Who or what are Strepsiptera? The Strepsiptera, or ‘twisted-winged parasites’ are an order of parasitic insects. They can be found all over the world, living inside a wide variety of insect hosts. They were discovered in 1793 and are defined as ‘entomophagous endoparasitoids’. Strepsipterans attack insect species from 34 families distributed across seven orders — from silverfish to true flies. Strepsiptera are considered a small insect order with only around 600 described species; although this figure is almost certainly a considerable underestimate. Whom they are most closely related to has been controversial, but recent studies suggest they are more closely related to beetles or their allies (the neuropterids) than to flies or other insects. What is so unusual about them? Being parasitoids, strepsipterans show a number of extraordinary life-style features; for instance, the sexes are dramatically dimorphic. Females almost universally live in the host from infection as first instar larvae, right until the end of their life cycle. Consequently, they have lost eyes, antennae, legs and wings, and instead retain a larva-like appearance during reproductive maturity. The result is a cryptic and morphologically simplified organism (Figure 1). This is counterbalanced by increased size and reproductive output. Males, by contrast, emerge after pupation in the host as small free-flying insects. Their only task in the outside world is to find a female. This must make sex rather cumbersome? True. Mating has to occur with the female inside the living host. The female extrudes a structure, the cephalothorax, through which the male inserts his sperm. Females give birth to live young, which is untypical for most insects, and the progeny reach the outside world via an external brood canal opening in the cephalothorax. The first instar larvae then actively seek out a new host — but how exactly they do this is not known. Is this true for all strepsipterans? No. In contrast to the above, one strepsipteran family (Mengenillidae) displays ‘transitional’ parasitic characteristics, i.e. pupation takes place outside the host, and the female is free-living. What happens to the hosts? Strepsipterans have a very interesting interaction with their hosts. They sit very close to the parasite–parasitoid boundary. While parasitoids (typically wasps) directly kill their hosts, the association between strepsipterans and their hosts lasts longer and is more stable than in other parasitoids. Little experimental work has been conducted on how strepsipterans alter the behaviour of their hosts. Initial studies suggest that paper wasps that have been stylopised — this term is used to describe insects parasitised by Strepsiptera — desert the colony to form aggregates outside of the nest. Stylopisation can also result in morphological alterations: for example, in infected plant and leaf hoppers external genitalia can be extremely reduced, or even lost entirely. Why are strepsipterans so little known? This may be primarily due to the fact that they hardly occur as free-living insects — except for some members of the family Mengenillidae and the brief female-searching expedition of males, which live for only five to six hours as adults. Adult female Strepsiptera are only distinguishable by the presence of the cryptic cephalothorax that protrudes from the cuticle of the host, and juveniles can only be discovered by host dissection. So, why should we care about them? Their unique biology makes them an exciting model system for a wide range of questions. In evolution and ecology, parasites are crucial subjects for research, from their role in food webs and biological control to the underlying causes of speciation and host specificity. The strepsipteran family Myrmecolacidae is of special interest because it is parthenogenetic and includes one of the smallest insect genomes so far recorded. Furthermore, Myrmecolacidae display a very rare strategy: males and females of the same species attack completely different host species (males typically infect ants, whereas females attack grasshoppers, crickets or praying mantids). Male hosts include the invasive red imported fire ant, Solenopsis invicta, a highly problematic pest species that has severe negative consequences for humans and wildlife. The flight and sensory systems of male strepsipterans are also of interest. For example, the anatomical organization of the eye has been proposed as a modern counterpart to the ancient trilobite visual system, and their forewings are functionally ‘analogous’ to the halteres of true flies. In addition to the unusual fan-like shape of the flight-providing hindwings, these structural oddities may offer important comparative insights into sensory evolution and the biomechanics of insect flight. Furthermore, while a number of insect groups demonstrate considerable sexual dimorphism, none are quite like Strepsiptera, the females of which are morphologically extremely simplified. By comparing Strepsiptera with different insect systems, developmental studies could offer important insights into the evolution of development and metamorphosis.
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