A map of brain neuropils and fiber systems in the ant Cardiocondyla obscurior

A wide spectrum of occupied ecological niches and spectacular morphological adaptations make social insects a prime object for comparative neuroanatomical studies. Eusocial insects have evolved complex societies based on caste polyphenism. A diverse behavioral repertoire of morphologically distinct castes of the same species requires a high degree of plasticity in the central nervous system. We have analyzed the central brain neuropils and fiber tract systems of the worker of the ant Cardiocondyla obscurior, a model for the study of social traits. Our analysis is based on whole mount preparations of adult brains labeled with an antibody against Drosophila-Synapsin, which cross-reacts strongly with synapses in Cardiocondyla. Neuropil compartments stand out as domains with a certain texture and intensity of the anti-Synapsin signal. By contrast, fiber tracts, which are composed of bundles of axons accompanied by glia and are devoid of synapses, appear as channels or sheaths with low anti-Synapsin signal. We have generated a digital 3D atlas of the Cardiocondyla brain neuropil. The atlas provides a reference for future studies of brain polymorphisms in distinct castes, brain development or localization of neurotransmitter systems.

[1]  J. Traniello,et al.  Division of Labor in the Hyperdiverse Ant Genus Pheidole Is Associated with Distinct Subcaste- and Age-Related Patterns of Worker Brain Organization , 2012, PloS one.

[2]  R. Menzel,et al.  Learning and memory in honeybees: from behavior to neural substrates. , 1996, Annual review of neuroscience.

[3]  L. Luo,et al.  Representation of the Glomerular Olfactory Map in the Drosophila Brain , 2002, Cell.

[4]  J. Oettler,et al.  THE EVOLUTION OF ALTERNATIVE REPRODUCTIVE TACTICS IN MALE CARDIOCONDYLA ANTS , 2010, Evolution; international journal of organic evolution.

[5]  B. Hansson,et al.  Projection patterns of gustatory neurons in the suboesophageal ganglion and tritocerebrum of mosquitoes , 2005, The Journal of comparative neurology.

[6]  S. O’Donnell,et al.  Brain organization mirrors caste differences, colony founding and nest architecture in paper wasps (Hymenoptera: Vespidae) , 2009, Proceedings of the Royal Society B: Biological Sciences.

[7]  Irina Sinakevitch,et al.  Ground plan of the insect mushroom body: Functional and evolutionary implications , 2009, The Journal of comparative neurology.

[8]  L. Luo,et al.  Comprehensive Maps of Drosophila Higher Olfactory Centers: Spatially Segregated Fruit and Pheromone Representation , 2007, Cell.

[9]  Joachim Schachtner,et al.  Anisometric brain dimorphism revisited: Implementation of a volumetric 3D standard brain in Manduca sexta , 2009, The Journal of comparative neurology.

[10]  T. Godenschwege,et al.  Invertebrate Synapsins: A Single Gene Codes for Several Isoforms in Drosophila , 1996, The Journal of Neuroscience.

[11]  Uwe Homberg,et al.  Evolution of the central complex in the arthropod brain with respect to the visual system. , 2008, Arthropod structure & development.

[12]  G. Jefferis,et al.  Drosophila Olfaction: The End of Stereotypy? , 2008, Neuron.

[13]  N. Strausfeld.  Organization of the honey bee mushroom body: Representation of the calyx within the vertical and gamma lobes , 2002, The Journal of comparative neurology.

[14]  V. Hartenstein,et al.  Neuroblast lineage-specific origin of the neurons of the Drosophila larval olfactory system. , 2013, Developmental biology.

[15]  S. Farris,et al.  Development and evolution of the insect mushroom bodies: towards the understanding of conserved developmental mechanisms in a higher brain center. , 2003, Arthropod structure & development.

[16]  Gene E. Robinson,et al.  Experience- and Age-Related Outgrowth of Intrinsic Neurons in the Mushroom Bodies of the Adult Worker Honeybee , 2001, The Journal of Neuroscience.

[17]  Julie H. Simpson,et al.  A Systematic Nomenclature for the Insect Brain , 2014, Neuron.

[18]  B. Beltz,et al.  A new look at embryonic development of the visual system in decapod crustaceans: neuropil formation, neurogenesis, and apoptotic cell death. , 1999, Journal of neurobiology.

