Functional Flight Muscles Research Articles

To fly or not to fly: Factors influencing the flight capacity of carabid beetles (Coleoptera: Carabidae)

This review considers factors affecting the flight capacity of carabid beetles and the implications of flight for carabids. Studies from the Dutch polders in particular show that young populations of carabids consist predominantly of macropterous species and macropterous individuals of wing-dimorphic species. Also populations of wing-dimorphic carabid species at the periphery of their geographical range contain high proportions of macropterous individuals. However, studies from Baltic archipelagos show that older populations of even highly isolated island habitats contain considerable proportions of brachypterous species and individuals. This suggests that macroptery is primarily an adaptation for dispersal and that there exists a mechanism for subsequently reducing the ratio of macropterous to brachypterous species under stable conditions, due to the competitive advantage of brachyptery. Populations in isolated habitats, such as islands and mountains, have high proportions of brachypterous species. Many macropterous species do not possess functional flight muscles. Species of unstable habitats, such as tree canopies and wet habitats, are mostly macropterous. Brachypterous species tend to disappear from disturbed habitats. There is uncertainty regarding the extent to which carabid dispersal is directed and how much passive. Both Den Boer and Lindroth recognized that mostly macropterous individuals of macropterous and wing-dimorphic species disperse and found new populations, after which brachyptery tends to rapidly appear and proliferate in the newly founded population. It is most likely that the allele for brachyptery would arrive via the dispersal of gravid females which had mated with brachypterous males prior to emigration. Whilst many studies consider wing morphology traits of carabid beetles to be species-specific and permanent, a number of studies have shown that the oogenesis flight syndrome, whereby females undertake migration and subsequently lose their flight muscles by histolysis before eventually regenerating them after reproducing, has been reported for a growing number of carabid species. Wing morphology of carabid beetles clearly offers strong potential for the study of population dynamics. This field of study flourished during the 1940's to the late 1980's. Whilst a considerable amount of valuable research has been performed and published, the topic clearly holds considerable potential for future study.

Lipogenesis in a wing-polymorphic cricket: Canalization versus morph-specific plasticity as a function of nutritional heterogeneity

The influence of variable nutritional input on life history adaptation is a central, but incompletely understood aspect of life history physiology. The wing-polymorphic cricket, Gryllus firmus, has been extensively studied with respect to the biochemical basis of life history adaptation, in particular, modification of lipid metabolism that underlies the enhanced accumulation of lipid flight fuel in the dispersing morph [LW(f)=long wings with functional flight muscles] relative to the flightless (SW=short-winged) morph. To date, biochemical studies have been undertaken almost exclusively using a single laboratory diet. Thus, the extent to which nutritional heterogeneity, likely experienced in the field, influences this key morph adaptation is unknown. We used the experimental approach of the Geometric Framework for Nutrition and employed 13 diets that differed in the amounts and ratios of protein and carbohydrate to assess how nutrient amount and balance affects morph-specific lipid biosynthesis. Greater lipid biosynthesis and allocation to the soma in the LW(f) compared with the SW morph (1) occurred across the entire protein-carbohydrate landscape and (2) is likely an important contributor to elevated somatic lipid in the LW(f) morph across the entire protein-carbohydrate landscape. Nevertheless, dietary carbohydrate strongly affected lipid biosynthesis in a morph-specific manner (to a greater degree in the LW(f) morph). Lipogenesis in the SW morph may be constrained due to its more limited lipid storage capacity compared to the LW(f) morph. Elevated activity of NADP+-isocitrate dehydrogenase (NADP+-IDH), an enzyme that produces reducing equivalents for lipid biosynthesis, was correlated with and may be an important cause of the increased lipogenesis in the LW(f) morph across most, but not all regions of the protein-carbohydrate landscape. By contrast, ATP-citrate lyase (ACL), an enzyme that catalyzes the first step in the pathway of fatty acid biosynthesis, showed complex morph-specific patterns of activity that were strongly contingent upon diet. Morph-specific patterns of NADP+-IDH and ACL activities across the nutrient landscape were much more complex than expected from previous studies on a single diet. Collectively, our results indicate that the biochemical basis of an important life history adaptation, morph-specific lipogenesis, can be canalized in the face of substantial nutritional heterogeneity. However, in some regions of the protein-carbohydrate landscape, it is strongly modulated in a morph-specific manner.

