Neural Nets Different Individuals: Its Own Germ Rondoni), Buffy Tuft-Eared Marmoset Cells As Well As Those of Its Sibling
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Current Biology Magazine an individual animal may contain bare-ear marmoset (Mico leucippe), Primer reproduction-competent germ cells black-crowned dwarf marmoset (Mico in its gonads from two genetically humilis), Rondon’s marmoset (Mico Neural nets different individuals: its own germ rondoni), buffy tuft-eared marmoset cells as well as those of its sibling. (Callithrix aurita) and black-headed Hence, their offspring may not marmoset (Callithrix nigriceps) are at Andreas Hejnol and Fabian Rentzsch be the genetic descendant of the vulnerable status in the International physiological parents. Union for Conservation of Nature “The nerve-net of the lower animals (IUCN) red list of threatened species contains the germ out of which has Does chimerism affect parental (http://www.iucnredlist.org/search). grown the central nervous systems of care? Chimerism has been noted to The buffy-headed marmoset (Callithrix the higher forms.” affect parental care especially male fl aviceps) is listed as an endangered — G.H. Parker: The Elementary parental care. It has been observed species by IUCN. Habitat destruction Nervous System, 1919 that fathers provide signifi cantly due to human encroachment as higher care to chimeric infants than well as the pet trade are among the Although modern evolutionary biology non-chimeric infants. major threats for extinction of these has abandoned the use of ‘lower’ or marmoset species. ‘higher’ for animals, the quote of G.H. Baby marmosets benefi t from male Parker captures quite well the current parental and alloparental care, Where I can fi nd out more? understanding of the nerve net as the what do genetics say? Very recently, Aeckerle, N., Drummer, C., Debowski, K., evolutionarily oldest organization of Viebahn, C., and Behr, R. (2015). Primordial a novel variant form of the so-called germ cell development in the marmoset the nervous system, the major organ love hormone, oxytocin, has been monkey as revealed by pluripotency factor system responsible for processing expression: suggestion of a novel model of reported in marmosets and some embryonic germ cell translocation. Mol. Hum. information and coordinating animal other close relatives. Interestingly, this Reprod. 21, 66–80. behaviour. The degree of complexity variant of oxytocin showed a clear Eng, C.M., Ward, S.R., Vinyard, C.J., and of a nervous system — in particular Taylor, A.B. (2009). The morphology of the correlation with litter size. Therefore, masticatory apparatus facilitates muscle force its organization into substructures it is believed that this variant form production at wide jaw gapes in tree-gouging such as brains and nerve cords — common marmosets (Callithrix jacchus). J. of oxytocin might be responsible for Exp. Biol. 212, 4040–4055. shows fascinating variations between male parental and alloparental care of Fereydouni, B., Drummer, C., Aeckerle, N., animals. Even within an individual, marmoset babies. Schlatt, S., and Behr, R. (2014). The neonatal the nervous system can show parallel marmoset monkey ovary is very primitive exhibiting many oogonia. Reprod. Camb. Engl. existing types of organizations that are How did the tiny marmosets evolve 148, 237–247. only partially connected, illustrated by Ford, S.M., Porter, L.M., and Davis, L.C. eds. from a larger bodied ancestor? In (2009). The Smallest Anthropoids (Boston, MA: the well-known central and peripheral contrast to other primates, marmosets Springer US). Available at: http://link.springer. nervous system. In general, the and their tamarin relatives have com/10.1007/978-1-4419-0293-1. architecture of the nervous system Mustoe, A.C., Cavanaugh, J., Harnisch, A.M., undergone a secondary decrease in Thompson, B.E., and French, J.A. (2015). Do is adapted to the specifi c needs and body size from a larger platyrrhine marmosets care to share? Oxytocin treatment lifestyle of the individual species. How reduces prosocial behavior toward strangers. ancestor. The marmoset genome Horm. Behav. 71, 83–90. these diverse and complex nervous suggested this may be due to positive Ross, C.N., French, J.A., and Ortí, G. (2007). systems evolved is an ongoing debate selection in fi ve genes related to the Germ-line chimerism and paternal care in among zoologists and evolutionary marmosets (Callithrix kuhlii). Proc. Natl. Acad. growth hormone/insulin-like growth Sci. USA 104, 6278–6282. biologists. factor axis, which have possible roles Rylands, A.B. ed. (1993). Marmosets and The simplest organization of a Tamarins: Systematics, Behaviour, and in body-size control. Furthermore, eight Ecology (Oxford, Oxford University Press). nervous system is commonly referred genes associated with adaptations The Marmoset Genome Sequencing and Analysis to as the nerve net. The term nerve for challenges of small body size were Consortium (2014). The common marmoset net is often used for a mesh-like genome provides insight into primate biology found. These genes are related to and evolution. Nat. Genet. 