Landscape structure and phenotypic plasticity in flight morphology in the butterfly Pararge aegeria

In evolutionary time, varying environments may lead to different morphs as a result of genetic adaptation and divergence or phenotypic plasticity. Landscapes that differ in the extent of habitat fragmentation may provide different selection regimes for dispersal, but also for other ecological functions. Several studies on flying insects have shown differences in flight morphology between landscapes, but whether such differences result from plastic responses have rarely been tested. We did a reciprocal transplant experiment with offspring of speckled wood butterfly females (Parargeaegeria) from three types of landscape differing in fragmentation: woodland landscape, landscape with woodland fragments and agricultural landscape with only hedgerows. Young caterpillars were allowed to grow individually on potted host grasses in small enclosures under the three landscape conditions (split‐brood design). Mortality in caterpillars was much higher in agricultural landscape compared to the other landscapes. Additive to the effect of landscape of development, landscape of origin also affected mortality rate in a similar way. Flight morphology of the adults resulting from the experiment differed significantly with landscape. Independent of the landscape of origin, males and females that developed in agricultural landscape were the heaviest and had the greatest wing loadings. Females that developed in agricultural landscape had higher relative thorax mass (i.e. greater flight muscle allocation) in line with adaptive predictions on altered dispersal behaviour with type of landscape. In males, relative thorax mass did not respond significantly relative to landscape of development, but males originating from landscape with woodland fragments allocated more into their thorax compared to males from the other types. We found significant G×E interactions for total dry mass and wing loading. Our results suggest the existence of phenotypic plasticity in butterfly flight morphology associated with landscape structure.     

Larval food stress differentially affects flight morphology in male and female speckled woods (Pararge aegeria)

Abstract 1. Adaptive plasticity in flight morphology can be of great importance for organisms, in order to deal with changing environments. When different demands are imposed to this morphology, different responses to environmental changes can be expected. 2. The aim of this study is to examine whether males and females of Pararge aegeria, which show different flight behaviours, respond differently to larval food stress. 3. In a food‐stress experiment, larvae of 35 families were reared on host plants subjected to a drought‐stress treatment with three groups: a control group, a low‐stress group and a high‐stress group. 4. Individuals from stress treatments significantly differed in wing morphology; they had lower wing loadings, and stressed females tended to have more pointed wings than females of the control group. 5. The difference in phenotypic response to food stress between both sexes may indicate that males and females benefit from different changes in morphology. In females, an increase in dispersal capacity may entail fitness benefits, whereas male morphology is mainly shaped by mate‐location strategy.     

Phenotypic variation in adult morphology and pupal colour within and among families of the speckled wood butterfly Pararge aegeria

Abstract .1. Larvae from eggs of fifteen wild-caught speckled wood females were reared individually under common conditions (LD 18:6 h and 17 °C) in the laboratory.
2. Pupal colour (green or brown) and the following adult morphological variables that are known or assumed to be related to behavioural variation (thermoregulation, flight, crypsis) were studied: size, relative thorax mass, area of yellow patches on the dorsal forewing, size of submarginal eyespots on the dorsal hindwing, colour of the dorsal thorax, dorsal basal wing, and dorsal distal wing.
3. The results of the breeding experiment indicate significant differences in adult morphological traits among families, sexes, and pupal colour types.
4. All adult morphological variables (except spot size and thorax colouration) differed significantly among families, suggesting genetic variation underlying the phenotypic variation. Heritabilities for these features were intermediate (0.38) to high (> 1).
5. Apart from known aspects (e.g. size), novel aspects of the sexual dimorphism were found: females had paler thoraxes than males, which relates to higher abundance of fur on the thorax and hence to thermoregulatory differences.
6. Green pupae produced larger individuals with a larger relative thorax mass than brown pupae. Green pupae produced adults with a paler basal wing colour in females, but not in males. These relationships are novel and suggest a trade-off between juvenile and adult investment.     

