Christine Martin1, Henry Jahn2, Mercedes Klein2, Jörg U Hammel3, Paul A Stevenson4, Uwe Homberg5,6, Georg Mayer7. 1. Department of Zoology, Institute of Biology, University of Kassel, 34132, Kassel, Germany. christine.martin@uni-kassel.de. 2. Department of Zoology, Institute of Biology, University of Kassel, 34132, Kassel, Germany. 3. Institute of Materials Physics, Helmholtz-Zentrum hereon, 21502, Geesthacht, Germany. 4. Physiology of Animals and Behaviour, Institute of Biology, University of Leipzig, 04103, Leipzig, Germany. 5. Department of Biology, Animal Physiology, Philipps-Universität Marburg, 35043, Marburg, Germany. 6. Center for Mind, Brain and Behavior (CMBB), University of Marburg and Justus Liebig University Giessen, 35032, Marburg, Germany. 7. Department of Zoology, Institute of Biology, University of Kassel, 34132, Kassel, Germany. georg.mayer@uni-kassel.de.
Abstract
BACKGROUND: The evolution of the brain and its major neuropils in Panarthropoda (comprising Arthropoda, Tardigrada and Onychophora) remains enigmatic. As one of the closest relatives of arthropods, onychophorans are regarded as indispensable for a broad understanding of the evolution of panarthropod organ systems, including the brain, whose anatomical and functional organisation is often used to gain insights into evolutionary relations. However, while numerous recent studies have clarified the organisation of many arthropod nervous systems, a detailed investigation of the onychophoran brain with current state-of-the-art approaches is lacking, and further inconsistencies in nomenclature and interpretation hamper its understanding. To clarify the origins and homology of cerebral structures across panarthropods, we analysed the brain architecture in the onychophoran Euperipatoides rowelli by combining X-ray micro-computed tomography, histology, immunohistochemistry, confocal microscopy, and three-dimensional reconstruction. RESULTS: Here, we use this detailed information to generate a consistent glossary for neuroanatomical studies of Onychophora. In addition, we report novel cerebral structures, provide novel details on previously known brain areas, and characterise further structures and neuropils in order to improve the reproducibility of neuroanatomical observations. Our findings support homology of mushroom bodies and central bodies in onychophorans and arthropods. Their antennal nerve cords and olfactory lobes most likely evolved independently. In contrast to previous reports, we found no evidence for second-order visual neuropils, or a frontal ganglion in the velvet worm brain. CONCLUSION: We imaged the velvet worm nervous system at an unprecedented level of detail and compiled a comprehensive glossary of known and previously uncharacterised neuroanatomical structures to provide an in-depth characterisation of the onychophoran brain architecture. We expect that our data will improve the reproducibility and comparability of future neuroanatomical studies.
BACKGROUND: The evolution of the brain and its major neuropils in Panarthropoda (comprising Arthropoda, Tardigrada and Onychophora) remains enigmatic. As one of the closest relatives of arthropods, onychophorans are regarded as indispensable for a broad understanding of the evolution of panarthropod organ systems, including the brain, whose anatomical and functional organisation is often used to gain insights into evolutionary relations. However, while numerous recent studies have clarified the organisation of many arthropod nervous systems, a detailed investigation of the onychophoran brain with current state-of-the-art approaches is lacking, and further inconsistencies in nomenclature and interpretation hamper its understanding. To clarify the origins and homology of cerebral structures across panarthropods, we analysed the brain architecture in the onychophoran Euperipatoides rowelli by combining X-ray micro-computed tomography, histology, immunohistochemistry, confocal microscopy, and three-dimensional reconstruction. RESULTS: Here, we use this detailed information to generate a consistent glossary for neuroanatomical studies of Onychophora. In addition, we report novel cerebral structures, provide novel details on previously known brain areas, and characterise further structures and neuropils in order to improve the reproducibility of neuroanatomical observations. Our findings support homology of mushroom bodies and central bodies in onychophorans and arthropods. Their antennal nerve cords and olfactory lobes most likely evolved independently. In contrast to previous reports, we found no evidence for second-order visual neuropils, or a frontal ganglion in the velvet worm brain. CONCLUSION: We imaged the velvet worm nervous system at an unprecedented level of detail and compiled a comprehensive glossary of known and previously uncharacterised neuroanatomical structures to provide an in-depth characterisation of the onychophoran brain architecture. We expect that our data will improve the reproducibility and comparability of future neuroanatomical studies.