Evolutionary Endocrinology of Hormonal Rhythms: Juvenile Hormone Titer Circadian Polymorphism in Gryllus firmus.

Daily rhythms for hormonal traits are likely widespread and important aspects of organismal (e.g., life history) adaptation. Yet they remain substantially understudied, especially with respect to variable rhythms within species. The cricket, Gryllus firmus, exhibits a genetically polymorphic circadian rhythm for the blood titer of the key hormone, juvenile hormone (JH). Gryllus firmus is also wing-polymorphic, consisting of a dispersing morph that delays reproduction and a flightless morph with substantially enhanced egg production. JH circadian phenotype strongly covaries with morph type: The blood JH titer is strongly rhythmic in multiple populations artificially-selected for the dispersing morph (LW(f) = long wings with functional flight muscles) and is essentially arrhythmic in populations selected for the SW (short-winged) morph. Association between JH titer cycle and LW(f) morph is also found in natural populations of G. firmus and in several related species in the field. This is one of the very few studies of endocrine titer variation in natural populations of an insect. The morph-specific cycle is underlain by a circadian rhythm in hormone biosynthesis, which in turn is underlain by a rhythm in a brain neuropeptide regulator of JH biosynthesis. The morph-specific JH titer circadian cycle is also strongly correlated with a morph-specific daily rhythm in global gene expression. This is currently the only example of a genetically-variable hormone circadian rhythm in both the laboratory and field that is strongly associated with an ecologically important polymorphism. The extensive information on the underlying causes of the morph-specific JH titer rhythm, coupled with the strong association between the JH circadian rhythm and wing polymorphism makes this system in G. firmus an exceptional experimental model to investigate the mechanisms underlying circadian hormonal adaptations. Genetic polymorphism for the JH titer circadian rhythm in G. firmus is discussed in context of circadian rhythms for endocrine traits reported for vertebrates and insects. Consequences of the failure to identify endocrine circadian rhythms on the accuracy of estimation of quantitative-genetic parameters, such as heritability and correlations between hormonal and fitness-related traits, are also discussed.

De Novo Transcriptome Assembly from Fat Body and Flight Muscles Transcripts to Identify Morph-Specific Gene Expression Profiles in Gryllus firmus

Wing polymorphism is a powerful model for examining many aspects of adaptation. The wing dimorphic cricket species, Gryllus firmus, consists of a long-winged morph with functional flight muscles that is capable of flight, and two flightless morphs. One (obligately) flightless morph emerges as an adult with vestigial wings and vestigial flight muscles. The other (plastic) flightless morph emerges with fully-developed wings but later in adulthood histolyzes its flight muscles. Importantly both flightless morphs have substantially increased reproductive output relative to the flight-capable morph. Much is known about the physiological and biochemical differences between the morphs with respect to adaptations for flight versus reproduction. In contrast, little is known about the molecular genetic basis of these morph-specific adaptations. To address this issue, we assembled a de novo transcriptome of G. firmus using 141.5 million Illumina reads generated from flight muscles and fat body, two organs that play key roles in flight and reproduction. We used the resulting 34,411 transcripts as a reference transcriptome for differential gene expression analyses. A comparison of gene expression profiles from functional flight muscles in the flight-capable morph versus histolyzed flight muscles in the plastic flight incapable morph identified a suite of genes involved in respiration that were highly expressed in pink (functional) flight muscles and genes involved in proteolysis highly expressed in the white (histolyzed) flight muscles. A comparison of fat body transcripts from the obligately flightless versus the flight-capable morphs revealed differential expression of genes involved in triglyceride biosynthesis, lipid transport, immune function and reproduction. These data provide a valuable resource for future molecular genetics research in this and related species and provide insight on the role of gene expression in morph-specific adaptations for flight versus reproduction.

