Flightless Morph Research Articles

Phenotypically plastic responses to environmental variation are more complex than life history theory predicts.

For insects that exhibit wing polyphenic development, abiotic and biotic signals dictate the adult wing morphology of the insect in an adaptive manner such that in stressful environments the formation of a flight-capable morph is favored and in low-stress environments, a flightless morph is favored. While there is a relatively large amount known about the environmental cues that dictate morph formation in wing polyphenic hemipterans like planthoppers and aphids, whether those cues dictate the same morphs in non-hemipteran (i.e., cricket) wing polyphenic species has not been explicitly investigated. To experimentally test the generality of environmental cue determination of wing polyphenism across taxa with diverse life histories, in this study, we tested the importance of food quantity, parasitic infection, and tactile cues on wing morph determination in the wing polyphenic sand field cricket, Gryllus firmus. Our results also show that certain stress cues, such as severe diet quantity limitation and parasitic infection, actually led to an increase in the production of flightless morph. Based on these findings, our results suggest that physiological and genetic constraints are important to an organism's ability to respond to environmental variation in an adaptive manner beyond simple life history trade-offs.

Cell death and wing reduction during the metamorphosis of sex-specific flightless morphs in winter geometrid moths.

Winter geometrid moths show striking sexual dimorphism by having female-specific flightless morphs. The evolutionary grades of wing reduction in winter geometrid moths vary and range from having short wings, vestigial wings, to being wingless. Although the ontogenetic processes underlying the development of the wingless or short-wing morphs in Lepidoptera has been well studied, the mechanisms underlying the development of vestigial wing morphs in winter geometrid moths during metamorphosis are poorly understood. In the winter geometrid moth Sebastosema bubonaria Warren, 1896, the males have functional wings, but the females have vestigial wings. Here, we studied the ontogenetic processes affecting wing reduction in the winter geometrid moth S. bubonaria using light microscopy and transmission electron microscopy, and compared the ontogenetic process of wing reduction in this species with that in another species of the wingless-female winter moth that we investigated previously. Our results showed that, in the vestigial-wing morphs, the loss of pupal wing epithelium was terminated in the middle of the wing degeneration process, whereas in the wingless morph, the pupal wing epithelium disappeared almost completely and the final appearance of the wings differed slightly among flightless morphs. We propose that the extent and location of cell death in the pupal wing play an important role in the various patterns of reduced wings that are observed in flightless moths.

Thermal Preferences of Cowpea Seed Beetles (Callosobruchus maculatus): Effects of Sex and Nuptial Gift Transfers.

Simple SummaryThe thermal environment is crucial for organismal functioning, and many cold-blooded organisms, including insects, behaviorally regulate their body temperature. Why do insects inhabit given thermal conditions? We propose that access to water affects thermal preference and that insects with poor access to water inhabit colder environments, which reduces evaporation and preserves water. We studied the seed beetle Callosobruchus maculatus, which, as adults, do not drink or eat; however, males provide their mates with sperm, as well as nuptial gifts, including nutrients and water sources. We compared preferred temperatures between males and females that had access to mates or remained unmated and measured the sizes of the transferred gifts. We found that females preferred higher temperatures than males, but these preferences did not change due to mating or the transfer of larger or smaller gifts. It appears that males and females receive and lose certain amounts of water during mating, but they do not alter their thermal preferences according to the amount of water they receive or lose.The thermal environment influences insect performance, but the factors affecting insect thermal preferences are rarely studied. We studied Callosobruchus maculatus seed beetles and hypothesized that thermal preferences are influenced by water balance, with individuals with limited water reserves preferring cooler habitats to reduce evaporative water loss. Adult C. maculatus, in their flightless morph, do not consume food or water, but a copulating male provides a female with a nuptial gift of ejaculate containing nutrients and water. We hypothesized that gift recipients would prefer warmer habitats than gift donors and that both sexes would plastically adjust their thermal preferences according to the size of the transferred gift. We measured the thermal preference in each sex in individuals that were mated once or were unmated. In the mated group, we measured the sizes of the nuptial gifts and calculated proportional body mass changes in each mate during copulation. Supporting the role of water balance in thermal preference, females preferred warmer habitats than males. Nevertheless, thermal preferences in either sex were not affected by mating status or gift size. It is likely that high rates of mating and gift transfers in C. maculatus living under natural conditions promoted the evolution of constitutive sex-dependent thermal preferences.

