Morphological and Transcriptomic Analysis of a Beetle Chemosensory System Reveals a Gnathal Olfactory Center

Abstract

BackgroundThe red flour beetle Tribolium castaneum is an emerging insect model organism representing the largest insect order, Coleoptera, which encompasses several serious agricultural and forest pests. Despite the ecological and economic importance of beetles, most insect olfaction studies have so far focused on dipteran, lepidopteran, or hymenopteran systems.ResultsHere, we present the first detailed morphological description of a coleopteran olfactory pathway in combination with genome-wide expression analysis of the relevant gene families involved in chemoreception. Our study revealed that besides the antennae, also the mouthparts are highly involved in olfaction and that their respective contribution is processed separately. In this beetle, olfactory sensory neurons from the mouthparts project to the lobus glomerulatus, a structure so far only characterized in hemimetabolous insects, as well as to a so far non-described unpaired glomerularly organized olfactory neuropil in the gnathal ganglion, which we term the gnathal olfactory center. The high number of functional odorant receptor genes expressed in the mouthparts also supports the importance of the maxillary and labial palps in olfaction of this beetle. Moreover, gustatory perception seems equally distributed between antenna and mouthparts, since the number of expressed gustatory receptors is similar for both organs.ConclusionsOur analysis of the T. castaneum chemosensory system confirms that olfactory and gustatory perception are not organotopically separated to the antennae and mouthparts, respectively. The identification of additional olfactory processing centers, the lobus glomerulatus and the gnathal olfactory center, is in contrast to the current picture that in holometabolous insects all olfactory inputs allegedly converge in the antennal lobe. These findings indicate that Holometabola have evolved a wider variety of solutions to chemoreception than previously assumed.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0304-z) contains supplementary material, which is available to authorized users.

Variations on a Theme: Antennal Lobe Architecture across Coleoptera

“…Difficult to characterize in synapsin or phalloidin stainings, backfills and antibody stainings against TKRP helped to identify numerous small glomeruli (Fig 4C–4G arrowheads) and to differentiate the AL from a structure which we identified as the lobus glomerulatus (LG) (Fig 4G), a deutocerebral structure typically found in hemimetabolous insects but recently also reported to occur in beetles [39]. In hemimetabolous insects, the LG has been described to receive first order gustatory and mechanosensory input from the mouthparts [71].…”

“…In hemimetabolous insects, the LG has been described to receive first order gustatory and mechanosensory input from the mouthparts [71]. A recent study in the beetle Tribolium castaneum suggested an innervation of the LG by OSNs based in sensilla of the mouthparts [39]. In all five investigated Coccinellidae, the ALs are remarkably small (Fig 1) and consist of numerous minute glomeruli (approximately 400–600 glomeruli per AL).…”

“…Data for from T . castaneum and Aethina tumida were obtained from Dreyer et al [38], Kollmann et al [40] and Dippel et al [39]. …”

“…Detailed information on the ALs of Coleoptera is scarce [21]—only the ALs of the scarab beetle Holotrichia diomphalia [37], of the red flour beetle Tribolium castaneum [34,38,39], and of the small hive beetle Aethina tumida [40] have been investigated in greater detail. Exhibiting 60–90 spherical glomeruli, the ALs in these species conform to the basic bauplan of a typical insect AL [21].…”

A mannitol/sorbitol receptor stimulates dietary intake in Tribolium castaneum

“…Sixty-two Gr genes in the antennae and 69 Gr genes in mouthparts are highly expressed, and this species shows expression of many more types of Grs than other insect species [15]. This expanded Gr family likely plays a functional role for host selection.…”