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Host-parasite hormonal interactions: An overview
Vol. 32, No. 4, pp. 295-298, Printed in Great Britain.All rightsreserved
J. Insect Physiol.
0022-1910/86
1986
HOST-PARASITE
$3.00 +O.OO
Copyright0 1986PergamonPressLtd
HORMONAL INTERACTIONS: AN OVERVIEW
PAULINE0. LAWRENCE Department of Zoology, 223 Bartram Hall, University of Florida, Gainesville, FL 32611, U.S.A.
INTRODUCTION Insect parasites are remarkably similar to other metazoan parasites in that they exhibit a high level of nutritional, physiological and behavioural interactions with their hosts. Unlike other parasites, however, the insect parasites’ period of intimate association with their hosts occurs only during their immature development. At this time, the avoidance of host immune responses and availability of nutrients for growth and development are of the utmost importance. The mechanisms by which these parasites meet their nutritional needs and avoid host defences are discussed elsewhere in this volume so they will not be addressed here. Instead, this paper will focus on the possible endocrine strategies insect parasites use to achieve optimal growth and development and to synchronize their life cycles with those of their hosts. A variety of hormones which are transported in the haemolymph of insects regulate their growth and development (see reviews by Downer and Laufer, 1983; Kerkut and Gilbert, 1985). Since many parasitic insects, especially the Diptera and Hymenoptera, live in their hosts’ haemolymph (Askew, 1971), they presumably exploit these hormones to their advantage. The primary hormones are juvenile hormone which is secreted by the corpora allata and maintains larval characters, and ecdysone which is secreted by the prothoracic glands or ring gland in Diptera and its conversion to moulting after initiates 20-hydroxyecdysone (Smith et al., 1980). The character of the moult is dictated by the presence or absence of juvenile hormone (Riddiford, 1980). In holometabolous insects, as shown in last-instar Munduca sextu, when a critical size for metamorphosis is attained juvenile hormone titres decline, the prothoracicotropic hormone from the brain is released (Nijhout, 1975; Nijhout and Williams, 1974), and a small commitment peak of ecdysone (Bollenbacher et al., 1979) initiates wandering behaviour (Truman and Dominick, 1983). Ecdysone then presumably acts via the brain to initiate juvenile hormone synthesis (Whisenton et al., 1985) which in turn stimulates the prothoracic glands via a factor from the fat body (Gruetzmacher et al., 1984a, b). Supposedly, this factor in conjunction with the second release of prothoracicotropic hormone causes the large ecdysone peak for pupation (Watson et al., 1985). While the dynamics of the inter-endocrine events in other Holometabola are not well understood, there appear to be three ecdysteroid peaks in Diptera, each initiating wandering, pupariation and pupation (Koolman, 1980; Richards, 1981).
Insect parasites attack all developmental stages of holometabolous insects. Some parasite species like Trichogramma restrict their development to the host egg (Salt, 1941) or are egg-larval parasites [e.g. Chelonus] (Askew, 1971). Others develop exclusively in larval stage hosts (e.g. Apanteles = Cotesiu spp.), in pupal hosts [e.g. Nusonia vitripennis] (Askew, 1971) or in larval-pupal hosts [e.g. Opius spp. and Biosteres spp.] (Clausen et al., 1965). While most parasites possibly share some endocrine communication with their hosts, it is impossible to attempt a discussion of all these relationships in this short overview (see also Beckage, 1985). Here I will discuss primarily the larval and larval-pupal endoparasitic Hymenoptera of Diptera and Lepidoptera. These parasites appear to fall into two categories: (1) those that depend directly on host hormones or indirectly through hormonally triggered changes in host physiology in order to synchronize their growth and development with the host’s and (2) those that interfere with the host’s hormonal system and/or produce hormonally active substances that cause the host to linger in the most beneficial stage (Riddiford, 1975). It seems that parasites in both these categories synchronize their life cycles with those of their hosts. However, they appear to utilize their hosts’ hormones differently. To elucidate these endocrine relationships, I will discuss examples of these two categories of parasites and suggest the bases for their different developmental strategies. SPECIESSHOWING RELIANCE
DIRECT OR INDIRECT ON HOST HORMONES
These parasites do not appear to alter host behaviour, development or morphology but are more obviously influenced by their hosts. Evidence for this was reported in Opius concolor, a braconid larval-pupal parasite of Ceratitis cupitata: first-instar parasites in developmentally arrested host larvae could not moult until after the host was injected with ecdysone and had pupariated. The parasite then moulted about 36 h later (Cals-Usciati, 1969, 1975). A related parasite, Biosteres longicaudatus, moulted in synchrony with pupation of its host Anastrepha suspensa within 24 h after the host’s pre-pupal ecdysteroid peak (Lawrence, this volume). Moulting was suppressed when 1st instars were isolated in abdomens of prewandering 3rd-instar hosts ligated posterior to the ring gland. The parasites moulted only if the host abdomens were parabiosed to host pupae (Lawrence, 1982) or treated with 20-hydroxyecdysone which also elicited host pupariation and subsequent larval-pupal apolysis (Lawrence, this issue). Synchronous moul-
