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Orthoptera: Gryllidae) Eur. J. Entomol. 109: 579–586, 2012 http://www.eje.cz/scripts/viewabstract.php?abstract=1744 ISSN 1210-5759 (print), 1802-8829 (online) Variations in the ultrastructure of the flight muscles of the polymorphic cricket, Gryllus firmus (Orthoptera: Gryllidae) CHENG-JI JIANG*, BAO-CHANG ZHANG*, WEN-FENG CHEN, QING-WEN ZHANG, ZHANG-WU ZHAO**, CHUN-JU AN and JIE-PING LI College of Agronomy and Biotechnology, China Agricultural University, Beijing 100193, P.R. China; e-mail: [email protected] Key words. Orthoptera, Gryllidae, Gryllus firmus, flight muscle, ultrastructure, juvenile hormone, Transmission Electron Microscope Abstract. Although there is a considerable amount of information on the ecology, genetics and physiology of life-history traits there is little information on the morphological variations associated with flight ability within species. In this paper, the morphology and ultrastructure of certain organelles in the flight muscles of Gryllus firmus are recorded using transmission electron microscopy. The ultrastructure of the flight muscles of 7-day-old female adults reveals that the ratio of thick to thin filaments is 1 : 3. Each thick fila- ment is surrounded by 6 thin filaments in a hexagonal arrangement. The length of the sarcomere of each myofibril is significantly shorter and diameter of the myofibrils significantly smaller in long-winged than in short-winged morphs. However, the thick fila- ments in the long-winged morph are denser than those in the short-winged morph. Furthermore, in the long winged morph there are a greater number of mitochondria than in the short-winged morph. These differences correspond with the fact that long-winged crickets are stronger fliers than short-winged crickets. INTRODUCTION muscle nuclei are closely distributed in inner membrane Flight is important for insect dispersal. In the jargon of (Ruppert et al., 2003). the aeronautics industry, flight pushes the envelope of Flight polymorphism (also called dispersal or wing organism design (Dickinson, 1997). Flight muscle is one polymorphism) occurs widely in the Insecta and involves of the most widely studied flight-related tissues in insects discontinuous variation in a wide variety of traits mainly because of the variation in the metabolic activity involved in flight and reproduction (Dingle, 1996; Zera & of the different types of muscle (Sacktor, 1970; Usher- Denno, 1997; Zera & Harshman, 2001). The flight mus- wood, 1975, Mentel et al., 2003). All muscles receive cles of the cricket Gryllus firmus are polymorphic and excitatory innervation from glutamatergic neurons, inhi- pink or white in colour (Zera et al., 1997). The white bitory innervation from GABAergic neurons and modula- muscles are small and have a few small muscle fibers, and tory innervation from octopaminergic dorsal unpaired in terms of in vitro enzyme activities and respiration rates median (DUM) neurons (Biserova & Pfluger, 2004). are less active than the pink muscles of fully winged Energy for flight is provided primarily by the very high adults (Zera & Deno, 1997). Crickets usually fly at night levels of glucose and lipid in the blood. Adipokinetic hor- and under laboratory conditions begin flying immediately mone (AKH) is very important in the metabolism of the lights are turned off. lipids and triggers the release of octopamine from The ultrastructure of the flight muscles, especially those octopamine-releasing neurons, such as the DUM neurons associated with insect growth and development is well (Birkenbeil, 1971), which in turn activates catabolic described (Herold, 1965; Reedy, 1968; Davies, 1974; enzymes, such as lipases and phosphorylases (Fassold et Mizisin & Ready, 1986; Novicki, 1989; Reedy & Beall, al., 2010). 1993; Mentel et al., 2003; Biserova & Pfluger, 2004). The The main insect muscles are the leg muscles, pleuroax- juvenile hormone (JH) is critical for both the growth and illary “steering” muscles and flight muscle (Biserova & degeneration of flight muscles (Novicki, 1989; Rose, Pfluger, 2004). There are two types of flight muscle in 2004). In the cricket Acheta domestica, the dorsal longitu- insects, direct and indirect. Crickets have direct flight dinal muscle increases in size during the first 2 days of muscles and what is called a synchronous flight muscle adulthood and begins to degenerate on day 4 when the system. This system is characterized by closely packed level of JH increases (Chudakova & Bocharova-Messner, flight muscles and relatively slow wing-beat frequencies. 1968; Srihari et al., 1975). Overall, low levels of JH are The closely packed flight muscles have the following required for muscle growth and high levels cause the characteristics: the peripheral muscle fibers are sur- flight muscle to degenerate. However, there is one rounded by a large number of mitochondria and the notable exception, during adulthood, the JH titer in the haemolymph undergoes a daily cycle with a high titer * These authors contributed equally to this work. ** Corresponding author. 