Wing-dimorphic Insects Research Articles

Pea aphid winged and wingless males exhibit reproductive, gene expression, and lipid metabolism differences.

Alternative, intraspecific phenotypes offer an opportunity to identify the mechanistic basis of differences associated with distinctive life history strategies. Wing dimorphic insects, in which both flight-capable and flight-incapable individuals occur in the same population, are particularly well-studied in terms of why and how the morphs trade off flight for reproduction. Yet despite a wealth of studies examining the differences between female morphs, little is known about male differences, which could arise from different causes than those acting on females. Here we examined reproductive, gene expression, and biochemical differences between pea aphid (Acyrthosiphon pisum) winged and wingless males. We find that winged males are competitively superior in one-on-one mating circumstances, but wingless males reach reproductive maturity faster and have larger testes. We suggest that males tradeoff increased local matings with concurrent possible inbreeding for outbreeding and increased ability to find mates. At the mechanistic level, differential gene expression between the morphs revealed a possible role for activin and insulin signaling in morph differences; it also highlighted genes not previously identified as being functionally important in wing polymorphism, such as genes likely involved in sperm production. Further, we find that winged males have higher lipid levels, consistent with their use as flight fuel, but we find no consistent patterns of different levels of activity among five enzymes associated with lipid biosynthesis. Overall, our analyses provide evidence that winged versus wingless males exhibit differences at the reproductive, gene expression, and biochemical levels, expanding the field's understanding of the functional aspects of morph differences.

Environmental Factors Predicting Dispersal Mode of the Wing-Dimorphic Psammophilous Beetle Mecynotarsus niponicus Lewis, 1895 (Coleoptera: Anthicidae) in a Sandy Floodplain: An Exploratory Analysis

Wing-dimorphic insects occur in diverse habitats in heterogeneous environments. However, little is known about the wing dimorphism of insects that inhabit floodplains and the possible environmental factors affecting their wing morphs. In this study, we used cantharidin-baited traps to collect and quantify the psammobiont beetle Mecynotarsus niponicus Lewis, 1895 (Anthicidae) in a sandy floodplain of the Tamagawa River, Japan, in a one-year repeated cross-sectional study design. Our analysis of the demographic characteristics of over 400 M. niponicus adults and public weather-related data showed that: 1) two distinct wing morphs, long-winged (macropterous) and short-winged (brachypterous) individuals, were present within the population; 2) macroptery rates were consistently lower but varied greatly (6.7–50.0%) within a year; and 3) higher macroptery was significantly associated with greater fluctuation in river water level, namely flooding (odds ratio, 2.96; 95% confidence interval, 1.78–4.91; P < 0.001). Thus, the macropterous form of M. niponicus may be advantageous in avoiding temporal habitat loss due to river flooding. These observations may represent a first step toward testing a flooding-dispersal hypothesis for the morph alteration of wing-dimorphic insects in floodplains.

A Review of the Phenotypic Traits Associated with Insect Dispersal Polymorphism, and Experimental Designs for Sorting out Resident and Disperser Phenotypes.

Dispersal represents a key life-history trait with several implications for the fitness of organisms, population dynamics and resilience, local adaptation, meta-population dynamics, range shifting, and biological invasions. Plastic and evolutionary changes of dispersal traits have been intensively studied over the past decades in entomology, in particular in wing-dimorphic insects for which literature reviews are available. Importantly, dispersal polymorphism also exists in wing-monomorphic and wingless insects, and except for butterflies, fewer syntheses are available. In this perspective, by integrating the very latest research in the fast moving field of insect dispersal ecology, this review article provides an overview of our current knowledge of dispersal polymorphism in insects. In a first part, some of the most often used experimental methodologies for the separation of dispersers and residents in wing-monomorphic and wingless insects are presented. Then, the existing knowledge on the morphological and life-history trait differences between resident and disperser phenotypes is synthetized. In a last part, the effects of range expansion on dispersal traits and performance is examined, in particular for insects from range edges and invasion fronts. Finally, some research perspectives are proposed in the last part of the review.

