Flagellate Tarsi & Stick Insects

And now, in a fit of laziness, I will reproduce a post I wrote earlier for the University of Kentucky's official blog, The Daily Entomologist (more accurately dubbed The Erratic Entomologist). Due to copyright concerns resulting from that blog's public nature, I was unable to publish this post with the illustrations: Life, et al. is not bound by such restrictions. Nonetheless, "Flagellate Tarsi & Stick Insects" will feature fewer pictures than hitherto, since the subject–an enigmatic family of Mesozoic insects called the Chresmodidae–hasn't ever been featured in any life restorations.

Anyway, the wonderful thing about paleontology is that the extinct things one encounters through it are not always directly analogous to modern life forms. Dinosaurs, trilobites and ammonites–the Holy Trinity of paleontology–are all certainly not alien, but they aren't just humdrum prehistoric blueprints of their current ecological counterparts, being rather something distinctive and apart. 

Fossilized insects, unfortunately, do not often diverge dramatically from modern ones: it seems that once a body-plan evolves among them it is never lost, and if its exponents die out utterly it will likely be recapitulated later on by an unrelated lineage. The notorious griffinflies (order Meganisoptera) that patrolled Earth's skies for 67 million years, including the 28-in.wingspan Meganeuropsis, were essentially hawk-sized dragonflies (a taxonomic oversimplification but an ecological truth); the various members of the superorder Dictyoptera (cockroaches, mantids and termites), both living and dead, are more or less Variations on the Theme of "I Am a Roach"–e.g., We Are Roaches With Sclerotized Forewings (Umenocoleidae), We Are Carnivorous Mantis-Like Roaches (Raphidiomimidae), I Am a Roach With Earwig-esque Cerci With Which I Probably Clasped My Mate (Fuziidae), and I Am a Roach With Leaping Hind Legs and a Name Like That of a Romulan (Skok). 

Thankfully, there are exceptions. The Kalligrammatidae were fluttering, colorful pollinators often termed "the butterflies of the Mesozoic"...but they were close kin of antlions (which they hardly resembled), and are only distant cousins of their extant namesakes. (See "Butterflies Before Butterflies, Flowers Before Flowers".) And, of course, there were the Chresmodidae, which are what I am posting about, although it may be hard to tell that from what I have written so far.

Chresmodids were spindly insects with slender, elongated legs. Females were winged; males, wingless. Their wing morphology (and venation), cerci, and ovipositor unanimously point to an affinity with the Polyneoptera, a varied assemblage of such organisms as grasshoppers, earwigs, and praying mantises (although chresmodids were classified elsewhere as recently as 1980). The fact that chresmodid nymphs are known (indicating that, like polyneopterans, they exhibited incomplete metamorphosis) seals the matter (Delclòs et al., 2008). But beyond that their relationships are debatable–this being but one of their interesting aspects.

Crummy picture of a crummy fossil of Chresmoda obscura

Glancing at a specimen of a chresmodid (particularly if it is a nymph) one is impressed with a general similarity in habitus to a water strider (Gerridae), a living bug with which all are familiar. This resemblance is not coincidental. Chresmodids, too, possessed velvety tarsi (feet)–an adaptation in water striders to prevent breaching the surface tension of the water on which they skate (which is far from the most peculiar of chresmodid tarsal features, as we shall see): paleontologists have thus deduced that the subjects of this post also hunted and scavenged on the surface of water, propelled by warping the ductile meniscus with pressure exerted through their feet (as can be seen in the photograph below). Interestingly, in Recent times only some members of the order Hemiptera (true bugs)–to which the Chresmodidae certainly do not belong–have such a lifestyle among the insects.

In flagrante delicto Quebecoi Aquarius remigis (Gerridae); caught in the act by Philippe Moniotte

If the analogy holds true, though, one can't help but notice that Chresmoda sp. grew to sizes far greater than any water strider: an adult female C. neotropica's wingspan was 55.6 mm (with far lengthier legs), and it wasn't even the largest species (Delclòs et al., 2008): by contrast, Gigantometra gigas, the largest water strider, has limbs that span 36 mm (Andersen, 1982). Given that Gerridae already push the limits of physics by walking on water, one wonders how the heck their vaster polyneopteran counterparts did so. Of course, the idea that they were aided by vegetative flotsam cannot be discounted; but if so, why have water striders (and other surface-inhabiting hemipterans) not also taken advantage of this and thus grown to comparatively behemoth sizes? A good number of chresmodids (including the largest species) lived on brackish waters (i.e. lagoons), meaning that they had the advantage of increased density (since more salt=denser water)–but members of Gerromorpha (the infraorder to which water striders & co. belong) are tolerant of salinity as well. 


