Comparison of life-long neurogenic processes in sea spiders and crustaceans - indications for an ancestral adult neurogenic system in Arthropoda?
Developmental Neurobiology
Evolution, Anthropology
Systematics and Morphology (Zoology)
Final Report Abstract
Adult neurogenesis, i.e., the production and integration of neural cells into adult nervous systems, is well known in vertebrates. By comparison, however, this phenomenon remains incompletely documented in most invertebrate groups. This holds also for the most diverse animal lineage Arthropoda, for which detailed data are only available in decapod crustaceans and in some insects. In this project, adult neurogenic processes in sea spiders (Pycnogonida) and crayfish as representatives of decapod crustaceans have been investigated. The project pioneers in obtaining first insights into the gene network governing embryonic and adult neurogenesis in the crayfish brain, which significantly helps to unequivocally identify and characterize the neural precursor cells involved at the molecular level. Among the hitherto studied genes/gene families studied are SoxB, Achaete-Scute homolog and Snail transcription factors, as well as the neuronal determinant Prospero and the neuronal marker Elav. All of these genes are expressed in the embryonic neurogenic gene cascade in characteristic spatio-temporal patterns similar to other crustaceans and insects. Further, only one of them, namely Prospero, appears to be not involved in the late developing adult neurogenic system. Combination of in vivo cell proliferation experiments (using BrdU) with subsequent gene expression studies reveals (partial) colocalization of cell proliferation and neurogenic gene expression, thus providing unambiguous support for the hitherto “only” proliferation-based identification of the neural precursor cells encountered within the adult system. The established procedures are a crucial prerequisite for adoptive transfer experiments aiming to show with molecular markers that neural differentiation of hemocytes, which have been transferred from donor to recipient crayfish, does occur – a highly intriguing instance of trans-differentiation suggested by recent studies. The conducted in vivo cell proliferation studies on sea spiders demonstrate persisting neurogenic processes throughout adult life of these animals. Furthermore, pulse-chase experiments applying two different cell proliferation markers allowed reconstruction of the migration direction of the new-born cells from an apically located neurogenic niche via specific migration streams into the interior of the ganglia. Hence, the project provides first compelling evidence for life-long neurogenic processes in an arthropod group outside of Tetraconata (i.e., crustaceans + insects). Although the crayfish and pycnogonid systems show several striking structural similarities, it is noteworthy that adult neurogenesis in pycnogonids is found in brain and ventral nerve cord, as opposed to the brain only – as is the case in crayfish. Future studies will seek to provide additional insights into the pycnogonid system for even more detailed comparison between both arthropod groups. This will include immunolabeling of neurotransmitters to further specify the type of adultborn cells, as well as gene expression studies as a step towards a “molecular fingerprint” of the involved adult neural precursor cell types. Given the likely phylogenetic position of pycnogonids as basal-most offshoot of the chelicerate lineage and the placement of crayfish well-nested within the mandibulate lineage, the presence of similar ancestral neurogenic systems in the arthropod stem species may be proposed, potentially in a segmental array as found in pycnogonids. Additional comparative studies of potential life-long neurogenic processes in other extant arthropod taxa, especially on myriapods as the sister-group of tetraconates, will help to rigorously test this hypothesis.
Publications
- (2016): “Adult neurogenesis: lessons from crayfish and the elephant in the room.” Brain Behavior and Evolution 87: 146-155
Beltz BS, Brenneis G, Benton JL
(See online at https://doi.org/10.1159/000447084) - (2016): “Pycnogonida (Pantopoda).” Book chapter in Structure and Evolution of Invertebrate Nervous Systems (Eds: Schmidt-Rhaesa A, Harzsch S, Purschke G), Oxford University Press
Brenneis G
- “Life-long production of neural cells in the CNS of sea spiders (Pycnogonida) – evidence for an ancestral system of adult neurogenesis in Arthropoda?” 109th Annual Meeting of the German Zoological Society. 2016. Kiel, Germany
Brenneis G, Scholtz G, Beltz BS
- (2017): “From egg to “no-body”: an overview and revision of developmental pathways in the ancient arthropod lineage Pycnogonida.” Frontiers in Zoology 14: 6
Brenneis G, Bogomolova EV, Arango CP, Krapp F
(See online at https://doi.org/10.1186/s12983-017-0192-2) - “First insights into the gene network underlying embryonic and adult neurogenesis in procambarid crayfish” The Benton Symposium. 2017. Wellesley College, USA
Brenneis G
