Microarchitecture of the tsetse fly proboscis

Abstract

BackgroundTsetse flies (genus Glossina) are large blood-sucking dipteran flies that are important as vectors of human and animal trypanosomiasis in sub-Saharan Africa. Tsetse anatomy has been well described, including detailed accounts of the functional anatomy of the proboscis for piercing host skin and sucking up blood. The proboscis also serves as the developmental site for the infective metacyclic stages of several species of pathogenic livestock trypanosomes that are inoculated into the host with fly saliva. To understand the physical environment in which these trypanosomes develop, we have re-examined the microarchitecture of the tsetse proboscis.ResultsWe examined proboscises from male and female flies of Glossina pallidipes using light microscopy and scanning electron microscopy (SEM). Each proboscis was removed from the fly head and either examined intact or dissected into the three constituent components: Labrum, labium and hypopharynx. Our light and SEM images reaffirm earlier observations that the tsetse proboscis is a formidably armed weapon, well-adapted for piercing skin, and provide comparative data for G. pallidipes. In addition, the images reveal that the hypopharynx, the narrow tube that delivers saliva to the wound site, ends in a remarkably ornate and complex structure with around ten finger-like projections, each adorned with sucker-like protrusions, contradicting previous descriptions that show a simple, bevelled end like a hypodermic needle. The function of the finger-like projections is speculative; they appear to be flexible and may serve to protect the hypopharynx from influx of blood or microorganisms, or control the flow of saliva. Proboscises were examined after colonisation by Trypanosoma congolense savannah. Consistent with the idea that colonisation commences in the region nearest the foregut, the highest densities of trypanosomes were found in the region of the labrum proximal to the bulb, although high densities were also found in other regions of the labrum. Trypanosomes were visible through the thin wall of the hypopharynx by both light microscopy and SEM.ConclusionsWe highlight the remarkable architecture of the tsetse proboscis, in particular the intricate structure of the distal end of the hypopharynx. Further work is needed to elucidate the function of this intriguing structure.Electronic supplementary materialThe online version of this article (10.1186/s13071-017-2367-2) contains supplementary material, which is available to authorized users.

Comparative morphology of the deer ked Lipoptena fortisetosa first recorded from Italy

“…Haarløv () concluded that L. cervi is a pool feeder and not a capillary feeder like some mosquitoes because it needs to injure the skin of the host in order to suck blood from a haemorrhage made by its teeth. Lipoptena fortisetosa shows mouthpart structures that are the same as those in L. cervi and both are very similar to the feeding apparatus of the Glossinidae (Snodgrass, ; Haarløv, ; Krenn & Aspöck, ; Gibson et al ., ). The mouthparts of tsetse flies include a proboscis that is equipped with arrays of teeth and rasps.…”

“…The mouthparts of tsetse flies include a proboscis that is equipped with arrays of teeth and rasps. The proboscis is formed by labella at the top of the organ and is divided lengthwise into a labrum and a labium that includes the hypopharynx (Gibson et al ., ).…”

Salivarian Trypanosomosis: A Review of Parasites Involved, Their Global Distribution and Their Interaction With the Innate and Adaptive Mammalian Host Immune System

“…Naturally, from a human and economic point of view, it is the mammalian infection stage that has attracted most attention in the past. It is only more recently that the parasite-vector interaction and biology has received more detailed attention and that also non- T. brucei infections have been studied in tsetse ( 73 , 74 ). These reports show that in fact both T. congolense and T. vivax are much more effective in establishing tsetse infections than T. brucei .…”

Salivarian Trypanosomes Have Adopted Intricate Host-Pathogen Interaction Mechanisms That Ensure Survival in Plain Sight of the Adaptive Immune System

“…Compared to the available knowledge of the T. brucei life cycle, the cycle of other salivarian trypanosomes is less well documented [30][31][32]. Interestingly T. congolense is Figure 1.…”