From bristle to brain: embryonic development of topographic projections from basiconic sensilla in the antennal nervous system of the locust Schistocerca gregaria.

The antennal flagellum of the locust S. gregaria is an articulated structure bearing a spectrum of sensilla that responds to sensory stimuli. In this study, we focus on the basiconic-type bristles as a model for sensory system development in the antenna. At the end of embryogenesis, these bristles are found at fixed locations and then on only the most distal six articulations of the antenna. They are innervated by a dendrite from a sensory cell cluster in the underlying epithelium, with each cluster directing fused axons topographically to an antennal tract running to the brain. We employ confocal imaging and immunolabeling to (a) identify mitotically active sense organ precursors for sensory cell clusters in the most distal annuli of the early embryonic antenna; (b) observe the subsequent spatial appearance of their neuronal progeny; and (c) map the spatial and temporal organization of axon projections from such clusters into the antennal tracts. We show that early in embryogenesis, proliferative precursors are localized circumferentially within discrete epithelial domains of the flagellum. Progeny first appear distally at the antennal tip and then sequentially in a proximal direction so that sensory neuron populations are distributed in an age-dependent manner along the antenna. Autotracing reveals that axon fasciculation with a tract is also sequential and reflects the location and age of the cell cluster along the most distal annuli. Cell cluster location and bristle location are therefore represented topographically and temporally within the axon profile of the tract and its projection to the brain.

Cuticular hydrocarbon reception by sensory neurons in basiconic sensilla of the Japanese carpenter ant.

To maintain the eusociality of a colony, ants recognize subtle differences in colony-specific sets of cuticular hydrocarbons (CHCs). The CHCs are received by female-specific antennal basiconic sensilla and processed in specific brain regions. However, it is controversial whether a peripheral or central neural mechanism is mainly responsible for discrimination of CHC blends. In the Japanese carpenter ant, Camponotus japonicus, about 140 sensory neurons (SNs) are co-housed in a single basiconic sensillum and receive colony-specific blends of 18 CHCs. The complexity of this CHC sensory process makes the neural basis of peripheral nestmate recognition difficult to understand. Here, we electrophysiologically recorded responses of single basiconic sensilla to each of 18 synthesized CHCs, and identified CHC responses of each SN co-housed in a single sensillum. Each CHC activated different sets of SNs and each SN was broadly tuned to CHCs. Multiple SNs in a given sensillum fired in synchrony, and the synchronicity of spikes was impaired by treatment with a gap junction inhibitor. These results indicated that SNs in single basiconic sensilla were electrically coupled. Quantitative analysis indicated that the Japanese carpenter ants have the potential to discriminate chemical structures of CHCs based on the combinational patterns of activated SNs. SNs of ants from different colonies exhibited different CHC response spectra. In addition, ants collected from the same colony but bred in separate groups also exhibited different CHC response spectra. These results support the hypothesis that the peripheral sensory mechanism is important for discrimination between nestmate and non-nestmate ants.

Evolution of the neuronal substrate for kin recognition in social Hymenoptera.

In evolutionary terms, life is about reproduction. Yet, in some species, individuals forgo their own reproduction to support the reproductive efforts of others. Social insect colonies for example, can contain up to a million workers that actively cooperate in tasks such as foraging, brood care and nest defence, but do not produce offspring. In such societies the division of labour is pronounced, and reproduction is restricted to just one or a few individuals, most notably the queen(s). This extreme eusocial organisation exists in only a few mammals, crustaceans and insects, but strikingly, it evolved independently up to nine times in the order Hymenoptera (including ants, bees and wasps). Transitions from a solitary lifestyle to an organised society can occur through natural selection when helpers obtain a fitness benefit from cooperating with kin, owing to the indirect transmission of genes through siblings. However, this process, called kin selection, is vulnerable to parasitism and opportunistic behaviours from unrelated individuals. An ability to distinguish kin from non-kin, and to respond accordingly, could therefore critically facilitate the evolution of eusociality and the maintenance of non-reproductive workers. The question of how the hymenopteran brain has adapted to support this function is therefore a fundamental issue in evolutionary neuroethology. Early neuroanatomical investigations proposed that social Hymenoptera have expanded integrative brain areas due to selection for increased cognitive capabilities in the context of processing social information. Later studies challenged this assumption and instead pointed to an intimate link between higher social organisation and the existence of developed sensory structures involved in recognition and communication. In particular, chemical signalling of social identity, known to be mediated through cuticular hydrocarbons (CHCs), may have evolved hand in hand with a specialised chemosensory system in Hymenoptera. Here, we compile the current knowledge on this recognition system, from emitted identity signals, to the molecular and neuronal basis of chemical detection, with particular emphasis on its evolutionary history. Finally, we ask whether the evolution of social behaviour in Hymenoptera could have driven the expansion of their complex olfactory system, or whether the early origin and conservation of an olfactory subsystem dedicated to social recognition could explain the abundance of eusocial species in this insect order. Answering this question will require further comparative studies to provide a comprehensive view on lineage-specific adaptations in the olfactory pathway of Hymenoptera.

