De-alation, flight muscle histolysis, and oocyte development in the striped ground cricket, Allonemobius fasciatus

ABSTRACT. Removal of hindwings from long-winged females of the striped ground cricket, Allonemobius fasciatus , DeGeer (Gryllidae), induces flight muscle histolysis and oocyte development. Such females develop oocytes as rapidly as do short-winged forms, while intact long-winged females retain their flight muscles and develop few oocytes.
Flight muscle histolysis occurs in starved long-winged females when they are de-alated. However, such females fail to mature oocytes. Implantation of corpora allata (CA) into long-winged females results in flight muscle histolysis as well as oocyte maturation even if their hindwings remain intact, indicating that flight muscle histolysis can take place without de-alation. It is likely that the CA are responsible for both flight muscle histolysis and oocyte development, and that CA activity is enhanced by de-alation.     

Juvenile hormone as a mediator of plasticity in insect life histories

Insects display much variation in life histories mediated by juvenile hormone. We focus on the contribution of JH to variations in migratory life histories. In many migrants such as the large milkweed bug and the monarch butterfly, JH directly influences migratory flight and the relation between flight and reproduction (oogenesis-flight syndrome). In the true armyworm, JH regulates interactions among female calling, pheromone production, ovarian development, and migration with varying blends of structurally related forms of JH and JH acid. A role for JH also occurs in wing polymorphisms. Aphids regulate wing production via JH-mediated maternal effects; and in crickets, JH esterase modulates the JH influence on wing form. In addition, JH is implicated in wing muscle histolysis. The comprehensive Fairbairn model for JH regulation of wing polymorphisms in flight behavior predicts that JH action will depend on the mode of genetic control, whether single locus or polygenic. Our own studies of the soapberry bug, Jadera haematoloma, reveal a four-morph wing polymorphism in a species rapidly evolving on a new host plant. There are long- and short-winged forms, and the long-winged form displays three degrees of flight muscle histolysis. The polymorphism is subject to both genetic and environmental variations that are mediated by JH. Application of methoprene increases the frequency of the short-winged forms, but there is both within- and between-population genetic variation and genotype by environment interaction (plasticity) in the response to JH. Arch. Insect Biochem. Physiol. 35:359–373, 1997. © 1997 Wiley-Liss, Inc.     

Oogenesis-flight syndrome in crickets: age-dependent egg production, flight performance, and biochemical composition of the flight muscles in adult female Gryllus bimaculatus

Age-dependent changes in flight performance, biochemical composition of flight muscles, and fresh mass of the flight muscles and ovaries were analysed in adult female two-spotted crickets, Gryllus bimaculatus. After the final moult the flight muscle mass increased significantly to a maximum at days 2 and 3. On day 2 the highest flight activity was also observed. Between days 2 and 3 the ovary weight started to rapidly increase due to vitellogenic egg growth, which continued at a high rate until day 10. With the onset of ovarial growth, flight performance decreased and the flight muscles started to histolyse. A high correlation between flight muscle mass and the content of protein, lipid, glycogen, and free carbohydrate in the flight muscle indicated that energy-rich substrates from the degrading flight muscles were used to fuel oogenesis, although flight muscle histolysis can provide only a small fraction of the substrates needed for egg production. In general, there was a clear trade-off between egg production and flight ability. Surprisingly, however, some females possessed well-developed ovaries but displayed no signs of flight muscle histolysis. This observation was corroborated by flight experiments which revealed that, although most flying females had small ovaries, some of them carried an appreciable amount of mature eggs, and thus, somehow managed to evade the oogenesis-flight syndrome.     