Nutrient regulation strategies differ between cricket morphs that trade‐off dispersal and reproduction

Summary Nutrient regulation should covary with life history, but actual demonstrations of this connection are rare. Here, we use a wing‐polymorphic cricket, Gryllus firmus, that trades off dispersal and reproduction; the long‐winged morph with functional flight muscles [LW(f)] is adapted for dispersal at the expense of egg production, while the short‐winged (SW) morph is adapted for egg production at the expense of flight. We explore the extent to which these two morphs differentially regulate macronutrient intake to best match their life‐history strategy. In a ‘choice’ experiment, we offered female crickets of each morph [LW(f) and SW] two nutritionally complementary foods varying in protein and digestible carbohydrate content. In a second ‘no‐choice’ experiment, we confined crickets to one of five foods, each with a different protein/carbohydrate ratio. In both experiments, and for both morphs, we measured food intake, mass gain and lipid concentration. In the ‘choice’ experiments, LW(f) females selected a more carbohydrate‐biased diet than SW females. The two morphs gained similar total mass, but the LW morph had higher lipid concentration. In the no‐choice experiment, the two morphs practised different nutrient ‘consumption rules’. SW females ate similar total nutrient amounts (protein plus carbohydrate) across diets, while LW(f) females decreased intake as the protein/carbohydrate ratio of the available food became increasingly imbalanced. Overall mass gain was marginally higher in the SW morph and lowest for both morphs on the diets that were extremely carbohydrate biased. LW(f) and SW females had similar lipid concentrations across the diets, even though LW(f) crickets ate less carbohydrate on the two carbohydrate‐biased diets. Our data suggest that for LW(f) females, there are costs of overeating nutrients in excess of requirements, but they are efficient at utilizing ingested nutrients. Our results shed new light on how the nutritional environment interacts with the direct trade‐off between dispersal and reproduction occurring in adult G. firmus crickets. Dispersal is linked to heightened diet selectivity and an emphasis on nutrients promoting flight fuel (lipid) storage over protein acquisition for egg laying, such that nutritional regulation complements the metabolic mechanisms that generate this trade‐off.

Colonists and desperadoes: different fighting strategies in wing-dimorphic male Texas field crickets

In many species, males fight one another for mates or resources. Fighting can vary among males, however, such that some males are highly aggressive whereas others are not. We observed that fighting was negatively associated with flight capability in the wing-dimorphic field cricket, Gryllus texensis. Long-winged males capable of flight had a significantly lower fighting propensity and displayed lower levels of aggression than short-winged, flight-incapable males in staged contests. Long-winged males no longer able to fly as a result of the histolysis of their flight muscles were more aggressive than long-winged males that had functional flight muscles, but were still less aggressive than short-winged males. Long-winged, flight-capable males were more aggressive after a brief flight just prior to an interaction with a rival, but only in contests with other flight-capable males. Flight capability and flight itself had no effect on the outcome of fights. Our results support the existence of an aggression flight syndrome in flight-dimorphic insects.

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.

THE GENETIC BASIS OF THE TRADE-OFF BETWEEN CALLING AND WING MORPH IN MALES OF THE CRICKET GRYLLUS FIRMUS.

Wing dimorphisms exist in a wide range of insects. In wing-dimorphic species one morph is winged has functional flight muscles (LW), and is flight-capable, whereas the other has reduced wings (SW) and cannot fly The evolution and maintenance of wing dimorphisms is believed to be due to trade-offs between flight capability and fitness-related traits. Although there are well-established phenotypic trade-offs associated with wing dimorphism in female insects, there only exist two studies that have established a genetic basis to these trade-offs. The present study provides the first evidence for a genetically based trade-off in male insects, specifically in the sand cricket Gryllus firmus. Because they have to expend energy to maintain the flight apparatus (especially flight muscles), LW males are predicted to call less and therefore to attract fewer females. To be of evolutionary significance, call duration wing morph, and wing muscle condition (size and functionality) should all have measurable heritabilities and all be genetically correlated. Differences between morphs in male G. firmus in the likelihood of attracting a female were tested in the laboratory using a T-maze where females chose between a LW male and a SW male. Call duration for each male was recorded on the sixth day of adult life. A significant difference in call duration was found between SW and LW males (SW = 0.86 ± 0.01, LW = 0.64 ± 0.01 h). SW males attracted significantly more females than did LW males (63% vs. to 37%). All the traits involved in the trade-off had significant heritabilities (call = 0 75 ± 0 33; wing morph = 0.22 ± 007; muscle weight = 0.38 ± 0.09) and genetic correlations (call and wing morph = -0.46 ± 0.20 for SW, -0.68 ± 0.16 for LW; LW call and muscle weight = -0.80 ± 0.14). These results provide the first documented evidence that trade-offs between a dimorphic trait and a fitness-related character in males has a genetic basis and hence can be of evolutionary significance.