Morphological and histological examination of short-wing formation in the winter moth Protalcis concinnata (Insecta: Lepidoptera, Geometridae).

Winter geometrid moths exhibit sexual dimorphism in wing length and female-specific flightlessness. Female-specific flightlessness in insects is an interesting phenomenon in terms of sexual dimorphism and reproductive biology. In the winter geometrid moth, Protalcis concinnata (Wileman), adult females have short wings and adult males have fully developed wings. Although the developmental process for wing reduction in Lepidoptera is well studied, little is known about the morphology and the developmental pattern of short-winged flightless morphs in Lepidoptera. To clarify the precise mechanisms and developmental processes that produce short-winged morphs, we performed morphological and histological investigations of adult and pupal wing development in the winter geometrid moth P. concinnata. Our findings showed that (a) wing development in both sexes is similar until larval-pupal metamorphosis, (b) the shape of the sexually dimorphic wings is determined by the position of the bordering lacuna (BL), (c) the BL is positioned farther inward in females than in males, and (d) after the short pupal diapause period, the female pupal wing epithelium degenerates to approximately two-thirds its original size due to cell death. We propose that this developmental pattern is a previously unrecognized process among flightless Lepidoptera.

Genetics and selective breeding of variation in wing truncation in a flightless aphid control agent

AbstractAugmentative biological control by predaceous ladybird beetles can be improved by using flightless morphs, which have longer residence times on the host plants. The two‐spot ladybird beetle, Adalia bipunctata (L.) (Coleoptera: Coccinellidae), is used for the biological control of aphids in greenhouses and on urban trees. Flightlessness due to truncated wings occurs at very low frequency in some natural populations of A. bipunctata. Pure‐breeding strains of this 'wingless' genotype of A. bipunctata can easily be obtained in the laboratory. Such strains have not been commercialized yet due to concerns about their reduced fitness compared to wild‐type strains, which renders mass production more expensive. Wingless strains exhibit, however, wide intra‐population phenotypic variation in the extent of wing truncation which is related to fitness traits. We here use classical quantitative genetic techniques to study the heritability and genetic architecture of variation in wing truncation in a wingless strain of A. bipunctata. Split‐families reared at one of two temperatures revealed strong family‐by‐temperature interaction: heritability was estimated as 0.64 ± 0.09 at 19 °C and 0.29 ± 0.06 at 29 °C. Artificial selection in opposite directions at 21 °C demonstrated that the degree of wing truncation can be altered within a few generations resulting in wingless phenotypes without any wing tissue (realized h2 = 0.72), as well as those with minimal truncations (realized h2 = 0.61) in two replicates. The latter lines produced more than twice as many individuals. This indicates that selective breeding of wing truncation may be exploited to improve mass rearing of flightless strains of A. bipunctata for commercial biological control. Our work illustrates that cryptic variation can also be a source for the selective breeding of natural enemies.

Diurnal and developmental differences in gene expression between adult dispersing and flightless morphs of the wing polymorphic cricket, Gryllus firmus: Implications for life-history evolution