46, 850–857. nervous system in which signals subunits of the respiratory complex Vargas-Pinilla, P., Paixão-Côrtes, V.R., Paré, P., can be transmitted in any direction. Tovo-Rodrigues, L., Vieira, C.M. de A.G., I, which plays an important role in Xavier, A., Comas, D., Pissinatti, A., Here we use this term only in a energy transduction and hence affects Sinigaglia, M., Rigo, M.M., et al. (2015). morphological and not in a functional metabolic rate and body temperature. Evolutionary pattern in the OXT-OXTR system sense. A basic nerve net consists of in primates: Coevolution and positive selection footprints. Proc. Natl. Acad. Sci. USA 112, an irregular arrangement of neurites Are marmosets endangered? Due to 88–93. from monopolar, bipolar or multipolar Vinyard, C.J., Wall, C.E., Williams, S.H., and its wide distribution and adaptability, Hylander, W.L. (2003). Comparative functional neurons (Figure 1A). The neurites the common marmosets — as well analysis of skull morphology of tree-gouging form a planar sheet that is connected as some other marmoset species — primates. Am. J. Phys. Anthropol. 120, to underlying myocytes or other 153–170. are not in danger of immediate contractile cells. On the opposite extinction. However, many other side, the nerve net is connected to marmoset species have a threatened Stem Cell Biology Unit, German Primate epithelial sensory cells — for example, Center, Leibniz Institute for Primate conservation status. Wied’s black- Research, Kellnerweg 4, D-37077 Göttingen, mechanoreceptors — and can also tufted-ear marmoset (Callithrix kuhlii) Germany. involve neurosecretory cells (Figure is near threatened, while golden-white *E-mail: [email protected] 1B). A nerve net thus can be suffi cient R782 Current Biology 25, R775–R792, September 21, 2015 ©2015 Elsevier Ltd All rights reserved Current Biology Magazine to form the integrative part between A B Sensory cell reception of the environment of an organism and its ability to react to Epidermis changes in these environmental cues. This architecture of a mesh-like Nerve net arrangement seems to be quite Ring versatile, as more or less elaborated musculature nerve nets can be found in most animal taxa, albeit at different scales, constituting either most of Longitudinal musculature an animal’s nervous system (as in cnidarian polyps) or innervating a particular organ or part of it (as in the vertebrate intestine). At the level Figure 1. Schematic drawings of nerve nets. of a whole animal, however, nerve (A) Ectodermal nerve plexus from the cnidarian Rhizostoma (from Hanström 1928, taken from Bozler 1927; with permission from Springer Science and Business Media). Multipolar neurons in blue, bipo- nets in a strict sense — without any lar neurons in grey. (B) Location of the nerve net in an idealized Bilaterian. The neurons of the nerve ganglion-like accumulations of nerve net are in red. Connections to the muscular sheets and sensory cell are shown. Panel B reproduced cells or bundles of neurites — are with permission from Pavans de Ceccatty, M. (1974). Perspect. Biol. Med. 17, 379–391. rarely found. Even in the cnidarian polyp Hydra, which has a classic which there is no proper exchange More detailed studies of the textbook example for a nerve net, but only a tangle of wires’, we nervous system of another some species have a distinct bundle know from molecular studies interesting group of animals, the of neurites that encircles its single that the morphologically rather Xenacoelomorpha, have revealed body opening. uniform neurons in animal nerve a basic organization of the nervous With the aim of discussing the nets in fact belong to different cell system in form of a net (Figures 2 evolution of neural nets, we focus types. Recent studies indicate that and 3). These rather small, mostly here mainly on animals in which nerve differentially expressed molecular marine worms are completely ciliated nets form a major part of the nervous markers — transcription factors and their nervous system is mainly system and that have positions in the as well as neuropeptides and composed of a basiepidermal animal tree of life that are informative neurotransmitters — assign specifi c nerve net. This nerve plexus forms for considerations of how nervous neurons to different identities and a two-dimensional mesh, which is systems have evolved (Figures 2 and 3). functions. connected to intraepidermal sensory It seems reasonable to assume cells and the underlying muscle The phylogenetic distribution of that the fi rst neurons of animals were sheet, composed of longitudinal nerve nets organized in a simple nerve net. and ring muscles. In fact, the For a better understanding of the The emergence of the nerve net is nervous system of Xenoturbella, origin of this ancestral organization thus connected with the evolution which is likely the sister group to of nervous systems, it is important of the neuron. Whether the nerve all remaining xenacoelomorphs, to examine which extant lineages of cell of animals has a single origin, or has negligible condensations and animals have retained a nerve net and possibly originated more than once, provides a textbook example of how it is integrated into the body.