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ting of the related braconids, Diachasma tryoni and Opius melleus, with pupariation of Drosophila and Rhagoletis pomonella, respectively, have been reported (Pemberton and Willard, 1918; Lathrop and Newton, 1933). The precise timing of the parasite moults relative to ecdysteroid titres in these hosts remains to be determined. Lathrop and Newton (1933) suggested that R. pomonella induced diapause in 0. melleus. However, according to their reports, this parasite overwintered as a full-grown larva. Based on the life cycle of a related parasite species [e.g. B. Zongicaudatus (Lawrence and Hagedorn, 1985)] all host tissues have been consumed before the fourth instar. Hence, direct host induction of diapause was unlikely. However, the nutritional quality of the host upon consumption by 0. melleus could have had an indirect effect. Corbet (1968) suggested that the osmolarity and, presumably, the nutritional quality of the lepidopteran Ephestia kuehniella influenced moulting of its parasite Nemeritis ( = Venturia) canescens. During wandering of the host, the parasite’s feeding increased and it moulted at the onset of host metamorphosis. Supposedly, this is an indirect result of host ecdysteroids since in Lepidoptera a commitment peak of ecdysteroids initiates wandering and preparation of the tissues for metamorphosis (Truman and Riddiford, 1974). Further evidence implicating host ecdysteroids in parasite development was reported by Schoonhoven (1962). Moulting of the tachinid parasite Eucarcelia ( = Carcelia) rutilla in diapausing pupae of Bupalus piniarius, was stimulated by a factor in the haemolymph of non-diapausing pupal hosts to which the diapausing hosts were parabiosed. He attributed this to increased ecdysteroid titres which occurred at the termination of host diapause. More direct evaluations of host ecdysteroid regulation of parasite development were reported by Baronio and Sehnal(l980). They found that ecdysone treatment of Galleria larvae stimulated the parasite Gonia cinerascens to moult to the second instar and migrate to the exuvial space of the host. When hosts were chilled, treated with juvenile hormone or received corpora allata implants, their metamorphosis was suppressed and the parasites did not moult. The above examples demonstrate an apparent obligatory relationship between the parasite’s first larval moult and the endocrine events related to host metamorphosis. Indeed, in vivo and in vitro studies have also established that parasite moulting (Lawrence, this volume), growth and longevity (Nenon, 1972) will not occur without 20-hydroxyecdysone or juvenile hormone (or its analogue) along with 20-hydroxyecdysone. Why do some parasites consistently linger in the first instar, regardless of their time of oviposition, prior to host metamorphosis? A possible explanation is that they may have no functioning prothoracic glands at this stage and must therefore utilize host ecdysteroids and presumably other hormones secreted at metamorphosis. Although the existence of a functioning prothoracic gland in parasite first instars has neither been demonstrated nor disproved, it has been shown that the parasite B. longicaudatus can take up ecdysone in vitro and convert it to 20-hydroxyecdysone (Lawrence and Hagedorn,
LAWRENCE
1985). It is therefore likely that parasites can pick up and utlize host ecdysteroids in vivo. The mechanisms of uptake have not yet been established but the anal vesicle in some species can take up nutrients (Edson and Vinson, 1977) and could also be an avenue for hormone uptake. Beckage (1985) suggested that ecdysteroid passage may be via the thin, non-hydrophobic integument that occurs in many parasite first instars. Ingestion, a more obvious means of hormone entry suggested by Riddiford (1975), is a simple and plausible alternative. Ingested ecdysone can be conjugated in the gut or pass via the gut of Teleogryllus commodus into the haemolymph (Greenwood, 1985). If hymenopterous parasites can likewise deactivate ecdysteroids consumed with host tissues and accumulate them in the blind gut, they could later reactivate and utilize these hormones. Claret et al. (1978) and Lawrence and Hagedorn (1985) found ecdysteroids in the haemolymph of last-instar parasites which had already consumed all of their hosts’ tissues. Early instars also contained ecdysteroids (Lawrence and Hagedorn, 1985). Although these parasites might have synthesized their own ecdysteroids, it is possible that the hormone came from the host via the parasites’ gut. Presumably, these parasites do not induce significant changes in host development; e.g. there were no differences in size, onset of wandering or larval-pupal apolysis between unparasitized A. suspensa larvae and those with up to 2 (sometimes 3) B. longicaudatus first instars (Lawrence, unpublished). Similarly, R. pomonella larvae parasitized by 0. melleus did not alter their behaviour at pupation (Lathrop and Newton, 1933). The apparent lack of host modification by these larval-pupal parasites could be related (among other things) to their nutritional and physiological requirements. Larval hosts may be nutritionally and physiologically adequate to support the growth of parasite eggs and first instars (host size may also be limiting to older parasite stages). Conversely, pupal hosts may be optimal for those parasite stages beyond the first instar and may even be sub-optimal for younger stages; e.g. less than 50% of B. longicaudatus eggs laid in wandering A. suspensa larvae hatched compared to >90% in first day, third-instar hosts (Lawrence et al., 1976). Since hormones influence protein and lipid metabolism in the fat body (Downer, 1972; Collins, 1974), their fluctuations at host metamorphosis could serve as a cue to the parasite of impending nutritional changes. Thus, parasites may be able to capitalize on these changing host conditions without significantly altering them. I have therefore coined the term physiological “conformers” to describe parasites in this group. SPECIES ALTERING HOST HORMONES AND DEVELOPMENT
A description of the host regulation phenomenon (Vinson and Iwantsch, 1980) included examples of parasitized hosts that showed no externally visible evidence of parasitism (e.g. an increase in host haemocytes). However, most examples consisted of parasite-associated (and/or induced) changes that were manifested in the host’s morphology, behaviour and development (Vinson and Iwantsch, 1980).
