Organization of the antennal lobes in the praying mantis (Tenodera aridifolia)

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Animals evolved sensory structures adapted to their lifestyles to maximize their interactions with their environment. In insects, olfaction plays pivotal roles in detecting food and seeking for sexual partners (Hansson, 1999). Olfactory information is initially encoded when olfactory molecules bind olfactory receptor neurons (ORNs) that are housed in olfactory sensilla, which are mainly distributed on the antennal surfaces (Hansson, 1999). The encoded information is mediated through ORN axons that run to the proximal part of the antennae (Nishino, Yoritsune, & Mizunami, 2009b; Nishino, Yoritsune, & Mizunami, 2010) and terminate at the primary processing centers in the central nervous system (antennal lobes [ALs]). In the ALs, the axonal terminals are organized in spherical neuropils, called glomeruli (Hansson, 1999). Axons of ORNs expressing the same type of olfactory receptor are believed to converge in the same glomerulus in insects (Vosshall, 2000; Jefferis, Marin, Watts, & Luo, 2002; Couto, Alenius, & Dickson, 2005; Haupt, Sakurai, Namiki, Kazawa, & Kanzaki, 2010). Thus, the number of glomeruli is more and less related to the number of different types of olfactory receptors expressed on ORNs (but see Goldman et al., 2005). Consequently, knowing the glomerular organization of a given species is important for understanding its olfactory capabilities. Furthermore, in insect species that use olfaction to detect sexual partners, males possess a large number of sex pheromone‐receptive sensilla on the surface of their antennae (Schafer & Sanchez, 1973), which are associated with the presence of macroglomeruli (MG), or a macroglomerular complex, that are significantly greater in size than their homologs in females (Rospars, 1983; Chambille & Rospars, 1985; Strausfeld & Reisenman, 2009; Watanabe, Nishino, Nishikawa, Mizunami, & Yokohari, 2010).
Mantises are insect predators that catch prey based on visual stimuli (Rilling, Mittelstaedt, & Roeder, 1959; Prete, 2004; Yamawaki, 2006), and many studies have focused on their visual systems. However, like other insect species, they also use olfactory cues in their feeding and courtship behaviors. For example, males can determine the mating status of females based on smell (Lelito & Brown, 2008). Furthermore, they can eat pieces of banana and associate this food reward with the odor of banana (Prete, Lum, & Grossman, 1992). Although the morphological features of antennae have been investigated in several species of mantises (Holwell, Barry, & Herberstein, 2007; Allen, Barry, & Holwell, 2012; Carle, Toh, Yamawaki, Watanabe, & Yokohari, 2014a, 2014b), little is known about their olfactory system. In fact, little is known about the olfactory capabilities of insect predators that heavily depend on their visual system to obtain food. Investigating olfaction in predatory insects is crucial to better understand how ecological factors, such as lifestyle (e.g. predation), have influenced the evolution of the olfactory system.
Compared with other insect species, the mantis antennae present a specific sensillar distribution, as observed in T. aridifolia (Carle et al., 2014a) and Sphodromantis lineola (Hurd et al., 2004), which may constitute good model organisms in which to investigate the target glomeruli of olfactory sensory neurons housed in cognate types of sensilla. This atypical sensillar distribution previously led us to divide the flagellum into six different parts (Carle et al., 2014a). Briefly, the proximal parts are equipped with only mechanosensory and hygro‐/thermoreceptive sensilla, whereas the distal parts additionally possess olfactory sensilla in females. Moreover, a large number of grooved peg sensilla are present mostly on the proximal parts of male antennae, which are speculated to be their sex‐pheromone sensilla (Holwell et al., 2007; Allen et al., 2012; Carle et al., 2014a, 2014b). In the present study, the anatomical organization of ALs in the praying mantis T.
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