Search

Size is a key to locomotion. In insects, miniaturization leads to fundamental changes in wing structure and kinematics, making the study of flight in the smallest species important for basic biology and physics, and, potentially, for applied disciplines. However, the flight efficiency of miniature insects has never been studied, and their speed and maneuverability have remained unknown. We report a comparative study of speeds and accelerations in the smallest free-living insects, featherwing beetles (Coleoptera: Ptiliidae), and in larger representatives of related groups of Staphylinoidea. Our results show that the average and maximum flight speeds of larger ptiliids are extraordinarily high and comparable to those of staphylinids that have bodies 3 times as long. This is one of the few known exceptions to the “Great Flight Diagram,” according to which the flight speed of smaller organisms is generally lower than that of larger ones. The horizontal acceleration values recorded in Ptiliidae are almost twice as high as even in Silphidae, which are more than an order of magnitude larger. High absolute and record-breaking relative flight characteristics suggest that the unique morphology and kinematics of the ptiliid wings are effective adaptations to flight at low Reynolds numbers. These results are important for understanding the evolution of body size and flight in insects and pose a challenge to designers of miniature biomorphic aircraft.

The wings of Ptiliidae, the coleopteran family containing the smallest free-living insects, are analyzed in detail for the first time. A reconstruction of the evolutionary sequence of changes associated with miniaturization is proposed. The wings of several species are described using light microscopy and scanning electron microscopy. The morphology and scaling are analyzed in comparison with larger representatives of related groups. The wings of all studied ptiliids show some degree of ptiloptery (feather-like shape, typical for extremely small insects). In larger ptiliids the wing contains at least five veins, has a wide blade, and bears a marginal fringe of 200-300 setae; in the smallest species it has three veins or fewer, a narrow blade, and about 40 setae along the margin. The setae are brush-like; peculiar outgrowths, denser towards the apex, increase the effective diameter of the setae. Morphometric analysis shows that the geometry of the wings and their elements strongly differs from those of other staphyliniform beetles, suggesting that the aerodynamics of the feather-like wings may also differ distinctly from the usual pattern.

Revealing the effect of brain size on the cognitive abilities of animals is a major challenge in the study of brain evolution. Analysis of the effects of miniaturization on brain function in the smallest insects is especially important, as they are comparable in body size to some unicellular organisms and next to nothing is known about their cognitive abilities. We analyse for the first time the structure of the brain of the adult featherwing beetle Nephanes titan, one of the smallest insects, and results of the first ethological experiments on the capacity of learning in this species. N. titan is capable of associative learning, in spite of the structural modification in its nervous system and the greatly reduced number of neurons compared to the nervous systems of larger insects. Microinsects can become useful model organisms for neurobiology. On the one hand, the structural simplicity and extremely small size of their central nervous system make it possible to study it very efficiently. On the other hand, their learning capacity and retained principal cognitive abilities make them suitable objects for behavioural experiments.

The coleopteran family Ptiliidae (featherwing beetles) includes some of the smallest insects known with most of the representatives of this family measuring less than 1 mm in body length. A small body size largely determines the morphology, physiology, and biology of an organism and affects the organization of complex sense organs. Information on the organization of the compound eyes of Ptiliidae is scarce. Using scanning electron microscopy we analyzed the eyes of representatives of all subfamilies and tribes and provide a detailed description of the eye ultrastructure of four species (Nephanes titan, Porophila mystacea, Nanosella sp. and Acrotrichis grandicollis) using transmission electron microscopy. The results are compared with available data on larger species of related groups of Staphyliniformia and scale quantitative analyses are performed. The eyes of Ptiliidae consist of 15–50 ommatidia 6–13 μm in diameter and all conform to the apposition acone type of eye with fused rhabdoms of banded organization. Each ommatidium has the typical cellular arrangement present also in the eyes of larger staphyliniform beetles, but strongly curved lenses, short cones, reduced pigment cells, a high density of pigment granules and certain modifications of the rhabdom seem typical of ptiliid eyes. Allometric analyses show that as body size decreases, the number of facets drops more steeply than their average size does.

Megaphragma is recorded for the first time in Columbia where it is represented by M. caribea that emerged from leaves of Terminalia catappa infested by the thrips (Heliothrips haemorrhoidalis and Selenothrips rubrocinctus). M. caribea has anucleate neurons, the third species of Megaphragma shown to have this feature.