Genetic and diurnal variation in the juvenile hormone titer in a wing-polymorphic cricket: implications for the evolution of life histories and dispersal

The wing-polymorphic cricket, Gryllus firmus, contains (1) a flight-capable morph (LW(f)) with long wings and functional flight muscles, (2) a flightless morph with reduced wings and underdeveloped flight muscles (SW), and (3) a flightless morph with histolyzed flight muscles but with fully developed wings (LW(h)). The LW(f) morph differed genetically from the SW morph and phenotypically from the LW(h) morph in the size of flight muscles, ovarian growth during the first week of adulthood, and the hemolymph titer of juvenile hormone (JH). This is the first study to document that phenotypes that differ genetically in morphological aspects of dispersal capability and in ovarian growth also differ genetically in the titer of a hormone that potentially regulates those traits. The JH titer rose 9-100-fold during the photophase in the flight-capable LW(f) morph but did not change significantly during this time in either flightless morph. Prolonged elevation of the in vivo JH titer in flight-capable females, by topical application of a hormone analogue, caused a substantial increase in ovarian growth and histolysis of flight muscles. The short-term, diurnal rise in the JH titer in the dispersing morph may be a mechanism that allows JH to positively regulate nocturnal flight behavior, while not causing maladaptive histolysis of flight muscles and ovarian growth. This is the first demonstration of naturally occurring, genetically based variation for diurnal change in a hormone titer in any organism.     

No Detectable Trade-Offs Among Immune Function,Fecundity, and Survival via a Juvenile Hormone Analog in the House Cricket

Hormones are key regulators of resource allocation among functions and thus play an important role in resource-based trade-offs. The juvenile hormone (JH) is an insect hormone that mediates resource allocation between immunity and life history components. Here, we have tested whether this is the case using the house cricket. We investigated whether increased levels of JH (using methoprene, a JH analog) enable an enhanced survival and fecundity (via egg number) at the cost of reduced hemocyte number (a trait that is associated with immune response in insects) in the house cricket, Acheta domesticus L. We had three groups of adult crickets of both sexes: experimental (methoprene and acetone), positive control (methoprene), and negative control (no manipulation). Prior to and after experimental treatments, we counted the number of hemocytes (for the case of both sexes) and recorded the number of eggs laid and survival of females after the manipulation. There was no difference in hemocyte number, egg number, and survival. These results do not support a JH-mediated trade-off among immune ability, survival, and fecundity. We provide arguments to explain the lack of JH-mediated trade-offs in the house cricket.     

Evolution and physiological consequences of de-alation in crickets

Wing shedding or de-alation is a common phenomenon among crickets. Its significance and effects on other traits were examined based on the results from experiments using artifical or natural de-alation. Artificial de-alation at adult emergence induces rapid egg production and flight muscle histolysis in several species examined. However, natural de-alation does not always shorten the pre-ovipositional period because it does not occur immediately after adult emergence and because oviposition starts before de-alation. In some cases, naturally de-alated females produce more eggs than to intact females during early adult life, but peak ovipositing activity occurs before de-alation. Therefore, retention of the hindwings does not suppress high ovipositing activity in such cases. It appears that de-alation is a result rather than a causal factor in ending migration. Ovarian development and flight muscle histolysis, which can be stimulated by de-alation, are controlled by the jevenile hormone, but the mechanism inducing de-alation remains unknown. The possible factors leading to the evolution of de-alation are discussed.     

Variation in singing behaviour among morphs of the sand field cricket,Gryllus firmus

1. Trade‐offs play a fundamental role in the evolution of many traits. 2. In wing‐polymorphic field crickets, the long‐winged morph can disperse from unfavourable environments, but has lower reproductive success than the short‐winged morph, because of costs associated with flight capability. 3. However, long‐winged individuals may minimise costs in favourable environments by histolysing their flight muscles and becoming flightless. 4. Few studies have examined how flight‐muscle histolysis affects male signalling and mate attraction. 5. We examined differences in singing activity and song characteristics among the flightless (short‐winged and histolysed long‐winged) and the flight‐capable male morphs, and female preferences for male song, in the sand field cricket. 6. We found: (i) both flightless morphs sang more than the flight‐capable morph, (ii) song characteristics varied among the three morphs, and (iii) females preferred songs characteristic of the long‐winged morphs. 7. Histolysis should increase mating success of long‐winged males because it increases singing activity. 8. Histolysed long‐winged males may have higher mating success than short‐winged males as they sing as frequently but produce more attractive songs. 9. Therefore, plasticity within the long‐winged morph may reduce costs of maturing in environments from which dispersal is not advantageous; non‐flying morphs may be pursuing different reproductive tactics.     

