Evolutionary genetics of dorsal wing colour in Colias butterflies

The evolution of butterfly wing colouration is strongly affected by its multiple functions and by the correlated evolution of wing colour elements. Both factors may prevent local adaptation to ecological conditions. We investigated one aspect of wing colouration, the degree of dorsal wing melanization, in the butterfly Colias philodice eriphyle across an elevational gradient and its correlation with another aspect of wing colouration, ventral wing melanization. Dorsal wing melanization increased with elevation and these differences persisted in a common environment. Full-sibling analysis revealed high heritability for males but only intermediate heritability for females. The correlation between ventral and dorsal melanization showed significant elevational and sex-specific differences. In males the two traits were highly correlated, whereas in females the strength of the correlation decreased with increasing elevation. We conclude that uncoupling of ventral and dorsal melanization has evolved in females but not in males and discuss possible mechanisms underlying uncoupling.     

Take-off flight performance in the butterfly Pararge aegeria relative to sex and morphology: a quantitative genetic assessment

Adult fitness components may strongly depend on variation in locomotory performance such as flight; this variation can be sex specific. Fast take-off to intercept females and competing males is an essential behavioral component of the territorial perching behavior in male speckled wood butterflies (Pararge aegeria L.). Females on the other hand avoid frequent take-offs particularly under suboptimal temperatures, typically showing fewer but longer flights than males. We estimated the heritability of take-off acceleration performance under suboptimal body temperatures by a restricted maximum-likelihood model. We calculated genetic correlations between this performance and a selection of morphological traits: size (body mass), flight muscle investment (relative thorax mass), and wing shape (forewing aspect ratio). Our results show significant additive genetic variation for mean acceleration performance and a similar but nonsignificant trend (P= 0.08) for maximal acceleration performance during take-off in males (h(2)= 0.15). In females, heritability was not significantly different from zero for either of the acceleration performance measures. Morphological traits and take-off performance were genetically linked in a sex-specific way. In males, relative thorax mass and forewing aspect ratio were positively genetically correlated with acceleration performance. In females, there was a negative genetic correlation between acceleration performance and abdomen mass, but not with residual abdomen mass (i.e., regressed on total body mass). To fully understand the evolution of sexual differences in flight performances and morphology, several other flight performances will have to be included. This multifunctional nature of flight and its consequences for the evolutionary study of flight has not yet been fully appreciated in the literature.     

Phenotypic plasticity and the evolution of trade-offs: the quantitative genetics of resource allocation in the wing dimorphic cricket, Gryllus firmus

In the wing dimorphic sand cricket, Gryllus firmus, there is a pronounced trade-off between flight capability and fecundity. This trade-off is found both between morphs and within the macropterous morph, in which fecundity is negatively correlated with the mass of the principle flight muscles, the dorso-longitudinal muscles (DLM). In this paper, we examine how this trade-off is affected by a reduction in food and its genetic basis. We find that the relative fitness of the two wing morphs is not changed although both fecundity and DLM mass are decreased. A quantitative genetic analysis shows that the trade-off function is genetically variable but that most of the variation occurs in the intercept rather than the slope of the function. Analysis further indicates a very high genetic correlation between environments (food ration) supporting the hypothesis of a strong functional constraint between reproduction and flight capability.     

Melanic through nature or nurture: genetic polymorphism and phenotypic plasticity in Harmonia axyridis

Abstract Individuals can adapt to heterogeneity in their environment through either local adaptation or phenotypic plasticity. Colour forms of the ladybird Harmonia axyridis are a classic example of local adaptation, in which the frequency of melanic forms varies greatly between populations. In some populations, there are also large seasonal changes in allele frequency, with melanism being costly in summer and beneficial in winter. We report that the non‐melanic morph of H. axyridis dramatically increases its degree of melanization at cold temperatures. Furthermore, there is genetic variation in reaction norms, with different families responding to temperature in different ways. Variation at different spatial and temporal scales appears to have selected for either genetic or phenotypically plastic adaptations, which may be important in thermoregulation. As melanism is known to have a large effect on fitness in H. axyridis, this plasticity of melanization may have hastened its spread as an invasive species.     

