Strepsiptera (twisted-winged parasites) is a cosmopolitan order of small insects (males, 1-7 mm; females, 2-30 mm) that are obligate insect endoparasites. The order comprises ~600 species placed within 10 extant and 2 extinct families. Strepsiptera derive their common name from the male front wing, which is haltere-like, and early workers considered it to be twisted in appearance when dried specimens were examined. All members of this group spend the majority of their life cycle as internal parasites of other insects and consequently have a highly specialized morphology, extreme sexual dimorphism, and a unique biology.
BIOLOGY
The adult male strepsipteran is free living and winged, whereas the adult female is entirely parasitic within the host, with the exception of one family (Mengenillidae) in which the female last instar leaves the host to pupate externally. Strepsiptera parasitize species from seven insect orders: Zygentoma, Orthoptera, Blattodea, Mantodea, Hemiptera, Hymenoptera, and Diptera. In one family (Myrmecolacidae), the males are known to parasitize ant hosts, whereas the females are parasites of Orthoptera and Mantodea. The life cycle of most strepsipteran species is unknown, and only a few species have been studied in detail.
The first instar is free living, emerges from the female brood canal, and disperses to the surrounding vegetation in search of a new insect host. In some species, the larvae have long abdominal setae that are used to propel them on to a new host. These larvae may be carried back to the nest of a social host to begin parasitizing the host’s larvae or may simply spring onto the early instars of a nonholometabolous host. In Stylops pacificus, the abdominal setae are short and the larvae are transported to the nest inside of the crop of the bee Andrena complex, where it will begin parasitizing a single egg of the bee.
Once a first instar enters a new host, it molts into an apodous larva and feeds transcutaneously from the host’s hemolymph. Elenchus tenuicornis undergoes two additional molts prior to pupation; apol-ysis is not followed by ecdysis in strepsipteran larvae, such that the cuticle of the second to the fourth instar forms the puparium. In Mengenillidae, both sexes leave the insect host to pupate externally. The remaining Strepsiptera pupate in the host with a portion of the head and thorax extruded from the host’s cuticle (Fig. 1C ).
Males will emerge from the puparium and seek out a female for mating. Virgin females release a pheromone to attract males, and in Stylopidia, the male copulates by rupturing the female’s brood canal opening between her head and prothorax in a process referred to as hypodermic insemination. Adult males live only a few hours, which makes them difficult to collect, although they are occasionally found at lights or may be lured to a virgin female kept in a cage in the field. Adult males do not feed and their mouthparts are partly modified into sensory structures. After insemination, females may live for a few weeks to a few months. In Xenos peckii, the female is typically inseminated in the fall and she remains in the wasp host until spring, when the planidial larvae emerge. The female may be an enormous endoparasite relative to the size of its host. For example, X. peckii may fill up to 90% of the abdominal cavity of the wasp host. It is
FIGURE 1 (A) First instar of Mengenilla chobauti. (B) Male pupa of Xenos peckii. (C) Cephalothorax of female X. peckii extruded from the abdominal tergites of the wasp host Polistes fuscatus. (D) Close-up of cephalothorax of female X. peckii. (E) Female Xenos vesparum. (F) Head and thorax of M. chobauti. (G) Male Triozocera bedfordiensis. (H) Male Coriophagus rieki.
relatively common to find a host that has been parasitized by multiple males and/or females.
MORPHOLOGY
First instars bear stemmata (simple, single-lens eyes), mandibles, maxillae, and a labium. Antennae are absent. Abdominal tergites are typically smooth, the abdominal sternites are serrate, and the legs are filiform with slender tarsi (Fig. 1A). In Mengenillidae, the pupae are free living and have legs, mouth, and a segmented abdomen. In the remaining Strepsiptera, the puparium is tanned and male pupae possess compound eyes, abdominal and thoracic segmentation, and developing wings, legs, and antennae (Fig. 1B).
The adult male has large compound eyes, with ommatidia separated by cuticle and/or setae, giving the eye a blackberry appearance. Antennae are flabellate and the mandibles are conical, except in Corioxenidae, which entirely lack mandibles (Fig. 1F). The first pair of wings is reduced, clubbed, and morphologically similar to the halteres of Diptera. The hind wings are enlarged and venation is reduced, and these wings are used for flight (Fig. 1G). The prothorax is small and saddle shaped, and the metathorax is large and bears the principal flight muscles. The trochanter is fused with the femora in the fore- and middle legs, the hind legs lack free coxae, and the tarsi have two to five segments and may lack a tarsal claw (Fig. 1H).
The adult female lacks wings, legs, and external genitalia, and only rudiments of the mouthparts, antennae, and eyes remain (Figs. 1D and 1E). The thorax and head are fused to form a heavily sclerotized cephalothorax, and this is the portion of the female that is extruded from between the abdominal segments of its host. The abdomen is large, segmentation is reduced, and the cuticle is unsclerotized, which allows nutrients to pass from the host to the developing embryos. The tracheation and the nervous system are reduced, and the reproductive system is highly modified, allowing the production of vast quantities of eggs that are freely distributed throughout the abdominal cavity.
CLASSIFICATION
A recent comprehensive morphological analysis has provided new insights into strepsipteran phylogeny. At the root of the strepsipteran tree are three distinct lineages represented only by fossils: the Baltic amber fossil Protoxenos (Protoxenidae), the Burmese amber fossil Cretostylops. and the Baltic amber fossil Mengea (Mengeidae). The most basal extant family is Mengenillidae, a primitive strepsipteran group with females that are free living, bearing rudimentary legs, antennae, and a single genital opening, and the males have robust mandibles and a hind wing with an elongated and sturdy MA vein. The majority of species belong to the group Stylopidia, the mono-phyly of which is supported by the fact that females are found in the host, the female has multiple genital openings, and the hind wing in the male has only residues of the MA1 vein. There are nine families that belong in Stylopidia and are arranged in the following order from the base to the apex of a comblike tree: Corioxenidae, Bohartillidae, Halictophagidae, Elenchidae, Protoelencholacidae, Myrmecolacidae, Callipharixenidae, Xenidae, and Stylopidae.
PHYLOGENY AND EVOLUTION
The phylogenetic position of Strepsiptera relative to other insect orders has been one of the most contentious issues in insect systemat-ics, and controversy still exists as to their phylogenetic affinity. There have been four phylogenetic hypotheses presented: (1) placement as a group somewhere within Coleoptera, as suggested by the superficial similarities in their parasitic lifestyle and morphology with certain beetle groups; (2) placement as sister group to Coleoptera, as suggested by the powering of flight via the hind wing; (3) placement outside of Holometabola, as suggested by the presence of larval stemmata; and (4) placement as sister group to Diptera, as suggested by DNA sequence data and other homologies. The latter hypothesis has been the most controversial and different interpretations of the molecular data have been presented, though the most recent sequence data continue to support this hypothesis. If Strepsiptera are indeed sister group to Diptera, then this gives rise to some intriguing possibilities in insect evolution. Functionally, the halteres of Diptera and Strepsiptera appear identical, both highly specialized to serve as a gyroscopic balancing mechanism during flight. Therefore, it is possible that the mesotho-racic halteres of Strepsiptera were derived via a specialized mutation in the genes controlling the development of the metathoracic halteres in Diptera, essentially causing the wings of the dipteran to switch positions to produce the type of wings as observed in Strepsiptera.