Effects of flight and food stress on energetics, reproduction, and lifespan in the butterfly Melitaea cinxia

Environmental change can have drastic effects on natural populations. To successfully predict such effects, we need to understand how species that follow different life-history strategies respond to stressful conditions. Here I focus on two stressors, increased flight and dietary restriction, and their effects on bioenergetics and life-history. Using the Glanville fritillary butterfly (Melitaea cinxia), I subjected mated females to three treatments: (1) control conditions, (2) repeated forced flight with unlimited food, and (3) repeated forced flight coupled with food restriction. Interestingly, flight increased fecundity: females in both flight treatments initiated oviposition earlier, laid more egg clutches, and had higher total fecundity than control females. However, food-restriction by 50% reduced clutch size and resulted in an approximately 25% decrease in total fecundity compared to flown females with unlimited food. There were no differences in egg wet mass, water content or hatching success. Flown females with unlimited food appeared to exhibit a trade-off between reproduction and lifespan: they had higher mass-independent resting metabolic rate and shorter lifespan than females in the other treatments. Mass-independent flight metabolic rate, reflecting flight capacity, did not differ among the treatments. There were no differences in the rate of metabolic senescence across the treatments. The current findings suggest a mechanistic link between flight and reproduction, potentially mediated by juvenile hormone signalling. It appears that this wing-monomorphic butterfly does not show an oogenesis-flight trade-off often found in wing-dimorphic insects. Nevertheless, nectar-feeding is needed for achieving maximum reproductive output, suggesting that diminishing nectar resources may negatively impact natural populations.

Variation in fighting strategies in male wing-dimorphic crickets (Gryllidae)

Because a trade-off between reproduction and dispersal has been commonly found in wing-dimorphic insects, males of different wing morphs may have a different demand on a mate or a territory. We hypothesized that males of wing-dimorphic insects may vary in fighting success over these two resources. To test this hypothesis, we compared morphological traits linked to fighting ability between long-winged (LW) and short-winged (SW) male Velarifictorus aspersus crickets (Gryllidae) and investigated their fighting success over a burrow or a mate. SW males gained more biomass than did LW males after molting to adulthood, indicating that morphological traits that can influence fighting ability differed between wing-dimorphic male crickets (Gryllidae). SW males won significantly more fights than did LW males when fighting for a mate. However, LW males were more aggressive than SW males when intruding the burrow of another male, and the winning probability of LW intruders was significantly greater than that of SW defenders. Fighting outcome significantly influenced the ownership of resources, and winning could help crickets (Gryllidae) become more successful in acquisition of the target resource. Our results suggested that trade-offs between life-history traits result in the differentiation of fighting strategies, such that both winged forms could succeed with their particular life-history strategy.

Gene Expression Profiling in Winged and Wingless Cotton Aphids, Aphis gossypii (Hemiptera: Aphididae)

While trade-offs between flight capability and reproduction is a common phenomenon in wing dimorphic insects, the molecular basis is largely unknown. In this study, we examined the transcriptomic differences between winged and wingless morphs of cotton aphids, Aphis gossypii, using a tag-based digital gene expression (DGE) approach. Ultra high-throughput Illumina sequencing generated 5.30 and 5.39 million raw tags, respectively, from winged and wingless A. gossypii DGE libraries. We identified 1,663 differentially expressed transcripts, among which 58 were highly expressed in the winged A. gossypii, whereas 1,605 expressed significantly higher in the wingless morphs. Bioinformatics tools, including Gene Ontology, Cluster of Orthologous Groups, euKaryotic Orthologous Groups and Kyoto Encyclopedia of Genes and Genomes pathways, were used to functionally annotate these transcripts. In addition, 20 differentially expressed transcripts detected by DGE were validated by the quantitative real-time PCR. Comparative transcriptomic analysis of sedentary (wingless) and migratory (winged) A. gossyii not only advances our understanding of the trade-offs in wing dimorphic insects, but also provides a candidate molecular target for the genetic control of this agricultural insect pest.