THE EVOLUTION OF THRESHOLD TRAITS: A QUANTITATIVE GENETIC ANALYSIS OF THE PHYSIOLOGICAL AND LIFE-HISTORY CORRELATES OF WING DIMORPHISM IN THE SAND CRICKET

Many traits are phenotypically discrete but polygenically determined. Such traits can be understood using the threshold model of quantitative genetics that posits a continuously distributed underlying trait, called the liability, and a threshold of response, individuals above the threshold displaying one morph and individuals below the threshold displaying the alternate morph. For many threshold traits the liability probably consists of a hormone or a suite of hormones. Previous experiments have implicated juvenile hormone esterase (JHE), a degratory enzyme of juvenile hormone, as a physiological determinant of wing dimorphism in the crickets Gryllus rubens and G. firmus. The present study uses a half-sib experiment to measure the heritability of JHE in the last nymphal stadium of G. firmus and its genetic correlation with fecundity, a trait that is itself genetically correlated with wing morph. The phenotypic and genetic parameters are consistent with the hypothesis that JHE is a significant component of the liability. Comparison of sire and dam estimates suggest that nonadditive effects may be important. Two models have been proposed to account for the fitness differences between morphs: the dichotomy model, which assumes that each morph can be characterized by a particular suite of traits, and the continuous model, which assumes that the associated fitness traits are correlated with the liability rather than the morphs themselves. The latter model predicts that the fitness differences will not be constant but change with the morph frequencies. Variation in fecundity and flight muscle histolysis are shown to be more consistent with the continuous model. Data from the present experiment on JHE are inconclusive, but results from a previous selection experiment also suggest that variation in JHE is consistent only with the continuous model.     

Environmental stress and quantitative genetic variation in butterfly wing characteristics

Butterfly wing characteristics are extensively used as model system in studies of development, quantitative genetics and phenotypic plasticity. In spite of its evolutionary relevance, however, the effect of stress on the expression of genetic variation itself has only rarely been studied. In this paper, we explore genetic variation of wing characteristics of the Speckled wood Pararge aegeria along a host plant drought stress gradient. Forewing area, basal and distal degree of melanization and the area of five yellow wing spots were measured. We found an increase in (additive) genetic variation in degree of melanization at higher drought stress, and a similar, yet non-significant, relationship for forewing size. As a result, both the upper limits of the narrow-sense heritability and the coefficient of additive genetic variation of wing size and melanization increased with drought stress. Patterns for the different yellow wing spots were less consistent, suggesting trait-specificity in the relationships between genetic variation and environmental stress.     

Genetic and phenotypic relationships between immune defense,melanism and life-history traits at different temperatures and sexes in Tenebrio molitor

Insect cuticle melanism is linked to a number of life-history traits, and a positive relationship is hypothesized between melanism and the strength of immune defense. In this study, the phenotypic and genetic relationships between cuticular melanization, innate immune defense, individual development time and body size were studied in the mealworm beetle (Tenebrio molitor) using three different temperatures with a half-sib breeding design. Both innate immune defense and cuticle darkness were higher in females than males, and a positive correlation between the traits was found at the lowest temperature. The effect of temperature on all the measured traits was strong, with encapsulation ability and development time decreasing and cuticle darkness increasing with a rise in temperature, and body size showing a curved response. The analysis showed a highly integrated system sensitive to environmental change involving physiological, morphological and life-history traits.     

