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.

     

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.     

Seasonal development and variation in abundance among four annual flight periods in a butterfly: a 20‐year study of the speckled wood (Pararge aegeria)

Insects typically spend the winter in a species‐specific diapause stage. The speckled wood butterfly, Pararge aegeria, is unique in having two alternative diapause stages, hibernating as larvae or pupae. In southern Sweden this creates a seasonal flight pattern with four annual adult flight periods: the first in May (pupal diapause), the second in June (larval diapause), and the third and fourth directly developing offspring generations in July and August, respectively. We address the raison d'être of the two diapause pathways by (1) outdoor rearing of cohorts, and (2) performing transect censuses throughout the season for 20 years. We contend that an early start of next season provides a benefit accruing to pupal diapause; conversely, a large proportion of the offspring from adults of the fourth flight peak are unable to reach the pupal stage before winter, providing a benefit accruing to larval winter diapause. The results obtained show that the two hibernation pathways are unlikely to be genetically distinct because of a strong overlap between the two offspring generations, and because sibling offspring from the third and fourth flight periods are likely to choose either of the two hibernation pathways, thereby resulting in a genetic mixing of the pathways. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 635–649.     

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.

     

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.     

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.     

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.     

Mate-locating strategies are related to relative body length and wing colour in the speckled wood butterfly Pararge aegeria

1. The mate-locating strategies of Pararge aegeria (L.) males were studied in relation to adult morphology (dorsal wing colour, forewing length, body length and forewing length : body length ratio) and generation.
2. Males locate females either by perching and defending territories, or by patrolling. Individuals were more consistent in their mating strategies than expected by chance.
3. Forewing length : body length ratio was positively correlated with thorax mass : body mass; relatively short-bodied males had relatively heavy thoraxes. Therefore, forewing length : body length ratio was an index of mass allocation.
4. Perching males had higher forewing length : body length ratios and were paler than patrolling males.
5. The higher forewing length : body length ratio was due to the differences in body length and not wing length. Perchers had shorter bodies than patrollers.     

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.     

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.     

The speckled wood butterflies Pararge xiphia and P. aegeria (Satyridae) on Madeira: distribution, territorial behaviour and possible competition

Madeira is home to two species of speckled wood butterfly. Pararge xiphia is endemic and is common at mid to high altitudes, within and around the edges of the indigenous laurel forest. In 1976 P. aegeria colonized the island and anecdotal reports suggest that it may have been responsible for the loss of P. xiphia from some of its former haunts. The aims of this paper were (1) to provide comprehensive data on the distribution, habitat preferences and recent changes of range of the two species and (2) to examine territorial behaviour to see if inter-specific competition is taking place. Census results show that there are basic differences between the species in altitudinal range and habitat, but they are found together at high densities at habitat boundaries. Repetition of some of the census routes after a 4-year gap suggests that P. aegeria is expanding its range into the areas dominated by P. xiphia. Behavioural data demonstrate that the males may be competing by causing each other to expend more energy in defence of territories. Although competition may be present, it is not yet possible to establish which species is more affected and how competition may have contributed to the recent changes in the species' ranges.     

Exploring sub-lethal effects of exposure to a nucleopolyhedrovirus in the speckled wood (Pararge aegeria) butterfly

This study investigated the sub-lethal effects of larval exposure to baculovirus on host life history and wing morphological traits using a model system, the speckled wood butterfly Pararge aegeria (L.) and the virus Autographa californica nucleopolyhedrovirus. Males and females showed similar responses to the viral infection. Infection significantly reduced larval growth rate, whilst an increase in development time allowed the critical mass for pupation to be attained. There was no direct effect of viral infection on the wing morphological traits examined. There was, however, an indirect effect of resisting infection; larvae that took longer to develop had reduced resource investment in adult flight muscle mass.     

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.     

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.     

Flight during oviposition reduces maternal egg provisioning and influences offspring development in Pararge aegeria (L.)

As a result of increased habitat fragmentation in anthropogenic landscapes, flying insects may be required to travel over larger distances in search of resources such as suitable host plants for oviposition. The oögenesis–flight syndrome hypothesis predicts that physiological constraints caused by an overlap in the resources used by thoracic muscles during flight and during oögenesis (e.g. carbohydrates, lipids and water) result in a resource trade‐off, with any resources used during flight no longer available for reproduction. Increased flight costs could therefore potentially result in a decrease in maternal provisioning of eggs. In the present study, the speckled wood butterfly Pararge aegeria (L.) is used to investigate whether increased flight during oviposition results in changes in maternal investment in eggs and whether this contributes to variation in the development of offspring in subsequent life stages. Forcing females to fly during oviposition directly influences egg size and embryonic development time, and indirectly influences (through changes in egg size) egg hatching success and larval development time. These effects are mediated through ‘selfish maternal effects’, with mothers forced to fly maximizing their fecundity at the expense of investment to individual egg size. The present study demonstrates that a change in maternal provisioning as a result of increased flight during oviposition has the potential to exert nongenetic cross‐generational fitness effects in P. aegeria. This could have important consequences for population dynamics, particularly in fragmented anthropogenic landscapes.