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Animal Evolution: Looking for the First Nervous System

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Animal Evolution: Looking for the First Nervous System Dispatch R655 cellular or symbiotic functions, cannot genome reduction in the symbiont, 10. Nakabachi, A., Ishida, K., Hongoh, Y., Ohkuma, M., and Miyagishima, S. (2014). be lost without harmful or fatal results. HGT from various sources to the host Aphid gene of bacterial origin encodes a But these genes can be replaced, genome to maintain symbiont function, protein transported to an obligate and perhaps ever more easily as and now the targeting of protein endosymbiont. Curr. Biol. 24, R640–R641. 11. Moran, N.A., and Jarvik, T. (2010). Lateral the interaction networks of the products from host to symbiont has transfer of genes from fungi underlies endosymbiont reduce in complexity, even been found [4,10]. These make carotenoid production in aphids. Science 328, 624–627. thus reducing pressures on proteins clean separation of endosymbiont from 12. Jorgenson, M.A., Chen, Y., Yahashiri, A., to co-evolve. In a sense, when genes organelle more difficult to see, Popham, D.L., and Weiss, D.S. (2014). The are transferred from symbiont or prompting us not to look for the point bacterial septal ring protein RlpA is a lytic transglycosylase that contributes to rod organelle to the host nuclear genome when a symbiont ‘becomes’ an shape and daughter cell separation in and their proteins targeted back, this is organelle, but rather to ask, ‘Is there Pseudomonas aeruginosa. Mol. Microbiol. 93, 113–128. a compensatory change [4,9,14,17]. really anything so special about 13. Acuna, R., Padilla, B.E., Florez-Ramos, C.P., But other compensatory transfers that organelles?’ Rubio, J.D., Herrera, J.C., Benavides, P., affect a symbiont or organelle can also Lee, S.J., Yeats, T.H., Egan, A.N., Doyle, J.J., et al. (2012). Adaptive horizontal transfer of a involve genes transferred from References 1. Mu¨ ller, M., Mentel, M., van Hellemond, J.J., bacterial gene to an invasive insect pest of unrelated donors [8,9,18]. In the case of Henze, K., Woehle, C., Gould, S.B., Yu, R.-Y., coffee. Proc. Natl. Acad. Sci. USA 109, organelles the identity of potential van der Giezen, M., Tielens, A.G.M., and 4197–4202. Martin, W.F. (2012). Biochemistry and evolution 14. Timmis, J.N., Ayliffe, M.A., Huang, C.Y., and donors of transferred genes is not of anaerobic energy metabolism in eukaryotes. Martin, W. (2004). Endosymbiotic gene transfer: always clear, but in insects gene Microbiol. Mol. Biol. Rev. 76, 444–495. organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5, 123–135. donors often appear to be pathogens, 2. Gray, M.W. (2014). The pre-endosymbiont hypothesis: a new perspective on the origin 15. Keeling, P.J. (2013). The number, speed, and specifically reproductive manipulators and evolution of mitochondria. Cold Spring impact of plastid endosymbioses in eukaryotic [7–9]. These bacteria skew the number Harb. Perspect. Biol. 6, a016097–a016097. evolution. Annu. Rev. Plant Biol. 64, 583–607. 3. Keeling, P.J., and Archibald, J.M. (2008). 16. Larkum, A.W.D., Lockhart, P.J., and Howe, C.J. and sex ratio of offspring in infected Organelle evolution: what’s in a name? Curr. (2007). Shopping for plastids. Trends Plant Sci. populations in different ways, and often Biol. 18, R345–R347. 12, 189–195. 17. Keeling, P.J., and Palmer, J.D. (2008). reside in insect germ line cells. The 4. Nowack, E.C.M., and Grossman, A.R. (2012). Trafficking of protein into the recently Horizontal gene transfer in eukaryotic evolution. frequency of transfer from these established photosynthetic organelles of Nat. Rev. Genet. 9, 605–618. groups is therefore probably due to Paulinella chromatophora. Proc. Natl. Acad. 18. Stairs, C.W., Eme, L., Brown, M.W., Mutsaers, C., Sci. USA 109, 5340–5345. Susko, E., Dellaire, G., Soanes, D.M., van der simple chance: their cell biology 5. Cavalier-Smith, T., and Lee, J.J. (1985). Giezen, M., and Roger, A.J. (2014). A SUF includes infection of the germ line, Protozoa as hosts for endosymbioses and Fe-S cluster biogenesis system in the mitochondrion-related organelles of the which provides ample opportunity for the conversion of symbionts into organelles. J. Protozool. 32, 376–379. anaerobic protist Pygsuia. Curr. Biol. 24, gene transfer that can be passed to 6. Martin, W. (2010). Evolutionary origins of 1176–1186. future generations. The same is true of metabolic compartmentalization in eukaryotes. 19. Theissen, U., and Martin, W. (2006). The Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, difference between organelles and single-celled eukaryotes (protists), 847–855. endosymbionts. Curr. Biol. 16, R1016–R1017. where all newly acquired genes are taken 7. Nikoh, N., McCutcheon, J.P., Kudo, T., 20. Bhattacharya, D., and Archibald, J.M. (2006). The difference between organelles and into the germline automatically [17]. Miyagishima, S.Y., Moran, N.A., and Nakabachi, A. (2010). Bacterial genes in the endosymbionts - response to Theissen and As the prevalence of intimate and aphid genome: absence of functional gene Martin. Curr. Biol. 16, R1017–R1018. stable endosymbiotic associations transfer from Buchnera to its host. PloS Genet. 