Morphological and physiological sexual selection targets in a territorial damselfly

• 1 Several morphological and physiological traits may shape fitness through the same performance measure. In such cases, differentiating between a scenario of many‐to‐one mapping, where phenotypic traits independently shape fitness leading to functional redundancy, and a scenario where traits strongly covary among each other and fitness, is needed.
• 2 A multivariate approach was used, including morphological and physiological traits related to flight ability, a crucial performance measure in flying insects, to identify independent correlates of short‐term mating success (mated versus unmated males) in the territorial damselfly Lestes viridis.
• 3 Males with higher flight muscle mass, higher relative thorax mass, and more symmetrical hindwings, all traits presumably linked to manoeuvrability, were more likely to be mated. Unexpectedly, although relative thorax mass is often used as a proxy for flight muscle mass, both traits were selected for independently. Mated males had a higher thorax fat content than unmated males, possibly because of enhanced flight endurance.
• 4 The finding of several independent targets of sexual selection linked to flight ability is consistent with a scenario of many‐to‐one mapping between phenotype and performance. Identifying such a scenario is important, because it may clarify situations where animals may show suboptimal values for some phenotypic traits shaping a performance measure, while still having high performance and fitness. We argue in the discussion that the functional approach of sexual selection provides a potent tool for examining unresolved issues in both sexual selection theory, as well as life‐history theory.

     

The common quantitative genetic basis of wing morphology and diapause occurrence in the cricket Gryllus veletis

A covariation between wing morphology and diapause occurrence has been observed in many insect species, but the genetic basis of this covariation has never been established. This study measures the heritability of, and genetic correlation between, these two ecologically important threshold traits in the cricket Gryllus veletis. A total of 81 full-sib families were reared in the laboratory to estimate these parameters. A comparison of laboratory and field samples showed that these two traits are highly plastic. The heritability of wing morphology was 0.25 (0.09), the heritability of diapause occurrence was 0.77 (0.11) and the genetic correlation between them was 0.61 (0.19). These estimates did not differ between males and females. The significance of these quantitative genetic parameters is discussed with reference to the monomorphism of natural populations of G. veletis for diapause occurrence and with reference to the trade-off between the ability to disperse by flight and the ability to diapause found in at least one closely related species. A survey of the literature reveals that genetic correlations between diapause occurrence or wing morphology and various other traits are common in insects, suggesting that these two traits are often genetically integrated in insect life-histories.     

Responses of disparate phenotypically-plastic,melanin-based traits to common cues: limits to the benefits of adaptive plasticity?

The evolution of perfect adaptive phenotypic plasticity of a given trait may be influenced by, among other things, phenotypic costs associated with the expression of a given trait value, relative to alternative trait values. One potential cause of such phenotypic costs is the allocation of limited resources to multiple traits. When multiple traits rely on the same resource, trait values for one adaptively plastic trait might be unavoidably associated with maladaptive trait values for other traits. I address this problem in three traits of Pieris rapae L. (the small cabbage white butterfly) that all rely on the pigment melanin and are adaptively plastic, but have very different functions: wing pattern, immune defense, and pupal color. Cool, short-day rearing conditions simultaneously increased total wing melanization and decreased a melanin-based immune response in females, consistent with predictions. However, cool, short days also reduced the melanin-based immune response in males, despite little effect on male wing melanization. Furthermore, contrary to predictions, these patterns were not altered by differences in dietary resources. Finally, dark-colored rearing backgrounds during pupation substantially increased pupal melanization in both sexes, but was not associated with differences in wing melanization. These results offer only mixed support for the hypothesis of melanin-based trade offs as a source of phenotypic costs to adaptive plasticity in these traits. However, patterns of sexual dimorphism for these traits suggest trade offs might be at work at another level: relative to males, females have consistently more heavily melanized wings but less heavily melanized pupae and immune responses. The reduced immune response under cool, short-day conditions may also have implications for the evolutionary ecology of these butterflies.     

