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      Division of labor and brain evolution in insect societies: Neurobiology of extreme specialization in the turtle ant Cephalotes varians

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          Abstract

          Strongly polyphenic social insects provide excellent models to examine the neurobiological basis of division of labor. Turtle ants, Cephalotes varians, have distinct minor worker, soldier, and reproductive (gyne/queen) morphologies associated with their behavioral profiles: small-bodied task-generalist minors lack the phragmotic shield-shaped heads of soldiers, which are specialized to block and guard the nest entrance. Gynes found new colonies and during early stages of colony growth overlap behaviorally with soldiers. Here we describe patterns of brain structure and synaptic organization associated with division of labor in C. varians minor workers, soldiers, and gynes. We quantified brain volumes, determined scaling relationships among brain regions, and quantified the density and size of microglomeruli, synaptic complexes in the mushroom body calyxes important to higher-order processing abilities that may underpin behavioral performance. We found that brain volume was significantly larger in gynes; minor workers and soldiers had similar brain sizes. Consistent with their larger behavioral repertoire, minors had disproportionately larger mushroom bodies than soldiers and gynes. Soldiers and gynes had larger optic lobes, which may be important for flight and navigation in gynes, but serve different functions in soldiers. Microglomeruli were larger and less dense in minor workers; soldiers and gynes did not differ. Correspondence in brain structure despite differences in soldiers and gyne behavior may reflect developmental integration, suggesting that neurobiological metrics not only advance our understanding of brain evolution in social insects, but may also help resolve questions of the origin of novel castes.

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          Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration.

          All fields of neuroscience that employ brain imaging need to communicate their results with reference to anatomical regions. In particular, comparative morphometry and group analysis of functional and physiological data require coregistration of brains to establish correspondences across brain structures. It is well established that linear registration of one brain to another is inadequate for aligning brain structures, so numerous algorithms have emerged to nonlinearly register brains to one another. This study is the largest evaluation of nonlinear deformation algorithms applied to brain image registration ever conducted. Fourteen algorithms from laboratories around the world are evaluated using 8 different error measures. More than 45,000 registrations between 80 manually labeled brains were performed by algorithms including: AIR, ANIMAL, ART, Diffeomorphic Demons, FNIRT, IRTK, JRD-fluid, ROMEO, SICLE, SyN, and four different SPM5 algorithms ("SPM2-type" and regular Normalization, Unified Segmentation, and the DARTEL Toolbox). All of these registrations were preceded by linear registration between the same image pairs using FLIRT. One of the most significant findings of this study is that the relative performances of the registration methods under comparison appear to be little affected by the choice of subject population, labeling protocol, and type of overlap measure. This is important because it suggests that the findings are generalizable to new subject populations that are labeled or evaluated using different labeling protocols. Furthermore, we ranked the 14 methods according to three completely independent analyses (permutation tests, one-way ANOVA tests, and indifference-zone ranking) and derived three almost identical top rankings of the methods. ART, SyN, IRTK, and SPM's DARTEL Toolbox gave the best results according to overlap and distance measures, with ART and SyN delivering the most consistently high accuracy across subjects and label sets. Updates will be published on the http://www.mindboggle.info/papers/ website.
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            Genetic and genomic analyses of the division of labour in insect societies.

            Division of labour--individuals specializing in different activities--features prominently in the spectacular success of the social insects. Until recently, genetic and genomic analyses of division of labour were limited to just a few species. However, research on an ever-increasing number of species has provided new insight, from which we highlight two results. First, heritable influences on division of labour are more pervasive than previously imagined. Second, different forms of division of labour, in lineages in which eusociality has arisen independently, have evolved through changes in the regulation of highly conserved molecular pathways associated with several basic life-history traits, including nutrition, metabolism and reproduction.
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              Sculpting neural circuits by axon and dendrite pruning.

              The assembly of functional neural circuits requires the combined action of progressive and regressive events. Regressive events encompass a variety of inhibitory developmental processes, including axon and dendrite pruning, which facilitate the removal of exuberant neuronal connections. Most axon pruning involves the removal of axons that had already made synaptic connections; thus, axon pruning is tightly associated with synapse elimination. In many instances, these developmental processes are regulated by the interplay between neurons and glial cells that act instructively during neural remodeling. Owing to the importance of axon and dendritic pruning, these remodeling events require precise spatial and temporal control, and this is achieved by a range of distinct molecular mechanisms. Disruption of these mechanisms results in abnormal pruning, which has been linked to brain dysfunction. Therefore, understanding the mechanisms of axon and dendritic pruning will be instrumental in advancing our knowledge of neural disease and mental disorders.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: Writing – review & editing
                Role: Data curationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                27 March 2019
                2019
                : 14
                : 3
                : e0213618
                Affiliations
                [1 ] Department of Biology, Boston University, Boston, MA, United States of America
                [2 ] Ikerbasque, Basque Foundation for Science, Bilbao, Spain
                [3 ] Department of Computer Science and Artificial Intelligence, Basque Country University, San Sebastian, Spain
                [4 ] Donostia International Physics Center (DIPC), San Sebastian, Spain
                [5 ] Departamento de Biología y Geología, Física y Química Inorgánica, Área de Biodiversidad y Conservación, Universidad Rey Juan Carlos, Madrid, Spain
                [6 ] Graduate Program for Neuroscience, Boston University, Boston, MA, United States of America
                Universidade de Sao Paulo Faculdade de Filosofia Ciencias e Letras de Ribeirao Preto, BRAZIL
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-3435-4080
                Article
                PONE-D-18-32494
                10.1371/journal.pone.0213618
                6436684
                30917163
                a1962e29-62c5-4bda-bb8e-9be43b35b532
                © 2019 Gordon et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 12 November 2018
                : 25 February 2019
                Page count
                Figures: 4, Tables: 1, Pages: 16
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: IOS 1354291
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100010665, H2020 Marie Skłodowska-Curie Actions;
                Award ID: 660976
                Award Recipient :
                This research was supported by grant IOS 1354291 from the National Science Foundation to JFAT, a Marie Skłodowska-Curie Individual Fellowship to SA (funded by the European Union's Horizon 2020 research and innovation program under grant agreement No BrainiAnts-Project 660976), and participation of AZ in the Undergraduate Research Opportunities Program at Boston University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
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                Social Sciences
                Sociology
                Social Systems
                Biology and Life Sciences
                Zoology
                Animal Physiology
                Biological Defense Mechanisms
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                Organisms
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                Invertebrates
                Arthropoda
                Insects
                Hymenoptera
                Ants
                Biology and Life Sciences
                Psychology
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                Psychology
                Behavior
                Animal Behavior
                Animal Sociality
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                Developmental Biology
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                All image and spreadsheet files are available from the Zenodo database (accession number 1477421).

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