Is your oldest sister a warty comb jelly?

A paper published this week in 'Science' is revising the lowest branches on the animal kingdom's evolutionary tree, as well as upending how evolution is thought to progress. 

Bruno Vellutini/Sars International Center for Marine Molecular Biology/University of Bergen, Norway
Are comb jellies, also called sea walnuts, the world's first animals?

Our oldest ancestors are warty comb jellies.

That might not sound too flattering, but it’s an improvement. Until now, our earliest relatives, the first branch in the animal kingdom’s proverbial tree, were thought to be sponges, the sessile, collagen wads.

A new paper published this week in the journal Science reports that ctenophores, a phylum of animals that includes a species colloquially known as warty comb jellies, are Earth’s earliest extant animals, making them sister to all other animal kingdom phyla. The findings are a revision to the base of Earth’s animal tree, putting ctenophores where sponges had been.

It’s also a revision counter-intuitive to how evolution is often imagined. That’s because ctenophores, which have nervous systems and muscles, appear to be more sophisticated animals than are sponges, which lack both these things.

In other words, the evolution of the world’s earliest members of the animal kingdom did not follow the neat, linear logic of simpler organisms preceding more complicated ones. The narrative, so the warty comb jellies tell us, is squishier than that.

“It’s a good cautionary tale,” says Joseph Ryan, a research fellow at The National Human Genome Research Institute’s Genome Technology Branch and the lead author on the paper. “This concept of complexity is not a good anchor for phylogenetic relationships.”

The Animal Kingdom is divided, first, into the non-bilaterian clade and the bilaterian clade. The bilaterian clade is enormous – it contains most of the world’s animals, including everything from horseflies to hamsters to humans. The non-bilaterian clade forms the base of the kingdom’s evolutionary tree, beginning about 600 million years ago, and it numbers just four phyla.

One of them is the Ctenophora phylum, or comb jellies that all have in common eight rows of hairs (hence “comb”) dripping down their sides. The other three phyla are: Porifera, or sponges; Placozoa, or “flat animals” that resemble amoebas in form; and Cnidaria, which includes sea anemones, corals, and jellyfish.

Though arrangements of these four phyla have varied, scientists have often said that the cnidarians are the most recent of these four groups. The placozoans had come before them, and poriferans had been the earliest animals.

This timeline had made morphological sense. The sponge looks like the earliest animal – meaning, “sponges look simple,” says Dr. Ryan. It has no nerves. It doesn’t even have muscles within which to arrange such things as nerves. Placozoans also appear simple: no nerves, no muscles. The cnidarian phylum’s magnificent jellyfish, though, seems more complex, with both nerves and muscles.

But, where to put the ctenophores?

Sometimes, ctenophores have been plotted as sisters to the cnidarians. Like cnidarians, ctenophores are marine, gelatinous, and entrancingly serene-looking. And, like cnidarians, ctenophores have nerves, though a ctenophore arranges them differently, as a neat little system that glows and blinks iridescent through its translucent form, as if the animal had swallowed an LED rave necklace.

Physical evidence had also suggested that ctenophores are close relatives to bilaterians. That’s because ctenophores have what is called a mesoderm, one of three embryonic layers that develop into tissues. This layer is present in all bilaterians, but it is unique to ctenophores in the non-bilaterian clade. Both cnidarians and poriferans have just two of the layers, lacking a mesoderm, and placozoans’ tissues are not organized in layers.

Since 2008, though, scientists had begun to propose what seemed like a preposterous idea: what if ctenophores, despite their apparent sophistication, were in fact the earliest animals?

“It was dismissed because it doesn’t seem correct,” says Ryan. "People were shocked."

Until now, scientists had not had enough genetic data to resolve the issue, since a full genome had not yet been sequenced from the ctenophores, even though one was available for at least one species in the other four earliest phyla. 

In the latest research, the team sequenced the genome of the ctenophore Mnemiopsis leidyi, often called a warty comb jelly, or sometimes a sea walnut. This is a bantam, glittering animal, resembling an unusually unhurried snowflake. Its genome is small, too. At about 16,500 genes, it is in the bottom seven percent in genome size, relative to all animal genomes cataloged in the Animal Genome Size Database.

Based on an analysis of the animal’s full genome, the team reports that ctenophores are much more distant from cnidarians than had been thought – so distant, in fact, that ctenophores should be put at the very bottom of the tree, even preceding sponges.

“The first split in the animal tree was between the lineage that gave rise to ctenophores, and the lineage that gave rise to all other animals, including ourselves,” says Casey Dunn, an evolutionary biologist at Brown University and a co-author on the paper, in an email to The Monitor. 

But that presents two problems, both of which seem to violate a basic principle of evolution: if the first branch of animals in the kingdom’s tree had a nervous system, how is it that neither the second branch, the sponges, nor the third branch, the “flat animals,” have one?

And how is it that the first branch of animals has a mesoderm, when none of the animals in the next four branches has one?

Well, in short, because evolution is complicated, the authors say – traits are lost, and traits gained; and then, traits are re-lost, and traits are re-gained.

The team’s findings show that the neural genes in ctenophores and sponges are similar, though the sponges do not in fact have a nervous system. So, it’s possible that the ctenophores and sponges’ common ancestor had a nervous system. That ancestor’s neural genes were then passed to both ctenophores and sponges, but were expressed in just the ctenophores. In other words, this ancient organism, now extinct, could have been more sophisticated than scientists had thought.

“It has always been thought that the last common ancestor was a simple creature that lacked neural and muscle cell types,” says Andreas Baxevanis, head of the Computational Genomics Unit at The National Human Genome Research Institute and a co-author on the paper, in an email to The Monitor.

This latest research “brings these long-held tenets into question,” he says.

Another option is that the ctenophore's nervous system evolved independently, after the phylum diverged from the rest of the animal kingdom, says Ryan. This appears to have been the case with the ctenophores’ mesoderm, he says. The researchers found that ctenophores’ mesodermal cell types differ from those of bilaterians, suggesting that the mesoderm did not exist in a common ancestor but evolved separately in both groups, he says. 

“Like the nervous system, the mesoderm appears to have had a complex evolutionary history,” write the authors, in the paper.

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