Path analysis of the genetic integration of traits in the sand cricket: a novel use of BLUPs

This study combines path analysis with quantitative genetics to analyse a key life history trade-off in the cricket, Gryllus firmus. We develop a path model connecting five traits associated with the trade-off between flight capability and reproduction and test this model using phenotypic data and estimates of breeding values (best linear unbiased predictors) from a half-sibling experiment. Strong support by both types of data validates our causal model and indicates concordance between the phenotypic and genetic expression of the trade-off. Comparisons of the trade-off between sexes and wing morphs reveal that these discrete phenotypes are not genetically independent and that the evolutionary trajectories of the two wing morphs are more tightly constrained to covary than those of the two sexes. Our results illustrate the benefits of combining a quantitative genetic analysis, which examines statistical correlations between traits, with a path model that focuses upon the causal components of variation.     

Heritability of flight distance for Cydia pomonella

Cydia pomonella L. (Lepidoptera: Tortricidae) is considered to be rather sedentary, but some individuals undertake flights of several kilometres in the field. This paper investigates the genetic influence on this variability. The flight capacity was measured in the laboratory by a flight mill and its heritability was estimated for two different strains. The laboratory strain was kept for more than 45 generations and the field strain from Embrach (northern Switzerland) was recently collected in the field.The multiple-trait-restricted-maximum-likelihood method was used for the estimation of genetic variances and covariances. A mixed full-sib/half-sib design was applied for the field strain and a full-sib design for the laboratory strain. The heritability of total distance was 0.57 for the field strain and 0.37 for the laboratory strain (both sexes). In addition, a heritability of 0.38 for total distance was estimated by parent-offspring regression for the laboratory strain. All three values were significantly different from zero P<0.05 and show that there is a significant additive genetic influence on flight capacity.The genetic correlations between total distance and other flight traits (total duration, flight velocity, longest flight) were between 0.84 and 1.00 for both strains and suggest that these traits actually belong to a single one. High genetic correlations were also found between total distance and the morphological traits body weight and wing length for the field strain, whereas a negative correlation was found between total flight distance and body weight for the laboratory strain. This difference between the two strains was interpreted as a possible trade-off between flight capacity and fecundity.     

Intraspecific variation in wing and pupal melanization in copper butterflies (Lepidoptera: Lycaenidae)

Melanin is a widespread pigment causing variation in skin darkness, with darker phenotypes typically reaching higher equilibrium temperatures than lighter ones. Therefore, selection is expected to favour darker phenotypes in colder environments. In the present study, we show intraspecific variation in pupal (and wing) melanization along an altitudinal gradient in two species of copper butterflies. Both, pupal and wing melanization increased with increasing altitude. Consistent with the thermal melanism hypothesis, darker (high-altitude) pupae reached higher equilibrium temperatures than paler (low-altitude) ones. However, as temperature differences were rather small despite pronounced differences in melanization, we cannot rule out that factors (e.g. ultraviolet protection, disease resistance) other than temperature comprise the principal selective agents. Mechanistically, variation in melanization might be related to variation in hormone titres, as demonstrated by low-altitude pupae showing higher ecdysteroid and juvenile hormone titres compared to high-altitude ones. Furthermore, we report sex differences in wing melanization, with males being darker than females, which is potentially related to a higher flight activity of males.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 301–312.     

GENETIC CORRELATIONS AMONG TRAITS DETERMINING MIGRATORY TENDENCY IN THE SAND CRICKET,GRYLLUS FIRMUS

Migration by flight is an important component of the life cycles of most insects. The probability that a given insect will migrate by flight is influenced by many factors, most notably the presence or absence of fully-developed wings and functional flight musculature. Considerable variation has also been reported in the flight propensity of fully-winged individuals with functional flight musculature. We test the hypothesis that these components of migratory tendency are genetically correlated in a wing-dimorhic cricket, Gryllus firmus. Flight propensity and condition of the dorsal longitudinal flight muscles (DLM) are examined in fully-winged (LW) crickets from lines selected for increasing and for decreasing %LW, as well as from unselected control lines. Increased %LW is found to be associated with increased flight propensity among individuals with intact DLM, and with retention of functional DLM. The opposite is true for lines selected for decreased %LW. These results indicate both phenotypic and genetic correlations among behavioral, physiological, and morphological traits determining migratory tendency. We propose that these correlations may result from the multifunctional role of juvenile hormone, which has been reported to influence wing development, flight muscle development and degeneration, and flight propensity. Finally, we discuss the potential influence of genetic correlations for migratory traits on the evolution and maintenance of migratory polymorphisms in insects.     

