Wednesday, 16 February 2022

The Life of a Charnia masoni (and friends) - A Speculative Essay (Part 1)

(Disclaimer: This is called a speculative essay for a reason. While an attempt was made at accuracy, this was ultimately written for a speculative evolution project, brand new but already in need of an overhaul, about what life would be like on Earth if Ediacaran lifeforms had not gone extinct. Because of that and because some aspects of these lifeforms’ biology is still genuinely mysterious even to experts, a lot of things had to be guessed or speculated on by myself and I am certainly not an authority on these matters. For transparency, things based on actual scientific work will be marked with citations, while highly speculative statements by me will be marked with an [S]. Any divulgence into the esoteric or philosophic is also primarily a stylistic choice. This post and its follow-ups, in an altered form, will likely serve as the project’s introductory text, but since this is a group project I will mostly not be responsible for any future creations based off the stuff written here. So don’t come to me to complain about things like Dickinsoniasaurus rex or whatever not being hard-spec enough for you, that’s what Rhynia is already for.)


Fig. 1: Charnia masoni, one of the first members of the Ediacaran biota ever scientifically recognized.

Are those who are out to deny the truth not aware that heaven and earth were once a single entity, which We then split apart? And that We made every living thing out of water? Will they then not begin to believe?

If He wills it, He can make you, oh humanity, disappear and in your place bring forth other beings; and ever is God able to do that.

  • The Holy Quran, verses 21:30 and 4:133 (translation based off Muhammad Asad’s work)

The year is around 575’000’000 before the present. The exact date or time of day is hard to determine using our modern timekeeping systems. The moon is still much closer to the Earth than it is today and has not slowed our planet’s rotation down as much, so a day is closer to twenty-two hours than twenty-four. Let us just say it is morning. And while this morning was long ago for us, for the Earth it was just one of many that had come before, for by this point our planet was already 3’985’000’000 or more years old. The first times the morning sun shone over the Earth was in the Hadean, when the air was but a wild mix of carbon dioxide and methane and the seas were a boiling mess at the mercy of the moon’s ever stronger tides. And yet in this chaos there already formed signs of life. In the alkaline thermal vents on the ocean bottom formed through serpentinization in an oxygenless environment complex molecules, eventually capable of self-replicating and mutating. Once those two properties arose, natural selection did the rest and out of these raw components the first cells evolved. The Hadean was followed by the Archaean, in which these first lifeforms divided into the domains Bacteria and Archaea. The former eventually evolved photosynthesis, transforming the oceans and the atmosphere with oxygen, while at the same time evolving forms that could use the new molecule for their metabolism. Some of the archaeans made use of this, by enslaving the oxygen-respirators, thus turning them into mitochondria and themselves evolving into the first eukaryotes. Geochemical signs of steranes, a molecule only produced by eukaryotes, shows that this already happened by 2.7 billion years ago during the Late Archaean (Knoll 2003). 

Fig. 2: Fossils from the Francevillian biota, around 2.1 billion years old (taken from El Albani et al. 2014). Time was not kind to them.

Soon thereafter the Proterozoic Eon began and the eukaryotes greatly diversified. And they did not stay unicellular until suddenly animals appeared in the Cambrian, as many people like to think. Already 2.4 billion years ago, in rocks from South Africa, can be found fossils of multicellular mycelia from fungi (Bengtson et al. 2017). This is a rather underappreciated find, as it shows that eukaryotes were ready to experiment with multicellularity rather soon after they evolved and that fungi are possibly a lot older than both plants and animals. These first beginnings, which if unadulterated might have led to Earth becoming a truly bizarre mushroom world, unfortunately faced great challenges, as at the same time these mycelia grew, a grand catastrophe was already on its way. The process of photosynthesis had now advanced so much that much of the former methane in the atmosphere had fused into the much less potent greenhouse gas carbon dioxide. As the sun’s luminosity back then was still much fainter than it is today, the weakening of the greenhouse effect led to the Huronian glaciation, the first Snowball Earth phase in which nearly the whole planet is thought to have been covered in ice shields. It lasted about 300 million years. The process may have significantly halted photosynthesis on a global scale, allowing for the gradual build-up of new gases, leading again to the end of this ice age. Something weird happened again immediately after the glaciers receded. In rocks from Gabon can be found mysterious fossils from 2.1 billion years ago. Both physiological and geochemical evidence indicates that these were not only eukaryotes, but also, again, multicellular lifeforms (El Albani et al. 2014), but unlike their predecessors from before the ice age they were now large enough to be seen by a human with the naked eye. They came either in strange, string-like shapes or as flat “nipples” with an egg-yolk-like core and a surrounding frill. What exactly they were is hard to say. Broadly, they resemble modern dictyostelids, a form of slime mold that can switch between both unicellular and multicellular phases, but the Gabon fossils are not only larger than slime molds, being able to grow up to 17 cm wide, but also more complex and seem to have lived in a marine environment. They seem to have been capable of at least some coordinated growth, so they could have potentially evolved higher grades of organisation if given the opportunity, but their time was cut short as well. The Gabonionta arose during an unusual oxygenation spike and went completely extinct after oxygen levels fell again (El Albani 2014). Who knows what life today might be like if things had been different?

Fig. 3: The typical body-types of sponges. Red are filtering surfaces/chambers, while grey is the so-called mesohyl, a jelly-like substance possibly related to the hydroskeleton of more derived animals.

Low oxygen conditions were from then on the norm in the Proterozoic, but certain lineages still experimented with multicellularity, some more successful than others. In 1.6 billion year old rocks from India we find a 3 cm large organism named Tawuia or Chuaria that might have been another form of slime mold or a multicellular acritarch. Then 1.2 billion years ago we find the oldest algae (Knoll 2003), the ancestors of what would one day become our plants. Among these oldest algal fossils was the red algae Bangiomorpha pubescens, which is the oldest multicellular organism from which sexual reproduction is known.  About 400 million years after Bangiomorpha another important development happened in a different branch of the eukaryotes. Choanoflagellates are today a type of protist that filters the water for food using a sort of ciliated-umbrella and a flagellum. Some of these cells can band together to form tree-shaped colonies, perhaps to give each other a sturdier holdfast and to increase filtering area. During the Tonian period, close relatives of these organisms banded together and formed permanent colonies, which then eventually reached enough specialization to act as a single organism. In Namibian rocks from 760 million years ago we thus find Otavia antiqua, the oldest known, sponge-like organism, if not proper sponge. There are possibly even older sponge fossils from 890 million years ago (Turner 2021). These were the first members of the new clade Metazoa, better known as animals. Their age, while being perfectly in line with molecular finds, is rather amazing as they predate the Late Proterozoic Oxygenation. This shows that animal-like life can arise even in low-oxygen environments. Even if it is not all that complex. Sponges have simple shapes and simple lives. After their mobile larva, the planula, settles down, they develop into vase-shaped structures with perforated walls. These body walls are often supported by tiny spicules of spongin or other minerals, forming a skeleton. Each pore or chamber is lined with flagellate cells, resembling very much those of the choanoflagellates, which by whipping the water create a current that the sponges use to filter water. Some sponges might have a slightly more complex anatomy than simple vase-shapes by building internal filtering tunnels and chambers inside their walls. Sponges curiously also already possess various precursors to things that would later evolve into nerve cells and muscle-based movement in later animals (Dunn et al. 2021), but, despite having existed for over half a billion years, they have never evolved more complex body forms beyond those which we can already find in these Proterozoic rocks. The reason is that, for all their potential, sponges inherently lack organisation. While they have differentiated cells, all sponges lack true tissues (except for the Homoscleromorpha, which seem to have convergently evolved basement membranes similar to cnidarians). Each cell of the body, when needed, can evolve into every other cell-type available and if you put a sponge in a blender, every little surviving piece will develop into a new sponge from scratch. While this sounds great on paper, it also means that no group of cells in the sponge-body can specialize itself for a single task, but has to always stay somewhat amorphous and simple for the case it has to change later. Without true tissues, sponges cannot evolve dedicated organs, such as skin, muscles, a brain or a digestive tract, and therefore are unable to achieve a more complex degree of organisation. Greater changes in their world had to happen for the next breakthrough.

Fig. 4: Trichoplax adhaerens, possibly one of the simplest, free-moving animals one could ever find. Note how there appears to be no body symmetry.

