More on the Origin of SiphonapteraAuthor(s): George W. ByersSource: Journal of the Kansas Entomological Society, Vol. 69, No. 3 (Jul., 1996), pp. 274-277Published by: Allen Press on behalf of Kansas (Central States) Entomological SocietyStable URL: http://www.jstor.org/stable/25085682Accessed: 19/05/2009 07:27

Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available athttp://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unlessyou have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and youmay use content in the JSTOR archive only for your personal, non-commercial use.

Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained athttp://www.jstor.org/action/showPublisher?publisherCode=kes.

Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printedpage of such transmission.

JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We work with thescholarly community to preserve their work and the materials they rely upon, and to build a common research platform thatpromotes the discovery and use of these resources. For more information about JSTOR, please contact support@jstor.org.

Kansas (Central States) Entomological Society and Allen Press are collaborating with JSTOR to digitize,preserve and extend access to Journal of the Kansas Entomological Society.

http://www.jstor.org

JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY 69(3), 1996, pp. 274-277

More on the Origin of Siphonaptera

George W. Byers

Department of Entomology, Snow Entomological Museum,

University of Kansas, Lawrence, Kansas 66045-2119

abstract: Six characteristics of Siphonaptera in addition to those mentioned by other authors indicate that they have more in common with nematocerous Diptera than with

Mecoptera.

No entomologist argues with the view that the wingless fleas (Siphonaptera) descended from winged ancestors; their holometabolous development and their thoracic structure, including musculature and

pleural sutures as in other pterygotes, provide strong supporting evidence. It is now generally accepted by both morphologists and systematists that Siphonaptera are in a monophyletic group including also the orders Mecoptera and Diptera, a group called Anthophora by Hennig (1969), or Mecopterida by

Boudreaux (1979). Hennig did not include Siphonaptera in his Anthophora with certainty because their males were thought not to have a sperm-pump. But a few years later Kristensen (1975:35) drew attention to a paper by Gunther (1961) describing a sperm-pump in male fleas (but possibly not homologous to those of Mecoptera and Diptera).

At the level of Mecopterida or Anthophora, agreement on the phylogenetic relationships of the three included orders ceases. Based upon selected morphological evidence, systematists using cladistic

methods have regarded Siphonaptera as a sister-group to Mecoptera or a sister-group to Diptera. The current preponderance of opinion seems to favor the closer relationship of fleas to Mecoptera. Having some familiarity with both Mecoptera and the lower Diptera (Nematocera), I would like to add my thoughts to the argument. This note is not intended to be a complete review of the controversy. For a review, see Boudreaux (1980).

As long ago as 1935, Tillyard stated categorically that "the Siphonaptera or fleas are not descended from Diptera, as has usually been believed." Instead, he thought they were derived from Permian

Permochoristidae, or possibly Paratrichoptera (Tillyard, 1935:44). That fleas?ectoparasites of mam mals and birds?had their origin in the late Paleozoic Era, long before the appearance of either

mammals or birds, as shown in Tillyard's phylogenetic diagram, seems a bit farfetched. He probably visualized a variety of intermediate taxa along the line drawn from modern Siphonaptera back to those Permian groups. Hinton (1958) offered support for the Siphonaptera-Mecoptera relationship, citing primarily evidence from the immature forms. Kristensen (1975) similarly favored the derivation of Siphonaptera from some mecopteran-like ancestor. Like Hinton, he regarded the morphological and

developmental similarities between Siphonaptera and Diptera as evolutionary convergences. Roth schild (1975) also considered Siphonaptera most closely related to Mecoptera, calling attention to the occurrence of multiple sex chromosomes in fleas and in Boreus, and the presence of proventricular acanthae in both these groups. She also mentioned the work of Baccetti (1972) on the similar structure of sperm cells in fleas and some Mecoptera. Schlein (1980) described similarities between adult fleas and the genera Merope, Panorpa or Boreus of Mecoptera with respect to (1) small, thoracic pleural sclerites (the "link plates" of fleas), (2) articulation of the anterior coxae, (3) cuticular ingrowths associated with the eyes, (4) position of the first abdominal spiracles and (5) probable wing bases on the metathoracic pleural arch of fleas.

