Protandry and postandry in two related butterflies: conflicting evidence about sex-specific trade-offs between adult size and emergence time

Natural selection acting on timing of metamorphosis can be sex-specific, resulting in differences in timing between males and females. Insects with discrete generations frequently show protandry: males usually mature before females. Both Euphydryas editha and E. aurinia butterflies followed this trend. The present study was motivated by the unusual observation of consistent postandry in addition to protandry. In a single E. editha population observed over 20 years the emergence period of males was longer than that of females, both the first and last emerging individuals being males. Variance of timing among individual E. editha larvae is imposed by spatial patchiness of the snowmelt that releases them from winter diapause. If individual larvae released late from diapause were to compensate for their lateness by shortening their development times, they would be small at maturity. If such compensation were only partial, they would be both late and small. Size and timing would become associated. If females were more prone to such partial compensation than males, the observations of postandry could be explained and the prediction made that any tendency for late individuals to be small should be stronger in females than in males. This was the case: in 1 year late males were the same size as early males, in a second year they were larger. Late females were significantly smaller than early females in both years. In E. aurinia, results were opposite both to theoretical prediction and to the observations from E. editha: although the male emergence period was longer than that of females exactly as in E. editha, late males were smaller than early ones, while late females were not small. The data from E. editha support the hypothesis of a sex-specific trade-off between size and emergence time, the data from E. aurinia do not.     

Effect of photoperiod on the development and diapause of the green lacewing Chrysopa pallens (Neuroptera: Chrysopidae)

To investigate the physiology of Chrysopa pallens, the effect of photoperiod on diapause and development was examined in a Japanese population (33.4°N). The response stage for diapause of C. pallens was considered to be the prepupal stage. The critical photoperiod for diapause induction at 20.0°C was between 13 h light : 11 h dark (LD 13:11) and LD 14:10. The larval developmental period was affected by photoperiod: larvae in diapause took longer to complete their development. This difference of larval developmental period in relation to photoperiod was considered to be an adjustment of larval diapause timing.     

Estimating female reproductive success of a threatened butterfly: influence of emergence time and hostplant phenology

We estimated lifetime reproductive success of Euphydryas editha bayensis (Nymphalidae), a federally listed threatened butterfly, based on age-specific fecundity and both adult and offspring survival. Our results indicate that the relative timing of adult emergence and larval hosplant senescence strongly influenced reproductive success of females. For 1992, we estimated that only 8–21% of the eggs laid by females emerging on the 1st day of the 4-week flight season would produce larvae that reach diapause. This figure dropped to 1–5% for females emerging 7 days into the flight season. Within our entire sample, we estimated that 64–88% of the females produced offspring with less than a 2% probability of reaching diapause. These estimates are particularly striking given that they are based on only one source of larval mortality — prediapause starvation due to hostplant senescence. This dependence of reproductive success on the relative timing of female emergence and hostplant senescence may reduce effective population size and render E. editha bayensis especially vulnerable to local extinction events.     

Coevolution of the checkerspot butterfly Euphydryas chalcedona and its larval food plant Diplacus aurantiacus: larval response to protein and leaf resin

Summary Prediapause larvae of the checkerspot butterfly Euphydryas chalcedona were raised from hatch until entrance into diapause on artificial diets. The proportions of protein and host plant leaf resin differed among the diets. Larval size growth rates and mortality were monitored and overall rates and efficiencies of food use were computed.Larval survivorship, growth rate and size of larvae at idapause were significantly enhanced by increasing dietary protein content, particularly over the range found in leaves of the host plant. In contrast, an increasing dietary content of Diplacus aurantiacus leaf resin significantly depressed larval surviviorship, growth rates and size of larvae at diapause. A simple dosedependent interaction was observed between the effects of dietary leaf resin and protein on larval success. Dietary content of leaf resin and protein significantly influenced some measures of food utilization efficiency (ECI and ECD), but not others (AD and NUE).The negative interaction between the effects of dietary leaf resin and protein content suggests the leaf resin phenolic compounds reduce the availability of protein to the larvae. The results for efficiency indices of larval food use are potentially in conflict with this interpretation.The influence of host plant leaf resin and protein on larval success, coupled with the relation between photosynthesis and leaf nitrogen content, are consistent with the hypothesis that productivity can be enhanced by herbivore deterrence resulting from leaf resin production.     

