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Developmental Strategy of the Endoparasite Xenos Vesparum (Strepsiptera, Insecta): Host Invasion and Elusion of Its Defense Reactions

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Developmental Strategy of the Endoparasite Xenos Vesparum (Strepsiptera, Insecta): Host Invasion and Elusion of Its Defense Reactions CORE Metadata, citation and similar papers at core.ac.uk Provided by Royal Holloway - Pure JOURNAL OF MORPHOLOGY 268:588–601 (2007) Developmental Strategy of the Endoparasite Xenos vesparum (Strepsiptera, Insecta): Host Invasion and Elusion of Its Defense Reactions Fabio Manfredini,1 Fabiola Giusti,1 Laura Beani,2 and Romano Dallai1* 1Dipartimento di Biologia Evolutiva, University of Siena, Siena 53100, Italy 2Dipartimento di Biologia Animale e Genetica ‘‘Leo Pardi’’, University of Florence, Florence 50125, Italy ABSTRACT To successfully complete its endoparasitic zoan parasites. Small pathogens are phagocytized development, the strepsipteran Xenos vesparum needs to by hemocytes, whereas parasitoids and other mac- elude the defense mechanisms of its host, the wasp roparasites are encapsulated: hemocytes recognize Polistes dominulus. SEM and TEM observations after the foreign invader as nonself and change from artificial infections allow us to outline the steps of this freely circulating cells to adhesive cells, forming a intimate host–parasite association. Triungulins, the mo- bile 1st instar larvae of this parasite, are able to ‘‘softly’’ multilayered sheath of cells. From an evolutionary overcome structural barriers of the larval wasp (cuticle perspective, relatively few studies have focused on and epidermis) without any traumatic reaction at the the behavioral ecology of immature parasites: ‘‘ex- entry site, to reach the hemocoel where they settle. The ploitative organisms that live in continuous, inti- parasite molts 48 h later to a 2nd instar larva, which mate association with their host,’’ forced to adapt moves away from the 1st instar exuvium, molts twice themselves to a changing environment (Brodeur more without ecdysis (a feature unique to Strepsiptera) and Boivin, 2004). In this chain of events both cel- and pupates, if male, or develops into a neotenic female. lular and humoral components of host immune Host encapsulation involves the abandoned 1st larval response might be compromised, and profound exuvium, but not the living parasite. In contrast to the changes in life-history parameters are likely to usual process of encapsulation, it occurs only 48 h after host invasion or later, and without any melanization. In occur. further experiments, first, we verified Xenos vesparum’s Xenos vesparum belongs to Strepsiptera ability to reinfect an already parasitized wasp larva. (Insecta), a cosmopolitan order of obligate endopar- Second, 2nd instar larvae implanted in a new host did asites of other insects. Strepsiptera have a direct not evoke any response by hemocytes. Third, we tested life cycle; therefore, the first organism infected is the efficiency of host defense mechanisms by implanting the final host, which may be infected at different nylon filaments in control larval wasps, excluding any developmental stages by the 1st instar larva of the effect due the dynamic behavior of a living parasite; parasite, the so-called triungulin (the infective within a few minutes, we observed the beginning of a motile stage). The primary host of X. vesparum typical melanotic encapsulation plus an initial melaniza- (Stylopidae) is Polistes dominulus (Vespidae), a tion in the wound site. We conclude that the immune response of the wasp is manipulated by the parasite, primitively eusocial paper wasp. Like other mem- which is able to delay and redirect encapsulation bers of the order (except Mengenillidae), X. vespa- towards a pseudo-target, the exuvia of triungulins, and rum shows a striking sexual dimorphism. Males, to elude hemocyte attack through an active suppression after the 4th larval instar, follow a complete holo- of the immune defense and/or a passive avoidance of metabolous development: they pupate and emerge encapsulation by peculiar surface chemical properties. as free-living winged adults from the puparium, J. Morphol. 