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      The insect central complex as model for heterochronic brain development—background, concepts, and tools

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          Abstract

          The adult insect brain is composed of neuropils present in most taxa. However, the relative size, shape, and developmental timing differ between species. This diversity of adult insect brain morphology has been extensively described while the genetic mechanisms of brain development are studied predominantly in Drosophila melanogaster. However, it has remained enigmatic what cellular and genetic mechanisms underlie the evolution of neuropil diversity or heterochronic development. In this perspective paper, we propose a novel approach to study these questions. We suggest using genome editing to mark homologous neural cells in the fly D. melanogaster, the beetle Tribolium castaneum, and the Mediterranean field cricket Gryllus bimaculatus to investigate developmental differences leading to brain diversification. One interesting aspect is the heterochrony observed in central complex development. Ancestrally, the central complex is formed during embryogenesis (as in Gryllus) but in Drosophila, it arises during late larval and metamorphic stages. In Tribolium, it forms partially during embryogenesis. Finally, we present tools for brain research in Tribolium including 3D reconstruction and immunohistochemistry data of first instar brains and the generation of transgenic brain imaging lines. Further, we characterize reporter lines labeling the mushroom bodies and reflecting the expression of the neuroblast marker gene Tc- asense, respectively.

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          The online version of this article (doi:10.1007/s00427-016-0542-7) contains supplementary material, which is available to authorized users.

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          Principles of insect morphology

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            Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria.

            To elucidate the evolutionary origin of nervous system centralization, we investigated the molecular architecture of the trunk nervous system in the annelid Platynereis dumerilii. Annelids belong to Bilateria, an evolutionary lineage of bilateral animals that also includes vertebrates and insects. Comparing nervous system development in annelids to that of other bilaterians could provide valuable information about the common ancestor of all Bilateria. We find that the Platynereis neuroectoderm is subdivided into longitudinal progenitor domains by partially overlapping expression regions of nk and pax genes. These domains match corresponding domains in the vertebrate neural tube and give rise to conserved neural cell types. As in vertebrates, neural patterning genes are sensitive to Bmp signaling. Our data indicate that this mediolateral architecture was present in the last common bilaterian ancestor and thus support a common origin of nervous system centralization in Bilateria.
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              The central complex and the genetic dissection of locomotor behaviour.

              The central complex is one of the most prominent, yet functionally enigmatic structures of the insect brain. Recently, behavioural, neuroanatomical and molecular approaches in Drosophila have joined forces to disclose specific components of higher locomotion control in larvae and adult flies, such as those that guarantee the optimal length and across-body symmetry of strides and an appropriate activity.
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                Author and article information

                Contributors
                +49 551 395426 , gbucher1@uni-goettingen.de
                Journal
                Dev Genes Evol
                Dev. Genes Evol
                Development Genes and Evolution
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                0949-944X
                1432-041X
                7 April 2016
                7 April 2016
                2016
                : 226
                : 209-219
                Affiliations
                [ ]Department of Evolutionary Developmental Genetics, Johann-Friedrich-Blumenbach Institute, GZMB, CNMPB, Georg-August-University Göttingen, Göttingen Campus, Göttingen, Germany
                [ ]Institute of Medical Microbiology, Otto-von-Guericke-University, Magdeburg, Germany
                [ ]Department of Biology, Animal Physiology, Philipps-University, Marburg, Germany
                [ ]Department of Biology, Neurobiology, University of Konstanz, Constance, Germany
                Author notes

                Communicated by Angelika Stollewerk

                Author information
                http://orcid.org/0000-0002-4615-6401
                Article
                542
                10.1007/s00427-016-0542-7
                4896989
                27056385
                4223435a-2a6d-4269-bee6-45007d4e3cc6
                © The Author(s) 2016

                Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 8 February 2016
                : 17 March 2016
                Categories
                Review
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                © Springer-Verlag Berlin Heidelberg 2016

                Developmental biology
                central complex,brain,heterochrony,evolution,tribolium,drosophila
                Developmental biology
                central complex, brain, heterochrony, evolution, tribolium, drosophila

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