Phytohormone-mediated plant resistance and predation risk act independently on the population growth and wing formation of potato aphids, Macrosiphum euphorbiae

Aphids increase production of winged individuals as a generalized response to multiple threats, including predators, competitors, and poor host plant quality. While wing formation in response to these individual threats is well documented, few investigations have evaluated whether combined threats lead to additive or non-additive outcomes. We tested the interactive effects of predation risk and plant quality on population growth and wing induction in the potato aphid, Macrosiphum euphorbiae. Plant quality was varied using phytohormonal manipulations of tomato (Solanum lycopersicum) to elevate or suppress the jasmonate and salicylate defense pathways. Predation risk was altered by exposing aphids to lethal or risk (unable to feed) individuals of the convergent lady beetle, Hippodamia convergens. Phytohormonal treatments resulted in >4-fold variation in aphid population growth and thus strongly affected plant quality; however, the percentage of winged individuals was no different across plant types. Predators similarly reduced aphid abundance, but also elicited a ~3-fold increase in wing formation, an effect that was similar in magnitude when comparing lethal with risk predators. The overall impact of plants and predators on aphids was largely additive, an outcome that was unexpected given the likelihood for interactions between these two factors and our prior results with other herbivores in this system. We discuss this discrepancy in the context of phenotypic plasticity, non-lethal predator effects, and the ecological challenges faced by wing dimorphic insects.

The role of macropters during range expansion of a wing-dimorphic insect species

Marked changes in distribution in consequence of global warming have been observed not only for highly mobile insect taxa, which are capable of flight, but also for wing-dimorphic species with predominantly short-winged individuals. In the special case of wing-dimorphic species, it is likely that the rarer long-winged (macropterous) morph plays an important role in the dispersal process, but little is known about how and to what extent it is involved. The aim of our study was to provide more information on the mechanisms behind dispersal processes in wing-dimorphic insects at expanding range margins. As solitary individuals are believed to play an important role in the range expansion of wing-dimorphic species (potential dispersers), we recorded the number of long-winged and short-winged solitary males at the local range margin of our model organism Metriopteraroeselii (Orthoptera: Tettigoniidae) in NW Germany. To investigate differences in dispersal capability (% macropters) between populations with different colonisation histories, we studied 43 populations of M. roeselii. Our results show that about 2/3 of the solitary males were long-winged and these long-winged individuals were significantly more frequent in recently colonised areas. Moreover, M. roeselii had a significantly higher dispersal capability (% macropters) in high-density populations and in recently established populations at the expanding range margin compared to populations characterised by medium- or long-term establishment nearer to the range core. Our study is the first that quantifies the importance of macropters for the recent range expansion of a wing-dimorphic species and it provides for the first time detailed insights into the complex dispersal processes that take place at the expanding range margin. It is likely that density stress and a changed genetic predisposition to become macropterous, and thus a combination of both ecological and evolutionary effects, leads to a high percentage of macropters in recently colonised areas.

Does wing dimorphism affect mobility in Metrioptera roeselii (Orthoptera: Tettigoniidae)?

Range shifts are among the most conspicuous effects of global warming. Marked changes in distribution are recorded both for highly mobile species of insects, which are capable of flight, and wing-dimorphic species with predominantly short-winged individuals. One of these species is the bush-cricket Metrioptera roeselii, which occasionally produces long-winged individuals. However, there is little known about the locomotory behaviour of wing-dimorphic insects. Yet to be able to predict potential range shifts it is necessary to know the dispersal potential of macropters. Therefore, an experiment was conducted in which individually marked M. roeselii were released at four sites. Different movement parameters, such as daily movement, activity radius, dispersal range, net displacement and crowding rate, were calculated. The statistical analyses showed that the movement of long-winged and short-winged individuals did not differ, but the percentage of individuals that were not seen again was twice as high for long-winged bush-crickets. These results suggest that most of the long-winged individuals that were seen again did not fly; i.e., they had the same basic mobility as the short-winged individuals. However, the comparatively low number of long-winged individuals that were seen again suggests that at least some macropters are long-distance dispersers, which is relevant for the dispersal process. The comparison of sexes showed that males were significantly more mobile than females. This sex-specific locomotory behaviour in M. roeselii might depend on a complex series of social interactions and physiological conditions.