268:588–601, 2007 Ó 2007 Wiley-Liss, Inc. which extrudes through the host abdominal ter- gites. During their short life-span (4–6 h), they KEY WORDS: endoparasitic development; host defense actively search for a receptive female. Neotenic elusion; encapsulation; melanization larviform females are the result of an involutive process. At the end of the 4th instar, they extrude Host–parasite relationships are important exper- imental models for understanding how the insect Contract grant sponsor: PAR. ‘‘innate’’ immune system (Schmidt et al., 2001) rec- ognizes a variety of invaders (e.g., endoparasitic *Correspondence to: Prof. Romano Dallai, Department of Evolu- wasps) and how parasites—more or less closely tionary Biology, University of Siena, Via A. Moro 2, Siena I-53100, related to the host—overcome the insect immune Italy. E-mail: [email protected] response. Hemocytes, the cellular component of Published online 16 April 2007 in the insect immune system (Lavine and Strand, Wiley InterScience (www.interscience.wiley.com) 2002), play a major role in defense against meta- DOI: 10.1002/jmor.10540 Ó 2007 WILEY-LISS, INC. ENDOPARASITIC DEVELOPMENT OF XENOS VESPARUM 589 P. dominulus larvae and the ability of X. vesparum to elude this response. Recently, an unusual immune defense has been described in Strepsiptera (Kathirithamby et al., 2003): the parasite Stichotrema dallatorreanum manipulates the tissues of the hosts Segestidae novaeguineae and S. defoliaria defoliaria (Orthop- tera, Tettigonidae) to build a ‘‘host-derived epider- mal bag,’’ a sort of ‘‘camouflage’’ against the host defense reaction. The immune elusion mechanisms of Xenos vesparum could exploit similar compo- nents of the host’s defense repertoire; alternatively they may represent a different adaptive strategy which has evolved during an ancient and deep Fig. 1. Distribution of 235 living Xenos vesparum parasites association with its host. (or exuvia in absence of living parasites) in 89 Polistes dominu- lus wasps (late larvae, pupae and adults). MATERIALS AND METHODS with their anterior region, the cephalothorax, Study Animals through the host cuticle. They are larviparous per- manent endoparasites, which at maturity fill most Nests of Polistes dominulus Christ were collected during late spring from various locations in Tuscany (Italy). Each colony of the wasp hemocoelic cavity, and lack distinct was housed in a 20 3 20 3 20 cm Plexiglas cage (with sugar, antennae, mouthparts, eyes, wings, legs, and water and Sarcophaga sp. larvae ad libitum) for 1 month, to external genitalia. The opening of the ventral verify that nests were not yet infected by strepsipterans in the canal in the cephalothorax allows both the extra- field. In all, nine colonies were artificially infected in laboratory genital insemination and the escape of the triun- with 1st instar larvae (triungulins) of Xenos vesparum Rossi. Our sources of triungulins were 13 wasps, collected from two gulins (Beani et al., 2005a). hibernating groups (Impruneta and Volterra), parasitized by a This characteristic protrusion of the cephalo- single female of X. vesparum. These females, extruding their theca of the puparium or the sclerotized anterior cephalothorax from wasp abdomen, released triungulins after portion of cephalothorax is called ‘‘stylopization’’ of 2–3 weeks at 12L/12D and 288C. the host (from the family Stylopidae). Stylopized wasps, regardless of their putative caste, neither work nor reproduce. Instead they desert the colony Artificial Infections and Dissections early on to form, first, summer extra-nidal aggre- Infections (15 in all) were started at mid-June and extended gations, where parasite mating is likely to occur until the beginning of August. After the temporary removal of (Hughes et al., 2004b), then autumn-winter dia- adult wasps from the experimental colony, the nest was placed pausing groups, where the fertilized Xenos vespa- under a stereo microscope. Using a needle, two to four triungu- rum females overwinter inside their hosts to infect lins were transferred (Fig. 2A–D) from the abdomen of stylop- ized wasps to ‘‘late’’ larval stages of Polistes dominulus (4th, new colonies the next spring (Beani, 2006). These 5th and sometimes 3rd instars, Fig. 2A), without removing females may be used as long-term dispensers of them from the nest and marking the cells with a distinct color. triungulins to infect wasp larvae in the laboratory. Triungulins were generally placed in the anterior portion of the We have monitored the endoparasitic develop- wasp body, dorsally and posterior to the mandibles. After 10 min the nest was then tied in its cage, so the wasps would not ment of Xenos vesparum inside the body of Polistes abandon the colony. dominulus by means of artificial infections. First, The majority of stylopized adult wasps in the field present a we focus on how the triungulin manages to pene- single extruded parasite (Hughes et al., 2004a, b), although af- trate the wasp larva, which is protected by com- ter dissections higher numbers of immature parasites were pact overlapping cuticle layers, and to evade the recorded (personal observations); moreover the parasite load wound healing reaction at the entry site (Rowley per brood in naturally infected nests is higher and variable (Hughes et al., 2003). We tried to simulate a natural infection and Ratcliffe, 1981). Second, we describe step-by- pattern, in which several triungulins are likely to reach one step the developmental stages of the parasite in larva. For this reason, and in order to increase the probability the hemocoel, up to its 4th instar which is well of successful infections (at least two parasites per host), we
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