Asymmetric life-history decision-making in butterfly larvae

In temperate environments, insects appearing in several generations in the growth season typically have to decide during the larval period whether to develop into adulthood, or to postpone adult emergence until next season by entering a species-specific diapause stage. This decision is typically guided by environmental cues experienced during development. An early decision makes it possible to adjust growth rate, which would allow the growing larva to respond to time stress involved in direct development, whereas a last-minute decision would instead allow the larva to use up-to-date information about which developmental pathway is the most favourable under the current circumstances. We study the timing of the larval pathway decision-making between entering pupal winter diapause and direct development in three distantly related butterflies (Pieris napi, Araschnia levana and Pararge aegeria). We pinpoint the timing of the larval diapause decision by transferring larvae from first to last instars from long daylength (inducing direct development) to short daylength conditions (inducing diapause), and vice versa. Results show that the pathway decision is typically made in the late instars in all three species, and that the ability to switch developmental pathway late in juvenile life is conditional; larvae more freely switched from diapause to direct development than in the opposite direction. We contend that this asymmetry is influenced by the additional physiological preparations needed to survive the long and cold winter period, and that the reluctance to make a late decision to enter diapause has the potential to be a general trait among temperate insects.     

Influence de la densité de population larvaire sur la taille des adultes,la durée de développement et la fréquence de la diapause chezPteromalus puparum L. [Hym., Chalcidien]

Summary The parasitoid waspPteromalus puparum was reared for many generations under controlled laboratory conditions: larval development in diapausing pupae ofPieris brassicae, 14 hours photoperiod, temperature of 21 °C or 25 °C. The fluctuations in the density of population appear to be the main source of variation for larval development. An increase in the number of larvae living in the same host pupa results in a decrease of adult size, a reduction of developmental time and a diminution of incidence of larval diapause. According to these results, it appears that a high population density hastens the occurrence of metamorphosis and makes it easier. It is suggested that various nervous stimulations, such as food shortage and interactions between larvae, may induce the onset of neurosecretion by the brain.      

Geographic and parental influences on diapause by a polyphagous insect herbivore

1 Facultative diapause permits insects to initiate an additional generation when conditions are favourable, or to enter diapause when they are not. Although the principle environmental cues for diapause induction are often temperature and photoperiod, we demonstrated recently that the quality of host plant consumed by the larvae of Choristoneura rosaceana (Harris) (Lepidoptera: Tortricidae) influences the proportion of larvae that enter diapause and therefore voltinism. 2 Previous work has also suggested that non‐Mendelian parental effects influence diapause by C. rosaceana larvae, but the mechanism was not established. Here, we report further evidence for parental effects on diapause and examine whether parental diet influences diapause induction. 3 We collected larvae of C. rosaceana from six sites at three latitudes in the Province of Québec. There was an increase in the proportion of larvae entering diapause with increasing latitude. Rearing larvae under identical conditions on artificial diet for two generations significantly reduced variation in diapause among populations within a given latitude, and supported the existence of parental effects that influence offspring diapause. 4 Experiments with different host plants and high‐ vs. low‐quality artificial diets provided no evidence that the parental effects on offspring diapause were based on the quality of food consumed by parents. Diapause in C. rosaceana appears influenced by a hierarchy of cues, including temperature, photoperiod, current larval diet and parental environment.     

Winter feeding leads to a shifted phenology in the browntail moth Euproctis chrysorrhoea on the evergreen strawberry tree Arbutus unedo

• 1 The browntail moth Euproctis chrysorrhoea is a highly polyphagous univoltine forest pest. Although its young larvae usually overwinter in diapause from early autumn to the beginning of spring, winter larval feeding has been reported when this species feeds on the evergreen woody shrub strawberry tree Arbutus unedo.
• 2 The present study investigated life‐history traits of four populations of E. chrysorrhoea feeding on A. unedo, including phenology of the different life stages, larval feeding activity and diapause incidence. By modelling the relationship between larval size and host plant leaf persistence, elevation and mean annual temperature, we also studied larval development in ten populations of this species sampled from a range of geographical locations in Spain, from both A. unedo and deciduous hosts.
• 3 The results obtained revealed that on A. unedo, E. chrysorrhoea phenology has shifted: from October to March, A. unedo larvae doubled their size, whereas, on deciduous Ulmus minor and Quercus faginea, larval size did not change. General linear models demonstrated that such differences were not related to environmental variables. We also found that on A. unedo larval feeding was arrested for 2 months, with this period representing a true diapause.
• 4 The results obtained in the present study suggest that E. chrysorrhoea populations are phenologically adapted to their local host plants, and that the presence of foliage is a key element in the phenological shift reported on A. unedo. These results may have implications with respect to the formation of E. chrysorrhoea host races.

