Twisted-Winged Parasites are Friggin' Awesome

If I may flatter myself by supposing that you are a regular reader of this blog, you may wonder why it has the name Life, et al., as opposed to Insects Enliven the Drab Ennui That is my Life (or something to that effect). Why—you may well ask—have I so far ignored the aspects of life that are unrelated to insects (especially parasitic ones), when the title of this blog suggests a vast scope in subjects? Well, I must say that I am well aware that there is more to existence than scurrying mantidfly larvae (to draw an example out of a hat); and I will discuss other subjects that are of concern to me at some point: my antipathy for Highlights for Children, for instance. But not today. Today I will pontificate on twisted-winged parasites. (This vernacular moniker is traduced by many as being used only in "older literature". Ignore that for now.) These are the members of the cosmopolitan insect order Strepsiptera (~600 species in 9/10 families; Pohl, 2002), named for the hind wings of the males, which twist like wrung-out cloths into resting positions. Twisted-winged parasites are not large (4 mm. long in the biggest species); and they are not well-known, either to the public, nor even to those who study them: neither does the fact that they are parasitic (duh) on other insects (of 7 orders; Pohl, 2000) assist entomologists in their study. 

Still, they have a degree of notoriety among entomologists, as was shown when I struck up a conversation with a fellow student at Ohio State University's Stone Laboratory some time ago, and happened to mention twisted-winged parasites.

"Yeah," my peer said, "those things are f*cking awesome."

A male member of Corioxenidae; photographed in Texas by Mike Quinn

Notwithstanding the 510-year-old F-bomb's usage by the fellow, I was happy to find someone with whom I concurred. The aforementioned twisted-winged parasite males are the best jumping-off point for a discussion of strepsipterans in general, since they are the only ones to approach even a modicum of normalcy. Even then, they comprise such a unique suite of features so as to be unmistakable: forewings reduced to halteres (Ulrich, 1930); flabellate antennae that (to me) recall the "great appendages" of arthropod carnivores that swam in the Cambrian Period; blackberry-like eyes that weirdly converge with those of the unrelated long-gone trilobites (Buschbeck et al., 2003); the aforementioned idiosyncratic hindwings; a genome smaller than any other charted insect's (Johnston et al., 2004); and a lack of the trochanter—a segment of the arthropod leg that all other insects possess. Males spend all their brief adult life seeking out a willing member of the opposite sex with which they will...er...perform their part in the Circle of Life (Cook & Derr, 2004). Consequently, these males have no need of mouthparts.

Female of Callipharixenos muiri (Kathirithamby, 1989)

But that's not the half of it. Twisted-winged parasites are some of the most sexually dimorphic creatures out there: as heretofore described, the adult males are active fliers; whereas the full-grown females (in all members of the suborder Stylopidia, which constitutes the majority of living strepsipterans) are inert parasitic bags which lack most of the features we normally associate with animate life: among these eyes, legs, gut, and mouths; only the cephalothorax is left to communicate with the external environment, protruding between the host's abdominal tergites (the abdomen being the portion of the body attacked by all twisted-winged parasites). These surreal miniature faces are a sign by which stylopization (affliction with twisted-winged parasite; Clausen, 1940) may be diagnosed; but the male pupariae (found on the same places on the host's body as the feminine cephalothoraces)—for prior to eclosion*, twisted-winged males are as much parasites as the ladies—are a more obvious indicator of the disease.

A male stylopid (lower left) humpin' an unseen female in a bee's butt; photographed by Colin Boyd

The mature stylopidian female is functionally reduced to a giant womb: the larvae hatch within their mother and swim freely throughout her organ-emptied body cavity (Kathirithamby, 2000), thriving on the maternal haemolymph† (2,252 were in one brood of Stylops swenki; Pierce, 1918); in a sordid twist, their conception involves traumatic insemination: a euphemistic way of saying that the male forcefully punctures his mate's cephalothoracic cuticle with a hypodermic penis (a great name for a rock band, as Dave Barry would remark) whilst clinging by unusually adhesive feet to the host (Pohl & Beutel, 2008): the lack of a visible genital aperture in the females led some (Smith & Hamm, 1914) to suggest that twisted-winged parasites practice parthenogenesis. Such a minimalist anatomy is in all life-forms a probable indicator of parasitism, and it is to this lifestyle that all twisted-winged parasites owe their strangeness.