Evaluating the life-history trade-off between dispersal capability and reproduction in wing dimorphic insects: a meta-analysis

A life-history trade-off exists between flight capability and reproduction in many wing dimorphic insects: a long-winged morph is flight-capable at the expense of reproduction, while a short-winged morph cannot fly, is less mobile, but has greater reproductive output. Using meta-analyses, I investigated specific questions regarding this trade-off. The trade-off in females was expressed primarily as a later onset of egg production and lower fecundity in long-winged females relative to short-winged females. Although considerably less work has been done with males, the trade-off exists for males among traits primarily related to mate acquisition. The trade-off can potentially be mitigated in males, as long-winged individuals possess an advantage in traits that can offset the costs of flight capability such as a shorter development time. The strength and direction of trends differed significantly among insect orders, and there was a relationship between the strength and direction of trends with the relative flight capabilities between the morphs. I discuss how the trade-off might be both under- and overestimated in the literature, especially in light of work that has examined two relevant aspects of wing dimorphic species: (1) the effect of flight-muscle histolysis on reproductive investment; and (2) the performance of actual flight by flight-capable individuals.

Modeling the Evolution of Phenotypic Plasticity in Resource Allocation in Wing‐Dimorphic Insects

In nature, resource availability varies spatially and temporally both within and across generations, leading to variation in the amount of energy available to individuals. The optimal allocation strategy can change, depending on the amount of resources available to allocate to life-history functions. If so, selection should favor the evolution of allocation strategies that can respond to variation in environmental resource levels. We address this issue by using two quantitative genetic simulation models in a model system for studying trade-offs, wing-dimorphic insects. Wing dimorphic insects typically exhibit a trade-off in the allocation of resources between migratory ability and reproduction. In our models, we focus on allocation as a genetic trait and model the evolution of phenotypic plasticity in this trait in response to spatiotemporal variation in resource availability. We show that the evolved allocation strategy depends on the predictability of resource levels across time. Specifically, selection favors higher investment in flight under poor conditions in predictable environments and lower investment in unpredictable environments.

Rapid range expansion of a wing-dimorphic bush-cricket after the 2003 climatic anomaly

During recent decades, many species have responded to global warming by poleward range expansions. We require a better mechanistic understanding of the nature and extent of such processes to assess how climate change might affect biodiversity. Wing-dimorphic bush-crickets are excellent objects to study dispersal and colonization processes at the range margin because the long-winged morphs (macropters) represent dispersal units of otherwise flightless species. Moreover, these insects produce noisy songs and can easily be mapped. The present study comprised a detailed investigation of the population dynamics and genetics at the edge of the range of Roesel’s bush-cricket, Metrioptera roeselii. We mapped the distribution of this insect in a previously unoccupied area of 185 km 2 and examined the genetic structure at the range margin using four polymorphic microsatellite loci. The results obtained demonstrate that the European heat wave in 2003 induced a strong immigration of macropters in the area stemming from multiple sources, whereas only few immigrants were recorded in the two subsequent years. Macropters were genotyped in a distance of up to 19.1 km from their origin, considerably exceeding the known dispersal distances for this species. Moreover, the data show that strong local founder effects are equalized on a large scale by the high number of immigrants from multiple sources. The present study demonstrates that macropters are of high significance for the range expansion of wing-dimorphic insects because a single-year climatic anomaly can induce strong dispersal processes. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 118‐127.

Mobility and lifetime fecundity in new versus old populations of the Glanville fritillary butterfly

Life history theory often assumes a trade-off between dispersal and reproduction, and such a trade-off is commonly observed in wing-dimorphic insects. The results are less consistent for wing-monomorphic species, for which it is more difficult to assess dispersal capacity and rate. Three replicate experiments were carried out in consecutive years on the Glanville fritillary butterfly in a large outdoor population cage to study the relationship between lifetime egg production and mobility. The experimental material included females originating from newly-established and old populations, as previous studies have shown dispersal capacity to depend on population age. There was a consistent and significant interaction between mobility and population age, such that in newly-established populations mobile females had higher fecundity than less mobile females, while in old populations there was no such relationship. As selection favours individuals with the highest fecundity, selection pressure on mobility is likely to be different between the two population types, which may contribute to maintenance of variation in dispersal rate in the metapopulation as a whole. Several other female traits also affected lifetime fecundity, including lifespan, number of matings and date of eclosion, although these effects were not consistent across the years. These results highlight the importance of conducting experiments in more than one year before generalizing about patterns in life history variation.

