Two decades after the discovery of adult‐born neurons in the brains of decapod crustaceans, the deutocerebral proliferative system (DPS) producing these neural lineages has become a model of adult neurogenesis in invertebrates. Studies on crayfish have provided substantial insights into the anatomy, cellular dynamics, and regulation of the DPS. Contrary to traditional thinking, recent evidence suggests that the neurogenic niche in the crayfish DPS lacks self‐renewing stem cells, its cell pool being instead sustained via integration of hemocytes generated by the innate immune system. Here, we investigated the origin, division and migration patterns of the adult‐born neural progenitor (NP) lineages in detail. We show that the niche cell pool is not only replenished by hemocyte integration but also by limited numbers of symmetric cell divisions with some characteristics reminiscent of interkinetic nuclear migration. Once specified in the niche, first generation NPs act as transit‐amplifying intermediate NPs that eventually exit and produce multicellular clones as they move along migratory streams toward target brain areas. Different clones may migrate simultaneously in the streams but occupy separate tracks and show spatio‐temporally flexible division patterns. Based on this, we propose an extended DPS model that emphasizes structural similarities to pseudostratified neuroepithelia in othermore »
- Award ID(s):
- 1755098
- Publication Date:
- NSF-PAR ID:
- 10340503
- Journal Name:
- Frontiers in Physiology
- Volume:
- 13
- ISSN:
- 1664-042X
- Sponsoring Org:
- National Science Foundation
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Abstract -
Decapod crustaceans, like mammals, retain the ability to make new neurons throughout life. In mammals, immune cells are closely associated with stem cells that generate adult-born neurons. In crayfish, evidence suggests that immune cells (hemocytes) originating in the immune system travel to neurogenic regions and transform into neural progenitor cells. This nontraditional immune activity takes place continuously under normal physiological conditions, but little is known under pathological conditions (neurodegeneration). In this study, the immune system and its relationship with neurogenesis were investigated during neurodegeneration (unilateral antennular ablation) in adult crayfish. Our experiments show that after ablation (1) Proliferating cells decrease in neurogenic areas of the adult crayfish brain; (2) The immune response, but not neurogenesis, is ablation-side dependent; (3) Inducible nitric oxide synthase (iNOS) plays a crucial role in the neurogenic niche containing neural progenitors during the immune response; (4) Brain areas targeted by antennular projections respond acutely (15 min) to the lesion, increasing the number of local immune cells; (5) Immune cells are recruited to the area surrounding the ipsilateral neurogenic niche; and (6) The vasculature in the niche responds acutely by dilation and possibly also neovascularization. We conclude that immune cells are important in both neurodegeneration and neurogenesismore »
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Changes in ambient temperature affect all biological processes. However, these effects are process specific and often vary non-linearly. It is thus a non-trivial problem for neuronal circuits to maintain coordinated, functional output across a range of temperatures. The cardiac nervous systems in two species of decapod crustaceans, Homarus americanus and Cancer borealis , can maintain function across a wide but physiologically relevant temperature range. However, the processes that underlie temperature resilience in neuronal circuits and muscle systems are not fully understood. Here, we demonstrate that the non-isolated cardiac nervous system (i.e., the whole heart: neurons, effector organs, intrinsic feedback systems) in the American lobster, H. americanus , is more sensitive to warm temperatures than the isolated cardiac ganglion (CG) that controls the heartbeat. This was surprising as modulatory processes known to stabilize the output from the CG are absent when the ganglion is isolated. One source of inhibitory feedback in the intact cardiac neuromuscular system is nitric oxide (NO), which is released in response to heart contractions. We hypothesized that the greater temperature tolerance observed in the isolated CG is due to the absence of NO feedback. Here, we demonstrate that applying an NO donor to the isolated CG reducesmore »
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Abstract Nervous system development has been intensely studied in insects (especially
Drosophila melanogaster ), providing detailed insights into the genetic regulatory network governing the formation and maintenance of the neural stem cells (neuroblasts) and the differentiation of their progeny. Despite notable advances over the last two decades, neurogenesis in other arthropod groups remains by comparison less well understood, hampering finer resolution of evolutionary cell type transformations and changes in the genetic regulatory network in some branches of the arthropod tree of life. Although the neurogenic cellular machinery in malacostracan crustaceans is well described morphologically, its genetic molecular characterization is pending. To address this, we established an in situ hybridization protocol for the crayfishProcambarus virginalis and studied embryonic expression patterns of a suite of key genes, encompassing threeSoxB group transcription factors, twoachaete –scute homologs, aSnail family member, the differentiation determinantsProspero andBrain tumor , and the neuron markerElav . We document cell type expression patterns with notable similarities to insects and branchiopod crustaceans, lending further support to the homology of hexapod–crustacean neuroblasts and their cell lineages. Remarkably, in the crayfish head region, cell emigration from the neuroectoderm coupled with gene expression data points to a neuroblast‐independent initial phase of brain neurogenesis. Further,SoxB group expression patterns suggest an involvement ofDichaete in segmentation, in concordance withmore » -
Synopsis Understanding the processes that shaped the distribution of species richness across the Tree of Life is a central macroevolutionary research agenda. Major ecological innovations, including transitions between habitats, may help to explain the striking asymmetries of diversity that are often observed between sister clades. Here, we test the impact of such transitions on speciation rates across decapod crustaceans, modeling diversification dynamics within a phylogenetic framework. Our results show that, while terrestrial lineages have higher speciation rates than either marine or freshwater lineages, there is no difference between mean speciation rates in marine and freshwater lineages across Decapoda. Partitioning our data by infraorder reveals that those clades with habitat heterogeneity have higher speciation rates in freshwater and terrestrial lineages, with freshwater rates up to 1.5 times faster than marine rates, and terrestrial rates approximately four times faster. This averaging out of marine and freshwater speciation rates results from the varying contributions of different clades to average speciation rates. However, with the exception of Caridea, we find no evidence for any causal relationship between habitat and speciation rate. Our results demonstrate that while statistical generalizations about ecological traits and evolutionary rates are valuable, there are many exceptions. Hence, while freshwater andmore »