Seasonal selection and resource dynamics in a seasonally polyphenic butterfly

Seasonal polyphenisms are widespread in nature, yet the selective pressures responsible for their evolution remain poorly understood. Previous work has largely focussed either on the developmental regulation of seasonal polyphenisms or putative ‘top‐down’ selective pressures such as predation that may have acted to drive phenotypic divergence. Much less is known about the influence of seasonal variation in resource availability or seasonal selection on optimal resource allocation. We studied seasonal variation in resource availability, uptake and allocation in Araschnia levana L., a butterfly species that exhibits a striking seasonal colour polyphenism consisting of predominantly orange ‘spring form’ adults and black‐and‐white ‘summer form’ adults. ‘Spring form’ individuals develop as larvae in the late summer, enter a pupal diapause in the fall and emerge in the spring, whereas ‘summer form’ individuals develop directly during the summer months. We find evidence for seasonal declines in host plant quality, and we identify similar reductions in resource uptake in late summer, ‘spring form’ larvae. Further, we report shifts in the body composition of diapausing ‘spring form’ pupae consistent with a physiological cost to overwintering. However, these differences do not translate into detectable differences in adult body composition. Instead, we find minor seasonal differences in adult body composition consistent with augmented flight capacity in ‘summer form’ adults. In comparison, we find much stronger signatures of sex‐specific selection on patterns of resource uptake and allocation. Our results indicate that resource dynamics in A. levana are shaped by seasonal fluctuations in host plant nutrition, climatic conditions and intraspecific interactions.     

The conceptual and practical implications of interpreting diet breadth mechanistically in generalist predatory insects

Seasonal polyphenism in animal colour patterns indicates that temporal variation in selection pressures maintains phenotypic plasticity. Spring generation of the polyphenic European map butterfly Araschnia levana has an orange–black fritillary‐like pattern whilst individuals of the summer generation are black with white bands across the wings. What selects for the colour difference is unknown. Because predation is a major selection pressure for insect coloration, we first tested whether map butterfly coloration could have a warning function (i.e. whether the butterflies are unpalatable to birds). In a following field experiment with butterfly dummies we tested whether the spring form is better protected than the summer form from predators in the spring, and vice versa in the summer. The butterflies were palatable to birds (blue tits Cyanistes caeruleus) and in the field the spring and summer form dummies were attacked equally irrespective of season. Therefore, we found no evidence that the map butterfly is warning‐coloured or that seasonal polyphenism is an adaptation to avian predation. Because insect coloration has multiple functions and map butterfly coloration is linked to morphology, life history and development it is likely that the interplay of several selection pressures explains the evolution of colour polyphenism. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Differences in pupal cold hardiness and larval food consumption between overwintering and non‐overwintering generations of the common yellow swallowtail,Papilio machaon (Lepidoptera: Papilionidae), from the Osaka population

To clarify differences in pupal cold hardiness and larval food consumption between overwintering and non‐overwintering generations of the common yellow swallowtail, Papilio machaon, we reared larvae from the Osaka population under photoperiods of 16 h light : 8 h dark (LD 16:8) (long day) or LD 12:12 (short day) at 20°C. We examined the relationship between food consumption and weight during the final larval stadium and pupae, and measured the pupal supercooling point (SCP). Although the ratio of assimilation to consumption did not differ significantly between photoperiods, the ratio of assimilation to pupal weight differed significantly between individuals reared under long and short days. All diapausing pupae were brown, whereas 56% of non‐diapausing pupae were green with the remainder brown. The mean pupal body length (L), dorsal width (W₁) and lateral width (W₂) were larger in non‐diapausing than in diapausing pupae, and the W₁/L and W₁/W₂ ratios differed significantly between non‐diapausing and diapausing pupae. SCP was approximately –20°C and did not differ among pupae 5, 15 and 30 days after pupation under long‐day conditions. However, under short‐day conditions, mean SCP gradually decreased, stabilizing at approximately –24 to –25°C by 30 days after pupation. After freezing, some diapausing pupae emerged as adults, whereas all non‐diapausing pupae died. Both egestion and assimilation were greater under long‐day conditions. The results revealed that pupae of this papilionid exhibit seasonal polyphenism in physiological and morphological traits. Energy from food appears to be expended on increasing cold hardiness in the overwintering generation and on reproduction in the non‐overwintering generation.     