6, e1000827. 1Division of Biological Sciences, University of has become more clear, the degree 8. Husnik, F., Nikoh, N., Koga, R., Ross, L., to which host and endosymbiont Duncan, R.P., Fujie, M., Tanaka, M., Satoh, N., Montana, Missoula, MT 59801, USA. 2 are integrated has been revealed to Bachtrog, D., Wilson, A.C.C., et al. (2013). Canadian Institute for Advanced Research, Horizontal gene transfer from diverse bacteria Botany Department, University of British be far less discontinuous than to an insect genome enables a tripartite nested Columbia, 3529-6270 University Boulevard, previously believed. Accordingly, the mealybug symbiosis. Cell 153, 1567–1578. Vancouver, BC, V6T 1Z4, Canada. 9. Sloan, D.B., Nakabachi, A., Richards, S., Qu, J., characteristics separating ‘symbiont’ Murali, S.C., Gibbs, R.A., and Moran, N.A. E-mail: [email protected], from ‘organelle’ have become less (2014). Parallel histories of horizontal gene [email protected] clear [3,4,19,20]. There is an transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. understandable desire to draw a Mol. Biol. Evol. 31, 857–871. http://dx.doi.org/10.1016/j.cub.2014.05.073 distinct line between the two for simplicity, but first we must ask, does this line exist? If so, it is best drawn by evolutionary and mechanistic distinctions, not by perceived Animal Evolution: Looking for the differences born of tradition, definitions, or historical contingency. First Nervous System Organelles were discovered first, have been studied for decades, and their bacterial origins dominated the The human brain is easily the most baffling bit of biology on the planet. How did discussion about endosymbiosis and the nervous system evolve? What came first: neurons or synaptic proteins? A new Trichoplax evolution for many years. They enjoy paper studying the pancake-shaped suggests it was not the neurons. a status apart from other biological entities: derived from bacteria, but Erik M. Jorgensen rise of complex, unfamiliar looking so different as to be given their own multicellular marine life forms, ended name. But the list of their ‘unique’ Something bad must have happened with an extinction that wiped out most characteristics is shrinking: stable around 542 million years ago: the of these creatures. Unfortunately, this endosymbioses promote extensive Ediacaran period, which had seen the event obscured our view on the Current Biology Vol 24 No 14 R656 evolution of the first nervous systems. speck of an animal. It was originally has a protein closely related to the We know that some Ediacaran discovered in 1883 crawling on the synaptic synaptotagmin and thus animals must have had nervous glass of a fish tank containing perhaps only Trichoplax will exhibit systems, as they left tracks and seawater. Its simple circular body plan, true synaptic behavior, i.e. tunnels, and thus could move in an only 1 mm in diameter, was described calcium-activated vesicle fusion. active, organized fashion. But at the time but the organism was largely Surprisingly, only ctenophores because they left no directly forgotten thereafter until its possess panexin gap-junction recognizable successors, we can’t rediscovery in the 1970s. proteins, which allow rapid infer how those first nervous systems Can this dog do tricks? Sure, the communication between cells by direct arose. The Cambrian explosion that essential ones: the pancake that is electrical conductance. All three phyla, followed gave rise to the familiar Trichoplax can glide along a surface, placozoa, porifera and ctenophora, animal phyla. Examination of their which implies coordination of beating lack pentameric ligand-gated ion genomes suggests that the nervous cilia. Moreover, when it comes across a channels altogether, and therefore system arose once, in a perfect state, patch of algae, it pauses over the food show no evidence of fast as all of the key molecular components source, presumably digesting them by neurotransmission by acetylcholine, of the nervous system are conserved secreting enzymes onto its ventral serotonin, dopamine, GABA or glycine. in the genomes of animals: the ion surface, for absorption via microvilli. It is possible that variants will channels used by excitable cells, Trichoplax also changes shape from a eventually be found when these draft an extensive repertoire of circular to an elongated disk genome sequences are fully neurotransmitters and synaptic sometimes. So is there evidence of a assembled. But the lack of most machinery. In fact at the level of nervous system underlying these classical neurotransmitter receptors neurotransmitter systems, the human behaviors? Now, through the work of is further supported by a lack of nervous system looks like a simplified Smith et al. [1], a full understanding of the vesicular transporters for version of the primordial nervous the anatomy of the w50,000 cells in acetylcholine, monoamines, GABA, system.
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