Analysis of the draft genome of a comb jelly and of gene-transcription profiles from ten other ctenophores hints at an independent evolutionary origin for the nervous systems of these organisms. See Article p.109
The ability of animals to respond rapidly and appropriately to changes in their environment is due to the presence of a nervous system consisting of up to billions of nerve cells. In this issue, Moroz et al.1 (page 109) present the genome of the comb jelly Pleurobrachia bachei, otherwise known as the sea gooseberry (Fig. 1a). Following a detailed examination of the developmental genes, structural genes and signalling molecules that are necessary for the set-up and function of nervous systems in other animals, the authors come to a radical conclusion: that the nervous system of comb jellies might have evolved independently of that of other animals.
Only two groups of animals do without a nervous system: sponges, which are simple animals attached to the sea bottom that do not show complex behaviours, and the placozoans, animals comprised of two flat sheets of cells that creep along the ocean floor absorbing nutrients. The simplicity of sponges and placozoans has led generations of zoologists to conclude that they are ancient animal groups, and may look very like the first multicellular animals that emerged on the planet more than 500 million years ago.
Over the past decade, however, extensive comparisons of protein and DNA sequences have led to surprising rearrangements at the base of the animal tree of life. In fact, it seems that previous assumptions about the origin of multicellular animals may be wrong, and that a group of gelatinous creatures, the ctenophores, collectively referred to as comb jellies, could be the first group to have branched off from the animal tree of life2. Further evidence for this reappraisal came from a whole-genome analysis of another comb jelly, Mnemiopsis leidyi, which indicated that ctenophores lack many molecular characteristics that are essential for all other animals3. For example, they do not have microRNAs, important controllers of gene expression in other animals4, or Hox genes, which encode transcription factors that are essential for patterning the body axis5.
So what are these mysterious animals that have turned the table on textbook ideas? Comb jellies are fabulous marine predators that propel themselves through the water column by means of blocks of cilia — the shimmering combs that give them their name. They catch their prey using innervated tentacles seamed with sticky cells called colloblasts and swallow it through their mouth, which opens into a sac-like gut. They have a nerve net with regional specializations, such as a sensory organ located at one pole of the body that is used for light reception and gravity sensing6. Notably, sponges and placozoans lack all of these features, so the proposal that the jellies evolved first seems odd.
However, Moroz et al. agree with the idea of ctenophores being one of the two first animal lineages (Fig. 1b). Their analysis, which alongside the Pleurobrachia genome includes gene-transcription profiles from ten other ctenophores, finds that many building blocks essential for nervous-system development in other animals are also missing from comb jellies. Furthermore, some molecules that are neuron-specific in other animals are present in the sea-gooseberry genome but, surprisingly, are expressed not in nerve cells but in other tissues. And of the 10 major common neurotransmitter molecules used by animals, Pleurobrachia employs only two (glutamate and its antagonist GABA) in the operation of its nervous system. On the basis of these characteristics, it would seem that an animal with such a small number of traditionally neural proteins would have a simple nerve net, as opposed to a central nervous system, and would not show any complex behaviour. On the contrary, however, comb jellies perform complex actions such as predation and horizontal diurnal migrations in the water column, so they must use different molecules in their nervous system.
The phylogenetic position of comb jellies at the base of the animal tree of life and the findings of Moroz and co-workers suggest a fascinating scenario — that comb jellies evolved a nervous system that is unrelated to that of other animals. Heretical hypotheses such as this strike a blow against the anthropocentric view that complex animals emerged gradually along one lineage only, culminating in humans, and that complex organ systems did not evolve twice. But such views do not reflect how evolution really works. Evolution does not follow a chain of events in which one lineage progresses continuously towards complexity while other branches stagnate7. Instead, it is an ongoing process in all lineages. When the animal tree branched more than 500 million years ago, one lineage gave rise to ctenophores and the other to all remaining animals alive today, and it seems that the two lineages independently evolved a rapid internal communication system.
However, the last word has not yet been said on this issue, because the branching sequence of the earliest animal groups is still hotly debated. Some researchers have expressed doubt that ctenophores are at the base, and claim that the lack of many genes in comb jellies can be explained by massive gene loss that mimics a simple genome8.
Regardless of where ctenophores finally end up on the tree, the development and evolution of the complex nervous system of these creatures will be an enigma for some time. If it turns out that comb jellies are not at the base of the tree and that animal neurons indeed originated only once, someone must figure out why the molecular biology underlying the comb-jelly nervous system is so different from that of other animals.
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