This article describes the morphology and ultrastructure of the brain of the greenhouse thrips, Heliothrips haemorrhoidalis (Thripidae), studied in a series of histological sections with the use of 3D reconstructions and TEM. The structural peculiarities of the brain organization and its features associated with body miniaturization as well as its quantitative characteristics (the number of cells and the volume of individual centers) are described for the first time in both the adult and the first-instar nymph of H. haemorrhoidalis. It is suggested that the limits of the nervous system miniaturization may be different in holo- and hemimetabolous insects.

The third communication in this series describes the structure of the brain in one of the smallest psocopterans, Liposcelis bostrychophila (Liposcelididae), studied in a series of histological sections with the use of 3D reconstructions and TEM. Like all microinsects, L. bostrychophila shows both oligomerization and concentration of ganglia, an increased relative volume of the brain, and a reduced number and size of neurons. In addition, reduction of one of the optic lobes is noted. The structural features of the neuropil brain centers in the early and late first-instar nymphs are described.

Aerodynamic force generation capacity of the wing of a miniature beetleParatuposa placentisis evaluated using a combined experimental and numerical approach. The wing has a peculiar shape reminiscent of a bird feather, often found in the smallest insects. Aerodynamic force coefficients are determined from a dynamically scaled force measurement experiment with rotating bristled and membrane wing models in a glycerin tank. Subsequently, they are used as numerical validation data for computational fluid dynamics simulations using an adaptive Navier–Stokes solver. The latter provides access to important flow properties such as leakiness and permeability. It is found that, in the considered biologically relevant regimes, the bristled wing functions as a less than$$50\%$$50%leaky paddle, and it produces between 66 and$$96\%$$96%of the aerodynamic drag force of an equivalent membrane wing. The discrepancy increases with increasing Reynolds number. It is shown that about half of the aerodynamic normal force exerted on a bristled wing is due to viscous shear stress. The paddling effectiveness factor is proposed as a measure of aerodynamic efficiency.Graphic abstract

Smaller animals display pecular characteristics related to their small body size, and miniaturization has recently been intensely studied in insects, but not in other arthropods. Collembola, or springtails, are abundant soil microarthropods and form one of the four basal groups of hexapods. Many of them are notably smaller than 1 mm long, which makes them a good model for studying miniaturization effects in arthropods. In this study we analyze for the first time the anatomy of the minute springtailMesaphorura sylvatica(body length 400 µm). It is described using light and scanning electron microscopy and 3D computer reconstruction. Possible effects of miniaturization are revealed based on a comparative analysis of data from this study and from studies on the anatomy of larger collembolans. Despite the extremely small size ofM.sylvatica, some organ systems, e.g., muscular and digestive, remain complex. On the other hand, the nervous system displays considerable changes. The brain has two pairs of apertures with three pairs of muscles running through them, and all ganglia are shifted posteriad by one segment. The relative volumes of the skeleton, brain, and musculature are smaller than those of most microinsects, while the relative volumes of other systems are greater than or the same as in most microinsects. Comparison of the effects of miniaturization in collembolans with those of insects has shown that most of the miniaturization-related features ofM. sylvaticahave also been found in microinsects (shift of the brain into the prothorax, absent heart, absence of midgut musculature, etc.), but also has revealed unique features (brain with two apertures and three pairs of muscles going through them), which have not been described before.

Body size reduction, also known as miniaturization, is an important evolutionary process that affects a number of physiological and phenotypic traits and helps animals to conquer new ecological niches. However, this process is poorly understood at the molecular level. Here, we report genomic and transcriptomic features of arguably the smallest known insect – the parasitoid wasp, Megaphragma amalphitanum (Hymenoptera: Trichogrammatidae). In contrast to expectations, we find that the genome and transcriptome sizes of this parasitoid wasp are comparable to other members of the Chalcidoidea superfamily. Moreover, the gene content of M. amalphitanum compared to other chalcid wasps is remarkably conserved. Among the very rare cases of apparent gene loss is centrosomin, which encodes an important centrosome component; the absence of this protein might be related to the large number of anucleate neurons in M. amalphitanum. Intriguingly, we also observed significant changes in M. amalphitanum transposable element dynamics over time, whereby an initial burst was followed by suppression of activity, possibly due to a recent reinforcement of the genome defense machinery. Thus, while the M. amalphitanum genomic data reveal certain features that may be linked to the unusual biological properties of this organism, miniaturization is not associated with a large decrease in genome complexity.

