Reproductive cost of flight capability: a comparison of life history traits in wing dimorphic planthoppers

Abstract. 1. Reproductive costs associated with flight capability were evaluated in the wing dimorphic planthopper, Prokelisia dolus Wilson, by comparing the life history of traits of winged (macropterous) and flightless (brachypterous) females under controlled laboratory conditions.
2. Macropters with large thoraces and fully developed wings maintain a greater investment in flight apparatus than brachypters with small thoraces and reduced wings.
3. Associated with greater flight capability in the macropter of P.dolus are shorter adult life, decreased total fecundity, and delayed age at first reproduction compared to brachypterous females.
4. Under field conditions where mortality is high, the difference in realized fecundity between the two wing forms living on similar resources is further exaggerated with the brachypter having the greater advantage.
5. When the life history traits of the wing forms of P. dolus are compared with traits for nine other species of planthoppers, two similarities emerge. First, the preoviposition period of the macropterous wing form is always longer than that for the brachypter resulting in a reproductive delay. Second, most studies show that macropters are less fecund than brachypters.
6. There is no general tendency among planthopper species for macropterous adults to live fewer days or develop more slowly as nymphs compared to their flightless counterparts.
7. The reproductive delay and reduced fecundity of the volent wing form of planthoppers supports the notion that flight capability is costly and that phenotypic trade-offs between flight and reproduction exist.     

Differences in haemolymph proteins in relation to diapause and wing dimorphism inPyrrhocoris apterus (L.) (Heteroptera: Pyrrhocoridae)

Three different cultures of dimorphic bug,Pyrrhocoris apterus, were analyzed concerning diapause and its relation to wing morph pattern. The proportion of macropterous bugs was considerably higher (36%) in the Mediterranean culture from Israel than that (1.3%) in the temperate culture from the Czech Republic. The macropterous morph- and brachypterous morphrelated types of reproduction arrest, differing by the length of pre-oviposition period, were distinguished in cultures analyzed. The reproduction arrest with an average pre-oviposition period of 38.2 days in Mediterranean macropters and 18.5 days in macropters from selected macropterous strain, was found to be typical for macropterous morph. Two different photoperiodic conditions induced macropterous morph-related reproduction arrest, the long-day (18 h light-6 h dark) photoperiod in macropterous strain macropters and the short-day (12 h light-12 h dark) photoperiod in Mediterranean macropters. The brachypterous morph-related reproduction arrest, characterized by pre-oviposition period longer than 90 days, occurred predominantly in diapausing brachypterous bugs. While the hibernal diapause of brachypterous bugs was characterized by a very high level of the 78- and 82-kDa proteins in haemolymph, their content in haemolymph of macropters during macropterous morph-related reproduction arrest was almost as low as in the reproductive adults. The variation of reproduction arrest in relation to wing dimorphism represents an important feature in the life strategy ofP. apterus.     

THE EVOLUTION OF WING DIMORPHISM IN INSECTS

Wing-dimorphic insects are excellent subjects for a study of the evolution of dispersal since the nondispersing brachypterous morph is easily recognized. The purpose of this paper is to develop a framework within which the evolution of wing dimorphism can be understood. A review of the literature indicates that the presence or absence of wings may be controlled by a single locus, two-allele genetic system or a polygenic system. Both types of inheritance can be subsumed within a general threshold model. An increase in the frequency of a brachypterous morph in a population may result from an increased relative fitness of this morph or the emigration of the macropterous type. The abundance of wing-polymorphic species argues for an increased fitness of the brachypterous form. An analysis of the life-history characteristics of 22 species of insects indicates that the brachypterous morph is both more fecund and reproduces earlier that the macropterous morph. Unfortunately, data on males are generally lacking. It is suggested that suppression of wing production results when some hormone, perhaps juvenile hormone, exceeds a threshold value during a critical stage of development. Further, it is known that in the monomorphically winged species Oncopeltus fasciatus both flight and oviposition are regulated by the titer of juvenile hormone. These observations are used to construct a possible pathway for the evolution of wing dimorphism. This suggests that evolution to a dimorphic species requires both an increase in the rate of production of the wing suppressing hormone and a change in the threshold level at which wing and wing-muscle production are suppressed. The stage in this evolutionary sequence that an organism will reach depends on the stability of the habitat.     