Antennal Morphology and Fine Structure of Flagellar Sensilla in Hippoboscid Flies with Special Reference to Lipoptena fortisetosa (Diptera: Hippoboscidae).

Lipoptena cervi (Linnaeus), Lipoptena fortisetosa Maa, Hippobosca equina Linnaeus, and Pseudolynchia canariensis (Macquart) are hematophagous ectoparasites that infest different animal species and occasionally bite humans. Hosts are located by a complex process involving different kinds of stimuli perceived mainly by specific sensory structures on the antennae, which are the essential olfactory organs. General antennal morphology, together with distribution and ultrastructure of sensilla, have been studied in detail with scanning and transmission electron microscopy approaches. Observations have revealed some common features among the four studied hippoboscids: (a) typical concealment of the flagellum inside the other two segments; (b) characteristic trabecular surface of the flagellum; (c) peculiar external microtrichia; (d) presence on the flagellum of basiconic sensilla and grooved peg coeloconic sensilla; (e) unarticulated arista. The ultrastructure of L. fortisetosa revealed that microtrichia and the flagellar reticulated cuticle are not innervated. Different roles have been hypothesized for the described antennal structures. Microtrichia and the reticulated cuticle could convey volatile compounds towards the flagellar sensory area. Peculiar sensory neurons characterize the unarticulated arista which could be able to detect temperature variations. Coeloconic sensilla could be involved in thermoreception, hygroreception, and carbon dioxide reception at long distances, while the poorly porous basiconic sensilla could play a role in the host odour perception at medium-short distances.

Nonanal modulates oviposition preference in female Helicoverpa assulta (Lepidoptera: Noctuidae) via the activation of peripheral neurons.

BACKGROUND: The insect olfactory system can recognize odorants for feeding, courtship, oviposition and avoiding natural enemies. Odorant cues from host plants play important roles in insect behaviours. Tobacco (Nicotiana tabacum) is the main cultivated host of the oriental tobacco budworm Helicoverpa assult. Volatiles of tobacco plants attract and stimulate oviposition in female moths. However, it is still not known how female H. assulta recognize tobacco volatiles and which odorant compounds are used as oviposition cues. RESULTS: We detected 14 volatile compounds emitted from a tobacco plant during vegetative growth, using gas chromatography-mass spectrometry. Electroantennogram tests indicated that eight of the 14 compounds induced responses in female H. assulta. Among these eight volatiles, nonanal greatly increased oviposition preference. Single-sensillum recording (SSR) results showed that many neurons housed in three types of short basiconic sensilla and four types of long basiconic sensilla responded to nonanal and heptanal as its structural analogue. The responses to nonanal were significantly stronger than those to the other compounds. Nonanal was the main ligand of OR67, an odorant receptor from H. assulta. This was demonstrated using an in vitro Xenopus oocytes expression system that supported the SSR results. CONCLUSION: Nonanal is a key signal volatile of tobacco plants that attracts female H. assulta moths to oviposit. © 2020 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Putative Sensory Structures Associated With the Food Canal of Tabanus atratus (Diptera: Tabanidae).

Putative sensory structures in the food canal, and distal vestibule region entering the canal of Tabanus atratus F., are described. Two pairs of sensilla were observed in the walls of the vestibule-a distal pair of the basiconic type, and a pair of setifiorm sensilla at the base of the vestibule. Vestibular sensilla were constant in type, number, and position. Conversely, setiform sensilla in right and left walls of the food canal varied in number from one fly specimen to another, and lacked evidence of pairing (i.e., sensilla in one wall did not necessarily have a counterpart in the other wall). Food canal sensilla were of setiform design, with the exception of a single basiconic sensilla in each lateral wall of the food canal in every fly. When the food canal was partitioned into four equidistant regions, setiform sensilla were aggregated in the two distal-most regions, with relatively few sensilla observed in the two proximal canal regions. This aggregation was significant, leading to rejection of the null hypothesis that setiform sensilla were evenly distribution throughout the length of the food canal. Basiconic sensilla were always located in the distal-most region of the food canal.