[19]  Stanley Heinze,et al.  Anatomical basis of sun compass navigation I: The general layout of the monarch butterfly brain , 2012, The Journal of comparative neurology.

[20]  Torsten Rohlfing,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[21]  C. Rieder,et al.  Greatwall kinase , 2004, The Journal of cell biology.

[22]  H. Reichert,et al.  The columnar gene vnd is required for tritocerebral neuromere formation during embryonic brain development of Drosophila , 2006, Development.

[23]  Volker Hartenstein,et al.  Development‐based compartmentalization of the Drosophila central brain , 2010, The Journal of comparative neurology.

[24]  W. Rössler,et al.  Caste-specific postembryonic development of primary and secondary olfactory centers in the female honeybee brain. , 2008, Arthropod structure & development.

[25]  Stanley Heinze,et al.  Anatomical basis of sun compass navigation II: The neuronal composition of the central complex of the monarch butterfly , 2013, The Journal of comparative neurology.

[26]  Wolfgang Rössler,et al.  Organization of the olfactory pathway and odor processing in the antennal lobe of the ant Camponotus floridanus , 2008, The Journal of comparative neurology.

[27]  Linda S. Kuebler,et al.  Distinct antennal lobe phenotypes in the leaf‐cutting ant (Atta vollenweideri) , 2010, The Journal of comparative neurology.

[28]  Nicholas J. Strausfeld,et al.  Arthropod Brains: Evolution, Functional Elegance, and Historical Significance , 2012 .

[29]  Sebastian Kirschner,et al.  Dual olfactory pathway in the honeybee, Apis mellifera , 2006, The Journal of comparative neurology.

[30]  Kei Ito,et al.  Systematic Analysis of Neural Projections Reveals Clonal Composition of the Drosophila Brain , 2013, Current Biology.

[31]  Hans-Christian Hege,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[32]  W. Rössler,et al.  Dual olfactory pathway in Hymenoptera: evolutionary insights from comparative studies. , 2011, Arthropod structure & development.

[33]  R. Menzel,et al.  Neural plasticity of mushroom body-extrinsic neurons in the honeybee brain , 2005, Journal of Experimental Biology.

[34]  E. Seyfarth,et al.  Peripheral synapses at identifiable mechanosensory neurons in the spider Cupiennius salei : synapsin-like immunoreactivity , 1999, Cell and Tissue Research.

[35]  G. Robinson,et al.  Larval and pupal development of the mushroom bodies in the honey bee, Apis mellifera , 1999, The Journal of comparative neurology.

[36]  Rüdiger Wehner,et al.  Delayed axonal pruning in the ant brain: A study of developmental trajectories , 2009, Developmental neurobiology.

[37]  R. Menzel,et al.  Odour coding is bilaterally symmetrical in the antennal lobes of honeybees (Apis mellifera) , 1998, The European journal of neuroscience.

[38]  C Giovanni Galizia,et al.  Parallel olfactory systems in insects: anatomy and function. , 2010, Annual review of entomology.

[39]  R. Menzel,et al.  Cognitive architecture of a mini-brain: the honeybee , 2001, Trends in Cognitive Sciences.

[40]  R. Menzel,et al.  Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera , 2001, The Journal of comparative neurology.

[41]  J. Heinze,et al.  Proximate mechanisms of male morph determination in the ant Cardiocondyla obscurior , 2006, Evolution & development.

[42]  R. Wehner,et al.  Visual experience and age affect synaptic organization in the mushroom bodies of the desert ant Cataglyphis fortis , 2010, Developmental neurobiology.

[43]  N. Strausfeld,et al.  Development of laminar organization in the mushroom bodies of the cockroach: Kenyon cell proliferation, outgrowth, and maturation , 2001, The Journal of comparative neurology.

[44]  Kei Ito,et al.  Optic Glomeruli and Their Inputs in Drosophila Share an Organizational Ground Pattern with the Antennal Lobes , 2012, The Journal of Neuroscience.

[45]  W. Gronenberg.  Subdivisions of hymenopteran mushroom body calyces by their afferent supply , 2001, The Journal of comparative neurology.

[46]  R. Menzel.  Neurobiology of learning and memory: The honeybee as a model system , 1983, Naturwissenschaften.

[47]  Embryonic development of the pars intercerebralis/central complex of the grasshopper , 1997, Development Genes and Evolution.