Effect of larval-rearing density on adult life-history traits and developmental stability of the dorsal eyespot pattern in the speckled wood butterfly, Pararge aegeria

Behavioural stresses such as crowding are thought to incur a metabolic cost to insect larvae, and fluctuating asymmetry (FA) has been shown to be a possible indicator of this stress. A study of a Madeiran population of the butterfly Pararge aegeria L. (Lepidoptera: Satyrinae) shows that larval crowding affects larval development and growth, with female larvae being more adversely affected than males. It was predicted that if larval crowding increases FA, male and female P. aegeria adults may show different responses to this stress. The FA of five different wing pattern elements on the dorsal hindwings of adult male and female P. aegeria that had been reared at different larval densities was measured. Crowding in P. aegeria resulted in a trait-specific and sex-specific increase in FA. Although a significant correlation between FA and longevity was not observed, there was a significant correlation with egg-laying rate. Stressed females increased their egg-laying rate. An increased egg-laying rate may carry a further fitness cost through the offspring of stressed females, because high egg-laying rates are associated with a decline in oviposition site quality.     

Annual growth rates in newly established populations of the butterfly Pararge aegeria

1. The likelihood of range changes in the event of climate change makes study of the foundation and establishment of populations of particular relevance and interest.
2. The butterfly Pararge aegeria has expanded its range in Britain over many decades. Since 1985, ten monitored sites in eastern England have been colonized and the pattern of population growth examined.
3. Geometric annual growth rates in the establishing populations were initially, on average, three- to fourfold but subsequently declined. The decline provides possible evidence that density-dependence limits final population densities, but other explanations are possible.     

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.     

Integration of wings and their eyespots in the speckled wood butterfly Pararge aegeria

We investigated both the phenotypic and developmental integration of eyespots on the fore- and hindwings of speckled wood butterflies Pararge aegeria. Eyespots develop within a framework of wing veins, which may not only separate eyespots developmentally, but may at the same time also integrate them by virtue of being both signalling sources and barriers during eyespot development. We therefore specifically investigated the interaction between wing venation patterns and eyespot integration. Phenotypic covariation among eyespots was very high, but only eyespots in neighbouring wing cells and in homologous wing cells on different wing surfaces were developmentally integrated. This can be explained by the fact that the wing cells of these eyespots share one or more wing veins. The wing venation patterns of fore- and hindwings were highly integrated, both phenotypically and developmentally. This did not affect overall developmental integration of the eyespots. The adaptive significance of integration patterns is discussed and more specifically we stress the need to conduct studies on phenotypic plasticity of integration.     

On the sex-specific mechanisms of butterfly flight: flight performance relative to flight morphology, wing kinematics, and sex in Pararge aegeria

Many evolutionary ecological studies have documented sexual dimorphism in morphology or behaviour. However, to what extent a sex-specific morphology is used differently to realize a certain level of behavioural performance is only rarely tested. We experimentally quantified flight performance and wing kinematics (wing beat frequency and wing stroke amplitude) and flight morphology (thorax mass, body mass, forewing aspect ratio, and distance to centre of forewing area) in the butterfly Pararge aegeria (L.) using a tethered tarsal reflex induced flight set-up under laboratory conditions. On average, females showed higher flight performance than males, but frequency and amplitude did not differ. In both sexes, higher flight performance was partly determined by wing beat frequency but not by wing stroke amplitude. Dry body mass, thorax mass, and distance to centre of forewing area were negatively related to wing beat frequency. The relationship between aspect ratio and wing stroke amplitude was sex-specific: females with narrower wings produced higher amplitude whereas males show the opposite pattern. The results are discussed in relation to sexual differences in flight behaviour.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 675–687.     

Seasonal plasticity in growth and development of the speckled wood butterfly, Pararge aegeria (Satyrinae)

Regulation of growth and development by photoperiod was studied in a population of the speckled wood butterfly, Purarge aegeria L. (Lepidoptera: Satyrinae), from southern Sweden. Individuals were reared in a range of photoperiodic regimes (9L. to 22L) and temperatures (13°C to 21° C). Plasticity was found for important life-history traits- generation time, growth rate and final weight and seasonal regulation of development in response to photoperiod was found to occur at two levels. Purarge aegeria hibernates as a third instar larva or in the pupal stage, cantering one of four major developmental pathways in response to photoperiod: (1) direct development in both the larval and pupal stages, (2) pupal winter diapause with or (3) without a preceding larval summer diapause, or (4) larval winter diapause. In addition to this high-level regulation of individual development, larval growth rate and pupal development rate also appear to be finally regulated by photoperiod within each major pathway. As photoperiods decreased from 22 h to 17 h at 17° C, growth rate among directly developing larvae increased progressively, as was the case for larva? developing according to a univoltine life cycle from 17 h to 14 h. At two photoperiods, 13 h and 16 h (corresponding to shifts between major pathways), both larval and pupal development were extremely variable with the fastest individuals developing directly and the slowest developing with a diapause. This indicates a gradual nature of diapause itself, suggesting that the two level may not he fundamentally different.     