Likely due to the growing success of large algae, the aforementioned oxygenation event took place. Either due to that or an increase in erosion thanks to the breakup of the supercontinent Rodinia (probably both), greenhouse-gas-levels in Earth’s atmosphere crashed again. During the aptly named Cryogenian, this began another Snowball Earth phase between 720 and 635 million years ago, consisting of the Sturtian ice age shortly followed by the Marinoan one. Right underneath the ice masses may have evolved the Placozoa, possibly through neoteny out of the planula-larvae of sponges if those are not a monophyletic group [S]. Placozoans, such as the modern Trichoplax, are tiny animals, just 1 mm across, which resemble multicellular amoeba. They crawl along surfaces using cilia and digest tiny food particles by engulfing them with their underside like a carpet. This behaviour may have very well evolved first through the grazing of algae growing on the underside of thin Cryogenian icesheets. While in many ways placozoans seem more primitive than sponges, they have a few things going for them. For one, they stay mobile throughout their lives, but perhaps more important is the fact that they have actual tissues. Placozoans are fully covered by an epithelium (skin), which surrounds a syncytium (connective tissue). If current phylogenetic models are correct, the placozoan epithelium and connective tissue might be homologous to the germ layers of later animals: The epithelium may be related to both the ectoderm (out of which in our embryos the skin and nervous system develop) and the endoderm (which in us develops into the digestive tract and associated organs). The syncytium, likely evolving out of the mesohyl of sponges, may also be related to the mesenchyme of diploblasts (cnidarians and comb jellies) and later the mesoderm of bilaterian animals like us (which develops into our muscles and bones, among other things). Regardless, placozoans could not and still cannot play out their potential. Like their forefathers, they lack any clear axes of symmetry. Despite living most of their lives pressed flat on the seafloor, their body does not actually have a top- or bottom-side, the epithelium is structurally the same in all directions. If you flip a placozoan on its non-existent back, it will carry on and crawl away like nothing happened. Neither do they have any internal cavities, out of which internal organs could evolve. Unlike both later animals and even the earlier sponges, placozoans do not go through a gastrulation phase in their development, where the outer epithelium folds into the body to become the endoderm. This might actually be a secondary loss of a trait that their ancestor did have, as nowadays placozoans mostly reproduce asexually by splitting apart like large amoebas. Sexual reproduction has become diminished to two individuals just swapping genes on occasion, like more basal protists do. Without internal organisation, placozoans are actually at the size limit at which multicellular cell balls can exist without suffocating (Butterfield 2025).

Fig. 5: The simple life and diet of a placozoan. They have no such thing as a gut and instead have to eat with their body surfaces like a multicellular amoeba.

After the Marinoan glaciation ended 635 million years ago, a new period began, now known as the Ediacaran. For the first 55 million years, most animal fossils remained microscopic (though not unimportant as we will later see).  Around 580 million years ago another short ice age, the Gaskiers glaciation followed. This age thankfully lasted only for a few hundred thousand years, but when it ended, things got weird.

Growth and Structure of a Charnia

So we are finally back to the starting point 575 million years ago, with our actual protagonist: a young specimen of the organism Charnia masoni. Charnia is named after the Charnwood Forest in Leicestershire, England, where its fossils were first discovered in 1956 by a little girl named Tina Negus. However, Charnia was a widespread genus and can also be found in Russia, Australia and North America. The individual we are observing today lived in what would one day become Newfoundland in Canada. Charnia’s identity had long been a mystery and the group it belongs to has likewise gone through many names, such as Petalonamae, Frondomorpha, Rangeomorpha, Vendobionta or Vendozoa (the Vend- prefix comes from the Vendian, an older name for the Ediacaran). I will settle here for the first one, Petalonamae (as per Cuthill & Han 2018). Ideas on the identities of these lifeforms have ranged from algae and giant lichen to stingerless jellyfish and, in some cases, even deuterostomes (the group we belong to). A growing consensus can now thankfully be discerned. Geochemical evidence, in the form of fossilized cholesterol, shows that these creatures were indeed animals (Bobrovskiy et al. 2018), but their morphology does not relate them to anything known today. Unlike a sponge, Charnia, clearly has tissues and unlike a placozoan, Charnia actually has style structure: It grows along two axes of symmetry (topward and outward) and its body is compartmentalized into distinctive sections. But Charnia still cannot be confidently placed inside the crown group of the Eumetazoa. Eumetazoa are the animals which possess, among other things, a mouth connected to an internal system of guts. Their crown group (meaning all living members) consists of the ctenophores (comb jellies), cnidarians (jellyfish, sea anemones, corals and such) and bilaterians (every other animal you can think of, including yourself). Ctenophores and cnidarians, due to being generally jellyfish-like, were once grouped together in the larger clade Coelenterata, but many of their similarities are actually convergent. Ctenophores seem to have diverged first from the Eumetazoan family tree, while cnidarians are more closely related to us. Anyway, Charnia and its fellow petalonams lacked any sign of a mouth or similar body opening. The conclusion most cladistic analyses therefore arrive at today is that these were stem-eumetazoans (Cuthill & Han 2018, Dunn et al. 2021). Close to us but not quite there yet.

Fig. 6: A broad-scaled family tree of animals (taken from Dunn et al. 2021). As you can see, Charnia and its relatives are sandwiched in a rather crucial part of the cladogram, between the more amorphous animals and the more structured ones.

But of course, viewing Charnia and its kin as just our precursors or as a missing link between the more primitive metazoans and the eumetazoans would do them a disservice. They were unique and a whole group, dare I say phylum, onto their own, with a bodyplan and mode of growth that had not been seen before or after, having been totally lost to time. Our little Charnia, growing there on its piece of Canadian seafloor, is made up of two parts, a holdfast and a frond. Making up the frond are the so-called first-order branches, which are the individual “arms” you see on the fossil. Each first-order branch is then itself made up of ring-like segments called second-to-fourth-order branches (Dunn et al. 2021). Each of these follow-up rings then seems to also be made up of rectangular-looking units, which I will call chambers.

Fig. 7: The labelling of Charnia’s body-parts, as per Dunn et al. 2021. Top left shows an older and less helpful approach which tried to give each branch its own number. Now each branch is called a first-order branch and each first-order branch is made up of a second-order (and following) branches.

At the beginning of its life (ignoring reproduction and embryonic stages for a moment) our Charnia is just a little holdfast, without the frond. To form the frond, the individual arms do not grow from a central stalk (Dunn et al. 2021), like with a fern-leaf, but instead something rather remarkable happens. Out of the sides of the holdfast first grow two lateral branches, which maybe exist to give the future frond better support [S]. Then out of the center of the holdfast grows a single first-order branch towards one side of its body. Out of one of that first-order branch’s second-order branches then grows the next first-order branch into the opposing direction. Out of that first-order branch’s second-order branch then grows another first-order branch into the previous direction. Each new first-order branch has slightly less second-to-fourth-order branches, meaning they get shorter (Dunn et al. 2021). This growth-process repeats itself until the classic, feather-like shape is reached and the resulting midline of the body ends up being zig-zagged. The left side and the right side of the body are not exact mirror images, but slightly shifted in relation to each other. This is called glide symmetry and it is a type of symmetry that really does not exist anymore in the modern animal kingdom. A few extinct worms have elements of this in their armor, but there is no animal anymore in which glide symmetry fundamentally controls the body. The exception might be sea pens, a type of cnidarian to whom Charnia has often been compared. Sea pens, however, are actually colonial organisms, like corals and Portuguese man o’ wars, with each arm of the frond technically being its own animal, called a zooid. The mode of growth of Charnia is incompatible with it being a colonial organism made up of multiple semi-independent zooids (Dunn et al. 2021), it really was a single, solitary animal that just grew this way.

Fig. 8: The growth and two life stages of a Charnia (taken from Dunn et al. 2021). The multi-colored parts on the right show how each branch is connected to the previous one at the base. What a Charnia would look like before it grows the frond remains mysterious and we will get back to that.

Knowing the fundamentals, it is interesting to observe how Charnia grew across its life. It grew apically, meaning the branches at the base of the frond were the oldest, while those at the tip were the youngest (Dunn et al. 2021). Once a certain size was reached, Charnia stopped growing new first-order branches and instead began “inflating” the existing branches either by growing them bigger or adding new higher-order branches (Dunn et al. 2021). Some Charnia-specimens could grow over 65 cm tall this way, making them among the largest organisms that had existed on Earth up until that time. The splitting-up of its life into two different growth-phases, differentiation with subsequent inflation, is a sign of some already quite complex control over its anatomy. At least complex compared with everything that came before.

Fig. 9: A sketch by me showing in blue what the interior cavity of Charnia may have been like. The dotted lines are speculative extensions of the channel into the branches and the holdfast.