Host-parasite hormonal interactions I therefore wish to introduce the term “regulators” to describe only those parasites in the latter group. Reduced host size and prolonged larval development have been reported for a variety of Lepidoptera attacked by Apanteles (= Cotesia) spp. (Stamp, 1981; Beckage and Riddiford, 1982; Porter, 1983; Schopf, 1984). These host changes are caused by elevated host juvenile hormone levels, the lack of conversion of ecdysone to 20-hydroxyecdysone as in Manduca sexta parasitized by A. congregatus (Beckage and Templeton, this issue) and depleted nutrients (Thompson, 1982). On the other hand, accelerated prepupal development in Trichoplusia ni due to Chelonus sp. parasitism is caused by abnormally depressed juvenile hormone levels (Jones, 1985). In Heliothis virescens, inhibited host pupation caused by Microplitis croceipes is related to suppressed host ecdysteroid levels (Webb and Dahlman, this issue). Parasitism also causes colour changes and changes in foraging behaviour of some hosts (%nson, 1976; Stamp, 1981). Though these parasite effects on their hosts show subtle differences, those studied to date all influence ecdysteroid and juvenile hormone levels. Since the fat body is the primary site of protein and fatty acid synthesis (Collins, 1974), 20-monoxygenase metabolism of ecdysone (Smith et al., 1980) and site of the lipoprotein synthesis necessary for prothoracic gland stimulation (Gruetzmacher et al., 1984b), it is possible that damage to the fat body caused by parasitism could account for the nutrient deficiencies and endocrine changes reported (see other papers, this issue); e.g. Iwantsch and Smilowitz (1976) demonstrated that pathological changes in the fat body of T. ni were due to Hyposoter exiguae which also prevented pupation of the host (Smilowitz, 1974; Iwantsch and Smilowitz, 1975) and depleted host lipids, fatty acids and glycogen reserves (Thompson, 1982). Thus, the mechanisms of parasite regulation of host physiology may be as complicated as the inter-endocrine regulation of insect metamorphosis itself. The fact that parasites may themselves secrete juvenile hormone, hormone mimics or other substances into the host, disrupting host development (Schopf, 1984; see also Beckage, 1985) further complicates the issue. Since virus-like particles are introduced by some ovipositing females into host haemolymph, these may also interfere with host endocrine function (Stoltz and Vinson, 1979). While moulting synchrony exists between some “regulator” species and their hosts (Beckage, 1985), it appears that others can moult independently; e.g. A. congregatus can develop in the same larval stage of M. sexta without further moulting of the host (see Beckage, 1985). There is also no apparent obligatory moulting between A. euphydryidis or Benjaminia euphydryadis and their host Euphydryas phaeton (see Stamp, 1984). Thus “regulators” may have a facultative (or less obligatory) endocrine relationship with their hosts than do “conformers”. If this is so then they should have functioning prothoracic glands. However, they may utilize host hormones to assess the endocrine and/or nutritional status of their hosts. Why then do these parasites regulate their hosts? Nutritional physiology may be one of the bases of
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this phenomenon. It is possible that the large size of most lepidopteran larvae relative to parasite size affords the latter a large quantity of the nutrients required for optimal growth. Thus, in order to maintain those optimal nutritional conditions, some “regulators” may disrupt endocrine and related events to prolong larval life, e.g. H. exiguae normally attacks early-instar T. ni and prevents host pupation. However, when late-instar hosts are attacked, parasites fare poorly (Smilowitz, 1974; Smilowitz and Iwantsch, 1973). On the other hand, parasites like Chelonus near curvimaculatus (Jones, 1985) and Alysiu manducator (Alston, 1920) that induce precocious host metamorphosis might have other nutritional needs, or other factors not as yet understood may be involved. SUMMARY
Parasite interactions with their hosts appear to fall into two major categories: (1) “conformers” and (2) “regulators”. While species in both categories synchronize their life cycles temporally with their hosts’ to allow continuity of generations, they appear to differ in the following ways: (a) In “conformers” the first moult is obligatorily synchronized with an apparent ecdysteroid increase and host metamorphosis. “Regulators” may or may not synchronize their first moult with their hosts’s, depending on the stage of the host attacked; (b) “Conformers” do not disrupt host development, morphology or behaviour, while “regulators” do, primarily by causing (directly or indirectly) changes in host juvenile hormone and ecdysteroid synthesis and metabolism. These effects may be exerted via the fat body or in the haemolymph by the introduction of viruses, hormones or hormone mimics. The mechanisms of these disruptive effects of parasitism may be as complicated as the normal inter-endocrine relationships within the host itself. REFERENCES
Alston A. M. (1920) The life history and habits of two parasites of blow-flies. Proc. 2001. Sot. Lond. 17, 195-243.