Locomotor activity in adult Pyrrhocoris apterus (Heteroptera) in relation to sex, physiological status and wing dimorphism

The pattern of locomotor (walking) activity was studied in adult males and females of short‐winged (brachypterous) and long‐winged (macropterous) morph of the flightless bug Pyrrhocoris apterus (Linnaeus) (Heteroptera: Pyrrhocoridae) under constant laboratory conditions. Walking activity was measured with a computerized video system and analysed with respect to sex, physiological status (reproduction, diapause and reproductive arrest of non‐diapause type) and wing dimorphism of the bugs. The largest duration was observed in the macropterous females with reproductive arrest of non‐diapause type (average 6 h per day) and the shortest duration in diapausing brachypterous females and males (average less than 2 h per day). This was reflected also in the overall time spent by walking during the first 14 days after imaginal ecdysis. The time spent by walking significantly increased in the macropterous morph as the bugs aged, whereas in diapausing brachypters the time spent by walking decreased with age. No linear relationship between walking activity and age was found in reproductive brachypterous morph. The bugs of all experimental groups moved mostly during the photophase and were almost inactive during the scotophase. Thus, walking activity in P. apterus is diurnal, irrespective of the wing morph, physiological status, sex and age. Contrary to the macropterous morph, where the locomotor activity of females during photophase was significantly higher than in males, no significant differences were found between the locomotor activities of brachypterous males and females. The observed differences in locomotor activity are discussed in relation to different roles of two wing morphs in the life history of this heteropteran.     

稻飞虱翅型纯系后代个体的翅型分化对光周期变化不敏感

【目的】为了明确光周期和遗传因子在稻飞虱翅型分化中的作用, 研究了3种稻飞虱（褐飞虱Nilaparvata lugens、白背飞虱Sogatella furcifera和灰飞虱Laodelphax striatellus）翅型纯系或近纯系在不同光照时数下的翅型分化比率。【方法】以经过5~45代连续翅型筛选后的褐飞虱、白背飞虱和灰飞虱的长翅型和短翅型纯系或近纯系为材料, 在室内分别测定了其在长光照（16和20 h）、短光照(4~12 h)和正常光照(14 h) 3类光周期条件下饲养后, 雌、雄成虫中长翅和短翅个体出现的比率及存活率。【结果】白背飞虱和灰飞虱的长翅型纯系M♂×M♀或短翅型纯系B♂×B♀在不同光周期下的翅型比率均无显著差异（P>0.05）。褐飞虱短翅型近纯系B♂×B♀的雌虫短翅率和成虫总短翅率在不同光周期下也无显著差异（P>0.05）, 但雄虫短翅率在正常光照14 h和短光照4 h下显著高于长光照20 h下的（P<0.05）。当褐飞虱短翅型达到纯系后, 其后代翅型在6~16 h光照条件下无显著差异。褐飞虱长翅型近纯系M♂×M♀的后代虽有短翅个体出现, 但是雌虫和雄虫的各自短翅率在不同光周期下无显著差异（P>0.05), 仅总体短翅率在12 h光照条件下的显著高于16 h下的（P<0.05）。褐飞虱长、短翅型杂交筛选品系M♂×B♀的雌虫短翅率随光照时数的延长而升高; 灰飞虱杂交筛选品系M♂×B♀的短翅雄虫随光照时数的缩短而增多（P<0.05）, 但当筛选代次达到45代时, 这种趋势不再显著。3种稻飞虱长翅型和短翅型纯系或近纯系若虫的存活率会稍低于长、短翅型杂交后代的存活率, 但长、短翅型品系的存活率在6~16 h光照条件下差异不显著(P>0.05)。【结论】稻飞虱翅型分化对光周期的反应受飞虱本身遗传背景的影响, 翅型纯系后代个体的翅型分化对光周期变化不敏感。     

Developmental and diel changes of adipokinetic hormone in CNS and haemolymph of the flightless wing-polymorphic bug,Pyrrhocoris apterus (L.)