The most fascinating discovery about Charnia and its relatives is that their internal anatomy was also more complex than previously thought. Many petalonams have an outward appearance resembling quilted and inflated air mattresses. It had long been thought that their interior was entirely filled with jelly or cytoplasma and also tightly sealed from the outside world, with the skin being the main organ of interaction with the surroundings, including digestion. It was also thought that the individual sections of the body, such as the branches of the frond, were virtually separate from each other, not interacting with the rest of the body. Newer examinations of Charnia and close relatives like Stromatoveris show this to not have been the case. Shortly after death, these animals’ bodies were filled in with sand and dirt, allowing for their three-dimensional preservation (Cuthill & Han 2018). There were no obvious wounds from which these sediments could have flowed into the body and the sediment-layers were continuous. This shows us multiple things: 1) At least some natural opening(s) must have existed that allowed these sediments to fill in Charnia’s body 2) Significant parts of Charnia were hollow and 3) Perhaps most importantly, the different sections of its body were internally connected. In fact, Charnia’s body seems to have had at least one interior channel that connected the bases of all first-order branches, which makes sense, as each branch descends from the one that came before (Dunn et al. 2021). It would be easy to call this channel a form of gut, but again, Charnia still does not have a mouth or anus to which this could connect. It is therefore perhaps more comparable to the interior filtering-channels seen in leuconoid sponges (see fig. 3, right). We will get back to this later.

What about the finer detail, the nuts, bolts and material of Charnia? Charnia was soft-bodied through and through, without hard parts, such as the spicule skeleton that sponges have. But nonetheless, its body was capable of maintaining its form even while being buried or filled with dirt. This strongly points towards Charnia and its petalonam-friends having had a so-called hydroskeleton (Butterfield 2020). Instead of being filled with jelly-like tissue, as had previously been thought, Charnia’s body was held erect by a skeleton of rings and layers not made of bone, but by slightly pressurized seawater. Apart from support, a hydroskeleton can also be used for respiration and, through hydraulics, even movement. Many modern animals still have such a hydraulic skeleton, for example annelid worms and echinoderms. If you are a human with a penis, your organ (or in some of the men I’ve met, organelle), is also held erect by a hydroskeleton. Foremost among the animals with a hydroskeleton are however the ctenophores and cnidarians. In them, this organ is called a mesoglea and it is possible that Charnia’s hydroskeleton was homologous with theirs. Assuming this, we can further deduce that Charnia’s mesoglea was outwardly covered by an epidermis (Butterfield 2020). This outer skin was then likely covered in a carpet of microscopic cilias, as is still the case in placozoans and especially ctenophores. The internal channels and chambers we discussed before were then also likely covered in an endodermis, the same type of tissue which forms our guts.

Fig. 10: The probable internal anatomy of Charnia’s feeding chambers, to which we will get soon (taken from Butterfield 2020), as well as how they likely filled with sediment and fossilized over time. Black shows the hydroskeleton, surrounded by an ecto- and endoderm with cilia. DOC and POC stand for dissolved and particulate organic carbon.

Did Charnia have things beyond a skeleton and skin? After all, in addition to these features, cnidarians and ctenophores also have muscles and nerves. The answer is: most likely not. Not only is there no sign of this in the fossils, but this can also be directly gleaned from how those fossils were preserved. We know from both living sessile cnidarians and their fossils that when they run the danger of being buried/have their guts filled with sediments, they actively contract and try to move away from the danger (Butterfield 2020). Sea anemones can in fact even detach from the ground and hop away from danger. We find no such behaviour in Charnia and close relatives, the fossils show that they let themselves be buried without any real resistance, which strongly implies that they did not yet have muscles with which to actively move the body or nerve cells with which to directly react to outside threats (Butterfield 2020 & Dunn et al. 2021). This of course does not mean that Charnia was completely numb to the world surrounding it. After all, the general awareness of animals, out of which eventually consciousness would evolve, did not suddenly begin with the appearance of a nervous system, let alone brains, but must itself have evolved out of earlier precursors (Godfrey-Smith 2017). Interaction between the organism’s interior with the exterior environment is a fundamental aspect of every known lifeform. Bacteria and plants already use chemical pathways to react to changes from the outside and change their current conditions accordingly, even if they are a lot slower at this than we are. They have some form of awareness, even if it is just in a broad sense. The placozoans preceding the petalonams furthermore had and still have fiber cells inside their body that react to neuropeptides (Dunn et al. 2021), which seems to be the direct precursor to a form of nerve cells. Sponges have similar precursors and a few species are able to move their body by contracting the pinacoderm cell-layer (Dunn et al. 2021). Even though generally thought of as sessile, some sponges can even crawl across the seafloor at very slow speeds, using the cilias of their filtering cells. Early petalonams like Charnia most likely had access to such a repertoire of senses and actions and so were able to react and perhaps even move, just at a speed way slower than what eumetazoans are capable of. More importantly for later, petalonams would have had all the necessary potential to evolve proper nerve- and muscle-cells themselves if given the chance. We can actually say this with certainty because we eumetazoans started out with the same basic tool-set as Charnia and went on to evolve all these traits independently from each other: The ctenophore nervous system evolved entirely independently from our own, while cnidarians and bilaterians do not use the same muscle cells (Butterfield 2020 & Dunn et al. 2021).

Since Charnia would have had some form of awareness, one could maybe ask what would it have felt like to be one. This is a question that we can philosophize about but will never be able to answer. After all, some humans cannot even imagine what other humans must feel like. The best assumption I can give is that it must have been peaceful, like how you felt when you were just an embryo.

Ecology and Lifestyle

Charnia’s environment was a strange one. As burrowing animals were still very small and rare, most of the seafloor was not yet as well-stirred as it is today. This allowed microorganisms to carpet the ground in thick films undisturbed. The Ediacaran was a period dominated by dense bacterial mats and algal lawns, turning a former Snowball Earth into a Slimeball Earth. This seems to have been crucial for most lifeforms of the time. For Charnia it was the ground it grew on, allowing it to anchor its holdfast onto a sticky film instead of needing to bury it into the soil like plants have to do with their roots. Charnia shared its home with other strange creatures. At its home of Mistaken Point can also be found other petalonams, such as rangeomorphs, of which Charnia was likely itself a basal member. These were other frond-shaped creatures, though sometimes of a different configuration than Charnia. Fractofusus for example lacked a holdfast and instead was made of two opposing fronds that lied flat on the ground. Bradgatia is similarly also made up of multiple fronds, but these all attached to each other at the base, making the organism look like a cabbage. Among its neighbours, Charniodiscus resembles Charnia the most. However, its holdfast was unnaturally elongated and at its end formed a big, circular foot with which it stayed attached to the bacterial mats like a plunger. Another form of life found in this so-called Avalon Assemblage (the oldest known type of petalonam ecosystem, named after the Avalon peninsula on which the Mistaken Point fossils were found) are medusoids, such as Aspidella. The exact identification of these organisms is still mysterious. As the name suggests, the medusoids were first thought to have been fossilized jellyfish, however closer analysis revealed that they were instead disk-shaped, gelatinous spheres growing on the seafloor. There is a distinct possibility that these were not animals at all, but microbial colonies or giant protists, similar to the modern xenophyophores (McMenamin 1998). At least some medusoid fossils likely were just trace fossils left behind by the holdfast of petalonams, such as the aforementioned Charniodiscus.

Fig. 11: What the neighbourhood of Charnia would have looked like (taken from Bottjer & Clapham 2006)

Now onto the most pressing question of how Charnia and friends made a living. At first, the very leaf-like shape of the body is of course very suggestive. Various animals do still exist today which live in symbiosis with algae and other microbes living in their bodies, such as corals and the very outlandish-looking snail Elysia chlorotica. Especially in the latter example one can see how an animal can assume plant-like shapes in order to profit from its symbiotes. Placozoans can also have microbial endosymbionts (though not algae) living inside them. Did Charnia therefore have algae or cyanobacteria living in its body, who in exchange for shelter gave it sugar? Could the internal channels of the branches have been there to house such symbiotes, making Charnia a sort of appartement complex for microbes? Unfortunately, the sedimentology of Mistaken Point indicates that it was actually a deep-sea environment. Charnia and friends were living in total darkness, well below the depth where photosynthesis would still be feasible. Of course, not all petalonams were living in the deep ocean and especially those living in shallow waters could have still employed this photosynthetic lifestyle. But Charnia was not among them. The next best explanation for it could then be osmotrophy, which is the passive absorption of nutrients suspended in water through osmosis. Certainly, the Ediacaran seas would have already been full of free nutrients in the form of waste products released from various bacterial mats, protists, giant algae and early animals. Osmotrophy is also a form of feeding employed today by many microbes, fungi and even some animals, such as sponges, corals and brachiopods. This has been seen as the preferred feeding mode for petalonams by many workers on the Ediacaran biota, most importantly Mark McMenamin (1998). I also endorsed this view in an earlier post. Unfortunately, newer research shows that most petalonams were too large for osmotrophy to still be feasible (Butterfield 2020). Furthermore, the animals who employ osmotrophy today only do it to supplement their regular diet. Charnia could therefore not have exclusively lived through osmotrophy alone.