Hormonal control of reproduction and reproductive behavior in crickets

In Orthoptera, the endocrine control of reproduction has been investigated mainly in Acrididae. Gryllidae are also good models for the study of hormonal control of reproduction and reproductive behavior. In this review, special attention will be focused on the house cricket, Acheta domesticus. In the house cricket, vitellogenesis is controlled according to the classical model described for most insect orders. However, whereas allatectomy completely abolished oocyte growth in A. domesticus, it did not totally suppress ovarian development and egg-laying in Teleogryllus commodus, Gryllus bimaculatus, and G. campestris. In the Gryllidae studied thus far, juvenile hormone (JH) is not needed for mating behavior. In adult A. domesticus, the expression of oviposition movement, although independent of the presence of the ovaries, is strictly controlled by JH III. Recent findings suggest hormonal actions on the central nervous system of the house cricket, and provide a stimulating basis for further research on the respective involvement of hormones and nervous system in the control of reproductive behavior in adult crickets. Arch. Insect Biochem. Physiol. 35:393–404, 1997. © 1997 Wiley-Liss, Inc.     

Effect of ecdysterone and juvenoid on the developmental involution of flight muscles in Acheta domestica

Morphogenesis and degeneration of the flight muscles in Acheta domestica was studied. The dorso-longitudinal flight muscles (DLMs) degenerate during the fourth day after adult ecdysis and the dorso-ventral flight muscles (DVMs) on the fifteenth day. In the presence of an intact innervation the degeneration of the DLMs can be retarded for 2 days by the injection of ecdysterone into very young adults. This retardation may also result in hypertrophy of the muscle fibres. The injection of ecdysterone, even in high doses, did not affect the flight muscle remnants. No notable changes have been found in the degeneration of DLMs by ovarectomy. Thus, the degeneration of flight muscles and the development of ovaries appear to be independent processes.The DLMs are homogeneous in fibre pattern in respect to succinic dehydrogenase, an important oxidative enzyme, and to ATPase activity, but the muscle fibres do not show any phosphorylase activity.     

Effects of suppressed oviposition activity and flight muscle histolysis on food consumption and ovarian development in a wing-dimorphic cricket: an explanation for sporadic conclusions related to physiological trade-offs

The effects of deprivation of oviposition substrate on food consumption and egg production were compared between the long-winged (LW) and the short-winged (SW) morph of a cricket, Modicogryllus confirmatus, to determine how suppressed oviposition activity would influence these traits in each wing morph. Food consumption was greatly suppressed in females deprived of oviposition substrate (-OS) compared to those given access to it (+OS) during the 2-week feeding trial in the SW morph but not in the LW morph. Some LW females shed their hindwings and histolyzed the flight muscles. Such de-alated LW (DLW) morphs tended to consume more food than intact LW (ILW) morphs. In all morphs, ovarian weight was heavier under -OS conditions than under +OS conditions during the second week of adulthood, although the differences were greater in SW morphs than in ILW morphs. In DLW morphs in which flight muscle histolysis was induced by artificial de-alation at adult emergence, the temporal changes in ovarian weight were similar to those of SW morphs.In SW morphs, food consumption was also significantly reduced when ovipositing females were deprived of oviposition substrate for 2 days compared to those allowed to oviposit continuously, but food consumption was not reduced in ILW or DLW morphs. SW females from which one ovary was extirpated at adult emergence, SW (-o), also showed a significant difference in food consumption when treated as above, indicating that food consumption was not determined simply by the number of ovarian eggs. The crop content was positively correlated to food consumption and smaller under -OS conditions than under +OS conditions. The 2-day deprivation of oviposition substrate caused no significant difference in the total number of deposited and ovarian eggs in any group, but the ovarian mass of developing oocytes tended to be smaller under -OS than under +OS conditions, particularly in SW morphs.These results indicate the possibility that some inconsistent results and conclusions discussed in recent studies, concerning the physiological trade-offs between flight capability and reproduction, were caused by the suppressed oviposition activity and failure to recognize the occurrence of flight muscle growth and histolysis in the test crickets.     