Askew R. R. (1971) ParasiticInsects. C. F. R. Woodward, London. Baronio P. and Sehnal F. (1980) Dependence of the parasitoid Gonia cinerascenson the hormones of its lepidopterous hosts. J. Insect Physiol. 26, 619-626. Beckage N. E. (1985)Endocrine interactions between endoparasitic insects and their hosts. A. Rev. Ent. 30,371-413. Beckage N. E. and Riddiford L. M. (1982) Effects of parasitism by Apanteles congregatus on the endocrine ehvsiologv of the tobacco hornwotm Manduca sexta. bei.
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Endocr. 47, 308-322.
Bollenbacher W. E.. Armi N.. Granter N. A. and Gilbert L. I. (1979) In vitroaciivation of i&&t prothoracic glands by the prothoracicotropic hormone. Proc. natn. Acad, Sci. U.S.A. 76, 5148-5152.
Cals-Usciati J. (1969) Influence de l’etat physiologique de l’h8te Ceratitis capitata Weid. (Diptera) sur le developpement du parasite 0piu.s concolor Szepl. (Hymenoptera). C. r. hebd. S&UK. Acad. Sci., Paris S&r. D. 269, 342-344.
Cals-Usciati J. (1975) R&percussion de la modification du ‘cycle normal de Ceratitis capitata Wied. (Dipthre Trypetidae), par irradiation y et injection d’ecdysone, sur le d&veloppment de son parasite Opius concolor Szepl. (Hymenoptkre Braconidae). C. r. hebd. SPanc., Acad. Sci., Paris Six. D. 281, 275-278.
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Claret J., Porcheron P. and Dray F. (1978) La teneur en circulantes au tours du dernier stade larvaire de 1’Hymenoptere endoparasite Pimpla instigator, et l’entree en diapause. C. r. hebd. Seam. Acad. Sci., Paris Ser. D. 286, 639-641. Clausen C. P., Clancy G. and Chock D. (1965) Introduction of parasites against the Oriental fruit fly, Dacus dorsalis in Hawaii. USDA-ARS Tech. Bull. no. 1322, pp. l-102. Collins J. V. (1974) Hormonal control of protein sequestration in the fat body of Calpodes ethlius. Can. J. Zool. 52, 639-642. Corbet S. A. (1968) The influence of Ephestia kuehniella on the development of its parasite Nemeritis canescens. J. exp. Biol. 48, 291-304. Downer R. G. and Laufer H. (1983) Endocrinology of Insects. pp. l-707. Alan R. Liss, New York. Edson K. M. and Vinson S. B. (1977) Nutrient absorption by the anal vesicle of the braconid wasp, Microplitis croceipes. J. Insect Physiol. 23, 5-8. Greenwood D. R. (1985) Metabolism of ingested and injected ecdysone in the cricket Teleogryllus commodus. VZZEcdvsone Workshoo. Edinburgh, Scotland. IAbstractl. Gruetzmacher M. C., Gilbert L. I.,-&anger N. ‘A., Goodman W. and Bollenbacher W. E. (1984a) The effect of juvenile hormone on prothoracic gland function during the larval-pupal development of Manduca sexta: an in situ and in vitro analysis. J. Insect Physiol. 30, 331-340. Gruetzmacher M. C., Gilbert L. I. and Bollenbacher W. E. (1984b) Indirect stimulation of the prothoracic glands of Manduca sexta by juvenile hormone: evidence for a fat body stimulatory factor. J. Insect Physiol. 30, 771-778. Iwantsch G. F. and Smilowitz Z. (1975) Relationships between the parasitoid Hyposoter exiguae and Trichoplusia ni: prevention of host pupation at the endocrine level. J. Znsect Physiol. 21, 115llll57. Iwantsch G. and Smilowitz Z. (1976) Relationshius between the parasitoid Hyposoter exiguae and Trich‘oplusia ni: parasitoid-induced histo- and cytopathology. J. Invert. Path. 27, 149-160. Jones D. (1985) The endocrine basis for developmentally stationary prepupae in larvae of Trichoplusia ni pseudoparasitized by Chelonus insularis. J. Comp. Physiol. B. 155, 235-240. Kerkut G. A. and Gilbert L. (1985) Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vols 7 and 8. Pergamon Press, New York. Koolman J. (1980) Ecdysteroids in the blowfly, Culliphora vicina. In Progress in Edcysone Research. (Ed. by Hoffmann J. A.), pp. 187-209. Elsevier/North-Holland Biomed. Press. Lathrop F. H. and Newton R. C. (1933) The biology of Opius melleus Gahan, a parasite of the blueberry maggot. J. Agric. Res. 46, 143-160. Lawrence P. 0. (1982) Biosteres longicaudatus: developmental dependence on host (Anastrepha suspensa) physiology. Exp. Parasit. 53, 396405. Lawrence P. O., Baranowski R. M. and Greany P. D. (1976) Effect of host age on development of Biosteres (Opius) longicaudutus, a parasitoid of the Caribbean fruit fly, Anastrepha suspensa. Fla Ent. 59, 33-39. Lawrence P. 0. and Hagedorn H. H. (1986) Relationship between the ecdysteroid titers of a host and those of its parasite. Znsect Biochem. 16, 163-167. Nenon J. (1972) Culture in vitro des embryos dun Hymenoptere kndoparasite polyembryonnaire: Ageniaspis fiscicollis. Role des hormones de synthesis. C. r. hebd. Seanc. Acad. Sci. Paris Ser. D. 274, 340993412. Niihout H. F. (1975) A threshold size for metamorphosis in The tobacco ‘hornworm, Manduca sexta (L.). Biol. Bull. mar. biol. Lab., Woods Hole 149, 214-225. Nijhout H. F. and Williams C. M. (1974) Control ofmolting and metamorphosis in the tobacco hornworm, Munduca sexta (L.): cessation of juvenile hormone secretion as a trigger for pupation. J. exp. Biol. 61, 493-501.