Besides that, the old idea of osmotrophy relied on the now outdated idea that Charnia could only feed passively through its exterior skin. The discovery that petalonams had interior chambers that could interact with the outside opens up a whole lot of new questions and possibilities. First and foremost: Where were the body openings? As said, petalonams, especially rangeomorphs like Charnia, have no sign of a coelenteron (Dunn et al. 2021), the central mouth connected to the gut of cnidarians and ctenophores, and not even something comparable to the operculum of sponges (the vase-hole at the top). With these openings being macroscopic and the grade of quality that these fossils are often preserved at, this seems to have been a genuine absence. What we cannot exclude, however, is Charnia having, instead of a single central mouth, a bunch of small to microscopic ones across the body, perhaps something similar to the filtering pores of sponges. These are such fine details that it is likely that they were simply not preserved during fossilization (Dunn et al. 2021). Indeed, even in Cambrian Burgess Shale-type fossil sites, which have a way higher grade of preservation than the Ediacaran ones Charnia was deposited at, many sponge fossils do not have their individual pores preserved (Butterfield 2020). Is it then possible that each unit of each branch of the frond could have been a filtering chamber with a small opening? We might actually have direct evidence of that (fig. 12). At least two flattened but exceptionally well-preserved specimens of Charnia actually do show a series of little, lense-shaped openings running across the arm (Butterfield 2020).

Fig. 12: A flattened Charnia-fossil showing possible openings of filtering chambers (taken from Butterfield 2020).

Underneath these can also be found structures similar to mesenteries, which corals use to expand the surface of their guts. The most likely explanation then for how Charnia lived was that each branch of the frond was composed of a series of little filtering chambers (as in fig. 10). The ciliated skin of Charnia transported dissolved and particulate organic material from the water towards the openings of those chambers, where they were then likely swallowed through cilial pumping. Inside the chambers, more pumping by the mesenteries circulated the food until the nutrients were absorbed by the chamber wall. This is very similar to how sea-pens and other colonial cnidarians feed, but it needs to be stressed again that current science shows that Charnia was a single animal and also not a cnidarian (Dunn et al. 2021). In that aspect, the fact that it could achieve such a feeding method without resorting to colonial growth makes it in some ways actually more complex/impressive than sea pens. A sea pen is an army, a Charnia was one John Rambo. The fact that all first-order branches of Charnia were internally connected to each other through a sort of channel also becomes even more intriguing. Possibly, like a strange mix of cnidarian, comb jelly and sponge, all of the feeding-chambers in the arms were connected to each other and through ciliary pumping transported food into the central channel [S]. From there, food and other resources could then have been further distributed, again through ciliary pumping, in any direction to where the body needed them [S]. Sponges, especially those with skeletons, can have pores which actually pump water outside of the body instead of into it, in order to create better flow. Charnia could have similarly coordinated some chambers to pump water in or pump water out, to better direct the internal flow of water and nutrients [S]. This hypothetical channel-system would in some ways be a perfect intermediate between the internal chambering of leuconoid sponges and the coelenteron gut of cnidarians/ctenophores, but at the same time it would be something wholly unique. It has many hallmarks of a gut, but instead of one mouth and one anus, it has many smaller openings and endings throughout the body. One wonders what evolution could have achieved with such a thing.

Now that we (sort of) know what Charnia ate, was there anything that in turn ate it? The Ediacaran is generally characterized as a time in which predatory animals did not exist yet, hence why ecosystems like Mistaken Point are often nicknamed as a “Garden of Ediacara” in reference to the biblical Garden of Eden. Apart from bore-holes in the shells of Cloudina, a very Late Ediacaran animal, and a possible bite-mark in an Ernietta (McMenamin 1998), there is little evidence that there were animals that could have fed on Charnia. At least on a macroscopic level. Among microbes, predation has probably existed since the very start of Eukarya, if not earlier. Just look at amoeba and flatworms under the microscope. It has in fact been proposed once that petalonams grew to such unprecedented sizes in order to escape microbial predators (McMenamin 1994), like how sauropod dinosaurs tried to become too big to eat for some theropods. Charnia would have nonetheless likely still faced danger from such micropredators in form of parasites. What possibly speaks against a world entirely devoid of macropredators are fossils from the Mid-Ediacaran Doushantuo Formation of China, which shows that essentially modern-looking jellyfish already existed by this time. All modern jellyfish are carnivorous in one form or another and, while hard to tell by fossils, it is not unreasonable to assume that the Doushantuo ones already possessed the characteristic stinging cells, as all jellyfish possess them today and the deepest split in their family tree likely happened in this time. Their stinging cells are used both for hunting and defence, but neither the typical prey nor the typical hunters of jellyfish were around at the time (Godfrey-Smith 2017) and jellyfish do not prey on large, sessile animals like Charnia… so what would they have used their stinging cells for?! Some parts of the past unfortunately have to remain mysterious. All we can say is that the Garden of Ediacara probably was not the paradise we once imagined.

Reproduction?

Where did our Charnia come from and how would it have made more of itself? The genus existed for millions of years, so it certainly had some reproductive strategy that worked. Did it simply bud-off copies of itself, did it release eggs in the water, did it go through embryonal or larval stages? How was its sex life? A study done on its neighbour Fractofusus may shed some light on this.

Fig. 13: Fractofusus misrai, reconstructed here reproducing itself through stolon-derived clones.

As it appears, Fractofusus was actually sophisticated enough to have had two different modes of reproduction it could switch between. The first one seems to have been asexual cloning through a stolon (Mitchell et al. 2015). A stolon is a sort of stalk or root which buds off from an organism to then grow clones of it along its length. Plants and fungi use stolons to reproduce and a few modern animals do too. While some polychaete worms use them to trail eggs and larvae behind their bodies while swimming, the majority of stolon-users among the animals are colonial organisms that clone themselves, such as bryozoans and corals. This might make you scratch your head, as we previously established that Charnia was not a colony of multiple zooids. However, Fractofusus may have been. If you look very closely at its two (possibly three as per Gehling 2007) fronds, it appears that these are not like the frond of Charnia. Rather, each branch of each frond seems to have been made up of an individual Charnia! This is actually a pattern seen in multiple rangeomorphs, such as Avalofractus and Rangea. Some of these even have elaborate, plant-like central stalks and bases connecting all of these little charns to each other, which is not seen in Charnia (Dunn et al. 2021). What this means is that what makes up individual branches inside the fronds of these more derived rangeomorphs are equivalent to the whole body of Charnia (Dunn et al. 2021). While this could be a form of highly advanced fractal growth of a single individual (basically a rangeomorph iterating its whole self with each branching of the body), combined with the stolon-reproduction in Fractofusus it seems more likely that these derived rangeomorphs were actually colonial organisms produced through cloning [S], with the connecting pieces/stalks between their branches perhaps being analogous to the stalk in sea pens or the coenosarc of corals [S]. But again, this does not mean that rangeomorphs were just Ediacaran representatives of sea pens. In sea pens, each zooid is equivalent to a tiny anemone, whereas in Rangea and Fractofusus, each zooid was basically a tiny Charnia, so there are fundamental anatomical differences. This seems to instead be a genuine case of convergent evolution, which should not be too surprising, as colonial, clonal growth has evolved multiple times among animals (I already mentioned bryozoans). Note also that, since the oldest definitive sea pen fossils only come from as recently as the Jurassic, they are the actual (cheap) copy.

Fig. 14: The variation of rangeomorph bodyplans (taken from Dunn et al. 2021). The grey areas show areas of homology, while the orange ones are uncertain. As you can see, what in Charnia constitutes the whole body is just a single leaf in other rangeomorphs. I personal pet theory therefore is that some of these rangeomorphs were colonial organisms, with the orange areas perhaps being similar to the coenosarc of corals or similar connecting pieces in other colonial organisms.

