Immortal alga

A 541-million-year-old seaweed falls short of setting the record for the oldest genus name, by half a millimeter
Published in Ecology & Evolution
Immortal alga
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BioMed Central
BioMed Central BioMed Central

A stem group Codium alga from the latest Ediacaran of South China provides taxonomic insight into the early diversification of the plant kingdom - BMC Biology

Background In recent years, Precambrian lifeforms have generated an ever-increasing interest because they revealed a rich eukaryotic diversity prior to the Cambrian explosion of modern animals. Among them, macroalgae are known to be a conspicuous component of Neoproterozoic ecosystems, and chlorophytes in particular are already documented in the Tonian, when they were so far expected to originate. However, like for other major eukaryotic lineages, and despite predictions of molecular clock analyses placing roots of these lineages well into the Neoproterozoic, a taxonomic constraint on Precambrian green algae has remained difficult. Results Here, we present an exceptionally preserved spherical, coenocytic unicellular alga from the latest Ediacaran Dengying Formation of South China (> ca. 541 Ma), known from both external and internal morphology, fully tridimensional and in great detail. Tomographic X-ray and electronic microscopy revealed a characteristic medulla made of intertwined siphons and tightly packed peripheral utricles, suggesting these fossils belong to the Bryopsidales genus Codium. However, its distinctly smaller size compared to extant species leads us to create Protocodium sinense gen. et sp. nov. and a phylomorphospace investigation points to a possible stem group affinity. Conclusions Our finding has several important implications. First, Protocodium allows for a more precise calibration of Archaeplastida and directly confirms that a group as derived as Ulvophyceae was already well diversified in various ecosystems prior to the Cambrian explosion. Details of tridimensional morphology also invite a reassessment of the identification of other Ediacaran algae, such as Chuaria, to better discriminate mono-versus multicellularity, and suggest unicellular Codium-like morphotypes could be much older and widespread. More broadly, Protocodium provides insights into the early diversification of the plant kingdom, the composition of Precambrian ecosystems, and the extreme longevity of certain eukaryotic plans of organization.

I, for one, think that we talk about Darwin too much, making him overshadow his contemporaries. In the preface of the Everyman’s Library edition of the Origin of Species, Richard Dawkins goes as far as saying that no one before Wallace and Darwin thought about biological evolution—as if Lamarck had not been cast away enough in his own time. Yet it is hard to deny that the failed (or non-forcibly-made) medical doctor made for an exemplary scientist in admitting the limits of his own theories, offering by principle the body of his work to execution by falsification long before Popper waved his epistemological flags.

Two of these empirical caveats that remain most famous are the so-called “abominable mystery” of the rise to dominance of flower plants, and “Darwin’s dilemma,” the apparently inexplicable absence of Precambrian fossils in the light of a gradual natural selection of a varied descent. We now know that these observations, first, were altered by biases of the fossil record, but also, second, that they simply highlight the incompleteness of Darwin’s original hypotheses when looking at longer time scales. These discrepancies gave rise to the notions of micro- and macroevolution that we are still trying to unify today.

Today, Darwin’s dilemma has moved towards the cause(s) and nature of the Cambrian explosion—the geologically sudden rise of animal phyla. The “dilemma” was originally embodied by the biomineralization associated with the diversification of these first animals, causing such a bias in the fossil record, yet the tremendously rich accumulation of “soft-bodied” fossil evidence during and before the Cambrian since Darwin has but emphasized ecosystem differences between Precambrian and Cambrian. Some recent data, from fossil arthropods for instance, has even pushed the origin of extant lineages closer to the beginning of the Cambrian Period, and shown that the major arthropod body plans arose within 20 million years.

For a long time, complex life before the Cambrian had boiled down to the “vendobionts” of the Ediacaran biota. For the most part, these simple but odd organisms are still regarded as a separate branch of life that went extinct before the Cambrian explosion, even if it seems their lifestyles and feeding strategies had much in common with modern animals. However, while generally larger, vendobionts represent but a fraction of known biological diversity during the Ediacaran, and none of it before that. One would need to account also for all prokaryotes, fungi, sponge-like forms, animal-like embryos, and algae. A lot of algae.

