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Home , Caenocholax, Cercopidae, Coreidae, Corioxenidae, Delphacidae, Elenchidae

The Biodiversity and Systematics of the entomophagous (Insecta)

Jeyaraney Kathirithamby, Department of Zoology and St Hugh’s College, Oxford. [email protected] [email protected]

ABSTRACT Strepsiptera are small group of entomophagous parasiroids of cosmopolitan in distribution. They parasitize seven orders of Insecta and the common hosts in Europe are , and .

INTRODUCTION Strepsiptera are obligate endoparasites the hosts of which include , Diptera, Hemiptera, Hymenoptera, Mantodea, , and Thysanura, and 33 families. The name of the group is derived form the Greek words: twisted ( Strepsi-) and wing (pteron ), and refers in particular to the twisted hind wing of the male while in flight. Representatives of the suborder Mengenillidia show more primitive characteristics and parasitise Thysanura (Lepismatidae), the only known apterygote to be parasitized. Strepsiptera are cosmopolitan in distribution and are difficult to find: often the host has to be located to find the strepsipteran. To date about 600 have been described, but many more await description and some could be cryptic species. The group is relatively well known in Europe (Kinzelbach, 1971, 1978), where details of Strepsiptera life history have been studied in tenuicornis Kirby (Baumert, 1958, 1959), a parasite of (Homoptera) and in vesparum (Christ) (Hughes et al ., 2003, 2004a, 2004b, 2005), a parasite of polistine paper (Hymenoptera: Vespidae). While most strepsipterans parasitize single taxa ( or halictid ), the males and females in the family parasitize hosts belonging to different orders: (Formicidae and Orthoptera, respectively) (Ogloblin, 1939, Kathirithamby and Hamilton, 1992). Reference web pages: http://working.tolweb.org/tree?group=Strepsiptera , http://tolweb.org/tree?group=Stylopidia&contgroup=Strepsiptera , http://tolweb.org/tree/eukaryotes/animals/arthropoda/hexapoda/strepsiptera/stylohosts.ht ml Morphology Strepsiptera exhibit extreme sexual dimorphism, and there are only two free-living stages: the 1 st host-seeking and the adult male. The sole mission of the short- lived (c. 3-5 hours) adult male is to seek and fertilize a female. The females are neotenic

2 and remain endoparasitic in the host, except in the family , where they emerge (like the males) to pupate externally from the host. The adult males have reduced forewings, fan-shaped hind wings, branched antennae, and raspberry-like eyes. The mesothoracic reduced fore-wings function like the halteres of Diptera. The large hind wings have no cross veins. The eyes are madeup of 15-150 eyelets which in recent families are separated by strips of microtrichia. Claws are absent in the more derived families. The ninth abdominal segment bears the simplified copulatory organs. The females are neotenic and in the suborder Stylopidia lack all external characters of . The only visible feature in the female Stylopidia is the extruded cephalothorax. The free-living females of Mengenilla have eyes, mouthparts, antennae, legs and a ventral genital opening, but lack wings. Insemination of the female takes place via the genital opening of the female Mengenilla, or via the brood canal opening in the cephalothorax of the female Stylopidia. The free-living 1 st emerge from the female and seek new hosts to parasitise. On entry into the host, the 1 st instars moult to an apodous second instar. Strepsiptera thus go through hypermetamorphosis, i.e. two morphologically distinct larval instars. The subsequent endoparasitic stages undergo apolysis without ecdysis, i.e. Strepsiptera shed the old cuticle but do not come out of it. There are about four endoparasitic larval instars. At the end of the last larval instar, in the suborder Stylopidia, the male extrudes through the host cuticle to form a puparium, at the end of which the male emerges as a free-living adult. The female Stylopidia extrudes through the host cuticle and becomes a neotenic adult. The host dies after the emergence of the free-living male and after the emergence of the live 1 st instar from the neotenic female. In Mengenillidae both the male and female emerge to pupae externally from the host and are free-ling as adults. Classification Strepsiptera are a monophyletic group. Kinzelbach (1971, 1978) divided the order into two suborders (Mengenillidia and Stylopidia), and nine families (one extinct and eight extant), on Hennigian approach based on morphological characters of adults (mainly males). A molecular analysis of the extant families (except one) shows seven families (McMahon and Kathirithamby, 2008). A combination of morphological reduction with