Anatomy of the adult and the first-instar nymph of Liposcelis bostrychophila (Psocoptera, Liposcelididae) is described in detail for the first time based on series of sections and 3D computer reconstruction. Despite its tiny size, no strong structural simplification is observed in Liposcelis. The main features of the anatomy of this species associated with miniaturization are the merging of individual skeletal elements and simplification of the endoskeleton in the nymph, lack of the midgut muscles, simplification of the tracheal and circulatory systems, oligomerization and concentration of ganglia, asymmetry of the central nervous system in the nymph, and the absence of several muscles. Changes in the relative volumes of organs during the postembryonic development of Liposcelis are analyzed and compared with other minute insects.

Anatomy of adults of Trichogramma evanescens (Hymenoptera: Trichogrammatidae) is described in detail for the first time based on series of sections and 3D computer reconstruction. The complex structure of the exoskeleton and musculature (except for reductions of individual muscles) is preserved in T. evanescens despite its tiny size. Considerable simplification is observed in the structure of the intestine, tracheal and circulatory systems, and in the reduced number of Malpighian tubules. Thus, the smallest Hymenoptera (Mymaridae and Trichogrammatidae) demonstrate both the effects of miniaturization universal for insects (reduction of the head endoskeleton, circulatory and respiratory systems) and specific ones.

The mouthparts and musculature of the head of Sericoderus lateralis are described. It is shown that the mouthparts of minute beetles preserve their complex structure and are not significantly affected by miniaturization. Such stability allows these features to be used in macrosystematics of groups with variable body size.

Anatomy of the adult fairyfly Anaphes flavipes (Hymenoptera, Mymaridae) is described in detail for the first time, based on series of sections and 3D computer reconstruction. Despite its tiny size, A. flavipes does not demonstrate strong morphological simplification, except for the merging of certain skeletal elements, a slight simplification of endoskeleton, lack of midgut muscles, a reduced number of Malpighian tubules, simplification of the tracheal and circulatory systems, asymmetry of the central nervous system, and the absence of several muscles.

During metamorphosis, the insect CNS undergoes both structural and allometric changes. Due to their extreme de-embryonization and parasitism, the formation of the CNS in egg parasitoids occurs at the late larval stage. Our study provides the first data on the morphological and volumetric changes of the CNS occurring during the pupal development of the parasitic wasp Trichogramma telengai Sorokina, 1987 (Trichogrammatidae). The prepupal-pupal development includes fusion and concentration of ganglia achieved by the loss of connectives. Volumetric analysis shows that during the pupal development the absolute body volume and CNS volume gradually decrease. The brain and thoracic synganglion slightly increase in volume during the pupal period and extremely decrease from late pupa to adult. The CNS neuropil volume increases from prepupa to adult. The mean cell diameter also decreases during the metamorphosis of the nervous system. The cell body rind volume decreases during pupal development; this decrease correlates with the decrease in the number of cells on the one hand and increase in the neuropilar volume on the other hand.

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 ofScydosella musawasensisHall, 1999 (Coleoptera: Ptiliidae), the smallest free-living insect, using scanning electron microscopy. The antenna ofS. musawasensisbears 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 ofS. 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 ofS. musawasensisand 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.

Body size reduction, also known as miniaturization, is an important evolutionary process that affects a number of physiological and phenotypic traits and helps animals conquer new ecological niches. However, this process is poorly understood at the molecular level. Here, we report genomic and transcriptomic features of arguably the smallest known insect-the parasitoid wasp, Megaphragma amalphitanum (Hymenoptera: Trichogrammatidae). In contrast to expectations, we find that the genome and transcriptome sizes of this parasitoid wasp are comparable to other members of the Chalcidoidea superfamily. Moreover, compared to other chalcid wasps the gene content of M. amalphitanum is remarkably conserved. Intriguingly, we observed significant changes in M. amalphitanum transposable element dynamics over time, in which an initial burst was followed by suppression of activity, possibly due to a recent reinforcement of the genome defense machinery. Overall, while the M. amalphitanum genomic data reveal certain features that may be linked to the unusual biological properties of this organism, miniaturization is not associated with a large decrease in genome complexity.