We have used an enzyme-linked immunoassay (ELISA) for determination of the AKH content in CNS (brain + corpora cardiaca + corpora allata) and haemolymph of adult macropterous and brachypterous females of the bug Pyrrhocoris apterus. The tests revealed that the AKH content fluctuates between 1 and almost 4 pmol/CNS during the first 14 days of adult life and significantly increased in order diapausing brachypters相似文献   

Wing structure and polymorphism in minute scavenger beetles (Coleoptera,Latridiidae)

The main structural elements of the hind wing in 56 species of the family Latridiidae (Coleoptera) are analyzed. In macropterous forms, wing venation is reduced to 3 modified veins. 10 areas of sclerotization of the wing membrane are distinguished. Three forms with different degrees of wing reduction are revealed: the brachypterous, the micropterous, and the apterous form. Among 56 species examined, 40 are represented only by the macropterous form; 2, 3, 5, and 6 species, by macropterous and brachypterous, macropterous and micropterous, micropterous, and apterous forms, respectively.     

Flight muscles polymorphism in a flightless bug, Pyrrhocoris apterus (L.): developmental pattern, biochemical profile and endocrine control

The flightless bug Pyrrhocoris apterus (L.) is polymorphic for both wing length and flight muscle development. The developed flight muscles of macropterous adults of both sexes first enlarge their volume during the first 5 days after adult emergence, but are then histolyzed in all males and females older than 10 and 14 days, respectively. The flight muscles of brachypterous adult males and females are underdeveloped due to their arrested growth. The total protein content of histolyzed dorsolongitudinal flight muscles from 21-day-old macropterous adults of both sexes is lower than that of developed dorsolongitudinal flight muscles in 5-10-days-old macropterous bugs, but substantially higher than the protein content of underdeveloped dorsolongitudinal flight muscles from adult brachypters. Histolyzed dorsolongitudinal flight muscles differ from the developed ones by decreased quantities of 18 electrophoretically separated proteins. Histolysis of developed dorsolongitudinal flight muscles is accompanied by significant decreases in citrate synthase, glyceraldehyde-3-phosphate dehydrogenase and β-hydroxyacyl-CoA dehydrogenase enzyme activities and an increase in alanine aminotransferase activity, and can be precociously induced by application of a juvenile hormone analogue. This is the first report of flight muscle polymorphism, histolysis of developed flight muscles and its endocrine control in insects displaying non-functional wing polymorphism.     

Molecular characterization of the flightin gene in the wing-dimorphic planthopper,Nilaparvata lugens,and its evolution in Pancrustacea

Flightin was initially identified in Drosophila melanogaster. Previous work has shown that Drosophila flightin plays a key role in indirect flight muscle (IFM) function and has limited expression in the IFM. In this study, we demonstrated that flightin is conserved across the Pancrustacea species, including winged insects, non-winged insects, non-insect hexapods and several crustaceans. The brown planthopper (BPH), Nilaparvata lugens (Stål) (Hemiptera: Delphacidae), a long-distance migration insect with wing dimorphism, is the most destructive rice pest in Asia. We showed that flightin was one of the most differentially expressed genes in macropterous and brachypterous BPH adults. In female BPHs, flightin was expressed in the IFM of macropterous adults, no expression was detected in brachypterous ones; while in male BPHs, flightin was not only expressed in the IFM of macropterous adults, but also in the dorsal longitudinal muscle (DLM) in the basal two abdominal segments of both macropterous and brachypterous ones. RNAi and transmission electron microscopy results showed that flightin played key roles in maintaining IFM and male DLM structure, which drive wing movements in macropterous adults and the vibration of the male-specific tymbal, respectively. Using Daphnia magna as an example of a crustacean species, we observed that flightin was expressed in juvenile instars and adults, and was localized in the antenna muscles. These results illustrate the functional variations of flightin in insects and other arthropod species and provide clues as to how insects with flight apparatuses evolved from ancient pancrustaceans.     

Sublethal effects of abamectin on the development,fecundity, and wing morphs of the brown planthopper Nilaparvata lugens