Against this formidable array of evidence, there have been a few proponents of the view that fleas

are more closely related to the Diptera than to the Mecoptera. One of the more detailed and complete counter-arguments was advanced by Boudreaux (1979:255-257). At the outset, he stated that "the features of fleas that seem to relate them to the Mecoptera rather than to the Diptera can be interpreted either as generally primitive insect characters or as convergences." He then took up, point by point, the arguments of Rothschild, Hinton, Kristensen and others and gave his reasons for not accepting them; later (Boudreaux, 1980) he reiterated these. For example, one of the most convincing characters linking Siphonaptera to Mecoptera, in Rothschild's view, was the presence of cuticular acanthae in

the proventriculus of fleas and of Boreus (Richards and Richards, 1969). Boudreaux (1980) found

Accepted for publication 25 June 1996.

VOLUME 69, NUMBER 3 275

proventricular acanthae in eight additional orders of insects and illustrated many of them, including those of a flea and a panorpid mecopteran. There are some obvious differences from one order to

another, but the structures appear to be homologous and probably differ according to the diet of each

species. The acanthae of both fleas and Mecoptera are elongate and hair-like, as also in some Cole

optera. Boudreaux postulated that such cuticular acanthae were characteristic of the common ancestor

of Mecopterida but were subsequently lost in Diptera because a differentiated proventriculus does not occur in that order.

These and other structural details have been used, one way or another, as evidence of the phylo genetic relationship of Siphonaptera (Rothschild, 1975; Boudreaux, 1979). In addition to these, but bearing them in mind, I would introduce a few further characters that might provide clues to the

evolutionary origin of fleas: Since fleas are typically ectoparasites of animals that return often to their nest or den, it is not

unreasonable to suppose that the ancestors of fleas were nest-inhabiting insects, even before their adults became blood-feeders. An example of such an insect among living groups of flies is the family Scatopsidae. But in the Mecoptera there is no such nest-occupant, as far as known.

We may further suppose that later ancestors of fleas became dependent on vertebrate blood, in a

way similar to that of such extant groups of insects as mosquitoes (Culicidae), black flies (Simuliidae), phlebotomine Psychodidae and many Ceratopogonidae. All these are nematocerous Diptera. Among

Mecoptera, however, no blood-feeders are known. One unusual aspect of the mouthparts of fleas is the loss of mandibles, the maxillary laciniae (called

mandibles in older literature) being the functional piercing stylets. Therefore, the ancestors of fleas possibly occurred among insects that have lost their mandibles. In mosquitoes, black flies, ceratopo gonids and other blood-feeding nematocerous flies, mandibles are retained?at least in those adults that drink vertebrate blood. In most families of Nematocera in which only the adult female is a blood

feeder, mandibles are lost in the respective males. Exceptions are in Simuliidae, a few Ceratopogonidae and rarely (as abnormal developments) in male mosquitoes (Crampton, 1942:32). In contrast, there is no loss of mandibles among the known Mecoptera (although they are short, relatively broad, somewhat dagger-shaped and do not reach the end of the rostrum in Nannochoristidae, and their function in

feeding is not known). Antennae of fleas typically are shorter than the head and have nine flagellomeres, which are short

and wide and tend to be compacted together. That the antennae are located in recesses in the sides of the head no doubt relates to the ectoparasitic habit of fleas. Nothing even remotely resembling fleas' antennae occurs in the Mecoptera, most families of which are characterized by long, slender antennae

with numerous subcylindrical flagellomeres (Meropeidae the only exception). In nematocerous Diptera, however, compact antennae with short, wide flagellomeres occur in some Mycetophilidae (e.g., Cer oplatus), Bibionidae (Dilophus), Simuliidae and some other families; these are surely instances of convergence.

The eyes of adult Siphonaptera are usually described as compound eyes reduced to single, simple eyes (Schlein, 1980). Snodgrass (1946), however, judged that they are "ventrally displaced ocelli," based on their retinal structure and the source of their nerves in the brain. They are altogether absent in a few species. This kind of reduction, seen in several ectoparasitic groups of Diptera, is not known in Mecoptera. The compound eyes of adult Nematocera are ordinarily multi-faceted but are single faceted in Baeonotus, probably a cecidomyiid and presumed not to be an ectoparasite.