Egg-laying by the speckled wood butterfly (Pararge aegeria): the role of female behaviour, host plant abundance and temperature

ABSTRACT.

• 1 Egg-laying by Pararge aegeria (L.) was studied in relation to host plant abundance, temperature and behaviour in one woodland site in central England.
• 2 Eggs were laid on the undersides of leaves of fifteen of thirty-one species of grass located in the study site. Most were deposited singly although on several occasions a number of females laid on a single leaf.
• 3 There was no clear relationship between host plant abundance and host plant use, the species used being widespread and abundant.
• 4 Most eggs were laid on plants within the temperature range 24–30°C. In spring and later summer these sites were in sunlit open areas but in midsummer they were in the woodland ground layer.
• 5 Females distributed their eggs over a large area, usually making a dispersal flight after laying an egg.

     

The effect of weather on the life cycle of the speckled wood butterfly Pararge aegeria

ABSTRACT.

• 1 Pararge aegeria (L.) is a very unusual butterfly of Britain, having a long period of adult activity, from April to October, without discrete flight periods. In central Britain it overwinters in two stages: pupae and third instar larvae, both being the progeny of late summer adults. Other larval stages die at the onset of cold winter weather. The overwintering stages give rise to the first adult generation in spring, split into two parts.
• 2 Different temperature regimes affect development rates in larvae and pupae differently. Late larval development is more rapid than that of pupae at low temperatures, thus in cool spring weather the overlap of the two parts of the first generation is greater than in warm spring weather.
• 3 Adults emerge continuously throughout the summer because larval development rates are variable. When summer is warm there is a partial third generation but when cool only two.
• 4 The timing of the end of the flight period is consistent with the hypothesis that both temperature and photoperiod are important in determining whether individuals enter diapause or develop directly. In warm summers larvae develop beyond a sensitive stage before critical daylength is reached and develop directly, but in cool summers individuals enter diapause because they are at the sensitive stage when critical daylength is reached.
• 5 It is suggested that variable development rates can facilitate parasite escape in autumn and increase the probability of adult success when weather is unpredictable, and this strategy is maintained because these benefits are greater than the cost of winter mortality of larvae.

     

Quantitative genetic variation in an island population of the speckled wood butterfly (Pararge aegeria)

Evidence of changes in levels of genetic variation in the field is scarce. Theoretically, selection and a bottleneck may lead to the depletion of additive genetic variance (V(A)) but not of nonadditive, dominance variance (V(D)), although a bottleneck may converse V(D) to V(A). Here we analyse quantitative genetic variation for the Speckled Wood butterfly Pararge aegeria on the island of Madeira about 120 generations after first colonisation. Colonisation of the island involved both a bottleneck and strong natural selection, changing the average value of traits. Several life history and morphological traits with varying levels of change since colonisation were analysed. In accordance with expectations, all traits except one showed relatively low levels of V(A), with an average heritability (h(2)) of 0.078. Levels of V(D) for these traits were relatively high, 20-94% of total variance and on average 80% of V(G). The exception was a morphological trait that probably had not experienced strong natural selection after colonisation, for which a h(2) of 0.27 was found. Another interesting observation is that the population seems resistant to inbreeding effects, which may be the result of purging of deleterious alleles.     