The functional basis of life history adaptation is a key topic of research in life history evolution. Studies of wing-polymorphism in the cricket Gryllus firmus have played a prominent role in this field. However, prior in-depth investigations of morph specialization have primarily focused on a single hormone, juvenile hormone, and a single aspect of intermediary metabolism, the fatty-acid biosynthetic component of lipid metabolism. Moreover, the role of diurnal variation in life history adaptation in G. firmus has been understudied, as is the case for organisms in general. Here, we identify genes whose expression differs consistently between the morphs independent of time-of-day during early adulthood, as well as genes that exhibit a strong pattern of morph-specific diurnal expression. We find strong, consistent, morph-specific differences in the expression of genes involved in endocrine regulation, carbohydrate and lipid metabolism, and immunity – in particular, in the expression of an insulin-like-peptide precursor gene and genes involved in triglyceride production. We also find that the flight-capable morph exhibited a substantially greater number of genes exhibiting diurnal change in gene expression compared with the flightless morph, correlated with the greater circadian change in the hemolymph juvenile titer in the dispersing morph. In fact, diurnal differences in expression within the dispersing morph at different times of the day were significantly greater in magnitude than differences between dispersing and flightless morphs at the same time-of-day. These results provide important baseline information regarding the potential role of variable gene expression on life history specialization in morphs of G. firmus, and the first information on genetically-variable, diurnal change in gene expression, associated with a key life history polymorphism. These results also suggest the existence of prominent morph-specific circadian differences in gene expression in G. firmus, possibly caused by the morph-specific circadian rhythm in the juvenile hormone titer.

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.

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.

The taxonomic impediment of unrecognised flight polymorphism in Notonectidae (Hemiptera:Heteroptera)

Foundation revisions of four genera within the Notonectidae (Hemiptera: Heteroptera: Nepomorpha) were reviewed to determine how the existence of previously unrecognised polymorphism of the wings or flight musculature might have led to confusion in the description of species. Specimens of the flightless morph may appear very different from flight capable ones. They are generally less pigmented and may be both smaller and less robust. In species descriptions the flightless morph can usually be readily diagnosed through the reduced pigmentation of the mesoscutellum. Flight-muscle and wing polymorphisms were found to be common in these genera. In Notonecta only one of the possible flying or flightless morphs was described in 51 of 60 species (85%), in Anisops in 64 of 80 species (80%), in Buenoa 26 of 35 species (74%), and in Enithares 11 of 33 species (33%). A greater recognition of the existence of flight polymorphism in this family can lead to more robust species descriptions and selection of type specimens. Within the four genera considered here alternative morphs are yet to be described in many species.

Morph-specific diurnal variation in allatostatin immunostaining in the corpora allata of Gryllus firmus: Implications for the regulation of a morph-specific circadian rhythm for JH biosynthetic rate

Previous studies have documented a circadian cycle in juvenile hormone (JH) biosynthesis in the long-winged, flight-capable morph, but not in the short-winged flightless morph of the cricket Gryllus firmus. One rapid and reversible inhibitor of in vitro JH biosynthesis by the corpora allata (CA) in crickets is the neuropeptide Phe-Gly-Leu/Ile-amide type of allatostatins (ASTs). To investigate the possible role of allatostatin regulation of the morph-specific circadian cycle of JH production, the quantity of this type of AST in the nerves within the CA was determined by the density of anti-AST-immunostaining in confocal images using the Image J program. The density of immunostaining was inversely related to the rate of JH biosynthesis: Immunostaining in the CA was high and did not differ between morphs early in the photophase when the in vitro rate of JH biosynthesis is low and equivalent in the morphs. However, during the end of the photophase, when the rate of JH biosynthesis rises dramatically in the flight-capable morph, but not in the flightless morph, immunostaining was significantly lower in the flight-capable compared to the flightless morph. These results indicate that morph-specific differences in delivery of AST to the CA and its probable release likely regulate the morph-specific circadian pattern of JH biosynthesis. Also, the negative correlation between AST density and JH production provides evidence for predicting the periods of altered release of these rapid-acting paracine regulators of JH biosynthesis.