     

Conspecific host discrimination by ovipositingEuphydryas editha butterflies: Its nature and its consequences for offspring survivorship

Ovipositing E. editha butterflies display post-alighting discrimination among patches of Collinsia torreyi, one of their major hosts in the General's Highway (GH) population at a montane site in California. Females tended to accept (i.e. oviposit on) dense patches of this host and to reject sparse patches. Possible behavioural mechanisms underlying this tendency are discussed. The consequences of this non-random pattern of oviposition for egg and larval survivorship were investigated and no differences were found in the survivorship of larvae on acceptable and unacceptable collinsias.     

INCORPORATION OF A EUROPEAN WEED INTO THE DIET OF A NORTH AMERICAN HERBIVORE

Populations of the butterfly Euphydryas editha living within a 30 times 100–km region on the eastern slope of the Sierra Nevada range were compared for oviposition preference and ability of larvae to grow and survive on two host plants, Collinsia parviflora and Plantago lanceolata. Since its introduction approximately 100 years ago, P. lanceolata has been incorporated in the diet of E. editha in one of the study populations. The populations differed in oviposition preference; only the population that uses P. lanceolata contains some individuals that prefer P. lanceolata. Larvae from two populations, one using both P. lanceolata and C. parviflora, the other using only C. parviflora, were not found to differ in relative abilities to grow or survive on P. lanceolata. The potential for E. editha to use P. lanceolata appears in populations that have had no prior exposure to this plant, while oviposition preference for this plant has evolved in the population in which the plant now grows.     

Diapause and biological cycle of Cydalima perspectalis (Walker) in the eastern Pyrenees

Boxwood is a very important component of the natural forests of the eastern Pyrenees. In the low altitudes of these forests, the invasive species Cydalima perspectalis (Walker) causes considerable damage, and there is concern that it will migrate towards the natural forests at higher altitudes. To determine the biological parameters of the local pest population, a semiartificial diet with lyophilized powdered Buxus sempervirens L. leaves was developed. The results obtained indicate that the studied population of C. perspectalis is very similar to the native Japanese population in terms of the number of larval instars to complete development, the development rate and the critical photoperiod for the induction of diapause. It has also been demonstrated that long photoperiods can shorten the duration of larval development. The diapause induction response was classified as type I, and diapause termination was classified as type III. At the two studied temperatures, 25º and 15ºC, the larvae seemed to require a similar number of days in diapause, approximately 3 months, to spontaneously resume development; temperatures can also prompt larvae to resume development. The critical photoperiod in the study area occurs during the second half of August, varying somewhat according to temperature. The greatest defoliation is caused by the offspring of the first generation, while the majority of the larval offspring of the second generation will enter diapause. The survival of natural boxwood in this area will depend on its ability to regrow one or two years after extensive defoliation and on the adaptation of several indigenous natural enemies in the region to feed on C. perspectalis.     

On the canopy structure manipulation to buffer climate change effects on insect herbivore development

Insect pest development is often linearly related to air temperature, without taking into account the multiple interactions between the particular host plant and pest, the microclimatic conditions actually experienced by the insect, and the non-linear response of insect development rate to temperature. In this study, using an integrative biophysical model, we have investigated effects of both climatic and tree structure changes on the development of a phytophagous leaf mining moth (Phyllonorycter blancardella), taking into account the heterogeneous microclimatic conditions provided by its host plant, the domestic apple (Malus domestica), the larval body temperature rather than the ambient air temperature, and a non-linear development rate model. Hourly body temperature dynamics of larvae homogeneously dispersed in tree canopies were simulated from hourly meteorological conditions (medium IPCC climate change scenario) within the canopy of apple trees. To analyse the effect of tree architecture on leaf miner development, both pruned and unpruned trees, and one, two and three scaffold branched trees were used. Body temperature dynamics was used to compute larval development time and mortality following the non-linear developmental model for this insect. The results showed that tree pruning influences significantly larval development time and mortality. Nevertheless, the effects of manipulating tree structure on larval development and survival were relatively weak compared with the impact of chosen climate variations. This survey also showed that the variability in insect development time within a year and insect mortality change markedly with climatic variations, and highlights the importance of using non-linear rate curves and insect body temperatures instead of air temperature in forecasting models of climate-related insect pest outbreaks.     