Pemberton C. E. and Willard H. F. (1918) A contribution to the biology of fruit fly parasites in Hawaii. J. Agric. Res. 15, 419465. Porter K. (1983) Multivoltinism in Apanteles bignellii and the influence of weather on synchronization with its host Euphydryas aurinia. Entomologia exp. appl. 34, 1555162. Richards G. (1981) The radioimmune assay of ecdysteroid titers of Drosoohila melanoaaster. Molec. Cell. Endocr. 21. 181-197. _ Riddiford L. M. (1975) Host hormones and insect parasites. In Invertebrate Immunity (Ed. by Maramorosch K. and Schope R. E.), pp. 339-353. Academic Press, New York. Riddiford L. M. (1980) Interaction of edcysteroids and juvenile hormone in the regulation of larval growth and metamorphosis of the tobacco hornworm. In Progress in Ecdysone Research (Ed. by Hoffmann J. A.), pp. 4099430. Elsevier/North-Holland Biomed. Press. Salt G. (1941) The effects of hosts upon their insect parasites. Biol. Rev. 16, 239-264. Schoonhoven L. M. (1962) Diapause and the physiology of host-parasite synchronization in Bupaius ptii&ius (Eeometridae) and Eucarcehu rutilhz Vill. (Tachinidae). Archs Neerf. Zbol. 15, 111-173. Schopf A. (1984) Endocrinological investigations of the host-parasite system: Pieris brassicae-Apanteles glomeratus. Entomologia exp. appl. 36, 265-272. Smilowitz Z. (1974) Relationships between the parasitoid Hyposoter exiguae (Viereck) and the cabbage looper, Trichopfusia ni (Hubner): evidence for endocrine involvement in successful parasitism. Ann. ent. Sot. Am. 67, 317-320. Smilowitz Z. and Iwantsch G. (1973) Relationships between the parasitoid Hyposoter exiguae and the cabbage looper, Trichoplusia ni: effects of host age on developmental rate of the parasitoid. Enuir. Ent. 2, 7599763. Smith S. L., Bollenbacher W. E. and Gilbert L. I. (1980) Studies on the biosynthesis of ecdysone and 20.hydroxy_ _ ecdysone in the tobacco hornworm, Manducu sexta. In Progress in Ecdvsone Research (Ed. bv Hoffman J. A.). pp.139-162. Eisevier/North-Holland Biomedical Press; New York. Stamp N. E. (1981) Behaviour of parasitized aposematic caterpillars: Advantageous to the parasitoid or the host? Am. Nat. 118, 715-725. Stamp N. (1984) Interactions of parasitoids and checkerspot caterpillars, Euphydryus spp. (Nymphaiidae). J. Res. Lepid. 23, 2-18. Stoltz D. B. and Vinson S. B. (1979) Viruses and parasitism in insects. Adv. Virus Res. 24, 125-171. Thompson S. N. (1982) Effects of the insect parasite, Hyposoter exiguae on the total body glycogen and lipid level of its host, Trichoplusia ni. Comp. Biochem. Physiol. 72B, 233-237. Truman J. and Dominick 0. S. (1983) Endocrine mechanisms organizing invertebrate behavior. Biosci. 33, 54655 1. Truman J. and Riddiford L. M. (1974) Physiology of insect rhythms II. The temporal organization of the endocrine events underlying pupation of the tobacco hornworm. Manduca sexta @..j i Insect Physiol. 29, 895-900. Vinson S. B. (1976) Host selection in insect oarasitioids. A. Rev. Em. 2$ 109-133. Vinson S. B. and Iwantsch G. F. (1980) Host regulation by insect parasitoids. Q. Rev. Biol. 55, 143-165. Watson R. D., Ciancio M. J., Gunnar W. P., Gilbert L. I. and Bollenbacher W. E. (1986) Regulation of insect prothoracic glands: Existence of a hemolymph stimulatory factor in Manduca sexta. J. Insect Physiol. 32, 487494. Whisenton L. R., Bowen M. F., Granger N. A., Gilbert L. I. and Bollenbacher W. E. (1985) Brain-mediated 20-hydroxyecdysone regulation of juvenile hormone synthesis by the corpora allata of the tobacco hornworm, Manduca sexta. Gen. Comp. Endocr. In press.