The brown planthopper Nilaparvata lugens negatively affects rice yield by sucking nutrients from the rice stem and spreading viruses. In this study, the effects of sublethal concentrations of abamectin on development, fecundity, and wing morphs of N. lugens were investigated. Treatment with sublethal concentrations of abamectin showed no significant effects on the developmental period of F₀ nymphs. Although LC₁₀ and LC₂₅ treatments resulted in 10% and 25% mortality, the LC₂₅ treatment significantly prolonged the lifespan of macropterous and brachypterous females. Abamectin-treated brachypterous females showed significantly lower fecundity than control females. Furthermore, abamectin treatment showed no significant effects on the developmental period of F₁ nymphs. However, LC₂₅ treatment significantly inhibited the fecundity of brachypterous F₁ females and significantly reduced the proportion of macropterous F₁ females and brachypterous F₁ males. LC₂₅ treatment showed no significant effects on the fecundity of macropterous F₁ females. Considering the proportion of macropterous and brachypterous F₁ females, the relative fitness of the macropterous F₁ nymphs in the control, LC₁₀, and LC₂₅ treatment groups was 1, 1.02, and 0.84, respectively, and that of brachypterous F₁ nymphs was 1, 0.79, and 0.93, respectively. Sublethal concentrations of abamectin inhibited N. lugens emergence. The present findings indicate the potential of abamectin for N. lugens field control.     

Alata-production by an aphid: The “interval timer” concept and maternal age effects

Throughout their lives alate Acyrthosiphon pisum aphids remained unable to produce more alatae in response to crowding. Similarly, the first-born progeny of most alatae were likewise unable to respond to crowding. In contrast, the first-born progeny of apterae responded exceptionally strongly to the crowding stimulus. Later-born progeny of both morphs responded similarly. These data are inconsistent with Lees' theory of “interval timers” since ability to produce alatae did not return simultaneously in all lines founded by alatae. The theory of interval timers must be either replaced or modified to take into account differences related to maternal age.     

Differential allocation of protein resources to flight muscles and reproductive organs in the flightless wing-polymorphic bug, <Emphasis Type="Italic">Pyrrhocoris apterus</Emphasis> (L.) (Heteroptera)

Differences in the growth of dorsolongitudinal flight muscles and gonads in 1–28 days old long-winged (macropterous) and short-winged (brachypterous) adults of the firebug (Pyrrhocoris apterus L.) and the resource allocation to these organs were studied by means of total protein analysis. We found predominant allocation of food resources to flight muscles compared to reproductive organs in both macropterous males and females during the first 5 days of adult life. Subsequent histolysis of developed flight muscles coincided with increased total protein content in some reproductive organs. Initiation of intensive food intake after starvation or application of higher dose of methoprene on macropterous adults changed the resource allocation in favour of growth of reproductive organs and induced precocious histolysis of flight muscles. It indicates an involvement of juvenile hormone in wing morph-related differential allocation of resources in the bug. Increased total protein contents in the ovaries and accessory glands of starved macropterous females and males treated with methoprene, respectively, indicate that proteins derived from the methoprene-induced histolysis of the flight muscles are re-utilized for the growth of the reproductive organs. It is the first report of persistence of differential resource allocation to flight muscles and reproductive organs in the wing-polymorphic insects with non-functional macropterism.     

Wing morph-specific differences in the metabolism and endocrine control of reserve mobilization in adult males of a flightless bug, <Emphasis Type="Italic">Pyrrhocoris apterus</Emphasis> (L.) (Heteroptera)

The differences in the metabolism and endocrine control of reserve mobilization in long-winged (macropterous) and short-winged (brachypterous) males of a flightless firebug (Pyrrhocoris apterus) were studied. We found that protein content in the gut was significantly lower in 5–10 day-old macropterous males due to their fasting and higher in 28 day-old ones than in the same aged brachypterous counterparts as the result of renewed food intake. Overall protease activity was significantly lower in 10–14 day-old macropters, while an abrupt increase in the activity starting on day 21 after adult ecdysis was also associated with renewal of the food intake. The levels of carbohydrates in haemolymph were only slightly lower in 1–10 day-old macropterous males than in the same aged brachypters. However, more than twofold higher lipid content in haemolymph of 7–10 day-old macropterous males than in the same aged brachypterous males was found. Higher mobilization of lipid reserves from the fat bodies in macropterous males was accompanied by more intensive adipokinetic response and higher levels of adipokinetic hormone in the body. It is the first report of endocrine regulation of wing morph-related differences in the lipid mobilization in males of wing-polymorphic insects.     

Fecundity of brachypterous and macropterous alatae in Drepanosiphum dixoni (Callaphididae, Aphididae)

In Drepanosiphum dixoni H. R. L. the heavier the adult the greater the fecundity. However, brachypterous alatae are more fecund than macropterous alatae in the first 10 days of adult life as well as in the first 10 days of reproductive life. There is no difference in the weight at birth between the offspring of brachypterous and macropterous alatae.