Since Charnia was, however, not a clonal colony, we might rule out stolon-based reproduction for it. Here Fractofusus’ second mode of reproduction becomes enlightening: on occasion it seems to have released little propagules into the water, which then drifted off until settling on the seafloor to grow up (Mitchell et al. 2015). For solitary petalonams like Charnia this would have been the most feasible mode of reproduction. What exactly was the nature of those propagules, or rather, how were they produced? Because they lack signs of obvious gonads, general assumption about petalonams has been that they produced them just through budding (see McMenamin 1998 for example). By that logic, after a certain age the tip or the fringes of Charnia’s frond would have simply shed off and regrown repeatedly, with the dispensed part floating in the water until landing and growing into a new Charnia, sort of how plants or starfish can grow clones of themselves from broken-off pieces. Like the stolon-based approach of derived rangeomorphs, this idea, however, also assumes that petalonams were only capable of asexual reproduction. At least I find there to be a serious problem with that idea. Asexual reproduction is successful for lifeforms in the short-term, like when recolonizing destroyed habitats, but in the long-term only being able to clone yourself becomes a serious detriment, because not only will your lineage evolve very slowly, once a disease or parasite adapts to successfully infect and kill your body, it will be able to infect all of your clones simultaneously as well, wiping your whole kind off the map. Lineages of asexual eukaryotes are therefore usually very short-lived in nature (Lane 2016) (prokaryotes circumvent these problems by frequently exchanging plasmids with each other like trading cards). Looking at the fossil record then, petalonams existed for at least 40 million years, probably way longer, and during that time underwent some quite steady evolutionary radiation. This both seems incompatible with purely asexual modes of reproduction. Looking at sponges for reference again, it seems pretty plausible for petalonams to have made use of sexual reproduction, at least sometimes, without having gonads. Sponges do not have them either but are hermaphrodites that can produce both sperm and eggs directly from their skin by transforming individual choanocyte or archaeocyte cells into them. The sperm-cells are usually spit into the water, until they meet another sponge, which then sucks them up through its filtering system to combine it with its own eggs inside. The fertilized eggs are then either released into the water or kept inside the body until hatching. While petalonams likely did not have the exact same cell types as sponges, there really is not much that would negate such a style of reproduction and variations thereof in them and maybe that is how the propagules of Fractofusus were produced [S]. Like sponges and many other sessile animals, petalonams could then probably use sexual and asexual reproduction selectively simply depending on the situation [S].


Fig. 15: A sketch by me showing embryological branch-off points in the development of animals. Dark-shaded sections are equivalent to the syncytium of placozoans, the mesohyl of sponges and the mesoglea of cnidarians, but note that in reality these organs might not be 1:1 homologous. I went for the idea that petalonam-development, like their cladistics, is somewhere in-between sponges and “coelenterates”. Like sponges they might go through a face where the blastopore (what would become the mouth in animals like us) attaches to the seafloor and grows shut, but instead of becoming a wide, open filtering cavity, the proto-gut becomes a series of interconnected filtering-chambers.

Assuming then that our particular Charnia was not the product of bud-cloning, but came from a fertilized egg, what would its life stages have looked like before it grew the frond? All metazoans begin life as a so-called blastula, which is basically a hollowed-out cell-ball, and so would have Charnia. In eumetazoans like us, the next step is then gastrulation: One side of the blastula dents into the hollow interior to form the ball into a bowl (imagine it like kicking into an airless basketball). The skin that still stays on the outside of the bowl becomes the ectoderm, the one that is now on the inside becomes the endoderm. In most animals, this dent in the blastula develops into the mouth (except for deuterostomes like us where it becomes the anus). Would petalonams like Charnia have also gone through such a gastrula-stage? The fact that they do not have mouths would mean no and what possibly affirms this is that the older placozoans do not go through one as well (though, again, this might be a secondary loss). But sponges, as always, make the matter more complicated. While it is controversial if it can actually be called that, the embryos of calcareous sponges and homoscleromorphs surprisingly also go through a phase that looks a lot like a gastrula, complete with the beginnings of what looks to be a mouth-opening! But what would then become a mouth in us actually attaches the sponge-embryo to the seafloor and grows shut again, becoming a holdfast while the rest of the body develops into its typical vase-shape with the osculum on top. What if the holdfast of Charnia was homologous with the holdfast of sponges and the protostome (the ur-mouth) of eumetazoans [S]? The embryo would have gastrulated and produced a (proto-)protostome, which then attached the organism onto the bacterial mat like a suction cup. Like in sponges, this opening then closes, but the body above would follow an interior design more similar to that of cnidarians/ctenophores with its mesoglea, epidermis and endodermis. The proto-gut, now cut-off from the vanished proto-mouth, then branches into the developing frond and builds up the individual filtering-chambers [S]. Such a development would be a good reconciliation for how petalonams had an internal anatomy like later animals without yet having a mouth.

The things that came

So, there we have everything, from the conception all the way to the adolescence of Charnia. A part of every life however is death and for our Charnia it could have surprisingly come in many ways. Obviously, we have fossils of individuals who suffocated in sand-slides and I already mentioned that there must have been diseases and parasites that befell these lifeforms from time to time. But our particular Charnia could have gone out in a more bombastic way. Most of the fossils at Mistaken Point were buried under ash after a nearby volcano erupted and spilled a pyroclastic flow into the ocean, turning the site into a Proterozoic Pompey. Not the nicest way to go, but certainly a memorable one.

Fig. 16: Tribrachidium heraldicum, a tri-radially symmetrical animal perhaps related to the petalonams.

But just because our Charnia is gone does not mean that we leave this chapter of life behind. The petalonams continued to evolve long after it. Around 560 million years ago, the Avalon faunas are followed by the Ediacara/White Sea Assemblages, named after the Ediacara Hills digsite in Australia and the White Sea region of Russia. Though note that the newer assemblage did not displace the older one, but rather they continued to exist besides each other. This is because the Avalon Assemblage represents deep-sea environments, whereas the Ediacara Assemblage represents shallow marine environments and coastal lagoons. What happened 560 million years ago is that some petalonams left the lightless depths and wandered into the more lively and energetic shallows. While forms like Charnia continued to exist, derived rangeomorphs, especially the possibly colonial ones, greatly diversified. Among solitary forms also appeared new organisms that experimented with new frond- and stalk-constructions. Swartpuntia’s frond for example now had three or more fans constructed around a central stalk. Other forms apart from the rangeomorphs began to appear as well:

Trilobozoa

Most iconic among the new forms are likely the trilobozoans, with their leader Tribrachidium heraldicum probably being the most iconic fossil from the Ediacaran. Tribrachidium has long been puzzling, as its body is triradially symmetrical, something which is not seen in modern animals anymore. It is made of three arms with raised ridges, which curl around each other to form a disc. At the base of each arm were little pits. This makes it resemble the triskeles of some ancient heraldic flags, hence the species name. A new study done on computer models of Tribrachidium in simulated water currents has finally revealed why this animal was constructed in such a way and how it likely fed: The curved arms caught the water flow (and therefore the food particles suspended in it) and redirected it towards the pits at the center of the body (Rahman et al. 2015). In the process, the flow was also slowed down until it then came to a stop right above the pits. Through simple gravity, the food particles would have then simply sunk down into the pits, where they were then absorbed and digested (Rahman et al. 2015). Possibly, the arms were lined with actively whisking cilia to further help direct the flow [S]. This again rules out osmotrophy in an Ediacaran creature, instead Tribrachidium was a suspension feeder like many modern animals. The tri-radial design finally makes sense in this light, as it allowed Tribrachidium to capture water currents from nearly all directions. This does make one wonder why a design like this has not evolved again ever since. Possibly, Tribrachidium’s hydrodynamics relied on the rough surface of the microbial mats in lived on, as this would have created more turbulent flow-dynamics immediately on the surface of the sea-floor (Rahman et al. 2015). Whatever the case may be, this feeding style seems to have been lucrative for a time, as many trilobozoans evolved that experimented with slightly different arm-configurations, perhaps to specialize on specific current speeds and particle sizes [S]. Close relatives included Anfesta, whose ridges did not spiral but grew straight from the center.


Fig. 17: The hydrodynamics of Tribrachidium. It appears to have actually fed better in fast currents than in slow ones (Rahman et al. 2015).

