New family tree of worms has roots in the 19th century

This post was chosen as an Editor's Selection for ResearchBlogging.orgNineteenth century biologists had a point when they divided the ringed worms into free-living hunters and sessile filter feeders. Their classification was dismissed in the 1970s, but a closer look at the genes of many different worms now shows that they were closer to the truth than their later colleagues.

The classification of worms got off to a false start thanks to Carl Linnaeus, the great-grandfather of taxonomy. After he had given mammals, reptiles, birds and fishes their own groups, he divided the remaining invertebrates (animals without a spine) into just two categories: insects and Vermes, or worms. Anything that was not an insect therefore was, by necessity, a worm. In this way Linnaeus lumped a diverse group of creatures was together into a single class. Corals, jellyfish, squids, worms themselves and other soft-bodied animals were all members of the bloated Vermes. Stephen Jay Gould famously described the Linnaean class of Vermes as a taxonomic wastebucket.1

The taxonomists that came after the Linnaeus spent a lot of time cleaning out this wastebucket. One of the first biologists to study worms in detail was Jean-Baptiste Lamarck. He liberated the ringed worms, or annelids, from the Vermes and placed them into their own, unique group. He recognized that their segmented body plan, gut, nerve cord and blood vessels make them different from other worm-like creatures without these features, such as snails and flatworms.

Tomopteris, a free-living worm belonging to the Errantia. When they are disturbed, they release glowing particles from their parapodia.

Later, in 1866, the French naturalist Quatrefages further divided the ringed worms into the Sedentaria and the Errantia. Not only do these two groups differ in their way of life, with the Errantia being free-living predators and the Sedentaria immobile filter feeders, they also differ in the way they look. The parapodia (little worm legs) of Sedentaria are smaller and less pronounced than those of Errantia for example.

This classification was used for over a century, but it was dismissed as an ‘arbitrary grouping’ that was used only for ‘practical purposes’ by biologists in the 1970s2. They argued that the similarities of Sedentaria and Errantia arose due to convergence, rather than reflecting a deep evolutionary split. In other words, they argued that some worms look the same because they have a similar way of life, and not because they are closely related. Just like the wings of a bird and and bat wings look similar even though the common ancestor of birds and bats had no wings. The revisionists came up with a new classification that featured a split between the bristled worms (polychaetes) and the collared worms (clitellates, which includes the famous and noble earthworm).

But when Torsten Struck and his colleagues analyzed hundreds of genes of 34 different species of ringed worms, they didn’t find this split. Instead, they found that most worms belonged to two groups that mirror the nineteenth century groupings of Errantia and Sedentaria3. The different lifestyles of the two groups aren’t arbitrary. On the contrary, they are the reflections of an ancient crossroads in the evolution history of ringed worms!

The new family tree of Annelids (red), showing that Sedentaria (blue) and Errantia (green) are distinct groups.

This means the end for the bristled worms as taxonomic group. Earlier studies already hinted that something was amiss, but Torsten Struck was surprised to see the revised classification from the 70s rejected with such confidence. This makes clear what the biggest problem is of classifying life solely on the way it looks: you cannot distinguish whether a certain feature was never there in the first place, or whether it became lost during evolution later on. Genes, if you look at enough of them, don’t have this problem, .

Take the collared worms, who adapted to a life in freshwater and in the earth. They lost the parapodia and bristles of their marine ancestors and evolved many changes in the way they reproduce. If you would classify earthworms based on these characteristics, they would appear to be more distantly related to other bristled worms than they really are.

With the new family tree in hand, Torsten Struck could reconstruct what the ancestors looked like (apparently, they were really cute!). The reconstruction of the ancestor of Errantia shows that it was already well adapted to a mobile and predatory way of life. It had well-developed antennae, two pairs of eyes (“‘all the better to see you with, my dear”) and parapodia which it used to move around quickly. The evolution of Sedentaria show the opposite trend. Their ancestor had no antennae and reduced parapodia. Other sensory organs were lost in different lineages of Sedentaria.

Meet the really cute ancestors of annelids, Errantia and Sedentaria

Scientists who use worms as model organisms should pay close attention to these results. The marine ragworm, or Platynereis dumerilii, has recently come in vogue for studying how eyes and organs evolved in animals. Many of its characteristics, like its large antennae and sensory palps, seem to be more characteristic of the family of Errantia, and not for the ringed worms as a group. Torsten Struck writes: “None of the model organisms alone will reveal the ancestral conditions which were present in Annelida. You can only achieve this with a comparative approach that includes several organisms.”

Tomopteris picture by Uwe Kilis.
Annelid phylogeny from reference 3.
Ancestral reconstruction adapted from reference 3

1 Gould, SJ (2001). A Tree Grows in Paris: Lamarck’s Division of Worms and Revision of Nature, The Lying Stones of Marrakech
2. FAUCHALD, K., & ROUSE, G. (1997). Polychaete systematics: Past and present Zoologica Scripta, 26 (2), 71-138 DOI: 10.1111/j.1463-6409.1997.tb00411.x
3. Torsten H. Struck, Christiane Paul, Natascha Hill, Stefanie Hartmann, Christoph Hösel (2010). Phylogenomic analyses unravel annelid evolution Nature

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