Morph-associated JH titer diel rhythm in Gryllus firmus: Experimental verification of its circadian basis and cycle characterization in artificially selected lines raised in the field

Previous studies demonstrated a high-amplitude, diel cycle for the hemolymph JH titer in the wing-polymorphic cricket, Gryllus firmus. The JH titer rose and fell in the flight-capable morph (long-winged, LW(f)) above and below the relatively temporally invariant JH titer in the flightless (short-winged, SW) morph. The morph-specific JH titer cycle appeared to be primarily driven by a morph-specific diel cycle in the rate of JH biosynthesis. In the present study, cycles of the JH titer and rate of JH biosynthesis in the LW(f) morph persisted in the laboratory under constant darkness with an approximate 24 h periodicity. The JH titer cycle also shifted in concert with a shift in the onset of the scotophase, was temperature compensated in constant darkness, and became arrhythmic under constant light. These results provide strong support for the circadian basis of the morph-specific diel rhythm of the JH titer and JH biosynthetic rate. Persistence of the JH titer cycle under constant darkness in multiple LW-selected and SW-selected stocks also provides support for the genetic basis of the morph-associated circadian rhythm. The morph-specific JH titer cycle was observed in these stocks raised in the field, in both males and females, in each of 3 years studied. The onset of the cycle in the LW(f) morph, a few hours before sunset, correlated well with the onset of the cycle, a few hours before lights-off, in the laboratory. The morph-specific JH titer cycle is a general feature of G. firmus, under a variety of environmental conditions, and is not an artifact of specific laboratory conditions or specific genetic stocks. It is a powerful experimental model to investigate the mechanisms underlying endocrine circadian rhythms, their evolution, and their impact on life history evolution.

The Effect of Diet Quality and Wing Morph on Male and Female Reproductive Investment in a Nuptial Feeding Ground Cricket

A common approach in the study of life-history trade-off evolution is to manipulate the nutrient content of diets during the life of an individual in order observe how the acquisition of resources influences the relationship between reproduction, lifespan and other life-history parameters such as dispersal. Here, we manipulate the quality of diet that replicate laboratory populations received as a thorough test of how diet quality influences the life-history trade-offs associated with reproductive investment in a nuptial feeding Australian ground cricket (Pteronemobius sp.). In this species, both males and females make significant contributions to the production of offspring, as males provide a nuptial gift by allowing females to chew on a modified tibial spur during copulation and feed directing on their haemolymph. Individuals also have two distinct wing morphs, a short-winged flightless morph and a long-winged morph that has the ability to disperse. By manipulating the quality of diet over seven generations, we found that the reproductive investment of males and females were affected differently by the diet quality treatment and wing morph of the individual. We discuss the broader implications of these findings including the differences in how males and females balance current and future reproductive effort in nuptial feeding insects, the changing nature of sexual selection when diets vary, and how the life-history trade-offs associated with the ability to disperse are expected to differ among populations.

Natural flightless morphs of the ladybird beetle Adalia bipunctata improve biological control of aphids on single plants

The challenge of using ladybird beetles for biological control of insect pests such as aphids is that the adult beetles tend to fly away from the host plants. Therefore, flightless ladybirds might improve biocontrol. There are several artificial ways to obtain flightless beetles, but it may be preferable to use natural variation in flight ability. We investigated, for the first time, biocontrol by inundative augmentation of natural flightless morphs of the ladybird beetle Adalia bipunctata. Microcosm experiments using single leaves with one of three species of aphid revealed no differences in consumption behavior between flightless and winged beetles. Monitoring for 48 h of single, caged pepper plants infested with aphids of Myzus persicae nicotianae or Aulacorthum solani showed that flightless beetles had a longer residence time on the plants than winged beetles. This only translated into significantly better biocontrol of M. persicae. Despite their difference in residence time, both beetle morphs reduced the population growth of A. solani. This is probably explained by the tendency of A. solani to drop from the plant upon disturbance, and we predict that flightless beetles may outperform winged ones in the long term. Overall, our results provide a proof of principle that natural flightless A. bipunctata can improve biocontrol of aphids by ladybird beetles. However, we recognize that the effect of biocontrol will vary with the species of aphid used and that further examination in long term and large scale experiments is required.