579 Fig. 1. Basic structure of the flight muscles. A – a longitudinal section of the flight muscle of a LW cricket (×6000); B – a l SW cricket (×6000). Tr – trachea; Mt – mitochondrion; Ky – nucleus; Mf – myofibril; Sr – endoplasmic reticulum; Va – vacuole. The Z band is black and the Z lines are the two black lines. There are both light and dark bands in a sarcomere. about 4 h before lights off, which is maintained for only a LW(f) crickets began flying after day 5 of adulthood and SW short period (Zhao & Zera, 2004b). crickets began reproducing on day 4. Therefore, 7 day old It is unknown whether this short spike in JH concentra- females were used in the comparitive study of dispersal and tion affects flight-muscle tissue and in order to determine reproduction. Samples consisting of five crickets were sepa- rately collected at 12:00 (control), 21:00 (1 h before lights off) whether this is the case transmission electron microscopy and 24:00 (2 h after lights off) hours. This experiment was (TEM) was used to record the ultrastructure of adult repeated 3 times. flight muscles before and after flight. Tissue treatment for TEM MATERIAL AND METHODS The flight muscles were dissected and fixed in 2.5% glutaral- Insects, morph designations and rearing conditions dehyde overnight. After fixation, the samples were rinsed 3 times in 0.1M PBS buffer and post-fixed in 1% osmium tetrox- There are two morphs of Gryllus firmus (Orthoptera: Grylli- ide. Then the specimens were again washed in the 0.1M PBS dae), the sand cricket, which lives in the southeastern United buffer and dehydrated separately in a series of acetone States, a long-winged (LW) morph, some of which are capable solutions, namely 30%, 50%, 70%, 80%, 90% and 100%. After of flight and a short-winged (SW) morph that is obligatorily that, the muscles were preserved in Epon-Araldite resin over- flightless (Veazy et al., 1976). All SW females have white, non- night for embedding. Ultra-thin sections (500–1000A) obtained functional flight muscles that never fully develop. All LW using a LEICAUC6i type slicer were stained with uranyl acetate females initially have large, pink flight muscles at the adult and lead citrate, and then observed and photographed using a moult and are denoted as LW(f). After about 5–6 days some JEM-123 OLYMPUS TEM. The myofibrillar diameter was LW(f) individuals begin to histolyze their flight muscles and measured using a TEM micro-ruler. Numbers and shapes of become flightless (denoted LW(h); see Zera et al., 1997). Only mitochondria in the two morphs were counted in an area of 100 the ultrastructure of the flight muscles of LW(f) individuals was µm2. determined in the present study. The G. firmus used in this study came from LW- and SW-selected lines (Block-1; see Zera & Statistical analysis Cisper, 2001). Data were statistically analyzed using Repeated-Measures Crickets were reared under a 16L : 8D photoperiod at 28°C. ANOVA in GraphPad Prism 4.0 software. More details are pre- They were fed a standard diet. The details of the rearing condi- sented in the figure legends. The results shown in tables and fig- tions are the same as those described in Zera & Cisper (2001). ures are expressed as means ± standard errors. 580 Fig. 2. Cross-section of a myofibril in the fight muscle of a sand cricket (×25,000). Mf – myofibril; Mt – mitochondrion; T – thick filament; A – thin filament. The right image shows a magnified myofibril (×100,000). RESULTS cantly different at 12:00, 21:00 and 24:00 h (P < 0.01, F = Basic structure of flight muscles 85.09, DFn = 2, DFd = 72). Compared to controls sam- pled at 12:00, the mean lengths of the sarcomeres in LW TEM results showed adult female sand crickets have flight muscles were much shorter at 21:00, just before typical structural features with synchronous flight mus- flight, and the shortest sarcomere length occurred at cles. The long- and short-winged crickets had similar sub- 24:00, 2 h after lights off. Importantly, the sarcomeres of cellular structures (Figs 1A and B). the LW morph were more contracted than those of the Myofibrils SW morph (P < 0.01, F = 126.97, DFn = 1, DFd = 72) Viewed in cross-section, each myofibril is surrounded (Fig. 5). Moreover, the interaction between time of day by a large number of mitochondria, which are oval or and wing morph on sarcomere length was also extremely polygonal in shape and separated from the sarcoplasmic significant (P < 0.01, F = 63.83, DFn = 2, DFd = 72). The reticulum (Figs 1B and 2). One characteristic feature of wing morphs differ in sarcomere lengths at 21:00 and the myofibril is the accurate arrangement of myofilaments 24:00 h, which is the flight period (Fig. 5). Longitudinal during the development of the flight muscle. Each myosin sections of the flight muscles of LW and SW individuals filament (thick filament) is surrounded by six actin fila- are depicted in Fig.
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