Energy Allocation in Brachypterous versus Macropterous Morphs of the Pygmy Grasshopper Tetrix subulata (Orthoptera: Tetrigidae)

In wing dimorphic insects, there exists a trade-off between dispersal and reproduction. The brachypterous or short-winged morph reproduces faster while the macropterous or long-winged morph is better able to colonize new habitats. In the present study, energy reserves (carbohydrates, proteins and lipids) and energy consumption (derived from the electron transport activity) were quantified in brachypterous and macropterous males and females of the pygmy grasshopper Tetrix subulata (Linnaeus 1758). It was found that the macropterous morph consumes significantly more energy and has a significantly higher protein content in comparison with the brachypterous morph. Both parameters are probably related to better developed wing muscles in the macropterous morphs. No differences were found in carbohydrate and lipid content. It was also observed that energy consumption and protein content were significantly higher in males compared to females. These findings are probably related to the higher activity of males, which spend most of the time searching for females.

The evolution of threshold traits: effects of selection on fecundity and correlated response in wing dimorphism in the sand cricket

Abstract The quantitative genetic basis of traits can be determined using a pedigree analysis or a selection experiment. Each approach is valuable and the combined data can contribute more than either method alone. Analysis using both sib analysis and selection is particularly essential when there are likely to be nonlinearities in the functional relationships among traits. A class of traits for which this occurs is that of threshold traits, which are characterized by a dichotomous phenotype that is determined by a threshold of sensitivity and a continuously distributed underlying trait called the liability. In this case, traits that are correlated with the liability may show a nonlinear relationship due to the dichotomy of expression at the phenotypic level. For example, in wing dimorphic insects fecundity of the macropterous (long-winged) females appears in part to be determined by the allocation of resources to the flight muscles, which are almost invariably small or absent in the micropterous (short-winged, flightless) females. Pedigree analysis of the cricket Gryllus firmus has shown that wing morph, fecundity and the trade-off between the two have additive genetic (co)variance. It has also been shown that selection on proportion macroptery produced an asymmetric correlated response of fecundity. The present paper details the results of direct selection on fecundity and the correlated response in proportion macroptery. Selection for increased fecundity resulted in increased fecundity within both wing morphs and a correlated decrease in proportion macroptery. Similarly, selection for decreased fecundity resulted in a decrease within morphs and a correlated increase in the proportion of macropterous females. This provides additional evidence that the trade-off between fecundity and wing morphology has a genetic basis and will thus modulate the evolution of the two traits.

Physiology and ecology of dispersal polymorphism in insects.

Studies of dispersal polymorphism in insects have played a pivotal role in advancing our understanding of population dynamics, life history evolution, and the physiological basis of adaptation. Comparative data on wing-dimorphic insects provide the most definitive evidence to date that habitat persistence selects for reduced dispersal capability. The increased fecundity of flightless females documents that a fitness trade-off exists between flight capability and reproduction. However, only recently have studies of nutrient consumption and allocation provided unequivocal evidence that this fitness trade-off results from a trade-off of internal resources. Recent studies involving wing-dimorphic insects document that flight capability imposes reproductive penalties in males as well as females. Direct information on hormone titers and their regulation implicates juvenile hormone and ecdysone in the control of wing-morph determination. However, detailed information is available for only one species, and the physiological regulation of wing-morph production remains poorly understood. Establishing a link between the ecological factors that influence dispersal and the proximate physiological mechanisms regulating dispersal ability in the same taxon remains as a key challenge for future research.

Antagonistic and reinforcing pleiotropy: a study of differences in development time in wing dimorphic insects

AbstractMorphological dimorphisms are found in many different taxa. Wing dimorphism in insects, in which some individuals possess wings and associated flight muscles and are thus volant while others lack a functional flight apparatus and are thus flightless, is a typical example of such types of dimorphisms. It has been extensively studied and such studies have demonstrated that the volant form, although possessing the advantage of flight capability, suffers a fitness cost in a delay in the onset of reproduction after emergence into the adult form and a reduced fecundity. Previous comparative analyses have suggested that there is no consistent trend for development time (hatching to adult) to differ between the two morphs. The present study analyses the phenotypic and genetic correlations between development time and wing morph in the cricket Gryllus firmus. It is shown that the macropterous (volant) morph develops faster than the micropterous (flightless morph). This trade‐off is manifested at both thephenotypic and genetic level. Further, a comparative analysis shows that the same phenotypic trade‐off is generally found in other Orthopteran species so far studied, but in other orders the micropterous morph develops faster. Provided that the phenotypic trade‐off is genetically based, in the Orthoptera the fitness advantage of the earlier onset of reproduction in micropterous females is offset by the extended development time (antagonistic pleiotropy). However, in other orders there is reinforcing pleiotropy in that the micropterous females develop faster and reproduce sooner than the macropterous morph. These results highlight the complexity of fitness interactions and the need to study a phenomenon across several taxa.