Adaptive variation in growth rate: life history costs and consequences in the speckled wood butterfly,Pararge aegeria

An important assumption made in most lifehistory theory is that there is a trade-off between age and size at reproduction. This trade-off may, however, disappear if growth rate varies adaptively. The fact that individuals do not always grow at the maximum rate can only be understood if high growth rates carry a cost. This study investigates the presence and nature of such costs inPararge aegeria. Five females from two populations with known differences in life history (south Sweden and Maderia) were allowed to oviposit in the laboratory and their offspring were reared in environmental chambers under conditions leading to direct development. We measured several aspects of life history, including development times, pupal and adult weights, growth rate, female fecundity, longevity and larval starvation endurance. In both populations there seemed to be genetic variation in growth rate. There was no evidence for a trade-off between age and size at pupation. As predicted, larvae with high growth rates also lost weight at a relatively higher rate during starvation. High weight-loss rates were furthermore associated with a lower probability of surviving when food became available again. This is apparently the first physiological trade-off with growth rate that has been experimentally demonstrated. In both populations there were significant differences in growth rate between the sexes, but the populations differed in which sex was growing at the highest rate. In Sweden males had higher growth rates than females, whereas the reverse was true for Madeira. These patterns most likely reflect differences in selection for protandry, in turn caused by differences in seasonality between Sweden and Madeira. Together with the finding that males had shorter average longevity than females in the Swedish, but not in the Maderiran, population, this indicates that a lower adult quality also may be a cost of high growth rate. We argue that for the understanding of life history variation it is necessary to consider not only the two dimensions of age and size, but also to take into full account the triangular nature of the relationship between size, time and growth rate.     

Larval aestivation and direct development as alternative strategies in the speckled wood butterfly, Pararge aegeria, in Sweden

ABSTRACT.

• 1 Sweden has two disjunct populations of the speckled wood butterfly, Pararge aegeria L. The southern population has two generations per year but the central Swedish population is univoltine. When rearing larvae from central Sweden under normal photoperiodic conditions but at temperatures slightly above the ambient, 42% of the larvae developed directly and produced a second generation of adults the same summer. The egg—larval development time of the directly developing individuals was about 40 days, whereas that of the individuals developing along the univoltine pathway was about 100 days.
• 2 Larvae of the central Swedish population normally aestivate during part of the summer even though abundant food is available. In the closely related Lasiommata petropolitana F., which is the only Swedish satyrid that overwinters in the pupal stage besides P.aegeria, larvae do not aestivate, indicating that there does not seem to be any obligatory association between pupal hibernation and larval aestivation.
• 3 Development rates of aestivating and directly developing P.aegeria are equal up to the third larval instar. During the third and fourth instars, however, the development rate of aestivating individuals is retarded and females also have an additional fifth instar.
• 4 Since the central Swedish P.aegeria have the capacity to develop directly, and the southern Swedish ones have the capacity to aestivate, the evidence indicates that the outcome of the cost/benefit balance of univoltine versus bivoltine development differs between the two areas.

     

Genetics of fluctuating asymmetry in pupal traits of the speckled wood butterfly (Pararge aegeria)

Fluctuating asymmetry (FA), small random differences between left and right, has been extensively used as a measure of individual quality, though its usefulness in that respect is controversial. Whether FA is heritable has implications for sexual selection theory and for its usefulness as an indicator of stress. Heritability (h(2)) of FA is, however, difficult to estimate precisely and reliably. Here we report h(2)s of FA for two pupal traits in the speckled wood butterfly (Pararge aegeria). We used a restriction error maximum likelihood (REML) analysis in combination with a jackknife procedure to analyse a large mixed offspring-parent/half-sib/full sib data set. A five-generation selection experiment provided a second set of narrow sense h(2)s. Narrow sense h(2)s were not significant and on average -0.029 (REML-analysis) and 0.031 (selection experiment) for the pupal segment covering the fore leg (LEG) and 0.057 and 0.004 for a SPOT on that segment. Estimated percentage dominance variances were 0.057 (LEG) and 0.027 (SPOT) and not significantly different from 0. The h(2) estimates had been slightly increased by cage effects. Average FA for LEG after five generations of selection were higher in the high lines than in the low lines, and the control lines were in between. No difference in FA between lines was found for SPOT. Although differences between lines were not significant, a slight h(2) (<3%) for LEG could not be excluded. The genetic effect was, however, small compared with the effect of foodplant quality. Larvae grown on foodplants that were not watered enough for good growth showed significantly higher FA for LEG, but not for SPOT, compared with larvae grown on good foodplants.