Where exactly on the family tree one might place trilobozoans is hard to say and they have traditionally been considered their own phylum of stem-eumetazoans or stem-cnidarians. They can be three-dimensionally preserved, but no trace fossils or other signs of movement exist of Tribrachidium and friends, which likely means that, like Charnia, they had a hydroskeleton but no muscles yet. But glide-symmetry, arguably the hallmark of the petalonams/vendozoans, is not readily apparent in them, so they might not be related to them as well. However, the pits at the base of each arm are functionally likely similar to mouths… which would mean trilobozoans had at least three of them, which is not really reconcilable with cnidarians and more similar to the multiple, decentralized feeding-chambers of petalonams. The segmented appearance of Tribrachidium’s arms might also point towards them being constructed similarly to the fronds of rangeomorphs. For the thought-experiment that is to follow, I therefore propose this origin story: Trilobozoans might derive from Charnia-like rangeomorphs that lied flat on the microbial mats and grew three fronds instead of one (perhaps again being colonial forms?), radially splayed from each other from the holdfast [S]. With time these fronds began to curl around each other to direct water-flow. The filtering chambers along the arms gave up their feeding function, so the ridges could function better hydrodynamically, while the chambers at the arm-bases expanded their feeding-function to become proper “mouths” [S]. Channels likely still existed inside the arms to transport food throughout the body into digestive chambers inside the arms [S].

Proarticulata

Fig. 18: Some representative members of Proarticulata. Top, left to right: Spriggina and Dickinsonia. Bottom, left to right: Yorgia, Vendia and Archaeaspis. Before naming, the last one used to go by the nickname “Soft-Bodied Trilobite”. The glide-symmetry is the most obvious in Vendia, but can also be observed in all other members depicted here.

Most intriguing among the organisms appearing with the White Sea Assemblage are creatures such as Yorgia, Dickinsonia and Spriggina. Outwardly they look like bilaterally-symmetrical, worm- or trilobite-shaped creatures with segmented bodies and in some forms even a head. This led early researchers to propose that these were the ancestors of the Articulata (a hypothetical, now largely polyphyletic clade that includes annelids an arthropods), making them perfect precursors to the trilobites and other arthropods that were soon to follow in the Cambrian. Unfortunately, on second look, this seems to be untenable. On very close analysis, all proaticulatans are not perfectly bilateral, but exhibit glide-symmetry, like petalonams. This is especially apparent in forms like Yorgia, but can also be seen in Spriggina after detailed study (Ivantsov 2001). The flanges of Dickinsonia are also nearly identical to the fronds of rangeomorphs like Swartpuntia (Knoll 2003, Cuthill & Han 2018). The “heads” of proarticulatans are also not reconcilable with the heads of bilaterian animals, with analyses frequently failing to find evidence of eyes or a central mouth (McMenamin 1998). The same goes for things like legs or a central through-gut. Any resemblance to earthworms and trilobites is therefore purely superficial and proarticulatans are best interpreted as petalonams of very similar construction to Charnia, but lying flat on the sea-floor instead of hanging in the water. What was the frond and holdfast in Charnia became the body and cephalon in Spriggina.

Fig. 19: The trace fossil Epibaion, showing the crawling and feeding traces of Yorgia on the microbial mats. You can actually still see the body of the trace-maker if you look to the right. It is the same fossil as in fig. 18.

This surprisingly makes proarticulatans all the more intriguing, for, you see, they actually have trace fossils associated with them. This is again seen very well in Yorgia, where its trace fossil Epibaion is closely associated with the body fossil (these traces also show that the former holdfast was now the front of the body while crawling). The fossil Phyllozoon was likely also a trace fossil of something like Dickinsonia. So, did petalonams suddenly learn how to crawl? It certainly seems that way. As mentioned before, even sessile sponges are able to crawl to some degree and likely the whole skin of organisms like Charnia was covered in tiny cilia. While cilia are mostly used for transporting food, animals as large as comb jellies can also use them to swim, while placozoans use them to crawl (see fig. 5). The first petalonams probably had at least some limited capacity for ciliated crawling and the proarticulatans exploited this further to become full-time crawlers on top of the microbial mats. This seems to have also come with a change in diet, as the Epibaion traces show that Yorgia settled down on the mat, fed on its contents and then crawled to a new spot once finished. Proarticulatans were not filter-feeders anymore but had become active grazers. Though note that this was probably not the case with all of them, as especially the largest proarticulatans (who could grow up to 2 meters long) have no crawling or feeding traces associated with them (Knoll 2003). At least when they became adults, these giant petalonams probably were too large to still move with cilia, so they likely settled down and began filtering the water again like their ancestors.

Fig. 20: Ivantsov’s (2001) sketches of a larval Yorgia (left) and a Vendia (right). The dotted lines show where he suggests intestines or caeca could have run. Compare with my sketch from fig. 9.

This new lifestyle represents an important step in the anatomical complexity of petalonams. Charnia had mainly known two axes of symmetry (top-bottom and outward), whereas proarticulatans, crawling on the sea-floor, would have known at least three: Front-and-back (formerly top-bottom in Charnia), outward/sideways and a new top-bottom (top now being the frond-surface facing the water, bottom being the one facing the ground). Combined with them now crawling towards distinct directions, this means that the body had to be further compartmentalized. The bottom surface may have become specialized in crawling and feeding, while the top surface filtered the water or specialized in respiration (with certain filtering chambers perhaps becoming gills) [S]. Like the snail Elysia chlorotica, some proarticulatans may have used the algae-cells they consumed as symbiotes to do photosynthesis themselves [S]. This has indeed been put forward as an explanation for the flattened edges of Spriggina (McMenamin 1998). The need to streamline may also explain why these animals became outwardly more bilaterally symmetrical, as the same hydrodynamics that are imposed on modern animals forced them to adjust their ancestral glide-symmetry as good as possible into a pseudo-bilateral symmetry [S]. What changes all this imposed on the cephalon (the former holdfast) is especially fascinating. While crawling forward, this would have been the first part of the body to come into contact with fresh mat and therefore the first to feed. In forms like Yorgia, Vendia, Spriggina and Archaeaspis it becomes very apparent that the cephalon became wider and more shield-like compared to the holdfast of sessile petalonams, likely to sweep up the bacterial mats like a lawnmower. While they did not have a central mouth, internal casts of these fossils show that the cephalon may have been full of tiny feeding channels, likely connected to multiple feeding-pores at the bottom (Ivantsov 2001). These channels were then likely connected to the internal channel at the base of the frond-branches, which we discussed earlier with Charnia [S]. This could possibly affirm my idea that the holdfast/cephalon develops from a sponge-like protostome, which in proarticulatans, instead of growing shut or into a single big mouth, divides into multiple micro-mouths [S]. In the big-headed  forms the cephalon did possibly most of the feeding, while the frond became specialized for crawling. In contrast, forms like Dickinsonia, which have very small cephalons but very large fronds, likely did the opposite and mostly fed with their frond. One has to wonder though if the cephalon, especially in the former group, did more than just eat. After all, this was the organ that would have come first into contact with new food, new sediments, new currents and new threats. I had long been doubtful, but realizing this I must say that McMenamin (1998) was possibly, maybe even probably, right, when he proposed that these animals were evolving cephalization independently of bilaterians like us (hence why they happen to look vaguely similar to worms and arthropods). It is not unthinkable that the top of the cephalon had an array of primitive sensory cells of the same kind that were already present in sponges and placozoans. Chemical sensors that detect anoxia or toxins, cilia that detect changes in water flow and pressure, maybe even light-sensitive cells, the precursors to eyes. With independent movement, clear body structure and possible cephalization, the proarticulatans were well on their way towards developing a nervous system and muscles. Perhaps some of them even already had primitive versions of those, as a few specimens of Dickinsonia may show signs of muscular retraction (Knoll 2003).