THE ENDOCRINE-GENETIC BASIS OF LIFE-HISTORY VARIATION: THE RELATIONSHIP BETWEEN THE ECDYSTEROID TITER AND MORPH-SPECIFIC REPRODUCTION IN THE WING-POLYMORPHIC CRICKET GRYLLUS FIRMUS

Abstract The hormonal basis of variation in life‐history traits is a poorly studied topic in life‐history evolution. An important step in identifying the endocrine‐genetic causes of life‐history variation is documenting statistical and functional associations between hormone titers and genotypes/phenotypes that vary in life‐history traits. To this end, we compared the blood ecdysteroid titer and the mass of the ovaries during the first week of adulthood among a flight‐capable morph and two flightless morphs of the wing‐polymorphic cricket Gryllus firmus. Ecdysteroids are a group of structurally related hormones that regulate many important aspects of reproduction in insects. Both the ecdysteroid titer and ovarian mass were significantly higher in each of two flightless morphs compared with the flightcapable morph throughout the first week of adulthood. Genetically based differences in the ecdysteroid titer and ovarian mass between morphs from different selected lines were similar to phenotypically based differences among morphs from the same control (unselected) lines. By day 7 of adulthood, ovaries were typically 200–400% larger and the ecdysteroid titer was 60–300% higher in flightless versus the flight‐capable morph. In addition, highly significant, positive, phenotypic correlations were observed between the ecdysteroid titer and ovarian mass in pooled samples of the two flightless and flight‐capable crickets from control lines or from selected lines. The ecdysteroid titer was sufficiently elevated in the flightless morphs to account for their elevated ovarian growth. This is the first direct documentation that naturally occurring phenotypes/genotypes that differ in early fecundity, a key life‐history trait, also differ phenotypically and genetically in the titer of a key reproductive hormone that potentially regulates that trait.

Intermediary Metabolism and Life‐History Trade‐Offs: Differential Metabolism of Amino Acids Underlies the Dispersal‐Reproduction Trade‐Off in a Wing‐Polymorphic Cricket

Although the differential flow of metabolites through alternate pathways of intermediary metabolism is thought to be an important functional cause of life-history trade-offs, this phenomenon remains understudied. Using a radiolabeled amino acid, we quantified genetic differences in in vivo amino acid metabolism between morphs of the wing-polymorphic cricket Gryllus firmus that trade off early-age reproduction and dispersal capability. Lines selected for the flight-capable morph, which delays reproduction, oxidized a greater proportion of radiolabeled glycine and converted a greater amount into somatic lipid, mainly triglyceride (flight fuel). By contrast, lines selected for the flightless, reproductive morph converted a substantially greater proportion of glycine into ovarian protein. Compensatory interactions between amino acid and lipid metabolism make up a key aspect of specialization for dispersal versus reproduction in G. firmus: increased oxidation of amino acids by the flight-capable morph spares fatty acid for enhanced conversion into triglyceride flight fuel. By contrast, increased oxidation of fatty acid by the flightless morph spares amino acids for enhanced biosynthesis of ovarian protein. Studies of amino acid and lipid metabolism in G. firmus currently represent the most detailed analyses of genetic modifications of intermediary metabolism that underlie a functionally important life-history trade-off found in natural populations.

Biochemical basis of specialization for dispersal vs. reproduction in a wing-polymorphic cricket: Morph-specific metabolism of amino acids

The biochemical basis of specializations for dispersal vs. reproduction is an understudied aspect of dispersal polymorphism in insects. Using a radiolabelled amino acid, we quantified differences in in vivo amino acid metabolism between morphs of the wing-polymorphic cricket, Gryllus firmus, that trade-off early age reproduction and dispersal capability. Studies were conducted in crickets fed a variety of diets expected to influence amino acid and lipid metabolism. On the day of molt to adulthood, prior to the morph-specific trade-off between ovarian growth and biochemical preparation for flight (e.g. biosynthesis of triglyceride flight fuel), morphs did not differ in any aspect of amino acid metabolism. However, on day 5 of adulthood, when the morph-specific trade-off between ovarian growth and flight fuel production was manifest, the morphs differed substantially in each of the three aspects of amino acid metabolism studied: conversion to protein, oxidation, and conversion to lipid. Morphs also differed in degree of allocation of products of amino acid metabolism to ovaries vs. the soma. Most importantly, morphs differed in the relative metabolism of radiolabelled glycine through these pathways (i.e. biochemical trade-offs), and in the relative allocation of end products of amino acid metabolism to the soma vs. ovaries (allocation trade-offs). A functionally important interaction between amino acid and lipid metabolism was noted: greater oxidation of amino acids in the flight-capable morph spared fatty acids for enhanced conversion into triglyceride flight fuel. By contrast, greater oxidation of fatty acids by the flightless morph spared amino acids for enhanced conversion into ovarian protein. Diet significantly affected amino acid metabolism. However, MORPH×DIET interactions were rare and morphs differed in amino acid metabolism to a similar degree under the range of diets tested.