Differential allocation of resources underlies the dispersal-reproduction trade-off in the wing-dimorphic cricket, Gryllus rubens.

The cricket, Gryllus rubens (Orthoptera, Gryllidae), exists in natural populations as either a fully-winged (LW), flight-capable morph or as a short-winged (SW) morph that cannot fly. The SW morph is substantially more fecund than the LW morph. In this study we report on the physiological basis of this trade-off between flight capability and fecundity. Results from gravimetric feeding trials indicate that LW and SW morphs are equivalent in their consumption and digestion of food. However, during the adult stage, the LW morph is less efficient in converting assimilated nutrients into biomass. This may be a consequence of the respired loss of assimilated nutrients due to the maintenance of functional flight muscles in the LW morph. In both morphs the gross biomass devoted to flight muscles does not change significantly during the first 14 days of adult growth while there is a significant biomass gain in ovarian tissue mass during the same period. SW morphs have vestigial flight muscles and gain substantially more ovarian mass relative to the LW morphs. These data are consistent with a trade-off between flight muscle maintenance in the LW morph and ovarian growth in the SW form. This is the first evidence for a life-history trade-off that has a physiological basis which is limited to the allocation of acquired and assimilated nutrients within the organism.

Wing Dimorphisms and the Evolution of Migratory Polymorphisms among the Insecta

Many species of insects exhibit wing dimorphism, one morph having fully developed wings and the other morph having reduced wings and being incapable of flight. These wing dimorphisms provide visible manifestations of migratory polymorphisms. Since winged individuals do not, in principle, have to fly, the existence of forms with reduced wings suggests that there is a tradeoff between flight capability and other fitness components. Comparisons of the life histories of the fully winged and wing reduced morphs demonstrate that this tradeoff is most commonly expressed as a decrease in the age of first reproduction and increased fecundity in the morph with reduced wings. Given these tradeoffs, the evolution of wing dimorphism will depend upon its genetic basis, including correlations with other life history components. A review of the recent literature suggests that the heritability of wing morphology is high, and we suggest that this high heritability could be maintained, in part, by antagonistic pleiotropy. In dimorphic species, the winged morph is generally considered to be the migrant form. However, there are significant correlations, both within and among species, between the proportion of winged individuals, the proportion of winged individuals with functional flight muscles, and the flight propensity of those individuals. This suggests that the proportion of winged individuals and the propensity of the winged morph to migrate are intimately connected at both the physiological and population level. Therefore, the study of the evolution of wing dimorphism is important not only in its own right but also as a model of how migratory propensity evolves in monomorphically winged species.

Possibilities for flight in the carabid beetle Nebria brevicollis (F.) : The importance of food during larval growth.

The carabid beetle Nebria brevicollis (F.), despite being macropterous, has a very low flight potential. Only a few percent of the beetles has functional flight muscles, flight motivation is low, and the period favourable for flight is short. The inability to fly is caused mainly by arrested development of the flight muscles. Dispersers are formed only under favourable conditions in the larval stages as shown by laboratory experiments (much food, short daylength). In N. brevicollis dispersal by flight cannot be considered as a reaction to deteriorating conditions but just the other way round. Because of the usually low numbers of potential dispersers conditions during larval development are apparently suboptimal. However, N. brevicollis is widespread and abundant in our area. The "choice" of using energy for the metabolic costs of larval growth, and only secondarily for the building up of flight muscles does not prevent the species from fully exploiting the habitat.