Hormonal control of seasonal morphs by the timing of ecdysteroid release in Araschnia levana L. (Nymphalidae: Lepidoptera)

Araschnia levana L. occurs in two seasonal morphs. Larvae reared under short-day conditions become diapause pupae and emerge as red spring-morph butterflies. Long-day larvae become non-diapause pupae, which emerge as black and white summer morphs. Pupae reared under these different conditions were joined in parabiosis. Both underwent adult development without diapause and the long-day animals developed into the summer morph as normal. The morph of short-day animals depended on the time of parabiosis. When they were joined to fresh long-day pupae 1 day after their own pupation, summer morphs resulted. When parabiosis began 4 days after pupation or later, spring morphs resulted. Extirpation of the brain-corpora cardiaca-allata complex from long-day pupae affected neither non-diapause development nor the summer morph. Adult development could be prevented by removal of head and prothorax. When adult development was initiated in the remaining bodies by 20-hydroxyecdysone 14 days after pupation, the spring morph resulted.—Injection of 20-dydroxyecdysone into 3-day-old short-day pupae initiated adult development and led to the summer morph. Injections into 10-day-old short-day pupae led to the spring morph. The same was true in diapause pupae deprived of their brain-corpora cardiaca-allata complex. These results indicate that seasonal diphenism in A. levana is controlled only by the timing of ecdysteroid release, which initiates adult development. There is no direct influence of the brain on wing coloration.     

Differential Bird Predator Attack Rate on Seasonal Forms of the Map Butterfly (Araschnia levana L.): Does the Substrate Matter?

The European map butterfly (Araschnia levana L.) is a striking example of seasonal plasticity. Individuals of the spring generation are reddish with a fritillary‐like colour pattern, whereas the summer generation is black with a white dorsal stripe. Proximate factors explaining the development of the forms are well known, but ultimate explanations have not been tested experimentally yet. The reddish spring form is assumed to have a warning coloration, as found in other nymphalid butterflies that are unpalatable (Aglais urticae). We tested for differential predation by a visually hunting predator (Parus major) in a laboratory experiment using artificial butterflies designed to represent the spring and summer form. Birds were released individually in a flight cage where the alternative forms were presented. Summer forms were more frequently attacked than spring forms, which may point to some aversion against the reddish spring form. But there was also a strong effect of the interaction between seasonal form and type of substrate. Spring forms were much better protected from attacks on the brown substrate of dead leaves compared to the green substrate of nettle leaves. On the latter substrate, latency times before attacking spring forms were on average 2.5 times longer than for summer forms. Experiments with artificial butterflies simplify complex predator–prey interactions because they exclude potential taste or odour effects and they also exclude behavioural responses and interactions of the butterfly. However, our results based on static visual signals provide a promising first step to test the functional significance of this striking seasonal polyphenism.     

Effect of larval brain extracts derived from three swallowtail butterflies,Papilio helenus L., P. machaon L. and P. memnon L., on seasonal morph development of P. xuthus L. (Lepidoptera: Papilionidae)

Adults of the three papilionid butterflies, Papilio helenus L., Papilio machaon L. and Papilio memnon L., exhibit seasonal diphenism comprising spring and summer morphs. To elucidate the physiological mechanism underlying seasonal morph development in papilionid butterflies, we investigated whether a cerebral factor showing summer‐morph‐producing hormone (SMPH) activity is present in the brain of three Papilio species using an assay system with chilled male short‐day pupae of P. xuthus L. When 2% NaCl extracts derived from 20 larval brains of the three species were injected into abdomens of chilled male short‐day pupae of P. xuthus, all recipients destined to develop into spring‐morph adults developed into summer‐ and intermediate‐morph adults. On the other hand, all recipients injected with distilled water as a control developed into spring‐morph adults. These results indicate that a cerebral factor showing SMPH activity is present in the larval brain of the three Papilio species. Additionally, all recipients injected with 2% NaCl extracts derived from 20 adult brains of Bombyx mori L. also developed into summer‐ and intermediate‐morph adults. The results revealed that SMPH or a cerebral factor showing SMPH activity is widely distributed among lepidopteran insects.     

Regulatory mechanisms in phenotypic plasticity of diapause and nondiapause pupal colouration of the swallowtail butterfly Papilio machaon

Nondiapause pupae of Papilio machaon L. exhibit pupal colour diphenism comprising green–yellow and brown–white types. To understand the regulatory mechanism underlying the control of pupal colouration in P. machaon, the effect of environmental cues on diapause and nondiapause pupal colouration is investigated. When larvae reared under short‐day and long‐day conditions are allowed to pupate in sites with a smooth surface and a yellow background colour, all diapause pupae exhibit a brown–white type and 89.5% of nondiapause pupae exhibit a green–yellow type, respectively. With rough‐surface pupation sites, all diapause pupae exhibit brown–white and intermediate types, whereas a large proportion of nondiapause pupae exhibit brown–white and intermediate types, although some exhibit a green–yellow type. When extracts prepared from the head‐thoracic and thoracic‐abdominal regions of larval central nervous systems are injected into the ligated abdomens of P. machaon short‐day pharate pupae, all recipients exhibit a brown–white colouration. Furthermore, when each extract is injected into the ligated abdomen of Papilio xuthus L. short‐day pharate pupae with orange‐pupa‐inducing factor activity, recipients injected with the head‐thoracic extract exhibit the brown type, whereas those injected with the thoracic‐abdominal extract exhibit an orange colour. The results indicate that the response to the environmental cues of pupation site in P. machaon changes according to the photoperiodic conditions experienced during larval stages, and that at least two hormonal factors producing brown–white pupae are located in the larval central nervous system, with the secretion of these factors being regulated by the recognition of environmental cues in long‐day larvae.     