Intermediary Metabolism and Life-History Trade-offs: Differential Metabolism of Amino Acids Underlies the Dispersal-Reproduction Trade-off in a Wing-Polymorphic Cricket

Although the differential flow of metabolites through alternate pathways of intermediary metabolism is thought to be an important functional cause of life‐history trade‐offs, this phenomenon remains understudied. Using a radiolabeled amino acid, we quantified genetic differences in in vivo amino acid metabolism between morphs of the wing‐polymorphic cricket Gryllus firmus that trade off early‐age reproduction and dispersal capability. Lines selected for the flight‐capable morph, which delays reproduction, oxidized a greater proportion of radiolabeled glycine and converted a greater amount into somatic lipid, mainly triglyceride (flight fuel). By contrast, lines selected for the flightless, reproductive morph converted a substantially greater proportion of glycine into ovarian protein. Compensatory interactions between amino acid and lipid metabolism make up a key aspect of specialization for dispersal versus reproduction in G. firmus: increased oxidation of amino acids by the flight‐capable morph spares fatty acid for enhanced conversion into triglyceride flight fuel. By contrast, increased oxidation of fatty acid by the flightless morph spares amino acids for enhanced biosynthesis of ovarian protein. Studies of amino acid and lipid metabolism in G. firmus currently represent the most detailed analyses of genetic modifications of intermediary metabolism that underlie a functionally important life‐history trade‐off found in natural populations.

Intermediary Metabolism and Life History Trade-offs: Lipid Metabolism in Lines of the Wing-polymorphic Cricket, Gryllus firmus, Selected for Flight Capability vs. Early Age Reproduction

The extent to which modifications in intermediary metabolism contribute to life history variation and trade-offs is an important but poorly understood aspect of life history evolution. Artificial selection was used to produce replicate genetic stocks of the wing-polymorphic cricket, Gryllus firmus, that were nearly pure-breeding for either the flight-capable (LW[f]) morph, which delays ovarian growth, or the flightless (SW) morph, which exhibits enhanced early-age fecundity. LW(f) lines accumulated substantially more triglyceride, the main flight fuel in Gryllus, compared with SW-selected lines, and enhanced accumulation of triglyceride was strongly associated with reduced ovarian growth. Increased triglyceride accumulation in LW(f) lines resulted from elevated de novo biosynthesis of fatty acid and two morph-specific trade-offs: (1) greater proportional utilization of fatty acid for glyceride biosynthesis vs. oxidation, and (2) a greater diversion of fatty acids into triglyceride vs. phospholipid biosynthesis. Even though SW lines produced less total lipid and triglyceride, they produced more phospholipid (important in egg development) than did LW(f) lines. Differences between LW(f) and SW morphs in lipid biosynthesis resulted from substantial alterations in the activities of all studied lipogenic enzymes, a result that is consistent with expectations of Metabolic Control Theory. Finally, application of a juvenile hormone analogue to LW(f) females produced a striking SW phenocopy with respect to all aspects of lipid metabolism studied. Global alterations of lipid metabolism, most likely produced by alterations in endocrine regulation, underlie morph specializations for flight vs. early-age fecundity in G. firmus. Modification of the endocrine control of intermediary metabolism is likely to be an important mechanism by which intermediary metabolism evolves and contributes to life history evolution.