Factors governing the induction of diapause in Ephestia elutella and Plodia interpunctella (Lepidoptera)

Diapause in fully grown larvae of Ephestia elutella and Plodia inferpunctella was induced by low temperature and short photoperiods. Light intensities below 1 lx affected the induction of diapause in both species. At 20 and 25d?C, the critical photo-period for E.elutella was c. 14 h, and for P.interpunctella c. 13 h. The sensitive phase in both species occurred at about the time of the fourth larval moult. In E.elutella about seven short photoperiods were required for larvae to enter diapause. In P.interpunctella high population density during larval development increased the proportion of larvae entering diapause. The conditions inducing diapause in laboratory stocks, and in stocks collected from the field, were different. Laboratory stocks of both species did not enter diapause at 25d?C and required short photoperiods for diapause at 20d?C. Some larvae of the field stock of E.elutella entered diapause in constant darkness at 30d?C, the number being increased at low R.H., and almost all did in short photoperiods at 25°C. At 20T, most larvae of this stock entered diapause regardless of photoperiod, and at 15°C all did. In P.interpunctella up to one-third of larvae of the field stock entered diapause in short photoperiods at 25d?C, and all did if transferred to short photoperiods at 20d?C. In unheated premises, falling temperatures normally induce diapause in E.elutella each autumn, photoperiod only being important if temperatures are high. In P.interpunctella, photoperiod is a more important factor because it can override the effect of falling temperature to a greater extent than in E.elutella. In both species, however, different field populations may respond in different ways.     

Effects of host-plant species on diapause induction of the Kanzawa spider mite, Tetranychus kanzawai

In many herbivorous arthropods, incidence of diapause, which is considered to reflect the timing of diapause, changes depending on the host plants they utilize. Several theoretical studies suggest that the optimal timing of diapause induction depends on life‐history traits; if the development time of the arthropod is short, fecundity is high, or survival rate remains high throughout the season, the optimal timing of diapause induction would be shifted toward the end of the season. For herbivorous arthropods, these life history traits may change among their host plants. Here we examined whether a population of the Kanzawa spider mite, Tetranychus kanzawai Kishida (Acari: Tetranychidae), shows the predicted pattern of diapause induction on two host plants, the kidney bean [Phaseolus vulgaris (Leguminosae)] and Japanese Orixa [Orixa japonica (Rutaceae)], on which the mites show different performances. Rearing conditions were controlled in two ways. In the first experiment, day length and temperature were kept constant throughout the mite lifetime at either of three conditions from mid October to early November. In the second experiment, the conditions were changed from 20 °C and L11.5:D12.5 at immature stages to 18 °C and L11:D13 at adult stage in order to better approximate field conditions. In the first experiment, diapause incidence on P. vulgaris was lower than on O. japonica. This tendency became stronger in the second experiment, suggesting a difference in the timing of diapause induction among host plants. On the other hand, P. vulgaris was proven to allow high performance, i.e., greater lifetime fecundity and shorter development times, although it had no effect on the survival rate. The relationship between diapause incidence and performance is consistent with the prediction of theoretical studies that a short development time or high fecundity delays the timing of diapause induction.     

