Trends in Ecology & Evolution
OpinionComplex Homology and the Evolution of Nervous Systems
Section snippets
Homology in the Age of Systems Biology
‘Nothing comes from nothing’ – first attributed to Parmenides.
Homology, since Darwin, has meant similarity due to common descent. A character in two different species is homologous if that character was present in the common ancestor and maintained in the two extant species 1, 2, 3. This definition is clear when the character is well defined: two characters either are, or are not, homologous – there is no gradation [4]. However, complex characters like organs and tissues have many component
Nervous Systems and the Animal Tree
The debate about the evolution of animal nervous systems has focused primarily on whether they have a single origin or were independently derived in ctenophores, the comb jellies, and the common ancestor of all other animals 13, 14, 15. The debate was initiated by phylogenetic work suggesting that the ctenophores are the sister group to all other animals 14, 15, 16, a position traditionally ascribed to sponges (Figure 1). Although this placement remains controversial [17], several independent
Morphogenesis
Ontogenetic origin and morphogenetic gene networks are often considered key evidence for homology. It is becoming clear, however, that the relationship between morphogenes and the characters they encode is complex 24, 25. For instance, many morphogenes and signaling pathways associated with animal development were present in the unicellular ancestor of choanoflagellates and animals [7]. Interestingly, the developmental toolkit of ctenophores more closely resembles that of sponges, while that of
Chemical Transmission
Synapses are specialized junctions for the rapid diffusion of chemical signals from a secretory surface on the presynaptic cell to a receptive surface on the postsynaptic cell. A large protein scaffold exists in the postsynaptic cell that is the locus of various modulatory pathways 33, 34. Although synapses are often considered to be highly derived, nervous system-specific junctions, they actually depend on many proteins that are not specific to nervous systems or even to metazoans. For
Electrical Properties
Regulation of ionic gradients by pumps and channels is a ubiquitous property of cellular life forms. Neurons use the potential energy in these transmembrane ionic potentials to drive regenerative traveling electrical signals called action potentials (APs) that carry signals down axons. Many other organisms fire APs for signaling purposes, just as animals do [52].
APs are generated by proteins in the family of voltage-gated ion channels, found across eukaryotes 52, 53. APs in non-animals
Origin of Nervous Systems
Despite the complex phyletic patterns of nervous system-associated genes discussed above, we will put forward a consensus view of early nervous system evolution. For over 300 My, from the common ancestor of animals until the Ediacaran biota, animals were probably very small, perhaps microscopic. Yet they, and even their common ancestor with choanoflagellates, possessed many of the genes that power modern neurons. It seems likely, given their extensive molecular toolkit, that these early animals
Concluding Remarks
Advances in genomic techniques make it possible to pull phenotypes apart into their constituent mechanisms. Putting them back together for evolutionary inference is difficult. In reviewing the recent work on the early evolution of the nervous system, we observe several repeated and interrelated difficulties that will be common to any study on the molecular basis for phenotype evolution. How can molecular data best be used to inform studies of ancestral phenotypes?
Disagreements about the
Acknowledgments
This opinion article emerged from discussions originating from B.J.L.’s thesis committee. B.J.L. is supported by NIH NRSA 1F32GM112504-01A1. H.H.Z. (IOS-1443637) and H.A.H. (IOS-0843712, IOS-1354942, IOS-1501704) are supported by the US National Science Foundation.
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2020, NeuronCitation Excerpt :In BNNs, the architecture of the neural circuitry is optimized by evolution and ranges from largely diffuse nerve nets in jellyfish to series of ganglia in insects to the complex subcortical and cortical structures of mammals (Satterlie, 2011; Striedter, 2005). The detailed comparative mapping of biological neural circuit architectures, learning rules, and objective functions is an active field of research, and we have much to learn from evolution’s solutions across neural systems and across organisms (Nieuwenhuys et al., 1998; Liebeskind et al., 2016). Evolution can pre-train and optimize the synaptic weights of the networks.