A Tunisian female of Mengenilla moldrzyki (Mengenillidae); Pohl et al., 2012

Here—yet again—strepsipterans are unique among the Insecta: they are nearly the only true parasites known among that vast class, since they do not kill their hosts as a matter of course (refer to the earlier post "Little Bags of Horror" for the distinction between parasitism and the parasitoid life-cycle that many insects practice). The host may at least suffer, given that in some instances the female parasite may occupy as much as 90% of the abdomen; sterilization is thus a frequent symptom of stylopization (Whiting, 2003). Before you stereotype all strepsipteran females as lazy insect-castrating sacks (not that the males have particularly enriching lives either), however, I must bring to your attention the Mengenillidae: in these less-derived twisted-winged parasites both genders retain a free-living adulthood; the mature females still differ strongly from their male counterparts (being paedomorphic‡), but are nevertheless not so degenerate as the more specialized stylopidians (Silvestri, 1943). Mengenillids are consequently placed in a separate suborder (Mengenillidia) along with a number of extinct families and the most primitive living twisted-winged parasite, Bahiaxenos relicta (Bahiaxenidae) (Bravo et al., 2009).

As indicated previously, all strepsipterans spend at least some portion of their ontogeny as parasites; but all of them are at birth planidia—small, rapid-running larvae, much like those described in "Mantidflies: Chimeras of the Insect World"; their design bent to the purpose of swiftly dispersing in search of hosts. Some species' mothers aid their offspring's quest by ejecting planidia missile-like from the cephalothorax (Subramanium, 1922); the elongated setae seen in many families (see the line drawings at left) enable tremendous leaps to the bodies of bypassing victims (McQueen, 1998). Granted, I doubted the truthfulness of the reports of this jumping ability at first, given that my source also claims that the teaching of evolution directly leads to pornography addiction.

A male Caenocholax fenyesi (Myrmecolacidae) eclosing from an ant (Solenopsis invicta); Cook et al., 2005

Hosts vary to some degree according to the twisted-winged parasites' familial level: for example, Corioxenidae and Callipharixenidae plague true bugs (Heteroptera) (Esaki & Miyamoto, 1965; Kathirithamby et al., 2012), the latter sometimes sunk into the former (McMahon et al., 2011); Stylopidae prefer bees and wasps (Hymenoptera); Mengenillidae, silverfish (Lepismatidae). Halictophagidae are the most heterodox in host preference: one genus afflicts a fruit fly (Tephritidae) (Drew & Allwood, 1985), while another stylopizes pygmy mole crickets (Tridactylidae) (Maxumdar & Chaudhuri, 1999), and yet another cockroaches (Blattodea) (Kathirithamby & Kifune, 1994). Male planidia in Myrmecolacidae parasitize ants, whereas the females seek out grasshoppers (Whiting, 2003): such a wide gulf in hosts is unheard-of anywhere else in the animal kingdom.

If you are familiar with the various insects that begin their lives as planidia, you will know that this initial ontogenetic period invariably corresponds with hypermetamorphosis (complete metamorphosis with subdivision of the larval stage). Hence you could correctly surmise that twisted-winged parasites are hypermetamorphic too (Osswald et al., 2010): once a planidium has penetrated its host (often following the host's molt—the exoskeleton is then more pliant) and plunged into the fluid-filled interior, subsequent instars take a sedentary foot-lacking grub-like shape; a protective bag of exuviae gradually surrounds the larva, since each time it molts it doesn't shed its cuticle. One species masquerades as a part of its katydid host by enclosing itself in a sack of tissue derived from the host's epidermis, thereby deflecting the katydid's immune reaction (Kathirithamby et al., 2003).

Stylops melittae pupae protruding from a Czech wasp; picture credit given to Josef Dvořák

Pupation in both genders of the Mengenillidae occurs following a larval exit from the given afflicted silverfish; stylopidians pupate within their hosts instead. But there's a wrinkle—only the male stylopidians do this, forming a puparium much like a fly's: females dispense with such a stage. Since most twisted-winged parasites practice straightforward complete metamorphosis (holometabolism), albeit all of them with hypermetamorphosis thrown in, their placement in the vast clade called Endopterygota (consisting of all insects with holometabolous development) seems pretty much incontrovertible: but since stylopidian females go so far as to retain their larval eyes into adulthood, even that has been challenged (Kristensen, 1991).

