The bilaterian forebrain: an evolutionary chimaera.
Tosches, M.A. & Arendt, D.
Curr Opin Neurobiol. 2013 Dec;23(6):1080-9. doi: 10.1016/j.conb.2013.09.005. Epub2013 Sep 27.
The insect, annelid and vertebrate forebrains harbour two major centres of output control, a sensory-neurosecretory centre releasing hormones and a primordial locomotor centre that controls the initiation of muscular body movements. In vertebrates, both reside in the hypothalamus. Here, we review recent comparative neurodevelopmental evidence indicating that these centres evolved from separate condensations of neurons on opposite body sides ('apical nervous system' versus 'blastoporal nervous system') and that their developmental specification involved distinct regulatory networks (apical six3 and rx versus mediolateral nk and pax gene-dependent patterning). In bilaterian ancestors, both systems approached each other and became closely intermingled, physically, functionally and developmentally. Our 'chimeric brain hypothesis' sheds new light on the vast success and rapid diversification of bilaterian animals in the Cambrian and revises our understanding of brain architecture.
Profiling by image registration reveals common origin of annelid mushroom bodies and vertebrate pallium.
Tomer, R., Denes, A.S., Tessmar-Raible, K. & Arendt, D.
Cell. 2010 Sep 3;142(5):800-9.
The evolution of the highest-order human brain center, the "pallium" or "cortex," remains enigmatic. To elucidate its origins, we set out to identify related brain parts in phylogenetically distant animals, to then unravel common aspects in cellular composition and molecular architecture. Here, we compare vertebrate pallium development to that of the mushroom bodies, sensory-associative brain centers, in an annelid. Using a newly developed protocol for cellular profiling by image registration (PrImR), we obtain a high-resolution gene expression map for the developing annelid brain. Comparison to the vertebrate pallium reveals that the annelid mushroom bodies develop from similar molecular coordinates within a conserved overall molecular brain topology and that their development involves conserved patterning mechanisms and produces conserved neuron types that existed already in the protostome-deuterostome ancestors. These data indicate deep homology of pallium and mushroom bodies and date back the origin of higher brain centers to prebilaterian times.
Ancient animal microRNAs and the evolution of tissue identity.
Christodoulou, F., Raible, F., Tomer, R., Simakov, O., Trachana, K., Klaus, S., Snyman, H., Hannon, G.J., Bork, P. & Arendt, D.
Nature. 2010 Feb 25;463(7284):1084-8. Epub 2010 Jan 31.
The spectacular escalation in complexity in early bilaterian evolution correlates with a strong increase in the number of microRNAs. To explore the link between the birth of ancient microRNAs and body plan evolution, we set out to determine the ancient sites of activity of conserved bilaterian microRNA families in a comparative approach. We reason that any specific localization shared between protostomes and deuterostomes (the two major superphyla of bilaterian animals) should probably reflect an ancient specificity of that microRNA in their last common ancestor. Here, we investigate the expression of conserved bilaterian microRNAs in Platynereis dumerilii, a protostome retaining ancestral bilaterian features, in Capitella, another marine annelid, in the sea urchin Strongylocentrotus, a deuterostome, and in sea anemone Nematostella, representing an outgroup to the bilaterians. Our comparative data indicate that the oldest known animal microRNA, miR-100, and the related miR-125 and let-7 were initially active in neurosecretory cells located around the mouth. Other sets of ancient microRNAs were first present in locomotor ciliated cells, specific brain centres, or, more broadly, one of four major organ systems: central nervous system, sensory tissue, musculature and gut. These findings reveal that microRNA evolution and the establishment of tissue identities were closely coupled in bilaterian evolution. Also, they outline a minimum set of cell types and tissues that existed in the protostome-deuterostome ancestor.
The evolution of cell types in animals: emerging principles from molecular studies.
Nat Rev Genet. 2008 Nov;9(11):868-82.
Cell types are fundamental units of multicellular life but their evolution is obscure. How did the first cell types emerge and become distinct in animal evolution? What were the sets of cell types that existed at important evolutionary nodes that represent eumetazoan or bilaterian ancestors? How did these ancient cell types diversify further during the evolution of organ systems in the descending evolutionary lines? The recent advent of cell type molecular fingerprinting has yielded initial insights into the evolutionary interrelationships of cell types between remote animal phyla and has allowed us to define some first principles of cell type diversification in animal evolution.