No, it appears that Chresmoda sp. owe their gigantism to a unique aspect of their tarsi: namely, the fact that said tarsi were unreservedly flagellate, the 2 foremost tarsomeres (the segments which comprise an insect's foot) being subdivided into an excess of 40 tiny articles in what was apparently a means of spreading weight (Martínez-Delclòs, 1991). Why does this warrant italicization? Well, the foundational morphology from which all insects descend has no more than 5 podites: numerous lineages among the Insecta have less than that, but never more, with the strange exception of Chresmoda.

A Carcharodontosaurus saharicus skull compared to that of a Homo sapiens by Louie Psihoyos

In search of an explanation for the sinuous feet of the Chresmodidae we venture into the wily realm of developmental genetics. Possibly, a gene regulating segment multiplication in the antennae shifted to the legs, which, these limbs being serially homologous, is not implausible; or perhaps the gene responsible for tarsomere arrangement simply went overboard with the apical podites ("over-expression"). However, additional mutations in unrelated parts of the genome–specifically, those parts dealing with tarsal musculature–would be necessary in order for the newly super-multiarticulate feet to function. This could explain why this route for dealing with supporting one's weight on fluid occurred only once in the insects (Nel et al., 2004); but however it appeared, the chresmodids were certainly successful in their own time, living for at least 80 mya (Aalenian-Cenomanian Epochs) at both ends of Eurasia and in South America. What killed them off is open to conjecture, but the greenhouse event that occurred worldwide ~92 mya might have done it (Delclòs et al., 2008); if so, chresmodids' fellow victims included the fearsome carcharodontosaurids (among other things) (Brusatte and Sereno, 2005).

The gates of Hades swing wide and from the abyss comes Damon diadema!

Oddly enough, though, arachnids are no strangers to whip-like tarsi, the feature appearing independently in the orders Amblypygi, Uropygi, Schizomida, Palpigradi, and Opiliones. Of these, only Opiliones (harvestmen) have suchlike tarsi on all legs (as do Chresmodidae): the other four restrict antenniform feet to the foremost pair (as in the adjacent amblypygid). But as the epithet "antenniform" might suggest, these arachnids' augmented tarsi are entirely sensorial in function, in contrast to the chresmodids' ambulatory ones; furthermore, the members of the cited orders are exclusively terrestrial.

Sea spider (Phoxichilidiidae: Anoplodactylus evansi) photographed by Bill Rudman near New South Wales

In the 174 years chresmodids have been known their taxonomy has been a subject of prolonged debate and confusion. Ernst Friedrich Germar (1786-1853), author of the name Chresmoda (Germar, 1839), initiated the mess when he attributed that moniker to a colleague despite the work in the descriptive monograph being clearly his own; numerous species–Pygolampis gigantea (Germar, 1839), Propygolampis bronni (Weyenbergh, 1874), Saurophthirodes mongolicus (Ponomarenko, 1986), Sternarthron zitteli (Haase, 1890), Gryllidium oweni (Westwood, 1854)–and the genus Halometra (Oppenheim, 1888) were synonymized with the type (C. obscura) over the years (Handlirsch, 1906), often being initially classified in a separate order from their senior synonym: indeed, the poorly preserved S. zitteli was frequently classified as an arachnid (Petrunkevitch, 1955; Kuhn, 1977; Rowland & Sissom, 1980), and even compared to the bizarre sea spiders (class Pycnogonida) (Frickhinger, 1999) in what was probably an instance of systematist's desperation (akin to writer's block).

Water measurer (Hydrometra martini, Hydrometridae) photographed by Tom Murray

The Chresmodidae played taxonomic musical chairs for many years, being placed in the orders Mantodea (Germar, 1839), Hemiptera (Popov, 1980), Orthoptera, Phasmatodea (Martynov, 1928), Paraplecoptera (="Grylloblattaria") or floating somewhere in the clade Archaeorthoptera/Gryllones/Orthopterida (Rasnitsyn & Quicke, 2002). They have been regarded as water measurers (Hydrometridae), a living family of twig-like gerromorphans (Oppenheim, 1888); Frank M. Carpenter, then-curator of fossil insects at Harvard, alleged in 1992 that the holotype of Chresmoda was actually a plain ol' locust that had been accidentally confused with the typical chresmodid Propygolampis (Carpenter, 1992). Whodathunkit? However, Carpenter ungraciously kicked the bucket before he could elaborate on his theory, and searches of his workplace for drafts of a forthcoming manuscript substantiating his hypothesis turned up nothing.