Ripiphorus vierecki (Ripiphoridae), male, photographed by Margarethe Brummermann in Arizona

Thus we arrive at the enigma of the Strepsiptera's place in the insect family tree, debated for the past 220 years, and so infamous that among cladists a reference to "the Strepsiptera problem" requires no elaboration. Given their strangeness, it really is no wonder that taxonomic confusion reigned right from science's first apprehension of the weird little buggers; they were initially classified as ichneumon wasps in yet another case of Systematist's Desperation (Rossi, 1793). From 1813 (the year that William Kirby established the taxon) until the advent of cladistics, entomological orthodoxy held that the Strepsiptera were an order most closely related to the Coleoptera (beetles)—specifically to the wedge-shaped beetles (Ripihoridae); this was so accepted that some coleopterists included twisted-winged parasites in the beetle infraorder Cucujiformia (Crowson, 1960): they're even featured in my copy of Peterson's Field Guide to Beetles (1981). Wedge-shaped beetles exhibit some parallels with the twisted-winged parasites: flabellate antennae in males; hypermetamorphosis; and disuse of the forewings in flight (beetles have, by definition, protectively sclerotized forewings termed elytra). 

But these characteristics do not really form a convincing argument for kinship between the two: many unrelated male insects have extravagantly feathery antennae; hypermetamorphosis has arisen independently in insects several times; and beetle elytra, however ineffectually stunted they happen to be in Ripiphoridae, are functionally dissimilar to the strepsipteran halteres (Pix et al., 1993). Still, the ad hoc placement stood until molecular phylogeny came along in the 1990s and introduced a rival hypothesis. Analyses using genetics (Chalwatzis et al., 1996; Whiting et al., 1997) indicated that the Strepsiptera were a sister-group to the true flies (Diptera), a view not without precedent (Newman, 1864; Pierce, 1918). Both taxa have a wing-pair modified into halteres—but the gyroscopic stabilizers originate from the metathorax in flies, as opposed to the mesothoracic ones in twisted-winged parasites: a big evolutionary jump, in developmental terms; but not in the realm of impossibility with the aid of homeotic mutation (Whiting & Wheeler, 1994).

The two allegedly comprised a clade dubbed "Halteria". This theory, while popular, was not without controversy; an argument was made that the grouping of Strepsiptera and Diptera together was an artifact due to a cladistic phenomenon called "long-branch attraction" (Carmean & Crespi, 1995; Huelsenbeck, 1997), which I will not deign to explain (since I really have no idea what it is): thus it seemed that Halteria was artificial, and strepsipterans' descent remained up in the air. A slew of new (and reputedly improved) morphological/molecular phylogenies (Beutel et al., 2010; McKenna & Farrell, 2010) have now strongly pointed towards twisted-winged parasites' being beetles' closest kin (although not beetles themselves, as some have persisted in suggesting) (Niehuis et al., 2012). For the time being, thus, we may say that beetles are twisted-winged parasites' nearest relatives.



*Emergence from the pupa.
†The internal bodily fluid that bathes the organs of arthropods, analogous to vertebrate blood and lymph.
‡ Larva-like but sexually mature.
____________________________________________________________

Beutel, R. G.; Friedrich, F.; Hörnschemeyer, T.; Pohl, H.; Hünefeld, F.; Beckmann, F.; Meier, R.; Misof, B.; Whiting, M. F.; and Vilhelmsen, L. Morphological and molecular evidence converge upon a robust phylogeny of the megadiverse Holometabola [electronic version]. Cladistics, 27(4), 341-355. Retrieved 2/24/13 from http://onlinelibrary.wiley.com/doi/10.1111/j.1096-0031.2010.00338.x/abstract

Bravo, F.; Pohl, H.; Silva-Neto, A.; and Beutel, R. G. (2009). Bahiaxenidae, a “living fossil” and a new family of Strepsiptera (Hexapoda) discovered in Brazil [electronic version]. Cladistics: the International Journal of the Willi Hennig Society, 25(6), 614-623.

