Metamorphosis and adult development of the mushroom bodies of the red flour beetle, Tribolium castaneum

Abstract

The insect mushroom bodies play important roles in a number of higher processing functions such as sensory integration, higher level olfactory processing, and spatial and associative learning and memory. These functions have been established through studies in a handful of tractable model systems, of which only the fruit fly Drosophila melanogaster has been readily amenable to genetic manipulations. The red flour beetle Tribolium castaneum has a sequenced genome and has been subject to the development of molecular tools for the ready manipulation of gene expression; however, little is known about the development and organization of the mushroom bodies of this insect. The present account bridges this gap by demonstrating that the organization of the Tribolium mushroom bodies is strikingly like that of the fruit fly, with the significant exception that the timeline of neurogenesis is shifted so that the last population of Kenyon cells is born entirely after adult eclosion. Tribolium Kenyon cells are generated by two large neuroblasts per hemisphere and segregate into an early-born delta lobe subpopulation followed by clear homologs of the Drosophila gamma, alpha'/beta' and alpha/beta lobe subpopulations, with the larval-born cohorts undergoing dendritic reorganization during metamorphosis. BrdU labeling and immunohistochemical staining also reveal that a proportion of individual Tribolium have variable numbers of mushroom body neuroblasts. If heritable, this variation represents a unique opportunity for further studies of the genetic control of brain region size through the control of neuroblast number and cell cycle dynamics.

Novel antennal lobe substructures revealed in the small hive beetle Aethina tumida

“…The Pe, vL and mL can be separated in a densely synapsin stained core region and a less dense stained exterior region. This separation is in accordance to observations in the red flour beetle Tribolium castaneum (Zhao et al, 2008;Binzer et al, 2014) and . It also resembles observations from the African scarabid beetle Pachnoda marginata, where parts of the MB are separated into a central and an annular zone (Larsson et al, 2004).…”

Cytoarchitecture and ultrastructure of neural stem cell niches and neurogenic complexes maintaining adult neurogenesis in the olfactory midbrain of spiny lobsters, Panulirus argus

“…12F). The aNBs of decapod crustaceans and insects appear to be actively proliferating, insofar as they are readily labeled by single BrdU applications (Dufour and Gadenne, 2006;Zhao et al, 2008;Song et al, 2009; this study), whereas NSCs of mammals are labeled only after extended exposure to BrdU and thus are largely quiescent (Doetsch et al, 1999a,b).…”

“…These NBs produce intermediate progenitor cells that act as self-renewing transit-amplifying cells that give rise to GMCs (Bello et al, 2008;Boone and Doe, 2008;Bowman et al, 2008;Izergina et al, 2009;Boyan et al, 2010). Adult neurogenesis in the mushroom bodies of insects is based on continued mitotic activity of a few NBs surviving after larval development (Cayre et al, 1994(Cayre et al, , 1996(Cayre et al, , 2002Gu et al, 1999;Dufour and Gadenne, 2006;Mashaly et al, 2008;Zhao et al, 2008;Ghosal et al, 2009). These adult NBs appear to generate progeny as the canonical embryonic and larval NBs (Dufour and Gadenne, 2006;Zhao et al, 2008); however, the exact cell lineage that they produce has not yet been established.…”

“…In mammalian brains, adult neurogenesis predominantly produces new local interneurons of the olfactory bulb (periglomerular cells and granule cells) and the hippocampal dentate gyrus (granule cells; Kriegstein and Alvarez-Buylla, 2009). In brains of some insect species, adult neurogenesis generates new local interneurons (Kenyon cells) of the mushroom bodies (Cayre et al, 1994(Cayre et al, , 1996Gu et al, 1999;Dufour and Gadenne, 2006;Mashaly et al, 2008;Zhao et al, 2008;Ghosal et al, 2009). The mushroom bodies are large protocerebral neuropils that in most insects receive projections neurons (PNs) from the antennal lobes and thus represent the second stage of the central olfactory pathway; moreover, they are centers for multisensory integration (Strausfeld et al, 2009).…”

“…Adult neurogenesis in the mushroom bodies of insects is based on continued mitotic activity of a few NBs surviving after larval development (Cayre et al, 1994(Cayre et al, , 1996(Cayre et al, , 2002Gu et al, 1999;Dufour and Gadenne, 2006;Mashaly et al, 2008;Zhao et al, 2008;Ghosal et al, 2009). These adult NBs appear to generate progeny as the canonical embryonic and larval NBs (Dufour and Gadenne, 2006;Zhao et al, 2008); however, the exact cell lineage that they produce has not yet been established.In the olfactory deutocerebrum of adult decapod crustaceans, new neurons arise in small proliferation zones of invariant location at the inner (neuropil-facing) surface of the neuronal soma clusters (MC, LC). The proliferating cells in these zones are small and equivalent to GMCs in giving rise to immature neurons through one round of symmetrical cell divisions.…”