A plant pathogen modulates the effects of secondary metabolites on the performance and immune function of an insect herbivore

Host plant chemical composition critically shapes the performance of insect herbivores feeding on them. Some insects have become specialized on plant secondary metabolites, and even use them to their own advantage such as defense against predators. However, infection by plant pathogens can seriously alter the interaction between herbivores and their host plants. We tested whether the effects of the plant secondary metabolites, iridoid glycosides (IGs), on the performance and immune response of an insect herbivore are modulated by a plant pathogen. We used the IG‐specialized Glanville fritillary butterfly Melitaea cinxia, its host plant Plantago lanceolata, and the naturally occurring plant pathogen, powdery mildew Podosphaera plantaginis, as model system. Pre‐diapause larvae were fed on P. lanceolata host plants selected to contain either high or low IGs, in the presence or absence of powdery mildew. Larval performance was measured by growth rate, survival until diapause, and by investment in immunity. We assessed immunity after a bacterial challenge in terms of phenoloxidase (PO) activity and the expression of seven pre‐selected insect immune genes (qPCR). We found that the beneficial effects of constitutive leaf IGs, that improved larval growth, were significantly reduced by mildew infection. Moreover, mildew presence downregulated one component of larval immune response (PO activity), suggesting a physiological cost of investment in immunity under suboptimal conditions. Yet, feeding on mildew‐infected leaves caused an upregulation of two immune genes, lysozyme and prophenoloxidase. Our findings indicate that a plant pathogen can significantly modulate the effects of secondary metabolites on the growth of an insect herbivore. Furthermore, we show that a plant pathogen can induce contrasting effects on insect immune function. We suspect that the activation of the immune system toward a plant pathogen infection may be maladaptive, but the actual infectivity on the larvae should be tested.     

Host range of Ceutorhynchus assimilis (Coleoptera: Curculionidae), a candidate for biological control of Lepidium draba (Brassicaceae) in the USA

Ceutorhynchus assimilis has been selected as a potential biological control agent of Lepidium draba, which is a Eurasian invasive weed in North America. Preliminary studies indicated specificity of this weevil collected in southern France on L. draba. This result was in discord with the pest status of C. assimilis found in the literature. Host-specificity tests based both on field and laboratory experiments showed heterogeneity in the host spectrum of the weevils reared from different host-plants as determined by larval development. However, no distinguishable morphological differences could be visually detected between the populations feeding on different host-plants. All sampled populations of weevils were polyphagous as adults. Weevils reared from L. draba were specific to this plant for their complete larval development. Conversely, populations living on other wild and cultivated Brassicaceae species were not able to use L. draba as a host plant. Such differentiation is further highlighted by other biological aspects such as plant infestation rates, sex-ratio, duration of larval development, and differences in the timing of their life cycles. These results demonstrate that C. assimilis, an insect species formerly considered as a pest of Brassicaceae, is characterized by its host-range variability, with one population being potentially useful in the biological control of L. draba. Moreover, this example points to the need to test multiple populations of biological control agents in assessing risk.     

Diapause induction as an interplay between seasonal token stimuli,and modifying and directly limiting factors: hibernation in Chymomyza costata

Larvae of wild type (WT) strain of Chymomyza costata Zetterstedt (Diptera: Drosophilidae) enter diapause (stop developing) in response to short‐day signal at a constant 18 °C, whereas larvae of a non‐photoperiodic‐diapause (NPD) strain do not respond to photoperiodic signalling and continue in larval development irrespective of daylength. The present study shows that WT larvae also respond reliably to thermoperiodic signalling (daily cycles of temperature) under constant darkness, whereas the NPD larvae do not, suggesting that the pathways transducing the environmental token stimuli (photoperiod and thermoperiod) onto the diapause developmental programme might merge functionally in the central biological clock system known to be mutated in NPD strain. Temperature and larval population density modify the output of token stimuli signalling. High temperatures (>24 °C) tend to avert, whereas low temperatures (<18 °C), especially in combination with constant darkness, stimulate diapause induction in WT strain. Overcrowding (>200 larvae per 5 g of larval diet) lengthens the duration of larval development and induces a ‘diapause‐like’ developmental arrest of relatively weak intensity in up to 60% of larvae of both strains. At high temperatures (>30 °C), all WT larvae continue direct development but subsequently die during the pupal stage. Low temperature exposure (<12 °C) causes quiescence in the majority of the larvae of both strains. Starvation blocks development and causes mortality when applied in larvae younger than day 3 of the third instar. Older larvae survive starvation and their photoperiodically‐induced developmental pre‐programming is not affected. Collectively, the results show that diapause induction in C. costata is a result of various interacting effects of multiple environmental factors.     