Timema sp. (Timematidae) pornography created by Scott Peden

By far the most frequent ordinal attribution (if any) for Chresmodidae, however, is to the Phasmatodea, or stick and leaf insects. Some even went so far as to include the living Phylliidae (leaf insects) in the superfamily Chresmodoidea (Sharov, 1968). Unfortunately, the phylogeny of the Phasmatodea is, for lack of a better word, unclear; one predominant school of thought regards them as the sister-group of the Orthoptera (grasshoppers, crickets, etc.) (Beutel and Gorb, 2006): the other, as close kin of the Embioptera, an obscure order of subsocial insects known in the vernacular as webspinners. Orthopterans and embiopterans are so dissimilar that there appears to be little opportunity for compromise. Another view holds that extant Phasmatodea are not even monophyletic, with the oddball Timematidae being more closely related to Notoptera (icecrawlers and rockcrawlers) than to the remainder of the living species (Euphasmida) (Kjer et al., 2004).


Additionally, the identity of the prehistoric taxa to which the Chresmodidae are obviously related (yes! There are some!) has been debated over the years. These mostly Mesozoic fossils–of which the Cretaceous-Paleogene Susumaniidae (Gorochov, 1988), the Jurassic Necrophasma (Martynov, 1928), and the Triassic Aeroplanidae (Tillyard, 1918) are some examples–have been often classified as Phasmatodea (Gorochov, 1994), but for the most part they consist only of wings, meaning that their identity as stick insects is based entirely upon venation. Well and good, except that their putative living kin's wings are reduced and heavily sclerotized, if not absent outright, making modern stick insect wing venation difficult and/or impossible to study (Wedmann et al., 2007). Furthermore, since the body is usually lacking in these fossils, in them one cannot confirm the presence of a vomer (a portion of male stick insects' naughty bits): a telltale apomorphy of modern phasmatodeans. (Significantly, chresmodid males lacked a vomer.) Hence, these purported basal stick insects' identification has been doubted (Tilgner, 2001). However, the twin discoveries of Gallophasma–a clichéd "missing link" between the alleged pre-Neogene Phasmatodea and their present-day ilk (Nel et al., 2010)–and a susumaniid with a vomer (Nel & Defosse, 2011) would seem to confirm that chresmodids are, indeed, stick insects (although controversy remains; Bradler and Buckley, 2011). 

If so, then I must say that they are weird stick insects.


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Andersen, N. M. (1982). The Semiaquatic Bugs (Hemiptera: Gerromorpha): Phylogeny, Adaptations, Biogeography and Classification. Klampenborg: Scandinavian Science Press.

Beutel, R. G. and Gorb, S. N. (2006). A revised interpretation of the evolution of attachment structures in Hexapoda (Arthropoda), with special emphasis on Mantophasmatodea. Arhropod Systematics and Phylogeny, 64(1), 3-25.

Bradler, S. and Buckley, T. R. (2011). Stick insect on unsafe ground: does a fossil from the early Eocene of France really link Mesozoic taxa with the extant crown group of Phasmatodea [electronic version]? Systematic Entomology, 36(2), 218-222. Retrieved 2/28/13 from http://onlinelibrary.wiley.com/doi/10.1111/j.1365-3113.2010.00564.x/pdf 

Brusatte, S.L. and Sereno, P.C. (2007). A new species of Carcharodontosaurus (dinosauria: theropoda) from the Cenomanian of Niger and a revision of the genus. Journal of Vertebrate Paleontology, 27(4).

Carpenter, F. M. (1992). Superclass Hexapoda. In Moore, R. C. and Kaesler, R. L. (eds.): Treatise on Invertebrate Paleontology, R, Arthropoda pt. 4. Boulder & Lawrence: Geological Society of America & University of Kansas Press.

Delclòs, X.; Nel, A.; Azar, D.; Bechly, G.; Dunlop, J. A.; Engel, M. S.; and Heads, S. W. (2008). The Enigmatic Mesozoic Insect Taxon Chresmodidae (Polyneoptera): New Paleobiological and Phylogenetic Data, with the Description of a New Species from the Lower Cretaceous of Brazil. N. Jb. Palaeont. Abh., 247(3), 353-381. Retrieved 2/26/13 from http://www.bernstein.naturkundemuseum-bw.de/odonata/Chresmodidae.pdf

Frickhinger, K. A. (1999). Die Fossilien von Solnhofen (vol. 2). Korb: Goldschneck.

Germar, E. F. (1839). Die versteinerten Insekten Solnhofens. Nova Acta Leopoldina Carolina Akademia, 19(1), 187-222.