[48]  H. Nishino,et al.  Sex‐specific antennal sensory system in the ant Camponotus japonicus: Glomerular organizations of antennal lobes , 2010, The Journal of comparative neurology.

[49]  Arvind Suresh,et al.  Caste and sex specific olfactory glomerular organization and brain architecture in two sympatric ant species Camponotus sericeus and Camponotus compressus (Fabricius, 1798). , 2009, Arthropod structure & development.

[50]  Michael T. Mader,et al.  The Drosophila Standard Brain , 2002, Current Biology.

[51]  Wolfgang Rössler,et al.  Caste- and sex-specific adaptations within the olfactory pathway in the brain of the ant Camponotus floridanus. , 2008, Arthropod structure & development.

[52]  M. Seid,et al.  Socially induced brain development in a facultatively eusocial sweat bee Megalopta genalis (Halictidae) , 2010, Proceedings of the Royal Society B: Biological Sciences.

[53]  M. Hammer,et al.  Neurosecretory cells in the honeybee brain and suboesophageal ganglion show FMRFamide‐like immunoreactivity , 1991, The Journal of comparative neurology.

[54]  S. Fahrbach.  Structure of the mushroom bodies of the insect brain. , 2006, Annual review of entomology.

[55]  Volker Hartenstein,et al.  Postembryonic lineages of the Drosophila brain: II. Identification of lineage projection patterns based on MARCM clones. , 2013, Developmental biology.

[56]  Hanchuan Peng,et al.  Clonal Development and Organization of the Adult Drosophila Central Brain , 2013, Current Biology.

[57]  Mandyam V Srinivasan,et al.  Honeybee Communication: A Signal for Danger , 2010, Current Biology.

[58]  H. L. Nixon,et al.  New Evidence of Communication in the Honeybee Colony , 1952, Nature.

[59]  R. Stocker,et al.  Adult‐like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons , 2002, The Journal of comparative neurology.

[60]  Jan Oettler,et al.  The evolution of alternative reproductive tactics in male cardiocondyla ants. , 2010, Evolution; international journal of organic evolution.

[61]  Randolf Menzel,et al.  Guidance by odors in honeybee navigation , 2013, Journal of Comparative Physiology A.

[62]  W. Gronenberg,et al.  Mushroom body volumes and visual interneurons in ants: Comparison between sexes and castes , 2004, The Journal of comparative neurology.

[63]  R. Menzel,et al.  Three‐dimensional average‐shape atlas of the honeybee brain and its applications , 2005, The Journal of comparative neurology.

[64]  Torsten Rohlfing,et al.  Standardized atlas of the brain of the desert locust, Schistocerca gregaria , 2008, Cell and Tissue Research.

[65]  G. Robinson,et al.  Stimulation of muscarinic receptors mimics experience-dependent plasticity in the honey bee brain. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[66]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[67]  R N Singh,et al.  Neuroarchitecture of the tritocerebrum of Drosophila melanogaster , 1994, The Journal of comparative neurology.

[68]  G. Boyan,et al.  Building the central complex of the grasshopper Schistocerca gregaria: temporal topology organizes the neuroarchitecture of the w, x, y, z tracts , 2005 .

[69]  G. Robinson,et al.  Effects of experience and juvenile hormone on the organization of the mushroom bodies of honey bees. , 1995, Journal of neurobiology.

[70]  M. Hammer,et al.  Behavioral, neural and cellular components underlying olfactory learning in the honeybee , 1996, Journal of Physiology-Paris.

[71]  Qirui Zhang,et al.  Effect of the brain and suboesophageal ganglion on pupal development in Helicoverpa armigera through regulation of FXPRLamide neuropeptides , 2003, Regulatory Peptides.

[72]  Basil el Jundi,et al.  3 D standard brain of the red fl our beetle Tribolium castaneum : a tool to study metamorphic development and adult plasticity , 2014 .

[73]  Jaison J. Omoto,et al.  Postembryonic lineages of the Drosophila brain: I. Development of the lineage-associated fiber tracts. , 2013, Developmental biology.

[74]  J. Hildebrand,et al.  Serotonin-immunoreactive neurons in the median protocerebrum and suboesophageal ganglion of the sphinx moth Manduca sexta , 1989, Cell and Tissue Research.

[75]  N. Strausfeld.  Atlas of an Insect Brain , 1976, Springer Berlin Heidelberg.