One of the major trends in the evolution of parasitoid wasps is miniaturization, which has produced the smallest known insects. Megaphragma spp. (Hymenoptera: Trichogrammatidae) are smaller than some unicellular organisms, with an adult body length of the smallest only 170 µm. Their parasitoid lifestyle depends on retention of a high level of sensory reception comparable to that in parasitoid wasps that may have antennae hundreds of times larger. Antennal sensilla of males and females of Megaphragma amalphitanum and M. caribea and females of the parthenogenetic M. mymaripenne are described, including sensillum size, external morphology, and distribution. Eight different morphological types of sensilla were discovered, two of them appearing exclusively on female antennae. Two of the types, sensilla styloconica and aporous placoid sensilla, have not been described previously. Regression analyses were performed to detect and evaluate possible miniaturization trends by comparing available data for species of larger parasitoid wasps. The number of antennal sensilla was found to decrease with the body size; M. amalphitanum males have only 39 sensilla per antenna. The number of antennal sensilla types and sizes of the sensilla, however, show little to no correlation with the body size. Our findings on the effects of miniaturization on the antennal sensilla of Megaphragma provide material for discussion on the limits to the reduction of insect antenna.
Miniaturization is a major evolutionary trend prominent in insects, which has resulted in the existence of insects comparable in size to some unicellular protists. The adaptation of the complex antennal multisensory systems to extreme miniaturization is a fascinating problem, which remains almost unexplored. We studied the antennal sensilla of Scydosella musawasensis Hall, 1999 (Coleoptera: Ptiliidae), the smallest free-living insect, using scanning electron microscopy. The antenna of S. musawasensis bears 131 sensilla; no intraspecific variation in the number or position of the sensilla has been revealed. Nine different morphological types of sensilla are described according to their external morphological features and distribution: four types of sensilla trichodea, one type of sensilla chaetica, two types of sensilla styloconica, and two types of sensilla basiconica. Morphometric analysis of the sensilla of S. musawasensis, based on measurements of the lengths and diameters of sensilla and their location and number, showed the absence of significant differences between females and males. Comparative allometric analysis of S. musawasensis and larger Coleoptera showed that the number of sensilla and the size of sensilla chaetica decrease with decreasing body size. However, the number of the types of sensilla and the length and diameter of the multiporous sensilla basiconica revealed no correlation with the body size. Comparison of the acquired data with the results of our earlier study of the antennal sensilla of some of the smallest parasitic wasps is used to put forward hypotheses on the common principles of miniaturization of the antennal sensory systems of insects.
Extreme miniaturization implies a high degree of optimization, rendering the retention of non-functional organs almost impossible. Two unique non-porous placoid sensilla on the antennae of females of Megaphragma were described in the literature. Placoid sensilla in Hymenoptera have an olfactory function and always bear pores; the apparent absence of pores therefore raises the questions whether such sensilla are functional in Megaphragma and whether their surface sculpture had been sufficiently well examined. We examined in detail the external microsculpture and internal ultrastructure of the placoid sensilla using Focused Ion Beam Scanning Electron Microscopy and Scanning Electron Microscopy with various types of sputtering and show that these sensilla actually have a porous cuticle and are innervated by 11 or 12 neurons with branched cilia, which is typical of olfactory sensilla. Comparison of various methods of electron microscopy allows us to conclude that for an accurate determination of the morphofunctional types of sensilla, especially in miniature insects, it is necessary to study both the internal ultrastructure of the sensilla and their external morphology using carefully selected scanning electron microscopy methods.
Insect antennae are astonishingly versatile and have multiple sensory modalities. Audition, detection of airflow, and graviception are combined in the antennal chordotonal organs. The miniaturization of these complex multisensory organs has never been investigated. Here we present a comprehensive study of the structure and scaling of the antennal chordotonal organs of the extremely miniaturized parasitoid wasp Megaphragma viggianii based on 3D electron microscopy. Johnston’s organ of M. viggianii consists of 19 amphinematic scolopidia (95 cells); the central organ consists of five scolopidia (20 cells). Plesiomorphic composition includes one accessory cell per scolopidium, but in M. viggianii this ratio is only 0.3. Scolopale rods in Johnston’s organ have a unique structure. Allometric analyses demonstrate the effects of scaling on the antennal chordotonal organs in insects. Our results not only shed light on the universal principles of miniaturization of sense organs, but also provide context for future interpretation of the M. viggianii connectome.
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