Coevolution of traits determining migratory tendency: correlated response of a critical enzyme,juvenile hormone esterase,to selection on wing morphology

Migratory tendency in insects is a complex trait, composed of a suite of correlated behavioural, physiological, morphological and life history traits. We investigate the genetic and physiological basis of the coevolution of this suite of traits using laboratory lines of the wing dimorphic cricket, Gryllus firmus, selected for increasing and decreasing incidence of macroptery. Selection on wing morphology has produced strong direct responses in proportion macropterous as well as correlated (indirect) responses in wing muscle histolysis, flight propensity and fecundity. We investigate the hypothesis that these responses have been mediated by changes in the metabolism of juvenile hormone (JH) during the final nymphal stadium (the critical period for wing morph determination). Previous studies of Gryllus sp. have established that JH titre in this period is determined primarily by the activity of the degradative enzyme, juvenile hormone esterase (JHE). Assays of JHE activity in the final nymphal stadium of the replicated control and selected lines demonstrate highly significant differences in both mean activity and the probability of macroptery for a given level of activity (i.e., the threshold activity required to induce wing formation). These correlated responses in JH metabolism support the general hypothesis that the correlations among traits determining migratory tendency result at least in part from the common influence of JH during the final nymphal stadium. We discuss these results in the context of the quantitative genetic model for the evolution of polygenic, dichotomous traits (the threshold model), and present four general predictions concerning the coevolution of traits associated with ecological (i.e., trophic, life history, behavioural) dimorphisms.     

Recombinant juvenile hormone esterase as a biochemical anti-juvenile hormone agent: Effects on ovarian development in Acheta domesticus

By investigating the effects of recombinant juvenile hormone esterase (JHE) on the stimulation of ovarian development and egg laying in the house cricket Acheta domesticus L., we have tested the hypothesis that recombinant JHE (derived from the tobacco budworm Heliothis virescens) can be used as a biochemical anti-juvenile hormone (JH) agent. Recombinant JHE, produced by a genetically engineered baculovirus, was affinity-purified and injected into females of A. domesticus. JHE was cleared rapidly from the hemolymph of the crickets. However, upon repeated injection, significant reductions were seen in the extent of development of the ovaries and in the numbers of eggs laid. The effects of JHE could be rescued by topical application of the JHE inhibitor, OTFP. Thus, we have demonstrated an anti-JH effect on reproduction and that the recombinant JHE derived from a lepidopteran is active in an orthopteran insect. Arch. Insect Biochem. Physiol. 34:359–368, 1997. © 1997 Wiley-Liss, Inc.     

Juvenile Hormone and host-plant colonization by the black bean aphid, Aphis fabae

Abstract Host-plant colonization by winged, summer forms of Aphis fabae Scop, involves the resumption of embryogenesis and larviposition, leading eventually to flight muscle degeneration. Topical application of Juvenile Hormone I to young adults which (a) had access to the host plant, (b) were starved, (c) were starved and treated with precocene III, or (d) were decapitated shortly after the final ecdysis suggests that embryogenesis and flight muscle histolysis may be stimulated by an increase in Juvenile Hormone titres after settling. The duration of the pre-reproductive period and the initial reproductive rate were not significantly affected, possibly because other neuroendocrine factors are involved in parturition.     

The role of feeding,mating and ovariectomy on degeneration of indirect flight muscles of Dysdercus cingulatus (Heteroptera: Pyrrhocoridae)

Degeneration of indirect flight muscles takes place during the first gonotrophic cycle in females. Feeding and mating stimulate egg production and muscle histolysis. Starved virgin females do not histolyse the flight muscles. Mating has greater effect on muscle degeneration than feeding. Ovariectomy inhibits degeneration to a certain extent.     