Gorochov, A. V. (1988). On the classification of fossil orthopterans of the superfamily Phasmomimoidea (Orthoptera) with a description of new taxa [in Russian]. Trudy Zoologicheskogo Instituta Akademii nauk SSSR, St. Petersburg; 178, 32-44. 

Gorochov, A. V. (1994). Permian and Triassic walking sticks (Phasmatodea) from Eurasia. Paleontological Journal, 28(4), 83-97.

Haase, E. (1890). Beiträge zur Kenntnis der fossilen Arachniden. Zeitschriften der Deutschen Geologischen Gesellschaft, 42, 629-657.

Handlirsch, A. (1906). Ein Handbuch für Paläontologen und Zoologen. Leipzig: Engelmann. 

Kjer, K. M.; Carle, F. L.; Litman, J.; and Ware, J. (2006). A molecular phylogeny of Insecta. Arthropod Systematics & Phylogeny, 64(1), 35-44.

Kuhn, O. (1977). Die Tierwelt des Solnhofener Schiefers (5th edition). Wittenberg: Ziemsen.

Martínez-Delclòs, X. (1991). Insects hemimetàbols del Cretaci inferior del España. Tafonomia i Paleoautoecologia. University of Barcelona: doctoral thesis.

Martynov, A. V. (1928). A new fossil form of Phasmatodea from Galkino (Turkestan), and on Mesozoic phasmids in general. Annals and Magazine of Natural History, 10, 319-328.

Nel, A.; Azar, D.; Martínez-Delclòs, X.; and Makhoul, E. (2004). A new Upper Cretaceous species of Chresmoda from Lebanon–a latest representative of Chresmodidae (Insecta: Polyneoptera inc. sed.): first record of homeotic mutations in the fossil record of insects. European Journal of Entomology, 101(1), 145-151.

Nel, A.; Delfosse, E.; Robillard, T.; and Petrulevičius, J. F. (2010). An early winged crown group stick insect from the Early Eocene amber of France (Insecta, Phasmatodea). Systematic Entomology, 35, 340-346. 

Nel, A. and Delfosse, E. (2011). A new Chinese Mesozoic stick insect [electronic version]. Acta Palaeontologica Polonica, 56(2), 429-432. Retrieved 2/28/12 from http://www.app.pan.pl/archive/published/app56/app20091108.pdf

Oppenheim, P. (1888). Die Insectenwelt des lithographischen Schiefers in Bayern. Palaeontographica, 34, 215-247.

Petrunkevitch, A. I. (1955). Arachnida. In Moore, R. C. (ed.): Treatise on Invertebrate Palaeontology, Part P, Arthropoda Pt. 2 (vol. 2) (pp. 42-162). Lawrence: Geological Society of America & University of Kansas Press.

Ponomarenko, A. G. (1985). Fossil insects from the Tithonian "Solnhofener Plattenkalke" in the Museum of Natural History, Vienna. Annalen des Naturhistorischen Museums in Wien, 87A, 135-144.

Popov, Y. A. (1980). Superorder Cimicidea Laicharting, 1781. Order Cimicina Laicharting 1781. In Rohdendorf, B. B. and Rasnitsyn, A. P. (eds.): Historical development of the class of insects. Trudy Paleontologicheskogo Instituta, Akademiya Nauk S.S.S.R., Moskva; 175, 58-69.

Rasnitsyn, A. P. and Quicke, D. L. J. (2002). History of Insects. Dordrecht: Kluwer. 

Rowland, J. M. and Sissom, W. D. (1980). Report on a fossil palpigrade from the Tertiary of Arizona, and a review of the morphology and systematics of the order. Journal of Arachnology, 8, 69-86.

Sharov, A. G. (1968). Filogeniya ortopteroidnykh nasekomykh. Trudy Paleontologicheskogo Instituta, Akademiya Nauk S.S.S.R., Moskva; 118, 1-216.


Tilgner, E. (2001). The fossil record of Phasmida (Insecta: Neoptera). Insect Systematics and Evolution, 31(4), 473-480.

Tillyard, R. J. (1918). Mesozoic Insects from Queensland. 3. Odonata and Protodonata. Proceedings of the Linnean Society of New South Wales, 43, 417-435.

Wedmann, S.; Bradler, S.; and Rust, J. (2007). The first fossil leaf insect: 47 million years of specialized cryptic morphology and behavior. Proceedings of the National Academy of Sciences of the USA, 104(2), 565-569.

Westwood, J. O. (1854). Contributions to Fossil Entomology. The Quarterly Journal of the Geological Society of London, 10, 378-396.

Weyenbergh, H. (1874). Varia zoological et paleontologica. Periodico Zoologico, Sociedad Entomologica Argentina; 1, 77-111.

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.
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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.