Halteres
Halteres are a pair of small club-shaped organs on the body of some flying insects that provide information about body rotations during flight. They are present on insects belonging to two orders, Diptera and Strepsiptera. In dipterans, the halteres evolved from a pair of ancestral hindwings, while males of the much smaller strepsiterans have halteres evolved from a pair of ancestral forewings.
Halteres oscillate rapidly along with the wings and operate like vibrating structure gyroscopes: any rotation of the plane of oscillation causes a force on the vibrating halteres by the Coriolis effect. The insect detects this force with sensory organs called campaniform sensilla and chordotonal organs located at the base of the halteres and uses this information to interpret and correct its position in space. Halteres provide rapid feedback to the wing-steering muscles, as well as to the muscles responsible for stabilizing the head.
Background
The majority of insects have two pairs of wings. Flies possess only one set of lift-generating wings and one set of halteres. The order name for flies, "Diptera", literally means "two wings", but there is another order of insect which has evolved flight with only two wings: strepsipterans, or stylops; they are the only other organisms that possess two wings and two halteres. The strepsipterans have adapted their forewings into halteres, whereas dipterans have adapted their hindwings into halteres. This unique structure which detects rotations/perturbations during flight has never been described in nature elsewhere, though many flying insects have been shown to detect Coriolis forces from their non-specialised wings.Halteres are able to sense small deviations in body position using the gyroscopic properties of moving mass. What this means is that halteres beat up and down in time with the flapping of the wings along a linear pathway, but when the fly's body begins to rotate, the path of the beating halteres also changes. Now, instead of the halteres following a linear path, they begin to follow a curved path. The larger the perturbation they experience, the farther the halteres move from their original linear path. During these periods, the haltere is no longer moving in only two directions, but four. The force exerted on the halteres in response to this left right movement is known as Coriolis force and can be produced when any moving object is rotated in the three directions of rotation, yaw, pitch or roll. When this occurs, tiny bell-shaped structures at the base of the haltere experience strain as the haltere stalk bends in their direction. The nervous system can then transform the bending of these hairs into electrical signals, which the fly interprets as body rotation information. The fly uses this information to make corrections to its position and thereby restabilizes itself during flight. Further details explaining the dynamics and physiology of halteres are described below.
Halteres are typically only associated with flight stabilization, but their ability to detect body rotations can elicit compensatory reactions not only from the wing steering muscles, but also from neck muscles which are responsible for head position and gaze. Halteres may also be useful for other behaviors. Certain species of flies have been observed to oscillate their halteres while walking in addition to oscillating them during flight. In these individuals, halteres could thus be detecting sensory information during walking behavior as well. When the halteres are removed, these insects perform more poorly at certain walking challenges. However, how haltere information is processed and used during walking remains, with few exceptions, unclear. Specific examples of what has been found are described below.
History
Halteres were first documented by William Derham in 1714. He discovered that flies were unable to remain airborne when their halteres were surgically removed, but otherwise behaved normally. This result was initially attributed to the haltere's ability to sense and maintain equilibrium. In 1917 v. Buddenbrock asserted that something else was responsible for the flies' loss of flight ability. He claimed that the halteres should instead be considered "stimulation organs". In other words, that the activity of the halteres energized the wing muscular system, so that they acted as an on/off switch for flight. V. Buddenbrock attempted to show that activation of the halteres would stimulate the central nervous system into a state of activity which allowed the wings to produce flight behavior. It has since been concluded that this is not in fact true, and that the original assertion that halteres act as balance organs is the correct one. V. Buddenbrock was able to show that immediately after haltere removal flies were unable to produce normal wing movements. This was later explained by the fact that allowing flies a few minutes recovery time post-surgery resulted in total recovery of normal flight muscle control. Further, in an interesting side experiment performed by Pringle, when a thread was attached to the abdomen of haltereless flies, relatively stable flight was again achieved. The thread in these experiments presumably aided in keeping the fly from rotating, which supported the hypothesis that halteres are responsible for sensing body rotations.The original balancer theory, which was postulated by Pringle, only accounted for forces produced in two directions. Pringle claimed that yaw was the only direction of rotation that flies used their halteres to detect. Using high speed video analysis, Faust demonstrated that this was not the case and that halteres are capable of detecting all three directions of rotation. In response to this new discovery, Pringle reexamined his previous assumption and came to the conclusion that flies were capable of detecting all three directions of rotation simply by comparing inputs from the left and right sides of the body. Of course, this is not the actual mechanism by which flies detect rotation. Different fields of sensory organs located in different regions at the base of each haltere detect the different directions of rotation, which also explains why flies with one haltere are still able to fly without issue.