J. Insect Physiol.
0022-1910/86
1986
HOST-PARASITE
$3.00 +O.OO
Copyright0 1986PergamonPressLtd
HORMONAL INTERACTIONS: AN OVERVIEW
PAULINE0. LAWRENCE Department of Zoology, 223 Bartram Hall, University of Florida, Gainesville, FL 32611, U.S.A.
INTRODUCTION Insect parasites are remarkably similar to other metazoan parasites in that they exhibit a high level of nutritional, physiological and behavioural interactions with their hosts. Unlike other parasites, however, the insect parasites’ period of intimate association with their hosts occurs only during their immature development. At this time, the avoidance of host immune responses and availability of nutrients for growth and development are of the utmost importance. The mechanisms by which these parasites meet their nutritional needs and avoid host defences are discussed elsewhere in this volume so they will not be addressed here. Instead, this paper will focus on the possible endocrine strategies insect parasites use to achieve optimal growth and development and to synchronize their life cycles with those of their hosts. A variety of hormones which are transported in the haemolymph of insects regulate their growth and development (see reviews by Downer and Laufer, 1983; Kerkut and Gilbert, 1985). Since many parasitic insects, especially the Diptera and Hymenoptera, live in their hosts’ haemolymph (Askew, 1971), they presumably exploit these hormones to their advantage. The primary hormones are juvenile hormone which is secreted by the corpora allata and maintains larval characters, and ecdysone which is secreted by the prothoracic glands or ring gland in Diptera and its conversion to moulting after initiates 20-hydroxyecdysone (Smith et al., 1980). The character of the moult is dictated by the presence or absence of juvenile hormone (Riddiford, 1980). In holometabolous insects, as shown in last-instar Munduca sextu, when a critical size for metamorphosis is attained juvenile hormone titres decline, the prothoracicotropic hormone from the brain is released (Nijhout, 1975; Nijhout and Williams, 1974), and a small commitment peak of ecdysone (Bollenbacher et al., 1979) initiates wandering behaviour (Truman and Dominick, 1983). Ecdysone then presumably acts via the brain to initiate juvenile hormone synthesis (Whisenton et al., 1985) which in turn stimulates the prothoracic glands via a factor from the fat body (Gruetzmacher et al., 1984a, b). Supposedly, this factor in conjunction with the second release of prothoracicotropic hormone causes the large ecdysone peak for pupation (Watson et al., 1985). While the dynamics of the inter-endocrine events in other Holometabola are not well understood, there appear to be three ecdysteroid peaks in Diptera, each initiating wandering, pupariation and pupation (Koolman, 1980; Richards, 1981).
Insect parasites attack all developmental stages of holometabolous insects. Some parasite species like Trichogramma restrict their development to the host egg (Salt, 1941) or are egg-larval parasites [e.g. Chelonus] (Askew, 1971). Others develop exclusively in larval stage hosts (e.g. Apanteles = Cotesiu spp.), in pupal hosts [e.g. Nusonia vitripennis] (Askew, 1971) or in larval-pupal hosts [e.g. Opius spp. and Biosteres spp.] (Clausen et al., 1965). While most parasites possibly share some endocrine communication with their hosts, it is impossible to attempt a discussion of all these relationships in this short overview (see also Beckage, 1985). Here I will discuss primarily the larval and larval-pupal endoparasitic Hymenoptera of Diptera and Lepidoptera. These parasites appear to fall into two categories: (1) those that depend directly on host hormones or indirectly through hormonally triggered changes in host physiology in order to synchronize their growth and development with the host’s and (2) those that interfere with the host’s hormonal system and/or produce hormonally active substances that cause the host to linger in the most beneficial stage (Riddiford, 1975). It seems that parasites in both these categories synchronize their life cycles with those of their hosts. However, they appear to utilize their hosts’ hormones differently. To elucidate these endocrine relationships, I will discuss examples of these two categories of parasites and suggest the bases for their different developmental strategies. SPECIESSHOWING RELIANCE
DIRECT OR INDIRECT ON HOST HORMONES
These parasites do not appear to alter host behaviour, development or morphology but are more obviously influenced by their hosts. Evidence for this was reported in Opius concolor, a braconid larval-pupal parasite of Ceratitis cupitata: first-instar parasites in developmentally arrested host larvae could not moult until after the host was injected with ecdysone and had pupariated. The parasite then moulted about 36 h later (Cals-Usciati, 1969, 1975). A related parasite, Biosteres longicaudatus, moulted in synchrony with pupation of its host Anastrepha suspensa within 24 h after the host’s pre-pupal ecdysteroid peak (Lawrence, this volume). Moulting was suppressed when 1st instars were isolated in abdomens of prewandering 3rd-instar hosts ligated posterior to the ring gland. The parasites moulted only if the host abdomens were parabiosed to host pupae (Lawrence, 1982) or treated with 20-hydroxyecdysone which also elicited host pupariation and subsequent larval-pupal apolysis (Lawrence, this issue). Synchronous moul-
