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Johnston´S Organ As a Mechanosensory Element for Spatial Orientation in Rhodnius Prolixus

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Johnston´S Organ As a Mechanosensory Element for Spatial Orientation in Rhodnius Prolixus Johnston´s organ as a mechanosensory element for spatial orientation in Rhodnius prolixus Bibiana Ospina-Rozo; Manu Forero-Shelton, Jorge Molina Flagellar antennae in the class Insecta generally bear two basal segments (scape and pedicel) and a segmented flagellum lacking intrinsic muscles (Schneider, 1964). In the non-muscular joint between the pedicel and the flagellum is located the Johnston’s organ (JO). This organ is a chordotonal complex consisting of sub-unities called scolopidia, each one bearing one to three specialized sensory neurons (Yack, 2004). These neurons are capable of detecting the movement of the flagellum, and transducing it into action potentials (Yack, 2004). These two features: the lack of intrinsic muscles beyond the scape and the presence of the JO are considered synapomorphic traits for the class Insecta (Kristensen, 1998; Kristensen, 1981). The Johnston’s organ has been deeply studied in groups of Holometabolous insects, and it has been proven to have many important and diverse functions such as flight control (Sane et al., 2007), near- field hearing (Kamikouchi et al., 2009) and detection of electric fields (Greggers et al., 2013), among others. In holometabolous insects the JO can have variable number of scolopidia. Higher numbers and organization of scolopidia are considered either a strategy to enhance resolution like near-field sound detection in males of Aedes genus with 7000 scolopidia (Boo & Richards, 1975), or a way to ensure various functions as in Drosophila, where the JO consists of 200 scolopidia divided into 5 regions and capable of codifying wind direction, near-field sound and gravity direction (Kamikouchi et al., 2009). However, the function of the JO in basal groups remains unclear, and at the same time, the basal function of the JO is unknown. Since it is a synapomorphic trait for all insects (Kristensen, 1981), the JO could have had a simpler function in basal groups, and subsequently undergone an exaptation process, getting new functions according to different selective pressures over each group of insects. A possible basal function for the JO could be gravity sensing. That is because gravity sensing is essential for life on earth in order to ensure key processes inside the body and locomotion (Morey-Holton, 2003). Other mechanical stimuli are usually relevant only for certain groups of insects, while gravity affects all groups in the same way. And, as the JO is a graviceptor 1 in some groups of holometabolous insects (Kamikouchi et al., 2009), graviception could be a function present in basal groups and retained in some holometabolous groups. In order to test this hypothesis it is important to evaluate if the JO can perform as a graviceptor in basal groups of insects. Therefore, we have chosen to study the Heteroptera group which is part of the most successful radiation of hemimetabolous insects (Weirauch & Schuh, 2011), and has a JO consisting of a maximum of 50 scolopidia (Rossi & Romani, 2013). Among the diversity of species of Heteroptera we decided to work with Rhodnius prolixus because this species is showing a clear negative geotactic behavior (Gaunt & Miles, 2000), which lead us to think that gravity sensing is highly important for these insects in order to orient themselves while climbing. Our research´s aim was to determine if the Johnston’s organ (JO) of Rhodnius prolixus, being a complex of mechanosensory neurons, could act as a graviceptor bringing information about the direction of gravity, and thus helping the insect to monitor its spatial orientation. In order to establish if the JO in R. prolixus can perform as a graviceptor, it is necessary to study the process of transduction of the gravity force. Transduction process of any stimulus has three phases as reported by Yack (2004): 1) Coupling, how certain part of the body has a structural configuration allowing it to link the stimulus with the sensory neurons. 2) Transduction, how mechanical displacement of the neuron results in variation of membrane potential. 3) Coding, production of specific patterns of electrical impulses. Our study focusses in the coupling process of sensing gravity force with the antenna. In this phase it is necessary to know the external structure of the antenna, then the way it is affected by the stimulus action and finally the internal structure, meaning the organization and anchoring point of the JO. These three aspects have to be correlated in order to determine: 1) if the structural traits in the antenna are part of a structural design optimized to enhance the response to the gravity force action, and 2) if the anchoring point of the scolopidia is appropriate to allow their linking with the movement of the flagellum produced by gravity force. In order to explore the three aspects mentioned above and their correlations, we used basic physics