Flight-Muscle Polymorphism in the Cricket Gryllus Firmus: Muscle Characteristics and Their Influence on the Ve Olution of Flightlessness

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Flight-Muscle Polymorphism in the Cricket Gryllus Firmus: Muscle Characteristics and Their Influence on the Ve Olution of Flightlessness University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Anthony Zera Publications Papers in the Biological Sciences October 1997 Flight-Muscle Polymorphism in the Cricket Gryllus firmus: Muscle Characteristics and Their Influence on the vE olution of Flightlessness Anthony J. Zera University of Nebraska - Lincoln, [email protected] Jeffry Sall University of Nebraska - Lincoln Kimberly Grudzinski University of Nebraska - Lincoln Follow this and additional works at: https://digitalcommons.unl.edu/bioscizera Part of the Microbiology Commons Zera, Anthony J.; Sall, Jeffry; and Grudzinski, Kimberly, "Flight-Muscle Polymorphism in the Cricket Gryllus firmus: Muscle Characteristics and Their Influence on the vE olution of Flightlessness" (1997). Anthony Zera Publications. 5. https://digitalcommons.unl.edu/bioscizera/5 This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Anthony Zera Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. 519 Flight-Muscle Polymorphism in the Cricket Gryllus firmus: Muscle Characteristics and Their Influence on the Evolution of Flightlessness Anthony J. Zera^ tify the factors that affect dispersal in natural populations (Har- Jeffry Sail rison 1980; Dingle 1985; Pener 1985; Roff 1986; Zera and Mole Kimberly Grudzinski 1994; Zera and Denno 1997). An important finding of these School of Biological Sciences, University of Nebraska, studies is that dispersal capability has physiological and fitness Lincoln, Nebraska 68588 costs. Fully winged females typically begin egg development later and have reduced fecundity relative to flightless (short- Accepted by C.P.M. 1/9/97 winged or wingless) females (Pener 1985; Roff 1986; Zera and Denno 1997). This observation, together with more recent physiological comparisons of wing morphs, indicates that the attainment and maintenance of flight capability involves a sig- ABSTRACT nificant energetic cost, which reduces egg production (Tanaka Flight muscles of the cricket Gryllus firmus are polymorphic, ex- 1993; Zera and Mole 1994; Zera and Denno 1997). isting as pink or white phenotypes. White muscles are smaller in Although wing polymorphism derives its name from varia- size, have reduced number and size of muscle fibers, and have tion in wing length, wing morphs also differ in flight-muscle reduced in vitro enzyme activities and respiration rates relative to characteristics. Flight muscles are reduced in the flightless pink muscles of newly molted, fully winged adults. G. firmus is morph (Smith 1964; Pener 1985; Roff 1986). Muscle reduction also polymorphic for wing length. All newly molted long-winged is thought to be more important than wing reduction in elevat- adults exhibited the pink-muscle phenotype, while most newly ing the fecundity of the flightless morph (Zera and Denno molted short-winged adults exhibited the white-muscle phenotype, 1997); however, there is a paucity of anatomical, physiological, which resulted from arrested muscle growth. As long-winged adults and biochemical data on flight muscles in wing-polymorphic aged, fully grown pink muscle was transformed into white muscle insects (reviewed in Smith [1964] and Pener [1985]). This via histolysis. The substantially higher respiration rate of pink mus- paucity of information limits our understanding of the physio- cle likely contributes to the elevated whole-organism respiration logical mechanisms underlying the trade-off between flight ca- rate of long-winged females, which has been documented pre- pability and reproduction and has also likely resulted in an viously and which is thought to divert nutrients from egg produc- underestimate of the fitness cost of flight capability. tion. Histolyzed white flight muscle from long-winged crickets also The fitness cost of flight capability has typically been assessed exhibited significantly elevated respiration rate and enzyme activi- by comparing the decrease in fecundity of long-winged females ties compared with underdeveloped white muscle from short- that have not flown with that of short-winged females of wing- winged adults, although these differences were not as great as polymorphic insects (Harrison 1980; Roff 1986; Zera and those between pink and white muscles. Fecundity was much more Denno 1997). However, it has long been recognized that long- elevated in females with white versus pink flight muscles than it winged individuals of the same age often exhibit dramatic vari- was in females with short versus long wings. The fitness gain ation in flight-muscle status. Some long-winged females exhibit