3 modification and the unusual life history of Strepsiptera has made the placement of Strepsiptera the most enigmatic question in ordinal level systematics. Three fossil families/genera have been found in Cretatecous and Baltic amber. From Burmese amber (100 myo) a new Cretostylops , and in Baltic amber (40 myo) the oldest strepsipteran Protoxenos were described. Both these extinct genera have unusual features, particularly their large triangle-shaped mandibles, quite unlike the extinct family Mengeidae and recent species, which have delicate small mandibles (Grimaldi et al., 2005, Pohl et al., 2005). The suborder Mengenillidia is not represented in the Neotropics or in Mesoamerica. Two genera, Mengenilla and Eoxenos have been recorded extensively in Europe by Silvestru (1943). They parasitize ground dwelling Thysanura. The suborder Stylopidia has 6 extant families and is distinct from the Mengenillidia in that the females, during the neotenic adult stage, remain endoparasitic, except for their extruded cephalothorax. One of the largest and most recently evolved families within this suborder is the , which parasitize aculeates. Closely related to these is the family Xenidae which parasitize Vespidae and Sphecidiae. In the family Myrmecolacidae, females parasitize ants, while males parasitize polyneopterans (Orthoptera, Mantodea) (Ogloblin, 1939; Kathirithamby, 1991; Kathirithamby and Hamilton, 1992). Such disparate sexual differences in host use are unique among insects, and until recently completely confounded efforts to match males and females of the same species. Kathirithamby & Johnston (2004) showed that the male of fenyesi waloffi Kathirithamby & Johnston parasitizes a Dolichoderine ant, while the female parasitizes a cricket.

4 Table 1. List of genera . (Based on morphological data after Kinzelbach 1971, Kathirithamby 1989, with modifications after Pohl et al. 2005, Grimaldi et al. 2005, and preliminary molecular data, McMohan & Kathirithamby 2008). Order Strepsiptera

Family Protoxenidae Protoxenos (fossil) Family Incertae Sedis Cretostylops (fossil) Family Mengeidae Mengea (fossil) Family Mengenillidae Congoxenos Eoxenos Mengenilla Family Australoxenos Blissoxenos Corioxenos Dundoxenos Floridoxenos Loania Mufagaa Malayaxenos Proceroxenos Triozocera Uniclavus Viridipromontorius Family Myrmecolacidae Caenocholax Lyncholax Myrmecolax Paleomyrmecolax (fossil) Stichotrema Family Stylopidae Crawfordia Eurystylops Halictoxenos Hylecthrus Jantarostylops (fossil) Meliettostylops Ulrichia Family Xenidae Paraxenos

5 Pseudoxenos Xenos Family Bohartillidae Bohartilla Family Colacina Deinelenchus Elencholax Elenchus Protelencholax (fossil) Family Blattophagus Callipharixenos Coriophagus Dipterophagus Halictophagus Stenocranophilus Tridactylophagus

Key to Families Adult males : 1(2) Antennae 8-segmented; mandibles large and robust, triangular shaped, with broad base and generalized chewing structure……………...... ….……..2 - Antennae 6-7 segmented; mandibles, if present, small, narrow, and blade-like…3 2(1) Galeal lobe at base of maxillary palp; fossil…………………….…Protoxenidae Absence of galeal lobe at base of maxillary palp; fossil……………………….. ………………………………………………….…Cretostylops family In Certa 3(1) Legs with 5 tarsomeres, ending with a pair of strong claws, without sensory spots; antennae 6-7 segmented……………..………...... 4 (Suborder: Mengenillidia) - Legs with 2-4 tarsomeres, with neither claws nor sensory spots; or 5 tarsomeres ending with a pair of claws, or a single claw and sensory spots; antennae 5-7 segmented...... ……...... …………….5 (Suboder Stylopidia)

4(3) Prementum free, with short palps; CuA 1 short extending to about middle of wing; antennae 7-segmented with lateral flabellum on 3rd and 4 th segments; fossil……………………….…………………………...... Mengeidae

- Prementum fused to hypopharynx; CuA 1 extending almost to edge of wing, MA well developed and with anterior branch; antennae 6-segmented with lateral flabellum on 3 rd - 4th, or 3rd-5th segments; Host: Thysanura:

6 Lepismatidae ( ) ……………………..…………...... Mengenillidae 5(3) Mandibles absent; legs with 5 tarsomemer with a pair of claws, or a single claw, or 4 tarsomeres without claws; antennae 5-7 segmented with lateral flabellum on 3 rd -4th , 3rd –5th , or 3 rd –6th segments Host: Hemiptera: Blissinae, , , , , ….………………...Corioxenidae - Mandibles present, narrow, blade-like; legs 2-4 tarsomeres without claws; antennae 4-7 segmented with lateral flabellum on 3 rd , 3 rd -4th , 3 rd , 5th and 6 th or 3 rd -6th segments………..……………………………………………….…….....6 6(5) Legs with 3 tarsomeres; Host: Hemiptera: ,Cicadellidae, Coreidae, Delphacidae, Eurybrachyidae, , Fulgoroidae, , Membracidae Pentatomidae, ; Diptera: Tephritidae; Orthoptera: Tridactylidae; Blattodea: Blattilldae…..……...... Halictophagidae - Legs with 2 or 4 tarsomeres...... …...... 7 7(6) Legs with 2 tarsomeres; antennae 4-segmented; Host: Hemiptera: Delphacidae, , Flatidae, , …… …. .Elenchidae - Legs with 4 tarsomeres; antennae 5-7 segmented …………...... 8 8(7) Antennae 7-segmented, with flabellum on 3 rd , 5 th and 6 th segments; Maxillary base five times longer than base; Host: unknown…………………………….Bohartillidae - Antennae 4-7 segmented with flabellum on 3rd segment only; maxillary base equal to, or smaller than palpi………...... …...... 9 9(8) Antennae 4 segmented, with flattened flabella; Host: Hymenoptera: Sphecidae, Vespidae.……………….……….… …….…………...……………………...Xenidae - Antennae 5-6 segmented………………. …..………………………………..…… .10 10 (9).Antennae 6 segmented, with flattened flabella; Host: Hymenoptera: Andrenidae, Colletidae, Halictidae..….……………………………………………….….Stylopidae - Antennae 7-segmented, with rounded flabella (fig 22); Host (of male only): Hymenoptera: Formicidae (Formicinae, Myrmicinae, Pseudomyrmecinae, Dolichoderinae, Ponerniae)……..…………….………………...... Myrmecolacidae

Adult Females : 1. Free-living apterous, larviform, with eyes, mouth parts, antennae and legs; Host

7 (during larval stages): Thysanura (Lepismatidae-Zygentoma )…………Mengenillidae - Endoparasitoides during larval stages and cephalothorax of neotenic adult visible externally, rest of body endoparasitic; eyes, antennae, mouthparts, legs and wings absent… ……..…………………………………….………………….…………..…2 2(1) Brood canal opening apical in celpahothorax; ventral side turned towards host; Hosts: Hemiptera: Pentatomidae, Lygaeidae, Cydnidae, Coreidae and Scutelleridae ……………………………………………………………………………Corioxenidae - Brood canal opening ventral and at the junction of the head and thorax in cephalothorax; ventral side turned away from the host ...... 3 3(2) Head half or more as long as cephalothorax; dorsal side not membranous; segments 1-5 of abdomen with 1 genital aperture each; Hosts: Hemiptera: Delphacidae, Cercopidae, Cicadellidae Eurybrachidae, Fulgoridae, Issidae, Membracidae, Pentatomidae Tettigometridae; Diptera: Tephritidae; Orthoptera: Tridactylidae; Blattodea: Blattidae…………………….………………..…………Halictophagidae - Head less than half as long as cephalothorax, or dorsally membranous and raised; round bell-shaped cephalothorax...... 4 4(3) Cephalothorax dorsally flattened and sclerotised, lying between abdominal segments, often hidden; brood canal opening slit-shaped; abdominal segments 3-6, each, with 1 genital aperture; Parasitoides of Hymenoptera……………….…….….5 - Cephalothorax rounded and raised, not hidden; brood canal opening wide; Hosts: Orthoptera, Mantodea, and Homoptera…………………………………….………..6 5(4) Parasitoides of Sphecidae and Vespidae……………………………………..Xenidae :- Parasitoides of Andrenidae, Colletidae and Halictidae………..…………. Stylopidae. 6(5) Parasitoides of Orthoptera: Gryllidae, Tettigoniidae; Mantodea: Mantidae….. ….. …………….…………...... Myrmecolacidae - Parasitoides of Homoptera: Delphacidae, Dictyopharidae, Eurybrachidae, Flatidae, Fulgoridae, Richaniidae …………..………………………………………Elenchidae

8 REFERENCES Baumert, D. (1958) Mehrjährige Zuchten einheimischer Stresipteren an Homopteren. I. Hälfte Larven und Puppen von Kirby. Zool. Beitr. 3: 365- 421. Baumert, D. (1959) Mehrjährige Zuchten einheimischer Stresipteren an Homopteren. 2. Hälfte. Imagines, Lebenszyklus und Artbestimmung von Elenchus tenuicornis Kirby Zoologica Beit . 4, 343-409. Clausen, C. P. (1949) Entomophagous Insects. New York. McGraw Hill. 688p Crowson, R. A. (1981) The Biology of Coleoptera. London. Academic Press. P. Grimaldi, D., Kathirithamby, J., Schawaroch, V. (2005) Strepsiptera and triungula in Cretaceous amber. Systematics and Evolution Group 1, 36, 1-20. Grimaldi, D., Engle, M. (2005) . Cambridge. Cambridge University Press. 755p. Halbert, N. R, Ross, L. D., Kathirithamby, J., Wolley, J. B, Saff R. R , Johnston, J. S. (2001) Phylogenetic analysis as a means of species identification within Myrmecolacidae (Insecta: Strepsiptera). Tijdschrift voor Entomologie 144, 179 -186. Hughes, D. P., Beani, L., Turillazzi, S., Kathirithamby, J. (2003) Prevalence of the parasite in as detected by dissection of immatures. Insectes Sociaux 50, 62 -68. Hughes, D. P., Kathirithamby, J., Beani, L. (2004) Prevalence of the parasite Strepsiptera in adult Polistes wasps: field collections and literature overview. Ethology. Ecology and Evolution. 16, 363-375. Hughes, D. P., Kathirithamby, J. (2005) Cost of strepsipteran macroparasitism for immature wasps: Does modulate virulence? Oikos 110, 428-434. Hughes, D.P., Kathirithamby, J. Turillazzi, S., Beani, L. (2004) Social wasps desert the colony and aggregate outside if parasitized: parasite manipulation? Behavioural Ecology 15, 1037-1043. Kathirithamby, J. (1989) Review of the order Strepsiptera. Systematic 14, 41 -92. Kathirithamby, J. (1991) Stichotrema robertsoni spec. n. (Strepsiptera: Myrmecolacidae):