Evolution
It is generally accepted that the halteres evolved from the non-flight wings of insects – the hind-wings of Diptera and the fore wings of Strepsiptera respectively. Their movement, structure, function and development all support this hypothesis. Characterizations of the arrangement of sensory organs known as campaniform sensilla, found at the base of the haltere, show many similarities to those found at the base of the hindwings in other insects. The sensilla are arranged in a way so similar to that of hindwings, that were the halteres to be replaced with wings, the forces produced would still be sufficient to activate the same sensory organs. Genetic studies have also brought to light many similarities between fly halteres and hindwings. In fact, fly haltere development has been traced back to a single gene, which when deactivated results in the formation of a hindwing instead. Because just a single gene is responsible for this change, it is easy to imagine a small mutation here leading to the formation of the first halteres.Convergent evolution
Though no other structure with entirely the same function and morphology as halteres has been observed in nature, they have evolved at least twice in the class Insecta, once in the order Diptera and again in Strepsiptera. Also the winged males in scale insects have a reduced second pair of wings modified into halterer like organs. Another structure in the class Insecta also exists whose primary function is not the same as halteres, but that additionally serves a similar balancing function. This occurs in the order Lepidoptera and refers to the antennae of moths and butterflies.Strepsipteran haltere
ns are a unique group of insects with major sexual dimorphism. The females spend their entire lives in a grub-like state, parasitizing larger insects. The only time they ever come out of their host insect is to extend their fused heads and thoraces for males to notice. The males are also parasites, but they eventually will leave their host to seek their female counterparts. Because of this, they still retain the ability to fly. Male strepsipterans uniquely possess two hindwings, while their forewings have taken on the club-like form of halteres. Though strepsipterans are very difficult to locate and are additionally rather short-lived, Pix et al. confirmed that the specialized forewings that male Strepsiptera possess perform the same function as dipteran halteres. Rotational movements of the body combined with the oscillating halteres produce Coriolis forces that can be detected by fields of mechanosensors located at the base of the halteres. Using functional morphology and behavior studies, Pix et al. showed that these sensors then transmit body position information to the head and abdomen to produce compensatory movements. For simplicity, the remainder of this article will refer only to dipteran halteres.Lepidopteran antennae
Certain lepidopterans exhibit small amplitude oscillation of their antennae at constant angles during flight. Antennal movements in lepidopterans were originally hypothesized to aid in wind or gravity perception. A study performed using the hawk moth, Manduca sexta, confirmed that these tiny, antennal oscillations were actually contributing to body rotation sensation.Sane et al. determined that antennae were responsible for flight stabilization in hawk moths by removing the long part of the antenna, then reattaching it to determine its influence on flight performance. When the flagella were removed, the moths were no longer able to maintain stable flight. After reattachment of the flagella, flight performance was restored. The source of this difference was determined to be mechanosensory. There are two sets of mechanosensory organs located at the base of the lepidopteran antenna, Böhm's bristles and the Johnston organ. These fields of receptors respond to different directions of antennal movements. Antennae are also capable of sensing odor, humidity, and temperature. Sane et al. was able to demonstrate that it was the mechanosensors that were responsible for flight stability as opposed to the other sensory organs, because when the flagella were removed and then reattached, all antennal nerves were severed excluding those at the base.