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Résumé Les ailés brachyptères et les ailés macroptères de Drepanosiphum dixoni sont très semblables dans leurs structures. Les brachyptères sont dépourvus des muscles indirects du vol et leurs ailes, quoique de forme parfaite, sont plus courtes que celles des ailés macroptères.La fécondité est d'autant plus grande que l'insecte adulte est plus lourd. Cependant, les ailés brachyptères sont plus féconds que les ailés macroptères aussi bien pendant les 10 premiers jours de leur vie adulte (Fig. 1A) que pendant les 10 premiers jours de leur reproduction (Fig. 1B). La différence de fécondité est plus marquée quand on se réfère aux 10 premiers jours de la vie adulte, (comparer Fig. 1, A et B), car le délai entre la mue imaginale et le début de la reproduction est plus court chez les brachyptères (2, 4 jours) que chez les macroptères (3, 3 jours).On n'observe pas de différences dans le poids à la naissance de la descendance de chacune des 2 formes.Dans l'évolution de l'aptérisme chez les Aphides il est vraisemblable que l'avantage initial réside dans un accroissement de fécondité, comme chez D. dixoni. Un développement secondaire possible dans l'évolution du dimorphisme alaire chez les Aphides est celui observé chez A. fabae où les ailés produisent une plus petite descendance, la proportion de celle-ci qui naît dans les quelques premiers jours de la vie adulte étant plus élevée que chez les formes aptères.

     

高温对稻褐飞虱发育与生殖的影响

通过高温处理及交配产卵实验,探讨了高温对稻褐飞虱Nilaparvata lugens (Stal)发育与生殖的影响。研究了不同高温条件对褐飞虱若虫发育历期、产卵量、产卵前期、寿命等生物学特性的影响。34℃以上高温导致褐飞虱若虫发育历期延长。高温处理4龄若虫使羽化后的雌成虫产卵量减少。高温处理不同日龄雌成虫也致使其产卵量减少,其中以1日龄短翅型、3日龄长翅型的产卵量影响最大。高温处理后褐飞虱寿命缩短。高温恒温处理,对短翅型雌成虫的产卵前期影响不大,但能延长长翅型雌成虫的产卵前期;而高温变温处理致使短、长翅型雌成虫的产卵前期均延长。高温变温对褐飞虱生殖的影响程度大于高温恒温。高温处理组雌、雄成虫与对照组相应的成虫交配试验表明,高温对雌性的影响大于雄性。实验初步确定34℃为对褐飞虱发育与生殖产生影响的临界温度。     

Temporal pattern of feeding activity in the firebug Pyrrhocoris apterus and its relation to sex, wing dimorphism and physiological state of adults

Abstract.  The present study tested whether the pattern of feeding activity in the firebug Pyrrhocoris apterus (L.) is sex- and wing morph-related, diurnal or nocturnal, as well as whether the feeding rhythm persists in constant darkness. Temporal patterns of feeding activity are analysed in macropterous and brachypterous adults reared under long-day (LD 18 : 6 h) and short-day (LD 12 : 12 h) photoperiods, and in adults transferred to constant darkness. In females, the total feeding activity is highest in long-day reproductively active brachypters, intermediate in short-day diapausing brachypters, and lowest in macropters; the differences among males are substantially smaller. Although the total feeding activity of macropterous males is higher than in macropterous females, no sex-related differences are found in feeding activity of diapausing and reproductively active brachypters. The frequency of feeding exhibits sex-related differences, with obviously higher values in males. Mean feeding periods of macropterous and reproductively active brachypterous males are shorter than in females of the same wing morph. Mean interfeeding periods are longest in macropters, intermediate in diapausing brachypters, and shortest in reproductively active brachypters, and always lower in males than in females. The study shows that the feeding activity of P. apterus adults is age-, sex- and wing morph-related, and exhibits a diurnal pattern, except in reproductively active brachypterous females. The latter do not express a clear diurnal rhythm of feeding, presumably because of interactions with cycles of egg development and oviposition. The persistence of diurnal rhythm of feeding activity in short-day brachypterous females transferred to constant darkness indicates an endogeneity of this rhythm in P. apterus .     

