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The Biodiversity and Systematics of the Entomophagous Parasitoid Strepsiptera (Insecta)

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The Biodiversity and Systematics of the Entomophagous Parasitoid Strepsiptera (Insecta) The Biodiversity and Systematics of the entomophagous parasitoid Strepsiptera (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 Hymenoptera, Hemiptera and Thysanura. INTRODUCTION Strepsiptera are obligate endoparasites the hosts of which include Blattodea, Diptera, Hemiptera, Hymenoptera, Mantodea, Orthoptera, 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 species 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 Elenchus tenuicornis Kirby (Baumert, 1958, 1959), a parasite of Delphacidae (Homoptera) and in Xenos vesparum (Christ) (Hughes et al ., 2003, 2004a, 2004b, 2005), a parasite of polistine paper wasps (Hymenoptera: Vespidae). While most strepsipterans parasitize single taxa (leafhoppers or halictid bees), the males and females in the family Myrmecolacidae 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 instar host-seeking larva 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 Mengenillidae, 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 insects. 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 instars 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 Burmese amber and Baltic amber. From Cretaceous Burmese amber (100 myo) a new genus 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 Stylopidae, 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 Caenocholax 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 Corioxenidae 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 Stylops Ulrichia Family Xenidae Paraxenos 5 Pseudoxenos Xenos Family Bohartillidae Bohartilla Family Elenchidae Colacina Deinelenchus Elencholax Elenchus Protelencholax (fossil) Family Halictophagidae 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 ( Zygentoma ) ……………………..………….............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, Cydnidae, Pentatomidae, Lygaeidae, Coreidae, Scutelleridae ….………………...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
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