The Sensory Machinery of the Head Louse Pediculus humanus capitis: From the Antennae to the Brain

Abstract

Insect antennae are sophisticated sensory organs, usually covered with sensory structures responsible for the detection of relevant signals of different modalities coming from the environment. Despite the relevance of the head louse Pediculus humanus capitis as a human parasite, the role of its antennal sensory system in the highly dependent relation established with their hosts has been barely studied. In this work, we present a functional description of the antennae of these hematophagous insects by applying different approaches, including scanning electron microscopy (SEM), anterograde antennal fluorescent backfills, and behavioral experiments with intact or differentially antennectomized lice. Results constitute a first approach to identify and describe the head louse antennal sensilla and to determine the role of the antenna in host recognition. SEM images allowed us to identify a total of 35–40 sensilla belonging to seven different morphological types that according to their external architecture are candidates to bear mechano-, thermo-, hygro-, or chemo-receptor functions. The anterograde backfills revealed a direct neural pathway to the ipsilateral antennal lobe, which includes 8–10 glomerular-like diffuse structures. In the two-choice behavioral experiments, intact lice chose scalp chemicals and warm surfaces (i.e., 32°C) and avoided wet substrates. Behavioral preferences disappeared after ablation of the different flagellomeres of their antenna, allowing us to discuss about the location and function of the different identified sensilla. This is the first study that integrates morphological and behavioral aspects of the sensory machinery of head lice involved in host perception.

Sensory features of the human louse antenna: new contributions and comparisons between ecotypes

“…1A). Already described on the HL antenna (Ortega Insaurralde et al ., 2019), the single pore was observed for the first time in the BL. The single pore consists of a pit located on the flagellomere 3 (Fig.…”

“…1C,D). Based solely on morphological and behavioural studies of the HL, finger‐like and sharp‐end basiconica were suggested to have an olfactory role, whereas the round‐end basiconica would accomplish a gustatory role, although functional studies are necessary to confirm these hypotheses (Ortega Insaurralde et al ., 2019).…”

“…2A,B, Table 1, t‐test, bristles of the flagellomere 1: P = ns ; flagellomere 3: P = ns ). Based only on morphological observations, bristles could serve a mechanoreceptive function (Ortega Insaurralde et al ., 2019). It is important to note that the number and morphology of mechanoreceptive sensilla have been postulated to reflect insects' interactions with their habitats (McIver & Siemicki, 1984).…”

“…The sensory system of lice was studied through the description of its main sensory organ, i.e. the antenna, which shows few sensory structures or sensilla (Slifer & Sekhon, 1980; Ortega Insaurralde et al ., 2019). In particular, through morphological (histological techniques, scanning electron microscopy (SEM) and transmission electron microscopy (TEM) studies) and behavioural studies, antennal sensilla were associated with mechano‐, chemo‐ and thermo‐hygroreception functions in the body louse (Keilin & Nuttall, 1930; Wigglesworth, 1941; Slifer & Sekhon, 1980; Steinbrecht, 1994).…”

“…In particular, through morphological (histological techniques, scanning electron microscopy (SEM) and transmission electron microscopy (TEM) studies) and behavioural studies, antennal sensilla were associated with mechano‐, chemo‐ and thermo‐hygroreception functions in the body louse (Keilin & Nuttall, 1930; Wigglesworth, 1941; Slifer & Sekhon, 1980; Steinbrecht, 1994). More recently, SEM studies of the head louse antenna showed similar sensilla to the body lice, in addition to some chemoreceptive and thermoreceptor sensilla candidates (Ortega Insaurralde et al ., 2019).…”