Precocene II-induced alate production in isolated and crowded alate and apterous virginoparae of the aphid, Macrosiphum euphorbiae

Precocene II was applied at doses ranging from 0.05 to 0.70 μg per individual to newly moulted adult alate and apterous virginoparae of Macrosiphum euphorbiae kept isolated or in groups of 10 per plant, under an 18L:6D photoperiodic regime. While isolated controls of both morphs produced exclusively apterous progeny, alatae virginoparae were produced in generally dose-dependent proportions by precocene-treated individuals. Grouped controls of both morphs produced alatiform progeny as expected, but in precocene—treated groups, the proportions of alate progeny generally increased as a function of dose. The overall proportions of alate offspring produced, and numbers of days after treatment when morph production was affected, were generally greater for alatae than for apterae, indicating a greater sensitivity to precocene in alatae. However during the first few days after treatment, the alatizing effect of precocene was stronger for apterae, suggesting that the first embryos produced by alatae were irreversibly determined as apterae.In an experiment where isolated alatae and apterae received 0.5 μg of precocene II at different ages ranging from 1 to 13 days after the adult moult, the alatizing effect of the compound, measured by the persistence of alate production, varied with age and morph. While in alatae, the persistence decreased more or less regularly with age, in apterae it initially increased to a maximum in the middle of reproductive life, and subsequently decreased. The results provide support for the hypothesis that juvenile hormone is involved in regulating alary dimorphism in M. euphorbiae.     

Agamermis unka (Mermithidae) Parasitism of Nilaparvata lugens in Rice Fields in Korea

The mermithid Agamermis unka, a parasite of the brown planthopper (BPH), was found in many rice paddies in Gyeongnam Province, Korea. Nematode parasitism of adult BPH varied from year to year, reaching as high as 50% in paddies not treated with an insecticide. Parasitism was lower in insecticide-treated paddies. Generally, mermithid parasitism was higher in BPH adults collected from the lower part (19%) compared with adults collected from the upper part (8%) of the rice plant and in brachypterous (57%) compared with macropterous forms (8%). No difference in parasitism between first (54%) and second (57%) generation was observed.     

Feeding ability and survival during starvation of marine fish larvae reared in the laboratory

The larvae of Clyde and Baltic herring (Clupea harengus L.), cod (Gadus morhua L.) and flounder (Platichthys flesus L.) were reared and fed to examine the changes in feeding ability and survival during progressive starvation. The time to initial feeding for yolk-sac larvae and to the point-of-no-return (PNR, when 50% of the larvae, although still alive, are no longer strong enough to feed) for both yolk-sac and older larvae were determined. The yolk-sac larvae of Clyde and Baltic herring, cod and flounder begin to feed on days 6, 3, 5 and 6 post-hatching at rearing temperatures of 7.5, 9.2, 6.9 and 9.5°C, respectively. The time to reach the PNR for yolk-sac larvae of these species is only 3–5 days after yolk resorption. From the onset of starvation in older larvae the time to reach the PNR is 6–7 days for 36-and 60-day-old Clyde herring at 9.6 and 10.5°C and for 46-day-old Baltic herring at 13.1°C but it is 23 days for 32-day-old flounder at 12.3°C. In yolk-sac larvae the peak of feeding rate and intensity usually occurred on the day that the yolk became exhausted, or 1 day later. Older larvae could withstand longer periods without food than yolk-sac larvae, especially in flounder. While the feeding rate during starvation of older larvae slowly decreased the feeding intensity first increased significantly and then decreased. Survival of larvae remained high up to the PNR.     

A male fitness advantage to wing reduction in the oriental chinch bug,Cavelerius saccharivorus okajima (heteroptera: Lygaeidae)

A male fitness advantage to wing reduction was investigated for the oriental chinch bug, Cavelerius saccharivorus, which is wing dimorphic. Field surveys for the frequency of matings between wing morphs showed that the mating probability was much higher in brachypterous males than in macropterous males in the early breeding season. Brachypterous males copulated with not only brachypterous females but also macropterous females in this season. This led to a considerable rate (30%) of insemination of macropterous females just before emigration even in the early breeding season. A rearing experiment for the pre-reproductive period of females revealed that females mated with brachypterous males copulated and oviposited earlier than females mated with macropterous males. These results indicate that there is a fitness advantage to wing reduction in the males of C. saccharivorus in terms of the earlier sexual maturation.