The role of juvenile hormone and juvenile hormone esterase in wing morph determination in Modicogryllus confirmatus

The role of juvenile hormone (JH) and juvenile hormone esterase (JHE) in regulating wing morph determination was studied in the cricket Modicogryllus confirmatus. JHE activities were significantly higher in nascent long-winged (LW) vs short-winged (SW) crickets during the latter half but not during the first half of the last stadium. The magnitude and direction of the activity differences were similar to those previously documented between wing morphs of the cricket, Gryllus rubens. In contrast, activities of general esterase, an enzyme or group of enzymes with no demonstrated role in regulating the JH titer in insects, showed no or only minor differences between morphs. The magnitude and direction of the JHE activity variation is consistent with a regulatory role for this enzyme in some aspect of wing dimorphism. However, the timing of the differences (exclusively during the last half of the last stadium) argue against a role in regulating wing length development per se. Single or multiple applications of juvenile hormone-III to nascent LW individuals during the first few days of the last stadium significantly redirected development from long to short wings. Multiple applications of acetone, by itself, also increased the production of short-winged adults. For most treatments, all individuals with shortened wings also had undeveloped flight muscles. These data suggest that JH may play a role in wing morph determination in M. confirmatus but that it affects a different aspect of the polymorphism from JHE.     

Coordination between the electrical activity of developing indirect flight muscles and the firing activity of a population of neurosecretory cells in the silkmoth, Bombyx mori

The developing indirect flight muscles of pharate moths are characterized by a rhythmic discharge of a long bout of flight-pattern-like muscle potentials in the absence of contractions. The electrical activity of the dorsal longitudinal flight muscles (DLMs) in the silkmoth, Bombyx mori, was discernible as a cluster of many series of muscle potentials that last for several minutes on day 4 of the pupal period. The duration of the active phases and the period of rhythmic activity gradually increased to a peak value on day 7 or 8 and then declined until the end of the pupal period. Mean duration of the active phases (+/-SD) and the mean period of the rhythmic activity (+/-SD) at the peak were 38.7+/-8.7 min and 74.5+/-7.3 min, respectively. The rhythmic electrical activity of immature DLMs was closely coordinated with the rhythmic (bursting) activity of a population of neurosecretory cells that are known to produce pheromone-biosynthesis activating neuropeptide (PBAN) and its related peptides, which belong to the multifunctional peptide family, pyrokinin/PBAN. The DLMs always became active a few minutes after the neurosecretory cells, and the timing of onset of these two activities appeared to be strictly regulated by a neural mechanism. The implication of the coordinated activity for development and maturation of imaginal tissues, including the flight motor system, and possible functions of the neuropeptides in this development are discussed.     

Gecko phonotaxis to cricket calling song: A case of satellite predation

Insectivorous Mediterranean house geckos, Hemidactylus tursicus, are found in the field close to the burrows of calling male decorated crickets, Gryllodes supplicans. In playback experiments where adult geckos were presented with calls of these crickets or calls of frogs as controls, geckos exhibited positive phonotaxis to broadcast cricket calling song. This indicates that geckos orient to and approach male cricket calls, even though the crickets call from burrows where they are protected from the geckos. However, this behaviour enables the geckos to intercept and consume female crickets that also respond phonotactically to the cricket calls. Thus geckos act as ‘satellite predators’, a situation which may impose sex-biased mortality on female crickets.     