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.

     

Benthic ctenophore (Order Platyctenida) reproduction,recruitment, and seasonality in south Florida

Reproductive structures, modes, and seasonal patterns of size–class abundances are examined in two benthic platyctene (Family Coeloplanidae) ctenophore species present in dissimilar shallow marine environments in subtropical southeast Florida. Coeloplana waltoni, a minute (1–3 mm body length) epizoic associate of octocorals, occurs in exposed environments often under turbulent conditions, and Vallicula multiformis (2–10 mm) commonly occurs epiphytically on macroalgae in protected, calm‐water environments. Reproductive activity in C. waltoni is most active during the warm‐water summer season (June–October); gonadal development in V. multiformis occurs year‐round, and is most pronounced during sea‐warming periods in late spring (May) and late summer to early autumn (August–October), with release of cydippid larvae. Both species are hermaphroditic brooders, exhibiting paedogenesis (early gonadal development) at body lengths approximately one‐third (Coeloplana) to one‐sixth (Vallicula) of maximum adult size. Juvenile individuals (<0.6 mm) increased in abundance in C. waltoni during the summer reproductive period, and large (≥1 mm) pink‐colored individuals comprised 50% or more of samples from July through September. Seasonal abundance of gravid individuals and the timing of cydippid larval release in V. multiformis did not correspond closely with juvenile or adult population densities. Asexual fragmentation occurred in both ctenophore species, but was observed more frequently in individuals of V. multiformis. This asexual mode of reproduction probably accounted in part for the discordance between ctenophore abundances and larval recruitment events by sexual means. Morphological structures and behaviors associated with reproduction are described in this study. Uncommon images of reproductive products (gametes, embryos, larvae), spawning events, brooding, and asexual fragmentation are included, some for the first time in the published literature.     

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.     

Longer life span is associated with elevated immune activity in a seasonally polyphenic butterfly

Seasonal polyphenism constitutes a specific type of phenotypic plasticity in which short‐lived organisms produce different phenotypes in different times of the year. Seasonal generations of such species frequently differ in their overall lifespan and in the values of traits closely related to fitness. Seasonal polyphenisms provide thus excellent, albeit underused model systems for studying trade‐offs between life‐history traits. Here, we compare immunological parameters between the two generations of the European map butterfly (Araschnia levana), a well‐known example of a seasonally polyphenic species. To reveal possible costs of immune defence, we also examine the concurrent differences in several life‐history traits. Both in laboratory experiments and in the field, last instar larvae heading towards the diapause (overwintering) had higher levels of both phenoloxidase (PO) activity and lytic activity than directly developing individuals. These results suggest that individuals from the diapausing generation with much longer juvenile (pupal) period invest more in their immune system than those from the short‐living directly developing generation. The revealed negative correlation between pupal mass and PO activity may be one of the reasons why, in this species, the diapausing generation has a smaller body size than the directly developing generation. Immunological parameters may thus well mediate trade‐offs between body size‐related traits.     

Generation-dependent female choice: behavioral polyphenism in a bivoltine butterfly

Climatic and biotic circumstances vary as seasons shift, anddifferent cohorts of multivoltine species are likely subjectedto different selection regimes. The bivoltine butterfly Leptideareali (Réal's wood white; Lepidoptera: Pieridae) appearsduring May and June in central Sweden and has a partial secondgeneration in late July. We manipulated both generations toappear simultaneously and performed laboratory mating experimentsthat showed the presence of a behavioral polyphenism in matingpropensity, which is induced during the developmental stages.Females of the summer generation expressed higher mating propensitiesthan spring generation females. Spring females showed an increasein mating propensity with increasing age, whereas summer femalesaccepted most matings already when they were only 1 or 2 daysold. It is likely that larval time constraints, a lower abundanceof males and a lower risk of accepting a male of their univoltinesister species Leptidea sinapis (wood white), have relaxed selectionon mate discrimination among summer generation females. A majorchallenge for future research is to further investigate thedevelopmental pathways causing the polyphenism and the adaptiveimplications of cohort-dependent behaviors.     