Wing dimorphism and the migratory syndrome: Correlated traits for migratory tendency in wing dimorphic insects

AbstractThe hypothesis that the morphological, physiological, and behavioral traits comprising the migratory syndrome in insects are genetically correlated through pleiotropic effects of genes controlling the titre of a common hormonal determinant is explored. Evidence that juvenile hormone (JH) influences the component traits of the migratory syndrome is presented, and thus JH is assumed to be the underlying, common determinant. However, readers are cautioned that this does not imply that JH is solely responsible for these traits, nor is this necessary for the arguments presented. For wing dimorphic taxa, the “correlated traits hypothesis” predicts covariance within wing morphs between JH titre and the proportion winged. Four simple genetic models for wing‐morph determination are considered: single‐locus with short‐winged (SW) dominant; single‐locus with long‐winged (LW) dominant; polygenic, fixed threshold, shifting distribution; and polygenic, shifting threshold, fixed distribution. In each case, wing morphology is assumed to be a threshold trait with the liability being JH titre at some critical stage of development. All models predict covariation between %LW and the mean JH titre of at least one of the wing morphs, but the form and direction of the relationship depends critically on the genetic model used. The results suggest that we should expect the traits associated with the migratory syndrome, and hence the trade‐offs associated with the evolution of wing dimorphism, to be correlated with proportion winged and, in this sense, to be frequency‐dependent.

The evolution of dimorphic traits: predicting the genetic correlation between environments.

Many traits vary in a dichotomous manner, although the underlying genetic determination is polygenic. The genetic basis of such dimorphic traits can be analyzed using the threshold model, in which it is assumed that there is a continuously distributed underlying character and the phenotype is determined by whether the character is above or below a threshold. Threshold traits frequently vary with environmental variables such as photoperiod, temperature and density. This effect can be accounted for using a threshold model in which (1) there is a critical value of the environmental variable at which a genotype switches to the alternate morph, and (2) switch (threshold) points are normally distributed in the population. I term this the environmental threshold (ET) model. I show that the ET model predicts that across environments differing in only one factor the genetic correlation will be 1. This prediction is supported by data from three wing dimorphic insects. Evidence is presented that the genetic correlation between environments differing in two components (temperature and photoperiod) is less than 1.

Genetic and ontogenetic variation in behaviour: its possible role in the maintenance of genetic variation in the wing dimorphism of Gryllus firmus

Genetic variation may be preserved in populations by several different modes of behaviour. In this paper we examine the consequences of behaviour on genetic variation in traits that are determined by genetic factors and by environmental conditions experienced during ontogeny. The particular trait considered is wing dimorphism in the sand cricket Gryllus firmus. In this species, as is typical of wing dimorphic insects, the adult wing morph (macropterous or micropterous) is determined by both genetic constitution and the temperature experienced during a specific period of nymphal development. Wing morph may thus be controlled, in part, by the thermal preference of nymphs. The effective heritability of wing morphology will be increased if nymphs with a genetic disposition to a particular wing morph select the temperature that causes that morph to be expressed. By contrast, effective heritability will be decreased if nymphs show no preference, or nymphs select temperatures that reduce phenotypic variation among individuals. During the period of ontogeny when future wing morph is sensitive to temperature, nymphal crickets that are genetically disposed to become macropterous select lower temperatures than crickets that have the opposite genetic disposition. Likewise, nymphs that are being raised under conditions promoting macroptery select lower temperatures than nymphs being raised under conditions favouring microptery. The consequence of this behaviour is that genetic variation for wing morph may be masked, and hence preserved.