Purification, characterisation and titre of the haemolymph juvenile hormone binding proteins from Schistocerca gregaria and Gryllus bimaculatus

Juvenile hormone binding proteins (JHBPs) were extracted from the haemolymph of adult desert locusts, Schistocerca gregaria, and Mediterranean field crickets, Gryllus bimaculatus. The JHBPs were purified by polyethyleneglycol precipitation, filtration through molecular weight cut off filters and chromatography on a HiTrap heparin column. The juvenile hormone (JH) binding activity of the extracts was measured using a hydroxyapatite assay and the purification progress was monitored by native gel chromatography and sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE). The haemolymph JHBPs of both insects are hexamers composed of seemingly identical subunits. The JHBP of the locust has a native Mr of 480 kDa with subunits of 77 kDa, whereas the JHBP of the cricket has a Mr of 510 kDa with subunits of 81 kDa. The locust JHBP binds JH III with moderate affinity (KD = 19 nM). Competition for binding of JH II and JH I was about 2 and 5 times less, respectively. The cricket JHBP also has a moderate affinity for JH III (KD = 28 nM), but surprisingly, competition for binding of JH II was equal to that of JH III and JH I competed about 3 times higher. No sequence information was obtained for the locust JHBP, but the N-terminal sequence of the cricket JHBP shows ca. 56% sequence homology with a hexamerin from Calliphora vicina. Antisera raised against the purified JHBPs were used to measure age- and sex-dependent changes in haemolymph JHBP titres and to confirm that the JHBPs of both species are immunologically different.     

METHOPRENE INFLUENCES REPRODUCTION AND FLIGHT CAPACITY IN ADULTS OF THE RICE LEAF ROLLER,Cnaphalocrocis Medinalis (GUENỂE) (LEPIDOPTERA: PYRALIDAE)

Juvenile hormone (JH) influences many aspects of insect biology, including oogenesis‐flight syndrome tradeoffs between migration and reproduction. Drawing on studies of many migratory insects, we posed the hypothesis that JH influences migratory capacity and oogenesis in the rice leaf roller, Cnaphalocrocis medinalis. We treated adults moths (days 1, 2 and 3 postemergence) with the JH analog (JHA), methoprene, and then recorded the influences of JHA treatments on reproduction. JHA treatment on day 1 postemergence, but not on the other days, shortened the preoviposition period, although JHA did not influence total fecundity, oviposition period, or longevity. We infer day 1 postemergence is the JH‐sensitive stage to influence reproduction. Therefore, we treated moths on day 1 postemergence with JHA and recorded flight capacity, flight muscle mass, and triacylglycerol (TAG) accumulation. JHA treatments did not influence flight speed, but led to reductions in flight durations and flight distances. At day 3 posttreatment (PT), JHA‐treated females flew shorter times and less distance than the controls; JHA‐treated males, however, only flew shorter times than the controls. JHA treatments led to reductions in flight muscle mass in females at days 2–3 PT and reductions in TAG content in females at day 3 PT, but, these parameters were not influenced by JHA in males. These findings strongly support our hypothesis, from which we infer that JH is a major driver in C. medinalis oogenesis‐flight syndrome tradeoffs. Our data also reveal a JH‐sensitive stage in adulthood during which JH influences the oocyte‐flight syndrome in C. medinalis.     

Juvenile hormone regulation on the flight capability of Bactrocera dorsalis (Diptera: Tephritidae)

The oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), is considered a major economic threat in many regions worldwide. In order to better understand the flight capacity of B. dorsalis and its physiological basis, the functions and regulatory roles of juvenile hormone (JH) in the flight muscle of B. dorsalis were studied under a controlled environment. JH titer of B. dorsalis varied with age and sex. Females have higher JH titers and better flight capabilities than males, given that the increase in JH also corresponded to the ovarian development and maturation in females. The flight duration and distance of both males and females increased with the gradual increase of JH titer after adult emergences. Both JH titer and flight capability peaked in 15-d-old adult and declined subsequently with age. Flight activity stimulated the production of JH as adults flown for 24 h on the flight mills have the highest JH titers compare to adults flown on shorter flight durations. Adults treated with 0.5 µg and 5 µg of JH III were able to fly long durations and long distances, nevertheless when JH titer was too low or too high, it would restrict the flight ability of the fly. The mutual reinforcement of JH and flight activity provides fundamental understanding on the physiological aspects of the flight capability and dispersal, which facilitates strategies for the long-term control of this destructive pest.