The things that were to come

Around 548 million years ago, the Ediacara-type assemblages are followed by the Nama Assemblage, named after fossil localities in Namibia. Again, this does not mean a total displacement, as the two communities did coexist for a short time. Whereas Ediacara-types like the White Sea fauna were deposited on shallow continental shelves, Nama assemblages seem to have been even closer to the shore, at the mouths of river deltas. The world that the petalonams grew up in was now beginning to markedly change. Trace fossils show that burrowing animals now become more numerous, active and coordinated, with some now also beginning to make vertical burrows. The makers of these traces in all likelihood were our own ancestors, the first bilaterians. These of course did not come out of nowhere. Only two to three million years after the end of the Marinoan ice age, we find possible fossil embryos and eggs of such animals in the aforementioned Doushantuo Formation (Yin et al. 2007), though this classification is controversial. In Doushantuo strata dating between 600 and 590 (so even older than Charnia) can also be found a curious, tiny fossil named Vernanimalcula, which has been interpreted as an early adult bilaterian (Chen et al. 2004). This identification is also controversial (others have proposed that the fossils are in-filled bubbles inside the shells of acritarchs), but it is probably safe to say that bilaterians had already evolved before petalonams gained their giant (for the time) size. In the White Sea assemblage, we can already find in Kimberella a possible relative of molluscs and with Ikaria wariootia from Australia a similar, albeit more worm-like creature. These two likely grazed on the bacterial mats like the proarticulatans, but not to a degree where the mats could not regenerate quickly again. But the new, more complex burrowing bilaterians showing up with the Nama Assemblage were now doing more fundamental damage. Their stirring and mixing of the soil disturbed the placid soil that the microbial films relied on and so the bacterial mats that the petalonams evolved on were becoming gradually more broken up. For the very first time in earth history, armored animals evolved as well in the Nama assemblage, as we find tiny calcium carbonate shells from animals like Cloudina and Namacalathus, who may have been coral-like cnidarians or tubeworms. Regardless of all these changes, rangeomorphs, trilobozoans and proarticulatans continued to exist and even in the Nama Assemblage we see more evolutionary innovation with forms such as:

Erniettomorphs and other “Sand-Anchorers”

Among the sessile forms now started appearing creatures such as Ernietta. This was an animal which looked like a plastic-bag constructed of palisades of tubes. The lower part of the bag was buried by sand, both inside and outside the cavity, likely to act as an anchor, while the frills stood erect in the water (Ivantsov et al. 2015). At first it seems difficult to place this among petalonams or any other animals for that matter. Looking at the “seam” on the bottom of the bag, however, it appears that these tubes grew from each other through glide-symmetry, something unique to Charnia and other rangeomorphs (Dunn et al. 2021). Ernietta likely developed from a flat petalonam made of two opposing fronds that intentionally buried itself under sand, either by the way of a stolon or a burrowing larva [S]. The two fronds grow outward and upward out of the sand and then meet again, sort of like the leaves of a venus-fly-trap. The result is a partially sand-filled bag, whose fringes can now filter the water for food while being safely rooted in the soil. Since this was a shallow water organism, photosynthesis using symbiotes would have also been possible.

Fig. 21: Reconstruction of African Ernietta plateauensis (taken from Ivantsov et al. 2015). A bag-like creature where the bottom half was burrowed in sand, while the top hung in water, likely to filter-feed. Note how the seam at the bottom exhibits glide-symmetry.

Probably not directly related, but functionally similar was Pteridinium, which basically looked like a bathtub with a longitudinal wall cutting it in half. Pteridinium likely also descends from a bipolar frond, but with three vanes instead of two, sort of similar to Swartpuntia but without the stalk. The taphonomy indicates that the bathtubs were filled with sand and that way could also function like an anchor. Despite being mostly covered in shallow sand, there is some tentative geochemical evidence that Pteridinium fed through photosynthesis (McMenamin 1998), but since only the tips of the frond-vanes looked out of the ground, it is perhaps more likely that it mostly fed through filter-feeding.

Fig. 22: A cut through Pteridinium (taken from McMenamin 1998). As you can see, the bathtub terminology does not come from me.

While potential forms of sand-anchoring could already be observed in earlier medusoids, it seems likely to me that in these petalonams, this strategy specifically evolved to cope with the degradation of the microbial mats that earlier, holdfast-based forms had to rely on. Who needs scum when you got gravel?

Conulariida: Trilobozoans reloaded?

An interesting fossil found from the Late Ediacaran of the White Sea region is Vendoconularia. This animal greatly resembles the conulariids, a clade otherwise only known from the Paleozoic. Conulariida were radially symmetrical animals with shells that broadly resemble angular ice cream cones. Unlike the similarly shaped shells of some cephalopods, the conulariid shell is, uniquely among animals, constructed of multiple bony rods that were stacked on top of each other on all sides as the organism grew in length, sort of like how one would build a brick wall. These rods were made of calcium phosphate, the same kind of mineral that vertebrates use to build up their bones. The cone most likely stood erect in the water and its pointy tip was connected to the ground by a short stalk. Because most Paleozoic conulariids had a four-fold symmetry, it was long thought that they were part of or closely related to the Scyphozoa (true jellyfish, see fig. 6), but Vendoconularia shows that these organisms actually started out with a tri-radial symmetry (Ivantsov & Fedonkin 2002, Van Iten et al. 2005). Together with Lower Cambrian fossils such as Anabarites, this points towards conulariids having actually evolved from trilobozoans, evolving their tri-radial symmetry into a six-fold symmetry and from there then into a superficially jellyfish-like four-fold symmetry (Ivantsov & Fedonkin 2002). Likely, conulariids would not descend from spiral-armed trilobozoans like Tribrachidium, but the more straight-armed ones like Anfesta [S]. At some point these might have begun laying down a biomineralized skeleton beneath their arms/disk, gradually building up the cone-shell as the organism aged, similar to how corals develop [S]. While in Vendoconularia this skeleton is only very lightly mineralized (Ivantsov & Fedonkin 2002), there are probably two reasons for why this shell evolved: With the demise of microbial mats, trilobozoans could not rely on the previous hydrodynamics of the sea-floor surface anymore, so they began stacking themselves higher into the water column to catch better currents to feed on [S]. The shell likely also provided protection from small predatory animals, who, as the previously mentioned boreholes on Cloudina indicate, were becoming ever bolder in attacking larger organisms [S].

Fig. 23: The shell of Vendoconularia (taken from Ivantsov & Fedonkin 2002). Most life reconstructions show an anemone-like animal (a single mouth circled by tentacles) sitting in the cone-opening, but in my sketch I instead went with a version of Anfesta with three mouths and tentacles growing along the body-ridges. Yes, I know I am not a good artist, but you will probably get what I was trying to depict.

The possibly direct linkage of trilobozoans and conulariids is significant for two reasons. First and foremost is that Conulariida was an incredibly long-lived lineage, which only went extinct during the Lower Triassic 245 million years ago. In other words, their last members could have potentially met the direct ancestors of the dinosaurs. This would make Trilobozoa one of the longest-lived animal groups, beating out even the trilobites by a long shot. Second, Ordovician fossils of conulariids preserve soft tissues, which show them having tentacles similar to anemones. Those tentacles were then likely powered by muscles and nerves. This could be proof that conulariids and in turn trilobozoans are not petalonams, but stem-cnidarians or even proper scyphozoans. But no known cnidarians build shells of the same construction and of the same material as conulariids (Ivantsov & Fedonkin 2002). Furthermore, ctenophores obviously evolved muscled tentacles independently of cnidarians and so could have the trilobozoans and other petalonams as well [S].

The End?

Around 541 million years ago a major shift happened as the Ediacaran gave way to the Cambrian. The microbial mats completely collapsed, as animal-burrows became ever more complex and vertical. Predation also became a major issue for many animals, who now began defending themselves with mineralized shells and skeletons. This led to the major radiation of the so-called Small Shelly Fauna (which is elaborated more here), which likely saw the origin of typical shelled animals such as clams, snails and brachiopods. But while these began to flourish, many larger animals died out. The proarticulatans, despite being so promising, vanished completely, alongside most rangeomorphs and the classic trilobozoans. For the first 20 million years the SSF dominates, until the appearance of the first trilobites. By the time of the famous Burgess Shale 508 million years ago, the world was a completely different one, dominated by arthropods and close relatives, archaeocyathid sponges and worms of many kinds, but seemingly with no petalonams to be found. What happened?

Fig. 24: A possible family tree constructed by me. While I partially based this off Cuthill & Han 2018’s cladogram, most of this is highly speculative, so do not take it as gospel.