Pupal colour dimorphism in a desert swallowtail (Lepidoptera: Papilionidae) is driven by changes in food availability,not photoperiod

1. The swallowtail butterfly Battus polydamas archidamas Boisduval, 1936, exhibits polyphenism for pupal coloration (green and brown). It is distributed across arid regions with winter rains and is monophagous on Aristolochia plants, which emerge after the winter rains and dry out the during summer. Thus, day length does not covary positively with host plant productivity. It was hypothesised that pupal colour was driven by food availability, not photoperiod. The benefits of pupal coloration matching the colour of pupation sites in terms of field survival were also investigated to evaluate the adaptive value of pupa colour. 2. Larvae were reared under a factorial array of two photoperiods (LD 10:14 h and LD 14:10 h) and two food availability regimes (leaves ad libitum and available every other day) to assess the frequency of green and brown pupae. Field survival of green and brown pupae was quantified in three commonly used habitats that differ in background coloration (cacti, rocks and shrubs). 3. Food availability determined pupal colour. Larvae in the ad libitum regime resulted mostly in green pupae, while those with restricted food were mostly brown. In contrast, photoperiod did not influence pupal colour. Survival probability of pupae placed on cacti was higher than those placed on rocks and shrubs, and the lowest predation risk across habitats was for green pupae on cacti. 4. Food availability plays a major role in the seasonal polyphenism for pupal colour of specialist butterflies inhabiting arid environments with winter rains.     

Bi- and trivoltine complex life cycles in a Kanto (Japan) population of a wild bruchid Kytorhinus sharpianus

The partial trivoltinism and overwintering of Kytorhinus sharpianus Bridwell (Coleoptera: Bruchidae) was studied in the Kanto district, Japan. The later in the summer eggs were laid by the first-generation adults, the higher was the incidence of larval diapause in the second generation. The incidence of diapause also fluctuated between years, influencing the abundance of third-generation larvae. A relatively large proportion of third-generation larvae did not attain the diapause stage by the beginning of winter. The diapause development of larvae in diapause was completed by mid-January. Immature larvae of the third generation also overwintered and emerged as adults in the spring.     

Untersuchungen zur Veränderung der Unkrautflora bei mehrmaligem Getreidenachbau auf einer Tonschwarzerde des Thüringer Beckens

The latent effects of precocenes I and II (PI and PH) and juvenile hormone I (JHI) when topically applied to the last three instars of Spodoptera littoralis (Boisd.) larvae have been studied. Application of both PI or PII resulted in morphogenetic abnormalities resemble some effects induced by administration of JHI, e.g., larval‐pupal intermediate, partial or severe cases of untanned pupae and imperfect moths. In PII‐treatments, the effect was instar‐dose‐dependent. The intermediate dose (55 μg) was more effective on S. littoralis larvae than other doses. The effectiveness of both doses of 40 or 70 μg in production of deformed larvae and pupae decreased when applied as repeated doses instead of single ones. In Pi‐treatments, the lower dose (25 μg) was more harmful to Spodoptera larvae than the higher dose (70 μg). Repeated application by either lower or higher doses did not enhance the production of imperfect insects. Application of JHI induced symptoms ranging from supernumerary instars, larval‐pupal intermediate, untanned pupae and deformed adults. The effect was dose‐dependent. In all tested compounds, there apparently was a latent or delayed effects. Although the insects were treated while they were larvae the complete effects were not apparent until after the insect had become a pupa or an adult. More efforts will be needed to understand how does precocene interferes with the process of tanning or sclerotization?     

Red & black or black & white? Phylogeny of the Araschnia butterflies (Lepidoptera: Nymphalidae) and evolution of seasonal polyphenism

Phylogeny of the butterfly genera Araschnia, Mynes, Symbrenthia and Brensymthia (Lepidoptera: Nymphalidae: Nymphalini) is reconstructed, based on 140 morphological and ecological characters. The resulting tree shows that Araschnia is a sister group of the clade including Symbrenthia, Mynes and Brensymthia (Symbrenthia is paraphyletic in the respect of remaining genera; Symbrenthia hippalus is a derived species of Mynes). The species-level relationships within Araschnia are robustly supported as follows: (A. davidis (prorsoides ((zhangi doris) (dohertyi (levana burejana))))). Analysis of the wing colour-pattern characters linked with the seasonal polyphenism in the Araschnia species suggests that the black and white coloration of the long-day (summer) generation is apomorphic. Biogeographically, the origin of polyphenism in Araschnia predates the dispersal of some Araschnia species towards the Palaearctic temperate zone, and the ecological cause of the polyphenism itself is then probably not linked with thermoregulation. The possible mimetic/cryptic scenarios for the origin of Araschnia polyphenism are discussed.     

The effects of different cold‐temperature regimes on development,growth, and susceptibility to an abiotic and biotic stressor

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