One of the major trends in the evolution of parasitoid wasps is miniaturization, which has produced the smallest known insects.Megaphragmaspp. (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 ofMegaphragma amalphitanumandM. caribeaand females of the parthenogeneticM. mymaripenneare 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. amalphitanummales 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 ofMegaphragmaprovide material for discussion on the limits to the reduction of insect antenna.

Here is the first description of the visual organ of Acrotrichis grandicollis, a member of Ptiliidae family that includes the smallest free-living insects. The apposition eyes of A. grandicollis have the acone-type crystalline cone; a fused rhabdom is formed by eight retinula cells and surrounded by primary pigment cells. Secondary pigment cells are located only in the distal part of the ommatidium under the lens. The eye consists of about 50 facets about 12 μm in diameter. The A. grandicollis ommatidium ultrastructure has been compared with that of large Coleoptera. The results obtained enabled us to emphasize the compound eye specific features associated with the small body size.

The study of the influence of body size on structure in animals, as well as scaling of organs, is one of the key areas of functional and evolutionary morphology of organisms. Most studies in this area treated mammals or birds; comparatively few studies are available on other groups of animals. Insects, because of the huge range of their body sizes and because of their colossal diversity, should be included in the discussion of the problem of scaling and allometry in animals, but to date they remain insufficiently studied. In this study, а total of 28 complete (for all organs) and 24 partial 3D computer reconstructions of body and organs have been made for 23 insect species of 11 families and five orders. The relative volume of organs was analyzed based on these models. Most insect organs display a huge potential for scaling and for retaining their organization and constant relative volume. By contrast, the relative volume of the reproductive and nervous systems increases by a considerable factor as body size decreases. These systems can geometrically restrain miniaturization in insects and determine the limits to the smallest possible body size.

The body size, especially in cases of extreme reduction, is an important characteristic that strongly determines the morphology, physiology, and biology of animals. Miniaturization is a widespread trend in animal evolution and one of the principal directions of evolution in insects. Miniaturization-related features of insect morphology have been subject to intensive studies during the last few years, but the structure of the smallest insects remains insufficiently known. It is especially important to study hymenopterans of the genus Megaphragma, which include the smallest flying insects and a species in which an almost anucleate nervous system was recently discovered. This article is the first detailed study of the external and internal morphology of adults of Megaphragma mymaripenne and M. amalphitanum using histological methods, 3D computer modeling and other techniques. It is shown that in spite of the extremely small size the organization of Megaphragma retains a considerkable level of structural complexity. On the other hand, miniaturization leads to re-organizations of several organ systems. Unique structural features related to miniaturization have been found in both species: lysis of cell bodies and nuclei of neurons at late stages of pupal development, absence of the heart, and considerable reductions in the set of muscles. Comparative analysis of structure in the smallest insects representing different taxa has revealed common features of the evolutionary process of miniaturization in insects.

A new set of data on the internal and external structure of the adult and larva of the thrips Heliothrips haemorrhoidalis (Bouche, 1833) is presented. The structure of the internal systems of this thrips was revealed using modern methods of 3D computer modelling. The changes in shape and relative size are discussed as an outcome of miniaturization in comparison to the supposed ancestor of this species. The layout of the internal systems of thrips is compared to those of other insects similar in size: beetles of the families Ptiliidae and Corylophidae and wasps of the families Mymaridae and Trichogrammatidae.

Studies on the morphology of Trichogrammatidae are briefly reviewed. The external and internal morphology of Trichogramma and Megaphragma are described in detail. It is shown that in spite of minute size, external structures of adult Trichogrammatidae remain complex. Such internal structures of these wasps as the intestine and tracheal and circulatory systems are considerably simplified; the number of Malpighian tubules is reduced; some muscles are lost. It is shown that the nervous system of adult M. mymaripenne is almost anucleate, because in more than 95 % of cells of the central nervous system, cell bodies and nuclei undergo lysis at later stages of pupal development.