resulting from flightlessness has typically been estimated in previous fully developed flight muscles when reproduction commences, studies by comparing enhanced egg production of short-winged while others have histolyzed flight muscles at this time and and long-winged females, without considering the influence of thus are functionally flightless (Young 1965; Pener 1985). flight-muscle variation. Our results suggest that the magnitude of Flight-muscle polymorphism within the long-winged subpopu- this fitness gain has been substantially underestimated. lation would result in an underestimate of the costs of flight capability if flight-muscle histolysis elevates fecundity and if long-winged individuals with and without histolyzed flight Introduction muscles are not distinguished. The extent to which this occurs is unknown. Wing polymorphism in insects has been extensively studied The present study is the first in a series of investigations from physiological, genetic, and ecological perspectives to iden- that focuses on flight-muscle characteristics of long-winged and short-winged morphs of the wing-dimorphic cricket, Gryllus ^To whom correspondence should be addressed; E-mail: [email protected]. firmus. This species and its congener Gryllus rubens have been Physiological Zoology 70(5):519-529. 1997. © 1997 by The University of used in physiological studies on the trade-off between flight Chicago. All rights reserved. 0031-935X/97/7005-9680$03.00 capability and fecundity (Mole and Zera 1993; Zera and Mole 520 A. J. Zera, J. Sail, and K. Grudzinski 1994; Zera et al. 1994). Prior to the present study, only rudi- crickets. These crickets were reared singly with oviposition mentary information was available on any aspect of flight- material in which they oviposited their eggs. muscle variation in these species. The present study had three goals. The first was to obtain baseline information on the mor- Histology phology, development, and physiology of the various flight- muscle phenotypes in the long-winged and short-winged Dorsolongitudinal flight muscles were dissected out of long- morphs. The second was to determine the degree to which winged or short-winged crickets of various ages, fixed in Bou- reduced flight-muscle phenotypes that are produced by differ- in's fluid for 12 h, and dehydrated and infiltrated with paraffin. ent processes (arrested growth in juveniles vs. histolysis in Cross sections (7 |Lim) through the thickest portion of the adults) resemble each other in morphology, physiology, and muscles were stained with Masson's Triple Stain (Weesner impact on egg production. The degree to which this occurs is 1960) and were examined under a light microscope. Muscle expected to have an important influence on the evolution of fibers were oblong and mean fiber cross-sectional area per flightlessness (see Discussion). The third goal was to assess the muscle was calculated as follows: Maximum and minimum degree to which enhanced fecundity is associated with reduced fiber diameters were measured for each of six randomly chosen flight muscles rather than reduced wing length and the conse- fibers. The average cross-sectional area was computed as the quences of this on estimates of the cost of dispersal capability. product of the average maximum and minimum diameters. The total number of fibers per muscle was calculated by divid- ing the cross-sectional area of the entire muscle by the average Material and Methods fiber area. Insect Rearing Isocitrate Dehydrogenase and Citrate Synthase Activities Gryllus firmus, the sand cricket, occurs in the southeastern United States as a long-winged morph, some of which are Dorsolongitudinal flight muscles were dissected out of long- capable of flight, or as a short-winged form that is obligately winged or short-winged crickets of various ages and assayed flightless (Veazy et al. 1976). The G. firmus used were from for NADP+-dependent isocitrate dehydrogenase (IDH, EC the same laboratory colonies that were used in previous physio- 1.1.1.42) or citrate synthase (CS, EC 4.1.3.7) activity. These logical studies (Zera and Mole 1994; Zera et al. 1994). Standard enzymes were chosen to represent typical cytoplasmic and mi- rearing conditions (28°C, 16L : 8D photoperiod, 40-60 adults tochondrial enzymes of intermediary metabolism. CS activity per 38-L aquarium, no egg-laying substrate) are detailed in is also an indicator ofmitochondrial volume and aerobic capac- those reports. ity in insect flight muscle (Ready and Najam 1985). Dissected muscle was blotted dry, weighed and homogenized in 20 vol of 3-(N-morpholino)propanesulfonic acid buffer (ionic Developmental Profiles of Flight Muscles strength = 0.1), pH 7.1. The homogenate was centrifuged at and Reproductive Organs 13,000 g for 10 min and the supernatant was assayed for IDH
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