis, the loss of this capability might have conserved alpha- ketoglutarate for proline hydroxylation. There would have been nothing to lose but the ability to synthesize Iysine and everything to gain in evolutionary potential.
ONE PAPER VERSUS ALL THE OTHER WORK THAT SHOWS THAT FUNGI AND ANIMALS SPLIT 1.5 billion years ago? This paper was in 1979 and was published not in a peer reviewed journal but in a proceedings conference:
Life in the Universe. Proceedings of the Conference on Life in the Universe, held at NASA Ames Research Center, June 19-20, 1979. Editor, John Billingham; Publisher, MIT Press, Cambridge, Massachusetts, 1981. ISBN # 0-262-52062-1. LC # QB54 .L483, P.297, 1981
Seriously, you want to put this up against all the data that shows otherwise. We have some standards here, and you ain’t meeting them!
Is that a form of an argumentum ad populem?
Don’t things often start from a single simple item? Shouldn’t we observe every tiny bit of evidence carefully? Life writ large, is quite unusual, if not to say peculiar and mysterious. The very existence of an universe is a monumental question, if it were not for it’s quite patent reality! Perhaps we shouldn’t cling too tightly to what we seem to know, so that we may learn a bit more along the way? What was once true, has evolved as well, has it not? In any case, every contention must compete to live on and evolve, so who knows? It may go extinct or become a thriving extant concept!
This is gobbledybook which simply says scientific truth is provisional. But that doesn’t mean our knowledge doesn’t advance. Bye!
This post is one of the (many) reasons why this site is such a treasure. Even a long-lapsed chemist like me can understand the issue and the arguments. The informed comments above are the cherry on the icing. Thank you all!
Just to let people know, the reason for the paucity of science posts has been the immense amount of labor required to produce them. This one, for example, involved reading the paper twice, and then spending three hours writing the post. That’s about six hours total. I don’t have the time to spend doing that a lot, and it’s a lot harder than writing non-science posts.
That said, I”m heartened by the number of comments here, and that was another reason for the dearth of science posts: nobody seemed to comment, which I took to mean that people didn’t read them.
Your efforts are much appreciated. This post was excellent, extremely informative, lucid, and as always, well written. Thank you!
I’m sure that there are a lot of readers who, like me, find your scientific posts don’t leave a lot to comment upon – the subject is dealt with thoroughly and deftly. They’re good summaries of whatever topic you’re writing on.
Please keep them up – I always read them. They frequently cover aspects of biology that are outside of my field, and I find them valuable.
Keep ‘em coming whenever you can. I can imagine the time and effort required to read all the relevant literature, check and recheck your facts, and write with clarity. Each science piece is a gem.
I always read them but just don’t comment (not a biologist so don’t think I have much to add). This was terrific though. What an ingenious method. And, like so many great discoveries, seemingly so simple in hindsight!
Thank you Professor for this wonderful post. I learned a lot from it and I admire the way you write so clear and concise and easy to understand for a layman like me. I am sure it takes hours to finish a comprehensive post like this. Thank you. That’s what I love about this blog… I learn something new every day! Keep up the good work.
A great discussion of a fascinating topic.
Thanks for this fantastic post. I teach the ctenophore-sponge controversy to undergraduates. Maybe I can now stop calling it controversial?
I’m reserving judgement about where placozoans go. In Figure 3 there is very little synteny information for Trichoplax because they have such tiny genomes: less than 100 million base pairs. Implies that placozoan genomes got secondarily small along with the secondary loss of important morphological traits (gut, nerves, muscles).
Really interesting summary. My question is, has anyone any idea of the time period these changes took place over? Are we talking a million years or ten million?
Are we talking, ‘during the Cambrian’ or…?
Thank you for this post! Just adding my voice to the choir.
I come mostly for the free speech stuff, but posts like this top everything.