Adult neurogenesis in the mushroom bodies of red flour beetles (Tribolium castaneum, Herbst) is influenced by the olfactory environment

Abstract

holometabolous insects, such as the noctuid moth Agrotis ipsilon 58 , as well as several beetle species 59 including the red flour beetle Tribolium castaneum 60. T. castaneum is a member of the largest insect order (Coleoptera) 61,62 and a major pest of stored cereal products 61,63,64. With its annotated genome sequence 26,65-67 , an expanding genetic toolbox 68-70 including strong systemic RNA interference (RNAi) 71-73 , and its relative longevity of up to two years 74 , T. castaneum represents an eligible beetle model for studying adult plasticity. We concentrated on olfaction which is supposed to be a main input into the mushroom bodies of T. castaneum 26 , to answer whether the adult persisting neurogenesis is genetically predetermined and continuation of developmental processes or if it is activity-dependent. Results Identification of newly born cells. To label adult-born cells, we used the 5-ethynyl-2′-desoxyuridine (EdU) method 75,76. With this method, we reliably and exclusively labelled the mushroom body neuroblasts and their progeny, while neurogenesis is not present in other areas of the cerebral ganglion of the red flour beetle (Fig. 1A). The neuroblasts were distinguished from their progeny based on their larger size (Fig. 1B). We confirmed that in T. castaneum, adult-born Kenyon cells usually derive from two neuroblasts (NB) per hemisphere and send their axons into the core of the mushroom body peduncle (PED) and lobes as shown by Zhao and colleagues 60 (Fig. 1C). The neuronal identity of the EdU labelled cells was verified by demonstrating co-localization with the reporter signal (Fig. 1D-D") in the neuron labelling EF1-B-DsRed line 77 , as well as immunohistochemical staining against the glia cell marker reversed polarity 78 resulting in no co-localization (Fig. 1E-E").

A Systematic Review of the Behavioral Responses by Stored-Product Arthropods to Individual or Blends of Microbially Produced Volatile Cues

“…There have been relatively few studies evaluating how mycotoxins, an important health hazard in the food supply in some parts of the world [ 14 ], affect foraging by stored-product arthropods. We have included the few studies that could be found on this in the current study (e.g., [ 16 , 47 , 51 , 74 ]), but the lack of breadth in testing of both different mycotoxins and different arthropod species prevents robust generalization. Nonetheless, we do know from these studies that the mycotoxin deoxynivalenol (DON) apparently reduced the locomotory activity of Tenebrio molitor as well as induced dose-dependent changes in physiological activity of larvae [ 74 ].…”

“…We have included the few studies that could be found on this in the current study (e.g., [ 16 , 47 , 51 , 74 ]), but the lack of breadth in testing of both different mycotoxins and different arthropod species prevents robust generalization. Nonetheless, we do know from these studies that the mycotoxin deoxynivalenol (DON) apparently reduced the locomotory activity of Tenebrio molitor as well as induced dose-dependent changes in physiological activity of larvae [ 74 ]. Other studies have linked insect activity with increased mycotoxin production in grain [ 53 , 57 ], while some studies have shown that there may be tolerance to mycotoxins [ 16 ].…”

A crabs' high‐order brain center resolved as a mushroom body‐like structure

“…Remarkably, mushroom bodies are the unique sites of neurogenesis in the adult protocerebrum of insects (Cayre et al, 2007). Although adult mushroom body neurogenesis appears to be negligible or absent in Drosophila, worker honeybees, and ants (Fahrbach, Strande, & Robinson, 1995; Gronenberg, Heeren, & Hölldobler, 1996; von Trotha, Egger, & Brand, 2009), it was described in the mushroom bodies of both hemimetabolous insects such as crickets (Cayre et al, 1996), praying mantises (Cayre et al, 2007), and cockroaches (Gu, Tsia, Chiang, & Chow, 1999), and holometabolous insects such as beetles, milkweed bugs, and moths (Cayre et al, 2007; Dufour & Gadenne, 2006; Farris, Pettrey, & Daly, 2011; Trebels et al, 2020). Further supporting the proposed neuroanatomical identity of the globuli cells cluster, the protocerebral cluster that incorporated BrdU (Figure 2b) matches the position and shape of the hemiellipsoid body cluster previously described in other brachyurans such as Carcinus maenas (Figure 2b,d in [Hansen & Schmidt, 2001]; Figure 6 in [Schmidt, 1997]), Cancer pagurus (Schmidt & Harzsch, 1999), and Libinia emarginata (Figures 1, 2f, and 3g in [Sullivan & Beltz, 2005a]).…”

“…Remarkably, mushroom bodies are the unique sites of neurogenesis in the adult protocerebrum of insects (Cayre et al, 2007). Although adult mushroom body neurogenesis appears to be negligible or absent in Drosophila, worker honeybees, and ants (Fahrbach, Strande, & Robinson, 1995;Gronenberg, Heeren, & Hölldobler, 1996;von Trotha, Egger, & Brand, 2009), it was described in the mushroom bodies of both hemimetabolous insects such as crickets (Cayre et al, 1996), praying mantises (Cayre et al, 2007), and cockroaches (Gu, Tsia, Chiang, & Chow, 1999), and holometabolous insects such as beetles, milkweed bugs, and moths (Cayre et al, 2007;Dufour & Gadenne, 2006;Farris, Pettrey, & Daly, 2011;Trebels et al, 2020).…”

Mutually Exclusive Expression of Closely Related Odorant-Binding Proteins 9A and 9B in the Antenna of the Red Flour Beetle Tribolium castaneum

“…Antennal EAG responses in mV were recorded with the manufacturer's EAG program (Syntech, version 2.7, EAG 2000). The further analysis was performed as described in Trebels et al [43]. For subsequent EAG recordings, 10-15 DPI beetles were used and for analysis, male and female data were pooled, since no consistent differences were observed (Supplementary Figure S2).…”