30 June 2009

When did central nervous systems evolve?

ResearchBlogging.org“It has the most primitive form of nervous system of any bilateral animal,” intones the voiceover for the National Geographic video.

The “it” being referred to is an acorn worm, a little known kind of invertebrate that is actually relatively closely related to the vertebrates. Vertebrates belong to the chordate phylum, and acorn worms are hemichordates – literally, “half chordates.” Hemichordates are interesting in studies of chordate evolution (and thus, in a roundabout way, human evolution) because they hint at what features that very early chordates might have had. If a feature is shared by both hemichordates and chordates, that probably means it was present in the common ancestor of both.

One of the most unusual features of chordates is their dorsal nervous system. In most animals, the majority of the nervous system runs along the underside of the animal, but in chordates, it runs along the back. Hemichordates have a proverbial foot in both camps, with some neurons running dorsally and some ventrally. With such a strange organization, you might expect that the nervous system of hemichordates has been studied to death. But surprisingly, you’d be wrong.

This new paper by Nomaksteinsky and colleagues tries to answer a very basic question: do hemichordates have a central nervous system? While older studies agree that there are cords of neurons, they disagree over whether there are neuronal cell bodies in them, which most central nervous systems have.

Ptychodera flavaThe authors looked at Ptychodera flava (pictured). A big advantage that anatomists have now that classical anatomists didn’t is the ability to look for particular molecules using antibody labeling. Nomaksteinsky and colleagues were able to use a suite of labels that bind to molecules are found fairly specifically in particular kinds of neurons.

For instance, they found neuronal cell bodies with the neurochemical serotonin in the periphery, but not in a region called the collar. Taking the results for several different labels together, the overall pattern was not one of neurons sorted around higgledy-piggledy; rather, particular kinds of neurons were found in fairly specific locations, which is consistent with the sort of organization expected in a true central nervous system.

The authors do not venture an opinion as to whether the dorsal or ventral nerve cord in acorn worms is the evolutionary equivalent to the chordate dorsal cord, but clearly detailed anatomical work over development might help sort this out in future. One key point is that a central nervous system is a very old feature in the evolution leading to humans. Another key point is that, as with jellyfish, not to underestimate the complexity of nervous systems among the spineless.

Maybe that National Geographic video should get a new voiceover.

Reference

Nomaksteinsky, M., Röttinger, E., Dufour, H., Chettouh, Z., Lowe, C., Martindale, M., & Brunet, J. (2009). Centralization of the Deuterostome Nervous System Predates Chordates Current Biology DOI: 10.1016/j.cub.2009.05.063

2 comments:

AK said...

I only read the abstract, since I couldn't get through the firewall, and I don't want to be picky, but it's been known since 2003 that "the overall pattern was not one of neurons sorted around higgledy-piggledy;" or at least that "the expression of [twenty two] orthologs of genes that are involved in patterning the chordate central nervous system" are "expressed in the ectoderm [of the hemichordate Saccoglossus kowalevskii] in an anteroposterior arrangement nearly identical to that found in chordates."[1]  (The paper referenced is rather famous, or at least I've seen it referenced in several important books.)

IMO the key word may be found in this sentence (emphasis mine):  "We show here that juvenile and adult enteropneust worms in fact have a bona fide CNS, i.e., dense agglomerations of neurons associated with a neuropil, forming two cords, ventral and dorsal." The concentration of axons into a cord is probably a result of circulatory advances, for animals lacking myelination.  Even the concentration of cell bodies and neuropil into the tubular nerve cord is probably likewise. What matters (IMO) is the distinction between PNS neurons distributed throughout the epidermis, and CNS neurons whose somas are associated with neuropil.

Neuropil is very important, as recent research show that a great deal of calculation takes place in the membranes of the dendrites and glia, which are concentrated in the neuropil.

IMO we should ignore the question of concentration into cords, and consider the following: 

"The 22 expression domains of orthologs of chordate neural patterning genes of S. kowalevskii correspond strikingly to those in chordates, as summarized in figures 7B and 7D. There are differences such as the extent of overlap of edges of domains of otx, en, and gbx and other midlevel genes that are critical for forming boundaries within the chordate brain, but the relative domain locations are nonetheless very similar. This similar topography of domains is most parsimoniously explained by conservation in both lineages of a domain arrangement (a map) already present in the common ancestor, the ancestor of deuterostomes. An alternate explanation of the similar maps as due to the multiple cooption of 22 individual genes into a convergent topology is not likely, though convergence might be possible for a few genes.

At least 14 of the 22 conserved domains have similar locations in one or more protostome groups (Supplemental Table S1). Such similarities are most parsimoniously explained as a conservation of domains from the ancestral bilaterian.
"[1] 

While I agree this (Nomaksteinsky et al.) is very important research, it's inconceivable to me that a common bilaterian ancestor with such a distinct (and conserved) distribution of neural patterning genes would have lacked a system of nerves filling the function of a CNS, even if they had been distributed into a body-wide network.  Rather, I would say the most important aspect is that the "nervous system centralization predates the evolutionary separation of chordate and hemichordate lineages."[2]  Specifically, the evolution of a fully functional dorsal neural tube.

1.  Anteroposterior Patterning in Hemichordates and the Origins of the Chordate Nervous System

2.  Centralization of the Deuterostome Nervous System Predates Chordates abstract only

Zen said...

I appreciate the pickiness. :) Thanks for bringing in some subtlety into an overview that I freely admit was quick and dirty.