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.     

Heritability of resting metabolic rate in a wild population of blue tits

We report the first study with the aim to estimate heritability in a wild population, a nest box breeding population of blue tits. We estimated heritability as well as genetic and phenotypic correlations of resting metabolic rate (RMR), body mass and tarsus length with an animal model based on data from a split cross‐fostering experiment with brood size manipulations. RMR and body mass, but not tarsus length, showed significant levels of explained variation but for different underlying reasons. In body mass, the contribution to the explained variation is mainly because of a strong brood effect, while in RMR it is mainly because of a high heritability. The additive variance in RMR was significant and the heritability was estimated to 0.59. The estimates of heritability of body mass (0.08) and tarsus length (0.00) were both low and based on nonsignificant additive variances. Thus, given the low heritability (and additive variances) in body mass and tarsus length the potential for direct selection on RMR independent of the two traits is high in this population. However, the strong phenotypic correlation between RMR and mass (0.643 ± 0.079) was partly accounted for by a potentially strong, although highly uncertain, genetic correlation (1.178 ± 0.456) between the two traits. This indicates that the additive variance of body mass, although low, might still somewhat constrain the independent evolvability of RMR.     

Quantitative genetic parameters for wild stream‐living brown trout: heritability and parental effects

Adaptability depends on the presence of additive genetic variance for important traits. Yet few estimates of additive genetic variance and heritability are available for wild populations, particularly so for fishes. Here, we estimate heritability of length‐at‐age for wild‐living brown trout (Salmo trutta), based on long‐term mark‐recapture data and pedigree reconstruction based on large‐scale genotyping at 15 microsatellite loci. We also tested for the presence of maternal and paternal effects using a Bayesian version of the Animal model. Heritability varied between 0.16 and 0.31, with reasonable narrow confidence bands, and the total phenotypic variance increased with age. When introducing dam as an additional random effect (accounting for c. 7% of total phenotypic variance), the level of additive genetic variance and heritability decreased (0.12–0.21). Parental size (both for sires and for dams) positively influenced length‐at‐age for juvenile trout – either through direct parental effects or through genotype‐environment correlations. Length‐at‐age is a complex trait reflecting the effects of a number of physiological, behavioural and ecological processes. Our data show that fitness‐related traits such as length‐at‐age can retain high levels of additive genetic variance even when total phenotypic variance is high.     

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

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.     

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

Augmentative 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.     

The redder the better: wing color predicts flight performance in monarch butterflies

The distinctive orange and black wings of monarchs (Danaus plexippus) have long been known to advertise their bitter taste and toxicity to potential predators. Recent work also showed that both the orange and black coloration of this species can vary in response to individual-level and environmental factors. Here we examine the relationship between wing color and flight performance in captive-reared monarchs using a tethered flight mill apparatus to quantify butterfly flight speed, duration and distance. In three different experiments (totaling 121 individuals) we used image analysis to measure body size and four wing traits among newly-emerged butterflies prior to flight trials: wing area, aspect ratio (length/width), melanism, and orange hue. Results showed that monarchs with darker orange (approaching red) wings flew longer distances than those with lighter orange wings in analyses that controlled for sex and other morphometric traits. This finding is consistent with past work showing that among wild monarchs, those sampled during the fall migration are darker in hue (redder) than non-migratory monarchs. Together, these results suggest that pigment deposition onto wing scales during metamorphosis could be linked with traits that influence flight, such as thorax muscle size, energy storage or metabolism. Our results reinforce an association between wing color and flight performance in insects that is suggested by past studies of wing melansim and seasonal polyphenism, and provide an important starting point for work focused on mechanistic links between insect movement and color.