Buschbeck, E.; Ehmer, B.; and Hoy, R. (1999). Chunk versus point sampling: visual imaging in a small insect. Science, 286, 1178-1180.

Carmean, C. and Crespi, B. J. (1995). Do long branches attract flies? Nature, 373, 666.

Crowson, R. A. (1960). The phylogeny of Coleoptera. Annual Review of Entomology, 5, 111-134. 

Clausen, C. P. (1940). Entomophagous Insects. New York City: McGraw-Hill.


Chalwatzis, N.; Hauf, J.; van de Peer, Y.; Kinzelbach, R.; and Zimmermann, F. K. (1996). 18S ribosomal RNA genes of insects: primary structure of the genes and molecular phylogeny of the Holometabola. Annals of the Entomological Society of America, 89, 788-803.

Cook, J. L.; Calcaterra, L. and Nuñez, L. (2005). First record of Caenocholax fenyesi (Strepsiptera: Myrmecolacidae) parasitizing Solenopsis invicta (Hymenoptera: Formicidae) in Argentina, with a discussion of its distribution and host range. Entomological News, 115(2), 61.

Cook, J. L. and Derr, D. P. (2004). Antennal morphology of Caenocholax fenyesi (Strepsiptera: Myrmecolacidae) based on scanning electron microscopy. ESA Annual Meeting.


Drew, A. I. and Allwood, J. A. (1985). A new family of Strepsiptera parasitizing fruit flies (Tephritidae) in Australia. Systematic Entomology, 10, 129-134.

Esaki, T. and Miyamoto, S. (1965). The Strepsiptera parasitic on Heteroptera. Proceedings of the International Congress of Entomology, Montreal; 1, 375-381.

Huelsenbeck, J. P. (1997). Is the Felsenstein Zone a fly trap? Systematic Biology, 46, 69-74.

Johnston, J. S.; Ross, L. D.; Beani, L.; Hughes, D. P.; and Kathirithamby, J. (2004). Tiny genomes and endoreduplication in Strepsiptera. Insect Molecular Biology, 13(6), 581-585.

Kathirithamby, J. (1989). Review of the order Strepsiptera. Systematic Entomology, 14, 41-92.

Kathirithamby, J. (2000). Morphology of the female Myrmecolacidae (Strepsiptera) including the apron, and an associated structure analogous to the peritrophic matrix. Zoological Journal of the Linnean Society, 128, 269-287.

Kathirithamby, J. and Kifune, T. (1994). Strepsiptera (Insecta) parasitizing Onychostylus pallidiolus (Shiraki), the blattellid cockroach in southwestern-most Japan. Entomologist, 113, 217-219.

Kathirithamby, J.; McMahon, D. P.; Anober-Lantican, G. M.; and Ocampo, V. R. (2012). An unusual occurrence of multiparasitism by two genera of Strepsiptera (Insecta) in a mango leafhopper Idioscopus clypealis (Lethierry) (Hemiptera: Cicadellidae) in the Philippines [electronic version]. Zootaxa, 3268, 16-28. Retrieved 2/19/13 from http://mapress.com/zootaxa/2012/f/z03268p028f.pdf 

Kathirithamby, J.; Ross, L. D.; and Johnston, J. S. (2003). Masquerading as Self? Endoparasitic Strepsiptera (Insecta) Enclose Themselves in Host-Derived Epidermal Bag. Proceedings of the National Academy of Sciences of the United States of America, 100(13), 7655-7659.

Kristensen, N. P. (1991). Phylogeny of extant hexapods. In Naumann, I. D.; Cornell, P. B. C.; Lawrence, J. F.; Neilson, E. S.; Spradberry, J. P.; Taylor, R. W.; Whitten, M. J.; and Littlejohn, M. J. (eds.): The Insects of Australia: a Textbook for Students and Research Workers (2nd ed.) (pp. 125-140). CSIRO, Melbourne: Melbourne University Press.

Maxumdar, A. and Chaudhuri, P. K. (1999). Strepsipteran insects of the genus Tridactylophagus Subramaniam from India (Strepsiptera: Halictophagidae). Journal of South Asian Natural History, 4(1), 13-17.