A common theme, nonetheless, has subsisted: How close are these fossils to extant organisms? In Charles’ wake and legacy, this is the lean but tasty carcass where an Ediacaran palaeontologist will want to feed. The skirmish has been especially keen for the famous three-dimensionally-preserved Doushantuo embryos, with many similarities to those of modern animals, and sponges. Regardless of the outcome, the very nature of these debates points to the existence of forms very close to the roots of modern lineages.

A similar context has been characterizing the study of Precambrian algae: that is, having reasons to think some taxa could be included close to modern lineages, but without clear determination. The situation has been made harder by the fact that—with the exception of some red algae—these Precambrian fossils are preserved in two dimensions with a grain-size resolution limit, and, to boot, that superficial algal morphology can only go so far to help identify a taxon.

As someone who usually works on Cambrian animals, it was only fortuitous, and originally for general scientific advice, that my friend and colleague Shu Chai came sharing her research on the latest Ediacaran Gaojianshan biota, from the South Shaanxi province, People’s Republic of China, while I was working at Xian’s Northwest University. But it turned out to be, as I never really had realized it could, a gust of fresh air. Not that my regular work is stale—by any means, working on the early evolution of arthropods is a constant challenge—but, for the inquisitive mind, having to tackle the very new awakes more acute feelings of adventure and proportionally greater satisfaction at the moment of discovery. Not only this, but the fossils were exquisite and thus very promising, although I had no idea, when I started, of the extent of their novelty.

The detective work led us to step away from the Dasycladales avenue, which had been the working hypothesis of Shu and her advisor, Professor Hong Hua. By contrast to our fossils, these calcareous green algae—relatively well-known in the early Palaeozoic fossil record—were distinctly hollow, with straight “needles” coming out of a small core, and attached to the sea floor via a “foot,” or holdfast. Nevertheless, other similarities suggested the identity of our fossil might lie close to Dasycladales. It took some time to clear the ground and carefully navigate across fossil and extant Ulvophyceae, but finding the affinity with Codium was facilitated by the fact that this genus has gained unfortunate notoriety through its invasive species.

The fossils Shu Chai brought to me, we named Protocodium sinense, are morphologically identical to an immature, spherical Codium, except for the fact that they are about twice as small as the smallest known Codium morphs—which represents a difference of about half a millimeter. This realization struck—a true Eureka moment. For it was more than identifying a Precambrian alga, it was putting a name on something—anything—Precambrian. A genus (Codium, Protocodium) is a taxonomic abstraction without definite biological reality, and, as far as palaeontology is concerned, species—“morphotypes”—are generally not biologically defined either. But it is of little import here. What matters is that, for half a millimeter, the morphotype would belong to an extant evolutionary lineage, within the smallest systematic unit founded to hold modern species. Previous record holders were Cambrian, such as the graptolite Rhabdopleura, and assigning a known, modern genus name before the Cambrian explosion is in itself very symbolic. It means that some of the very same complex life forms of our own biosphere, which we can hold in our hands, had established their presence well before the Cambrian explosion. Importantly, the green alga in question here was a primary producer, a pillar of ecosystems.

To Darwin and his dilemma, this provides two answers, beyond the knowledge that a rich Precambrian fossil record exists. First, that the “dilemma” is grounded in the fact that a phenomenal biological turnover occurred at the Ediacaran-Cambrian transition, but also that some of the same actors of modern ecosystems, especially the primary producers of organic matter, had been in place much earlier, with the exact same morphology. Second, it shows that evolutionary stasis is a phenomenon of colossal importance, and that evolution by natural selection, for some organisms, is but a marginal factor of change—at least at the morphological level. The coding genome of Codium, on the other hand, evolved well enough to resolve the relationships between extant species. In that, Protocodium affirms an era with increased focus on the regulation of genes’ expression, whereby what we see, the phenotype, is the buffered output of the ever-changing machinery—in this case, a buffering so stubborn it has not changed in half a billion years. How is that, for a dilemma?

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