The general idea is that the End-Ediacaran extinction happened because the evolution of marine ecosystems had reached a natural tipping point once bilaterian animals gained a certain complexity and size. Petalonams, being muscle- and nerve-less bags of fluids that grew up in a serene garden world, were simply too unadaptable to cope with the major radiation of bilaterian animals. With the loss of bacterial mats at the hands of burrowing worms, the sessile forms lost their footing and the proarticulatans their food. The appearance of large predatory animals then gave them the rest. In this view, the extinction of the petalonams was inevitable as soon as our own ancestors evolved. In many ways this reminds one of the old ideas about dinosaur extinction, wherein the terrible lizards were too dumb, slow and reliant on swamps, so they were destined for extinction once the climate changed and mammals evolved. And this should make everyone immediately suspicious, because we all now know that was absolutely not the case. In general, the idea of annihilation-by-worms leaves open a lot of questions and problems, some of which eerily parallel the early debates about the End-Cretaceous extinction:

  • Erniettomorphs and other sand-anchorers seem to have already anticipated the loss of microbial mats, but went extinct anyway at the end of the Ediacaran. Why? Possibly they were the victims of predators, but:
  • Almost all of the large Cambrian predators (as in larger than 5 cm), the classics like Anomalocaris, Ottoia, Sidneya, trilobites, crustaceans and so on, only started appearing long after the end of the Ediacaran (Knoll 2003). As the Cloudina boreholes and the general size of the Small Shelly Fauna attests, the predators along the Ediacaran/Cambrian boundary would have been miniscule priapulid- or velvet-worm-like critters. For meter-long proarticulatans and rangeomorphs these would at best have been a nuisance, not a serious threat.
  • The idea that newer groups must automatically displace older ones is awfully chauvinistic and at odds with reality. After all, if the petalonams died out because they could not compete with bilaterians, how could the even more basic sponges and placozoans still exist today?
  • Related to the above, just as how the first mammals already appeared alongside the first dinosaurs, bilaterian animals were already living alongside the petalonams since at least the Avalon Explosion, if not earlier. Some like Kimberella and Ikaria lived placidly alongside the likes of Dickinsonia and Spriggina on the mats, so the petalonams would have had enough opportunity to adapt to their neighbours.
  • Conulariids, if they are indeed part of the Trilobozoa and Petalonamae, would be proof that petalonams had the capacity to evolve eumetazoan characteristics and persist long past Ediacaran-like ecosystems. If it had not been for the worst mass extinction in Earth’s history at the end of the Permian, they would likely still exist today.
  • Conulariids were not the only survivors. With Stromatoveris psymoglena from the Chengjiang biota we have a close relative of rangeomorphs such as Rangea surviving all the way into the Cambrian Stage 3 without much anatomical change (Cuthill & Han 2018). It lived there alongside typical Cambrian animals, such as trilobites, priapulids, echinoderms, lobopods and even early chordates. This shows that even petalonams of classic morphology could survive without the microbe-mat environment and even alongside typical Paleozoic faunas.

It all appears that petalonams were dominant and adaptable throughout their reign and maybe even halted the rise of bilaterians, just as how the dinosaurs halted mammalian evolution. What then did actually happen at the end of the Ediacaran? Geochemical evidence shows that the isotopic signature of δ13C massively drops right during this boundary, even harder than during the Marinoan or Gaskiers ice ages, but curiously there are no sedimentological signs of global glaciation (Knoll 2003). Furthermore, massive ocean anoxia occurred, especially in shallow marine environments. Both these events happened in a relatively short amount of time. These are all signs closely associated with mass extinction events, including the Permian-Triassic boundary. The Proterozoic was therefore most likely ended by a catastrophic event outside the power of both petalonams and bilaterians. What could have been the cause? Using the P-T-boundary for comparison, massive volcanic activity would seem to do the trick. However, in such an event, the oceans would also strongly acidify, which does not correlate well with the radiation of the Small Shelly Fauna at this boundary, as acidic water would have attacked their shells. An asteroid impact therefore seems perhaps more probable [S]. At the likely chance this asteroid landed in the deep ocean, we might not be able to find its crater anymore, as almost all of the oceanic crust recycles itself in cycles of 200 million years. Like at the end of the Cretaceous, the ash thrown into the atmosphere by this impact would have blocked out the sun for decades if not centuries, majorly disrupting ecosystems as it made photosynthesis hard to maintain. Algae would have suffered and the characteristic bacterial mats would have degraded even faster. Assuming that at least some of the later, shallow-water petalonam forms did indeed live by symbiosis with algae, even if just in addition to filter-feeding, this would have spelled disaster for them as well. By direct comparison, corals live much the same way and it is estimated that up to 98 percent of their species went extinct during the impact of the K-Pg-boundary. The near-total breakdown of photosynthesis would then explain the observed anoxia. Large organisms, especially the proarticulatans who were already suffering from the loss of their food-source, would then have suffocated. Like mammals after the extinction of the non-avian dinosaurs, the small bilaterians would then have emerged from their burrows having to fill up the void. The few surviving rangeomorphs such as Stromatoveris would then have been a classic example of a dead clade walking, while conulariids were to petalonams what birds are to other dinosaurs.


Fig. 25: In many ways the End-Ediacaran extinction mirrors the End-Cretaceous extinction (taken from Knoll 2003). What this means is that, like with the dinosaurs, the extinction of the petalonams was not predetermined but rather bad luck.

What do we do now with the growing knowledge that, in their end, Ediacaran animals really were the “dinosaurs” of the Proterozoic, as Knoll (2003) puts it? Well, if all the thought experiments on the internet and in the world of literature, which explore worlds in which the asteroid at the end of the Cretaceous never hit Earth, are anything to go by, it means that we can have a lot of fun by just asking: “What if?” What if the Ediacaran-Cambrian extinction event never happened or, alternatively, what if it did happen but wiped out Eumetazoa instead?

The things that could have come

"...if Ediacara had won the replay, then I doubt that animal life would ever have gained much complexity, or attained anything close to self-consciousness. The developmental program of Ediacara creatures might have foreclosed the evolution of internal organs, and animal life would then have remained permanently in the rut of sheets and pancakes - a most unpropitious shape for self-conscious complexity as we know it. If, on the other hand, Ediacara survivors had been able to evolve internal complexity later on, then the pathways from this radically different starting point would have produced a world worthy of science fiction at its best." (Gould 1989, p. 314).

These were evolutionary biologist Stephen Jay Gould’s few words on the Ediacaran biota in his list of thought experiments towards the end of Wonderful Life. So far this remains one of the few opinions given by a serious scientist on this hypothetical scenario (most other scientists involved in spec-evo are, like everyone else, obviously more interested in Holocene dinosaurs, the future or aliens). Another one was had by geologist Mark McMenamin in his book Garden of Ediacara, in which he, in direct contrast to Gould, argues that the possible cephalization in proarticulatans points towards the beginnings of a brain and therefore may have paved the path towards consciousness. Whose idea is more valid? Of course, because we do not have a time machine and therefore cannot alter the timeline, we will never know with certainty. But our insight into these lifeforms has improved well enough in the past two decades that we can make some quite educated guesses. Especially Gould’s assessment, which worked off the idea that petalonams were jelly-filled sacks that could only interact with their environment through their outer skin, seems to be untenable now. Petalonams did already possess internal organs in the form of a hydroskeleton and feeding chambers and they likely could have evolved more than that. But does this automatically mean that McMenamin was right and that they could have one day gained consciousness, maybe even self-aware intelligence?

Join me in the next part (hopefully soon to follow), where we explore some of the evolutionary potential of many of the Late Ediacaran organisms as they did not enter the Cambrian but instead Charles Walcott’s lost period of the Lipalian. One thing I can already say is that Gould was right in at least one aspect: This truly would have been a world worthy of science fiction.

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Literary Sources:

  • Asad, Muhammad: The Message of the Qur’an, Bristol 1980.
  • Godfrey-Smith, Peter: Other Minds. The Octopus and The Evolution of Intelligent Life, London 2017.
  • Gould, Stephen Jay: Wonderful Life. The Burgess Shale and the Nature of History, New York 1989.
  • Knoll, Andrew: Life on a Young Planet. The First Three Billion Years of Evolution on Earth, New Jersey 2003 (Second Paperback Edition).
  • Lane, Nick: The Vital Question. Why is Life the Way it is?, London 2016.
  • McMenamin, Mark/Dianna: Hypersea. Life on Land, New York 1994.
  • McMenamin, Mark: The Garden of Ediacara. Discovering the First Complex Life, New York 1998.

Papers:

Image Sources:

  • Fig. 1: Wikimedia
  • Fig. 2: El Albani et al. 2014.
  • Fig. 3: Wikimedia
  • Fig. 4: Wikimedia
  • Fig. 5: Wikimedia
  • Fig. 6 - 8: Dunn et al. 2021.
  • Fig. 10: Butterfield 2020.
  • Fig. 11: Bottjer & Clapham 2006.
  • Fig. 12: Butterfield 2020.
  • Fig. 13: Wikimedia
  • Fig. 14: Dunn et al. 2021.
  • Fig. 16: Wikimedia
  • Fig. 17: Rahman et al. 2015.
  • Fig. 18: Composite from Wikimedia and Ivantsov 2001.
  • Fig. 19: Wikimedia
  • Fig. 20: Ivantsov 2001.
  • Fig. 21: Ivantsov et al. 2015.
  • Fig. 22: McMenamin 1998, p. 27.
  • Fig. 23: Ivantsov & Fedonkin 2002.
  • Fig. 25: Knoll 2003, p. 222.