and mechanical engineering approaches. Our results are divided into three parts presented here each one as an independent manuscript. First of all, we studied the external morphology of the antenna, characterizing the length and diameter of the segments, shape and size of the non-muscular joints and cuticle thickness. Since R. prolixus is a hemimetabolous insect, and the five nymphal stages have very similar habits than the adults (Paurometabola according to McKamey (1999)), they were expected to have similar antennae. We analyzed the external morphology in the antenna of the five nymphs and the adult. These results are 2 presented in the first manuscript with emphasis in the non-muscular joints. We also evaluated thickness of the cuticle walls in the antenna of the first nymph, fifth nymph and the adults. These measurements were included as important parameters in the model developed and presented in the third manuscript. Then, we carried out a biomechanical analysis of R. prolixus antennae by changing the insect’s spatial orientation and seen the effect of the standard earth gravity on the position of the flagellum (distal part of the antenna). Results of this process are presented in the second manuscript. Once we had information about structure of the antenna and how it is affected by the gravity force, the next step was to observe the organization of the scolopidia in the JO inside the pedicel. Although previous studies had shown the longitudinal shape of a scolopale unit of the JO in R. prolixus (Wigglesworth & Gillet, 1934), our findings are important because they are showing the anchoring point of the scolopidia, the potential number of scolopidia in the JO, and their organization inside the pedicel. This information is available in the second manuscript too. Our third manuscript is in a certain way a combination of the first two manuscripts. By using finite element analysis (FEA), we explored the relevance of the main structural features observed of the antenna in the process of coupling the stimulus of gravity. And, we compared how gravity force acts on the very different structural designs of the antenna in three postembryonic stages of the life cycle in R. prolixus. Our findings support the hypothesis that the JO in R. prolixus could act as a graviceptor. The design of the antenna seems to be the key element to make it flexible enough to perform as a mechanical sensor. Also the antenna is bended by gravity only in specific areas located very close to the anchoring point of the scolopidia in the JO, which was confirmed by our biomechanical analysis and computerized modeling. In conclusion, the flagellar antenna of Rhodnius prolixus could be acting as a coupling organ for mechanical information possibly codified by the Johnston’s Organ. Also, gravity is a mechanical stimulus capable of affecting the flagellum position in accordance to changes in insect’s position. In order to study the second and third phases of the process suggested by Yack (2004), electrophysiological studies are still needed. This kind of studies could lead to understand which part of the information of the movement caused by gravity over the flagellum, is being codified and sent to mechanosensory processing centers in the brain, via the antennal nerve. The methodology described here is appropriate to study any kind of graviceptor under the real magnitude and direction of the gravity force stimulus. Also, our results are useful to understand the characteristics of the gravity stimulus. This information has to be used to determine the better way to administrate the 3 gravity stimulus to the antenna, and to interpret the obtained results in different stages of postembryonic development in insects. References Boo, K.S., & Richards, A.G. (1975) Fine structure of scolopidia in Johnston’s organ of male Aedes aegypti (L.) (Diptera: Culicidae). International Journal of Insect Morphology and Embryology, 4(6), 549–566. Gaunt, M., & Miles, M. (2000). The ecotopes and evolution of triatomine bugs (Triatominae) and their associated trypanosomes. Memórias Do Instituto Oswaldo Cruz, 95(4), 557–65. Greggers, U., Koch, G., Schmidt, V., Dürr, A., Floriou-servou, A., Piepenbrock, D., Göpfert, M., & Menzel, R. (2013). Reception and learning of electric fields in bees. Proceedings of the Royal Society, 280(1759), 20130528. Kamikouchi, A., Inagaki, H. K., Effertz, T., Hendrich, O., Fiala, A., Göpfert, M. C., & Ito, K. (2009). The neural basis of Drosophila gravity-sensing and hearing. Nature, 458(7235), 165– 171. Kristensen, N.P. (1981). Phylogeny of Insect Orders. Annual Review of Entomology, 26(1), 135-157. Kristensen, N. P. (1998). The groundplan and basal diversification of the hexapods. Arthropod Relationships, 55, 281-293. McKamey, S.H. (1999). Biodiversity of tropical Homoptera, with the first data from Africa. American Entomologist-Lanham-, 45(4), 213-222. Morey-Holton, E. (2003). The impact of gravity on life. In: Evolution on planet earth: The impact of the physical environment, New York, Academic Press, pp. 143 – 160. Rossi, M.V., & Romani, R.
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