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Part I

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EVOLUTIONARY ORIGINS OF NEURONS AND NERVOUS SYSTEMS

The first three chapters address the ancient history of neuron-related molecules and centralized nervous systems. In Chapter 1, Cecilia Conaco and colleagues review earlier findings that many of the molecules found in neuronal synapses, especially within the postsynaptic density, predate the evolution of neurons. The authors then use an analysis of gene coexpression patterns to show that these protosynaptic genes in sponges, which lack proper neurons, form several modules of interacting genes. With the evolution of neurons, these small modules fused into a larger module with a novel function, namely to build synapses. Thus, the research has moved beyond the relatively simple task of homologizing individual genes and begun to trace the evolution of complex and changing gene networks. An interesting, if as yet barely explored, implication of the idea that gene networks can change function is that the homologous gene networks may function in the development or function of nonhomologous structures (Striedter, 1998). This possibility is rarely acknowledged (Tomer et al., 2010).

In Chapter 2, Harold Zakon reviews the evolution of voltage-gated sodium (Na-v) channels. These channels probably descended from voltage-gated calcium channels, which were probably derived from voltage-sensitive potassium channels. Why did Na-v channels become the major driving force behind neuronal action potentials? The answer is probably because Na was plentiful in the ocean, where neurons first evolved, and because Na influx tends not to interfere with intracellular calcium signaling. Once incorporated into neurons, Na-v channels



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Part I EVOLUTIONARY ORIGINS OF NEURONS AND NERVOUS SYSTEMS T he first three chapters address the ancient history of neuron-related molecules and centralized nervous systems. In Chapter 1, Cecilia Conaco and colleagues review earlier findings that many of the molecules found in neuronal synapses, especially within the postsynaptic density, predate the evolution of neurons. The authors then use an analysis of gene coexpression patterns to show that these protosynaptic genes in sponges, which lack proper neurons, form several modules of interacting genes. With the evolution of neurons, these small modules fused into a larger module with a novel function, namely to build synapses. Thus, the research has moved beyond the relatively simple task of homologizing individual genes and begun to trace the evolution of complex and chang- ing gene networks. An interesting, if as yet barely explored, implication of the idea that gene networks can change function is that the homologous gene networks may function in the development or function of nonho- mologous structures (Striedter, 1998). This possibility is rarely acknowl- edged (Tomer et al., 2010). In Chapter 2, Harold Zakon reviews the evolution of voltage-gated sodium (Na-v) channels. These channels probably descended from v ­ oltage-gated calcium channels, which were probably derived from v ­ oltage-sensitive potassium channels. Why did Na-v channels become the major driving force behind neuronal action potentials? The answer is probably because Na was plentiful in the ocean, where neurons first evolved, and because Na influx tends not to interfere with intracellu- lar calcium signaling. Once incorporated into neurons, Na-v channels 1

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2 / Part I were modified in diverse, interesting ways. For example, they evolved regulatory sequences that allowed them to be clustered at the axon initial segment and at Nodes of Ranvier in myelinated axons. Additional modi- fications evolved after the ancestral Na-v gene was duplicated, once near the origin of vertebrates and then again (repeatedly) in several vertebrate lineages. One of the most interesting Na-v modifications is the evolution of resistance to TTX, which typically blocks Na-v channels, in pufferfishes and other species that use TTX to ward off predators. Glenn Northcutt analyzes, in Chapter 3, when and in which lin- eages complex brains evolved. Favoring a cladistic approach, Northcutt concludes that the last common ancestor of all bilaterian animals, liv- ing ­ 00–700 Mya, probably had a diffusely organized nervous system. 6 Cephalic neural ganglia apparently evolved soon thereafter and were retained in many lineages. Truly complex brains evolved even later and did so repeatedly, in mollusks, arthropods, and chordates (including ver- tebrates). This conclusion contrasts sharply with the conclusions of other researchers, who are struck by similarities in developmental gene expres- sion patterns among vertebrate, insect, and annelid nervous systems. To them, these similarities must represent homologies. That is, they argue that similar gene expression patterns must have existed in the last com- mon ancestor of fruit flies, vertebrates, and worms. Northcutt begs to differ, arguing that the expression of these genes in brains is caused by convergent evolution, perhaps by the co-option of gene networks that predate brains. This debate will require more data for a full resolution.