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ting of the related braconids, Diachasma tryoni and Opius melleus, with pupariation of Drosophila and Rhagoletis pomonella, respectively, have been reported (Pemberton and Willard, 1918; Lathrop and Newton, 1933). The precise timing of the parasite moults relative to ecdysteroid titres in these hosts remains to be determined. Lathrop and Newton (1933) suggested that R. pomonella induced diapause in 0. melleus. However, according to their reports, this parasite overwintered as a full-grown larva. Based on the life cycle of a related parasite species [e.g. B. Zongicaudatus (Lawrence and Hagedorn, 1985)] all host tissues have been consumed before the fourth instar. Hence, direct host induction of diapause was unlikely. However, the nutritional quality of the host upon consumption by 0. melleus could have had an indirect effect. Corbet (1968) suggested that the osmolarity and, presumably, the nutritional quality of the lepidopteran Ephestia kuehniella influenced moulting of its parasite Nemeritis ( = Venturia) canescens. During wandering of the host, the parasite’s feeding increased and it moulted at the onset of host metamorphosis. Supposedly, this is an indirect result of host ecdysteroids since in Lepidoptera a commitment peak of ecdysteroids initiates wandering and preparation of the tissues for metamorphosis (Truman and Riddiford, 1974). Further evidence implicating host ecdysteroids in parasite development was reported by Schoonhoven (1962). Moulting of the tachinid parasite Eucarcelia ( = Carcelia) rutilla in diapausing pupae of Bupalus piniarius, was stimulated by a factor in the haemolymph of non-diapausing pupal hosts to which the diapausing hosts were parabiosed. He attributed this to increased ecdysteroid titres which occurred at the termination of host diapause. More direct evaluations of host ecdysteroid regulation of parasite development were reported by Baronio and Sehnal(l980). They found that ecdysone treatment of Galleria larvae stimulated the parasite Gonia cinerascens to moult to the second instar and migrate to the exuvial space of the host. When hosts were chilled, treated with juvenile hormone or received corpora allata implants, their metamorphosis was suppressed and the parasites did not moult. The above examples demonstrate an apparent obligatory relationship between the parasite’s first larval moult and the endocrine events related to host metamorphosis. Indeed, in vivo and in vitro studies have also established that parasite moulting (Lawrence, this volume), growth and longevity (Nenon, 1972) will not occur without 20-hydroxyecdysone or juvenile hormone (or its analogue) along with 20-hydroxyecdysone. Why do some parasites consistently linger in the first instar, regardless of their time of oviposition, prior to host metamorphosis? A possible explanation is that they may have no functioning prothoracic glands at this stage and must therefore utilize host ecdysteroids and presumably other hormones secreted at metamorphosis. Although the existence of a functioning prothoracic gland in parasite first instars has neither been demonstrated nor disproved, it has been shown that the parasite B. longicaudatus can take up ecdysone in vitro and convert it to 20-hydroxyecdysone (Lawrence and Hagedorn,
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1985). It is therefore likely that parasites can pick up and utlize host ecdysteroids in vivo. The mechanisms of uptake have not yet been established but the anal vesicle in some species can take up nutrients (Edson and Vinson, 1977) and could also be an avenue for hormone uptake. Beckage (1985) suggested that ecdysteroid passage may be via the thin, non-hydrophobic integument that occurs in many parasite first instars. Ingestion, a more obvious means of hormone entry suggested by Riddiford (1975), is a simple and plausible alternative. Ingested ecdysone can be conjugated in the gut or pass via the gut of Teleogryllus commodus into the haemolymph (Greenwood, 1985). If hymenopterous parasites can likewise deactivate ecdysteroids consumed with host tissues and accumulate them in the blind gut, they could later reactivate and utilize these hormones. Claret et al. (1978) and Lawrence and Hagedorn (1985) found ecdysteroids in the haemolymph of last-instar parasites which had already consumed all of their hosts’ tissues. Early instars also contained ecdysteroids (Lawrence and Hagedorn, 1985). Although these parasites might have synthesized their own ecdysteroids, it is possible that the hormone came from the host via the parasites’ gut. Presumably, these parasites do not induce significant changes in host development; e.g. there were no differences in size, onset of wandering or larval-pupal apolysis between unparasitized A. suspensa larvae and those with up to 2 (sometimes 3) B. longicaudatus first instars (Lawrence, unpublished). Similarly, R. pomonella larvae parasitized by 0. melleus did not alter their behaviour at pupation (Lathrop and Newton, 1933). The apparent lack of host modification by these larval-pupal parasites could be related (among other things) to their nutritional and physiological requirements. Larval hosts may be nutritionally and physiologically adequate to support the growth of parasite eggs and first instars (host size may also be limiting to older parasite stages). Conversely, pupal hosts may be optimal for those parasite stages beyond the first instar and may even be sub-optimal for younger stages; e.g. less than 50% of B. longicaudatus eggs laid in wandering A. suspensa larvae hatched compared to >90% in first day, third-instar hosts (Lawrence et al., 1976). Since hormones influence protein and lipid metabolism in the fat body (Downer, 1972; Collins, 1974), their fluctuations at host metamorphosis could serve as a cue to the parasite of impending nutritional changes. Thus, parasites may be able to capitalize on these changing host conditions without significantly altering them. I have therefore coined the term physiological “conformers” to describe parasites in this group. SPECIES ALTERING HOST HORMONES AND DEVELOPMENT
A description of the host regulation phenomenon (Vinson and Iwantsch, 1980) included examples of parasitized hosts that showed no externally visible evidence of parasitism (e.g. an increase in host haemocytes). However, most examples consisted of parasite-associated (and/or induced) changes that were manifested in the host’s morphology, behaviour and development (Vinson and Iwantsch, 1980).