9 the first report of stylopization in minor workers of an ant ( Pheidole sp. Hymenoptera: Formicidae). Journal of the Entomological Society of South 54, 9-15 Kathirithamby, J. (1992) Strepsiptera, In: Naumann, I. D., Carne, P. B., Lawrence, J. F., Nielson, E. S., Spradberry, J. P., Taylor, R. W., Whitten, M.J., Littlejohn M. J. (Eds) Insects of . A textbook for students and research workers. 2nd edition. CSIRO, Melbourne. Melbourne University Press. 2 volumes, 684-695p. Kathirithamby, J. (1993) Strepsiptera of Panama and Mesoamerica. In: Diomedes, Q., Aiello, A. (Eds.). Insects of Panama and Mesoamerica: Selected Studies Oxford, Oxford University Press. 421-431p. Kathirithamby. J. (1995) Strepsiptera. In: Checklist delle Specie della Fauna Italiana , Ministero dell' Ambiente e Comitato Scientifico per la Fauna d' Italia. 17-18p. Kathirithamby, J. (2003) Strepsiptera. Stylopidia. The Tree of Life Web Project. http://tolweb.org/tree?group=Stylopidia&contgroup=Strepsiptera Kathirithamby, J. (2003) Strepsiptera: Host relations. Tree of Life Web project. http://tolweb.org/tree/eukaryotes/animals/arhtropoda/hexapoda/strepsiptera/stylohosts.ht ml Kathirithamby, J. (2006) Partial List of Strepsiptera species. Tree of Life Project. http://tolweb.org/notes/?note id=2978. Kathirithamby, J. (2008) Strepsiptera. In: Resh, V. H., Cardé, R. T. (Eds.) Encyclopedia of Insects . Springer. Kathirithamby, J.. Grimaldi, D. (1993) Remarkable stasis in some Lower Tertiary : descriptions, new records and review of Strepsiptera in the Oligo-Miocene amber of the Dominican Republic . Entomologica Scandinavica 24, 31-41. Kathirithamby, J. Hamilton, W. D. (1992) More covert sex; the elusive females of Myrmecolacidae. Trends in Ecol. Evol. 7, 345-351. Kathirithamby, J., Johnston, J. S. (2004) The discovery after 94 years of the elusive female of a myrmecolacid (Strepsiptera), and the cryptic species of Caenocholax fenyesi Pierce sensu lato. Proceedings of the Royal Society of London, B (Suppl. 3) 271, S5-S8. Kinzelbach, R. K. (1971) Morphologische Befunde an Fächerflüglern und ihre phylogenetische Bedeutung (Insecta, Strepsiptera). Zoologica 119, pp. 256.

10 Kinzelbach, R. K. (1978) Strepsiptera. Die Tierwelt Deutschlands. 65: 266pp . Kulicka, R. (1979) Mengea mengei sp. N. from the Baltic amber. Prace Museum Ziemi PAN 2, 109-112. . McMahon, D., Kathirithamby, J. (2008) A molecular phylogeny of Strepsiptera. In: 23 rd International Congress of Entomology, Durban. Abstract no.1909. Ogloblin, A. A. (1939) The Strepsiptera parasitic in ants. In: Inter. Congress of Entomology, Berlin. (1938) 2, 1277-1284. Pohl, H., Beutel, R. G., Kinzelbach, R. K. (2005) Protoxenidae fam. N. from Baltic amber – A “missing link” in Strepsiptera phylogeny. Zool. Scr. 34, 57-69. Silvestri, F. (1943) Studi sugli “Strepsiptera” (Insecta). III. Desertizione e biologia di 6 specie italiane di mengenilla. Boll. Lab. Zool. Gen. Agr. Fac. agr. Protici 32: 197-282.

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