Effects of temperature,photoperiod and soil humidity on induction of pseudopupal diapause in the bean blister beetle Epicauta gorhami

Larvae of the bean blister beetle Epicauta gorhami Marseul (Coleoptera: Meloidae) feed on grasshopper eggs in soil and undergo hypermetamorphosis. This beetle undergoes larval diapause in the fifth instar as a pseudopupa, a form characteristic of hypermetamorphosis in meloid beetles. The effects of temperature, photoperiod and soil humidity on larval development of E. gorhami are examined in a population in Miyazaki, Japan, using egg pods of Locusta migratoria L. as food. At lower temperatures (20 and 22.5 °C), all larvae become pseudopupae, regardless of the photoperiod. By contrast, at higher temperatures (27.5 and 30 °C), almost all larvae pupate at the end of the fourth instar, again regardless of the photoperiod. A long‐day photoperiodic response occurs only at an intermediate temperature (25 °C): under an LD 12 : 12 h photocycle, all larvae enter diapause, although the diapause incidence tends to decrease as the day length becomes longer. Pseudopupae are immobile and remain in diapause for ≥120 days when they are kept under the same conditions, except that diapause terminates within a relatively short time at 30 °C. Although lower soil humidity retards post‐feeding development, soil humidity has no effect on the diapause incidence. On the basis of the short developmental period and diapause avoidance under summer conditions, it is suggested that this beetle partially produces two generations a year in southwestern Japan.     

Experimental evidence of host race formation in Mitoura butterflies (Lepidoptera: Lycaenidae)

A population of herbivorous insects that shifts to a novel host can experience selection pressures that result in adaptation to the new resource. Host race formation, considered an early stage of the speciation process, may result. The current study investigates host shifts and variation in traits potentially involved in the evolution of reproductive isolation among populations of the juniper hairstreak butterfly, Mitoura gryneus. Mitoura are closely associated with their host trees (Cupressaceae) and exhibit host plant fidelity: in addition to larval development and oviposition, host trees support male leks and mating. Female oviposition preference for the natal host, and differential fitness of larvae when reared on natal versus alternate hosts, are indications that specialization and local adaptation to the natal host plant are occurring. Populations with single host plant associations (Juniperus ashei, J. pinchotii and J. virginiana) as well as populations with multiple hosts (both J. ashei and J. pinchotii) were examined. Concordance between female preference and larval performance was found for J. ashei‐associated populations. Population‐level variation in the patterns of female preference and larval performance, both within and among host associations, may reflect differences in the timing and direction of colonization of hosts. For a single nominal species that otherwise exhibits no morphological or phenological differences, the experimental assessment of specialization and host fidelity in M. gryneus provides strong support for the hypothesis of ongoing host race formation in these butterflies.     

Partial bivoltinism in a gregarious endoparasitoid: larval diapause as influenced by season and sharing a host

The yearly timing of the life cycle of a parasitoid is a key element of its life‐history strategy. I examine here factors influencing the expression of partial bivoltinism in Tetrastichus julis Walker (Hymenoptera: Eulophidae), a specialist parasitoid introduced to North America to attack its univoltine host, the cereal leaf beetle, Oulema melanopus (L.) (Coleoptera: Chrysomelidae). The varying tendency was assessed of individuals of this gregarious larval parasitoid to either emerge as adults in the same summer they mature, or to enter diapause to emerge the following year. Parasitized hosts were obtained by rearing cereal leaf beetles collected as mature larvae from grain fields in northern Utah (western USA) throughout the growing seasons in 2013 and 2014. Cocoons spun by these beetles were held to determine patterns over the spring and summer in the tendency of the parasitoid to forgo larval diapause. A high percentage (nearly 90% in 2013) of parasitoid individuals were found to forgo diapause and emerge in the same summer from earliest maturing hosts. This percentage rapidly declined to 20% or less of individuals forgoing diapause and emerging from cocoons as the summer advanced. The percentage of parasitoid individuals forgoing diapause increased significantly at a given time of season (early or late) as the number of conspecifics with which an individual shared a host larva increased. These results may reflect a trade‐off for individual parasitoids in which greater success in finding – and ovipositing in – host larvae the following spring vs. in summer, is countered by reduced survivorship in diapausing over the winter vs. emerging in the same summer in which the parasitoid matures. Expression of partial bivoltinism of T. julis, as affected strongly by both season and within‐host density, results in high rates of parasitism of cereal leaf beetles both early and late in the season.