Host-parasite hormonal interactions I therefore wish to introduce the term “regulators” to describe only those parasites in the latter group. Reduced host size and prolonged larval development have been reported for a variety of Lepidoptera attacked by Apanteles (= Cotesia) spp. (Stamp, 1981; Beckage and Riddiford, 1982; Porter, 1983; Schopf, 1984). These host changes are caused by elevated host juvenile hormone levels, the lack of conversion of ecdysone to 20-hydroxyecdysone as in Manduca sexta parasitized by A. congregatus (Beckage and Templeton, this issue) and depleted nutrients (Thompson, 1982). On the other hand, accelerated prepupal development in Trichoplusia ni due to Chelonus sp. parasitism is caused by abnormally depressed juvenile hormone levels (Jones, 1985). In Heliothis virescens, inhibited host pupation caused by Microplitis croceipes is related to suppressed host ecdysteroid levels (Webb and Dahlman, this issue). Parasitism also causes colour changes and changes in foraging behaviour of some hosts (%nson, 1976; Stamp, 1981). Though these parasite effects on their hosts show subtle differences, those studied to date all influence ecdysteroid and juvenile hormone levels. Since the fat body is the primary site of protein and fatty acid synthesis (Collins, 1974), 20-monoxygenase metabolism of ecdysone (Smith et al., 1980) and site of the lipoprotein synthesis necessary for prothoracic gland stimulation (Gruetzmacher et al., 1984b), it is possible that damage to the fat body caused by parasitism could account for the nutrient deficiencies and endocrine changes reported (see other papers, this issue); e.g. Iwantsch and Smilowitz (1976) demonstrated that pathological changes in the fat body of T. ni were due to Hyposoter exiguae which also prevented pupation of the host (Smilowitz, 1974; Iwantsch and Smilowitz, 1975) and depleted host lipids, fatty acids and glycogen reserves (Thompson, 1982). Thus, the mechanisms of parasite regulation of host physiology may be as complicated as the inter-endocrine regulation of insect metamorphosis itself. The fact that parasites may themselves secrete juvenile hormone, hormone mimics or other substances into the host, disrupting host development (Schopf, 1984; see also Beckage, 1985) further complicates the issue. Since virus-like particles are introduced by some ovipositing females into host haemolymph, these may also interfere with host endocrine function (Stoltz and Vinson, 1979). While moulting synchrony exists between some “regulator” species and their hosts (Beckage, 1985), it appears that others can moult independently; e.g. A. congregatus can develop in the same larval stage of M. sexta without further moulting of the host (see Beckage, 1985). There is also no apparent obligatory moulting between A. euphydryidis or Benjaminia euphydryadis and their host Euphydryas phaeton (see Stamp, 1984). Thus “regulators” may have a facultative (or less obligatory) endocrine relationship with their hosts than do “conformers”. If this is so then they should have functioning prothoracic glands. However, they may utilize host hormones to assess the endocrine and/or nutritional status of their hosts. Why then do these parasites regulate their hosts? Nutritional physiology may be one of the bases of
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this phenomenon. It is possible that the large size of most lepidopteran larvae relative to parasite size affords the latter a large quantity of the nutrients required for optimal growth. Thus, in order to maintain those optimal nutritional conditions, some “regulators” may disrupt endocrine and related events to prolong larval life, e.g. H. exiguae normally attacks early-instar T. ni and prevents host pupation. However, when late-instar hosts are attacked, parasites fare poorly (Smilowitz, 1974; Smilowitz and Iwantsch, 1973). On the other hand, parasites like Chelonus near curvimaculatus (Jones, 1985) and Alysiu manducator (Alston, 1920) that induce precocious host metamorphosis might have other nutritional needs, or other factors not as yet understood may be involved. SUMMARY
Parasite interactions with their hosts appear to fall into two major categories: (1) “conformers” and (2) “regulators”. While species in both categories synchronize their life cycles temporally with their hosts’ to allow continuity of generations, they appear to differ in the following ways: (a) In “conformers” the first moult is obligatorily synchronized with an apparent ecdysteroid increase and host metamorphosis. “Regulators” may or may not synchronize their first moult with their hosts’s, depending on the stage of the host attacked; (b) “Conformers” do not disrupt host development, morphology or behaviour, while “regulators” do, primarily by causing (directly or indirectly) changes in host juvenile hormone and ecdysteroid synthesis and metabolism. These effects may be exerted via the fat body or in the haemolymph by the introduction of viruses, hormones or hormone mimics. The mechanisms of these disruptive effects of parasitism may be as complicated as the normal inter-endocrine relationships within the host itself. REFERENCES
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