McKenna, D. D. and Farrell, B. D. (2010). 9-Genes Reinforce the Phylogeny of Holometabola and Yield Alternate Views on the Phylogenetic Placement of Strepsiptera. PLoS ONE, 5(7), e11887. Retrieved 2/24/13 from http://www.torna.do/s/9-genes-reinforce-the-phylogeny-of-holometabola-and-yield-alternate-views-on-the-phylogenetic-placement-of-Strepsiptera/

McQueen, R. (1998, June 1). Hitch-Hiking Insects [electronic version]. Creation. Retrieved 2/18/12 from http://www.answersingenesis.org/articles/cm/v20/n3/hitch-hiking-insects

Newman, E. (1864). Natural situation of Stylops among insects. Entomologist, 2, 231-232.

Niehuis, O.; Hartig, G.; Grath, S.; Pohl, H.; Lehmann, J.; Tafer, H.; Donath, A.; Krauss, V.; Eisenhardt, C.; Hertel, J.; Petersen, M.; Mayer, C.; Meusemann, K.; Peters, R. S.; Stadler, P. F.; Beutel, R. G.; Bornberg-Bauer, E.; McKenna, D. D.; and Misof, B. (2012). Genomic and Morphological Evidence Converge to Solve the Enigma of Strepsiptera. Current Biology, 22, 1-5.

Osswald, J.; Pohl, H.; and Beutel, R. G. (2010). Extremely miniaturized and highly complex: the thoracic morphology of the first instar larva of Mengenilla chobauti (Insecta, Strepsiptera). Arthropod Structure & Development, 39, 287-304. 

Pierce, W. D. (1918). The comparative morphology of the order Strepsiptera. U.S. National Museum Proceedings, 54, 391-501.

Pix, W.; Nalbach, G.; and Zeil, J. (1993). Strepsipteran forewings are haltere-like organs of equilibrium. Naturwissenschaften, 80, 371-374.

Pohl, H. (2000). Die Primärlarvenächerflügler—evolutionäre Trends (Insecta, Strepsiptera). Kaupia, Darmstädter Beiträge zur Naturgeschichte, 10, 1-144.

Pohl, H. (2002). Phylogeny of the Strepsiptera based on morphological data of the first instar larvae. Zoologica Scripta, 31, 123-134.

Pohl, H. and Beutel, R. G. (2008). The evolution of Strepsiptera (Hexapoda). Zoology, 111(4), 318-338. 

Pohl, H.; Niehuis, O.; Gloyna, K.; Misof, B.; and Beutel, R. G. (2012). A new species of Mengenilla (Insecta: Strepsiptera) from Tunisia. ZooKeys, 2012(198), 79-101. Retrieved 20/2/13 from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3368257/

Rossi, P. (1793). Observation de M. Rossi sur un nouveaugenre d'Insecte, voisin des Ichneumons. Bulletin de la Société Philomatique à ses Correspondants, 1(49).

Silvestri, F. (1943). Studi sugli 'Strepsiptera' (Insecta). III. Descrizione e biologia di 6 specie italiane di Mengenilla. Boll. Lab. Zool. Gen. Agr. Fac. Agr. Portici, 32, 197–282.

Smith, G. and Hamm, A. H. (1914). Studies in the experimental analysis of sex, pt. II: On Stylops and stylopization. Quarterly Journal of Microscopic Science, 60, 435-461.

Subramanium, T. V. (1922). Some natural enemies of the mango leafhoppers (Idiocerus spp.) in India. Bull. Ent. Res., 12, 465-467. 

Ulrich, W. (1930). Die Strepsipteren-Männchen als Insekten mit Halteren an Stelle der Vorderflügel. Zeitschrift für Morphologie und Ökologie der Tiere, 17, 552-624.


Whiting, M. F. (2003). Strepsiptera. In Resh, V. H. & Cardé, R. T. (eds.): Encyclopedia of Insects (pp. 1094-1096). Waltham: Academic Press.

Whiting, M. F. and Wheeler, W. C. (1994). Insect homeotic transformation. Nature, 368(696).

Whiting, M. F.; Carpenter, J. C.; Wheeler, Q. D.; and Wheeler, W. C. (1997). The Strepsiptera problem: phylogeny of the Holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology, 46, 1-68.