Enlarged coxae, characteristic of fleas, are found also in both the Nematocera (e.g., Sciaridae, Mycetophilidae) and the Mecoptera. But in most Mecoptera there is a well-developed meron along most of the posterior edge of the coxa of each pterothoracic leg; and this is absent in Siphonaptera and most Diptera. Some of the more primitive or generalized Diptera (e.g., some but not all Tipulidae) have the mesothoracic meron partially joined proximally with the coxa. During the evolution of

Diptera, it appears, the mesothoracic meron became totally separated from the coxa and incorporated into the lower pleuron. In fleas, no meron can be distinguished in either the mesothorax or the meta

thorax, probably because of the fusion of sclerites and disappearance of sutures. Similarly, no meron can be seen in the flightless crane fly Chionea, in which there is extensive fusion of thoracic sclerites

(Byers, 1983). The meron is poorly developed in the flightless Boreidae and is not differentiated in Apteropanorpa, in which there is much fusion of the thoracic sclerites; however, the meron is well

preserved in other flightless mecopterans, such as Apterobittacus, Anomalobittacus and the brachyp terous females of Panorpodidae. In a cleared, slide-mounted flea, an interior sclerotized ridge can be seen extending from the proximal end of the coxa to the distal end. Because some morphologists and

276 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

taxonomists had referred to the part of the flea's coxa posterior to this carina as the meron, Snodgrass (1946) stated that "the postcarinal part of a flea's coxa, however, has no anatomical identity with the

meron of such insects as Mecoptera, Triehoptera, and Lepidoptera." He continued, "The coxal ridges of the flea are mere strengthening devices, and similar ridges occur in other insects."

An obvious and long-recognized similarity shared by fleas and Diptera is the legless (apodous) condition of their larvae. All known larvae of Mecoptera, in contrast, have well-developed legs. The

darkly sclerotized (eucephalic) head capsule of a flea larva and the contrasting, pale thorax and ab domen have long led to comparison with various kinds of larval Nematocera, for example, the larvae of Mycetophilidae and Sciaridae. In larval Mecoptera, the pronotum is somewhat sclerotized, usually conspicuously darker than the rest of the thorax, unlike the condition in Nematocera. Larval fleas have small, down-turned prolongations on the tenth abdominal segment, called anal struts, which are push ing organs used in locomotion. Similar, probably homologous pushing structures also occur on the tenth abdominal segment of several kinds of larval Nematocera, such as Bibionidae, Mycetophilidae, Sciaridae and some Ceratopogonidae. These do not resemble the terminal hooks or anal papillae of

Nannochoristidae, the only larval Mecoptera with prolongations on the tenth abdominal segment. Larvae of some fleas, feeding on debris in the nests of their rodent hosts, eat mouse (rat, etc.)

droppings containing the eggs of rodent tapeworm (Hymenolepis). Intermediate stages of the parasite occur in the larvae, later in the pupae, and eventually in the adult fleas. After a mouse (or rat) eats an infested adult flea, the developmental cycle of the tapeworm is completed in the rodent. While such an infestation is utterly unknown in Mecoptera, I have found the cysticercoid stage of mouse

tapeworm (probably Hymenolepis sp.) in adult crane flies (Tipulidae) of the genus Chionea, larvae and adults of which can be found in mouse nests (Byers, 1983:105).

As can be seen, I am inclinded to suppose that the ancestors of extant Siphonaptera were among the Jurassic or early Cretaceous ancestors of some modern Nematocera, possibly the superfamily

Mycetophiloidea (Mycetophilidae, Sciaridae, Scatopsidae, and Cecidomyiidae) of some classifications. In spite of the described (and not already refuted) similarities between Siphonaptera and Mecoptera, I cannot easily visualize the origin of fleas among the Mecoptera. We know ancestral Mecoptera from the Permian onward, almost wholly on the basis of wings until well into the Cenozoic Era, from

which the fossils look very much like living forms; therefore, we must guess what those ancestors were like, based on extant species. The same is true of Diptera, from late Triassic until late Cretaceous or early Cenozoic.

This view of the origin of Siphonaptera, of course, makes the Order Diptera paraphyletic, which

my cladist colleagues cannot accept. While I am an admirer of Willi Hennig, the originator of the cladistic method in classification, as a great dipterist and phylogeneticist, I am not a cladist and am untroubled by the idea of paraphyly. The suborder Nematocera has itself recently been judged to be paraphyletic, on the basis of cladistic evidence (Oosterbroek and Courtney, 1995:268).

Acknowledgment I thank my colleague Byron Alexander for his helpful comments on an earlier version of this

expression of opinion; my thanks also to three anonymous reviewers for their thoughtful comments.

Literature Cited

Baccetti, B. 1972. Insect sperm cells. In Treherne, J. E., M. J. Berridge, and V B. Wigglesworth (eds.), Advances in Insect Physiology 9:315-397. Academic Press, New York.

Boudreaux, H. B. 1979. Arthropod Phylogeny with Special Reference to Insects. Wiley-Interscience, New York, 320 pp.

Boudreaux, H. B. 1980. Proventricular acanthae and their phylogenetic implications. Ann. Entomol. Soc. America 73:189-196.

Byers, G. W. 1983. The crane fly genus Chionea in North America. Univ. Kansas Sci. Bull. 52:59 195.

Crampton, G. C. 1942. The external morphology of the Diptera. Guide to the Insects of Connecticut. Part VI, The Diptera or True Flies of Connecticut, Fasc. 1:10-165.

Gunther, K. G. 1961. Funktionell-anatomische Untersuchung des mannlichen Kopulationsapparates der Flohe unter besonderer Beriicksichtigung seiner postembryonalen Entwicklung (Siphonap tera). Deutsch. Entomol. Zeitschrift, N. E 8:258-349.

Hennig, W. 1969. Die Stammesgeschichte der Insekten. Senckenberg-Buch, Frankfurt am Main., 436 pp. Hinton, H. E. 1958. The phylogeny of the panorpoid orders. Annual Review Entomol. 3:181-206.

VOLUME 69, NUMBER 3 277

Kristensen, N. P. 1975. The phylogeny of hexapod "orders." A critical review of recent accounts. Zeitschr. Zool. Syst. Evolutionsforsch. 13:1-44.

Oosterbroek, P. and G. Courtney. 1995. Phylogeny of the nematocerous families of Diptera (Insecta). Zool. J. Linnean Soc. 115:267-311.

Richards, P. A. and A. G. Richards. 1969. Acanthae: a new type of cuticular process in the proven triculus of Mecoptera and Siphonaptera. Zool. Jahrb. Anat. Ontog. Tiere 86:158-176.

Rothschild, M. 1975. Recent advances in our knowledge of the order Siphonaptera. Annual Review Entomol. 20:241-259.

Schlein, Y. 1980. Morphological similarities between the skeletal structures of Siphonaptera and

Mecoptera. In Traub, R. and H. Starcke (eds.), Fleas. Proc. Internat. Conf. on Fleas, Ashton Wold/Peterborough, U. K., 21-25 June 1977, pp. 359-367. A. A. Balkema, Rotterdam. 420 pp.

Snodgrass, R. E. 1946. The skeletal anatomy of fleas (Siphonaptera). Smithson. Misc. Collns. 104(18): 1-89.

Tillyard, R. J. 1935. The evolution of the scorpion-flies and their derivatives (Order Mecoptera). Ann. Entomol. Soc. America 28:1-45.

NOTICE

The Journal of the Kansas Entomological Society would like to in crease membership of the Editorial Board. Persons interested in serving as Subject Editors should contact Leonard C. Ferrington Jr. by e-mail (tendipes@falcon.cc.ukans.edu) or telephone (913-864-7700) for ad ditional details.

Article Contentsp. [274]p. 275p. 276p. 277

Issue Table of ContentsJournal of the Kansas Entomological Society, Vol. 69, No. 3 (Jul., 1996), pp. 211-278Front MatterNatural History of a Ground-Nesting Solitary Bee, Crawfordapis luctuosa (Hymenoptera: Colletidae) [pp. 211-221]A Revision of Parachrysopiella (Neuroptera: Chrysopidae) [pp. 222-233]A Revision of Rothium Moore and Legner (Coleoptera: Staphylinidae: Aleocharinae) with a Discussion of Its Phylogenetic Relationships [pp. 234-256]A Report of Chauliodes (Megaloptera: Corydalidae) in the Purple Pitcher Plant, Sarracenia purpurea L. (Sarraceniaceae) [pp. 257-259]Molecular Diagnostics of Three Diabrotica (Coleoptera: Chrysomelidae) Pest Species [pp. 260-266]Short CommunicationsInterference Competition and Scavenging by Crematogaster Ants (Hymenoptera: Formicidae) Associated with the Webs of the Social Spider Anelosimus eximius (Araneae: Theridiidae) in the Central Amazon [pp. 267-269]Storage Conditions for Maintaining Osmia cornifrons (Hymenoptera: Megachilidae) for Use in Germplasm Pollination [pp. 270-272]Neotype Designations and Synonyms of Some Texas Caddisflies (Trichoptera) [pp. 272-273]More on the Origin of Siphonaptera [pp. 274-277]

Back Matter