Pupal colour dimorphism in California Battus philenor: pupation sites, environmental control, and diapause linkage

ABSTRACT.

• 1 Natural pupation sites and corresponding pupal colour (green or brown) were determined for samples of Battus philenor (L.) from two Californian populations.
• 2 Larvae pupate off the ground on trees, shrubs and man-made objects.
• 3 The vertical distribution of pupation sites and relative frequencies of pupae formed on narrow twigs and broad substrates show interpopulation variability, and seem to be determined by habitat-specific and possibly behavioural differences among populations.
• 4 The percentage of‘mismatched’pupae in green leafy environments (brown) is greater than that on wide substrates (green). Heterogeneity in samples of the latter suggest strong but sporadic predation pressure on non-cryptic pupae in exposed areas.
• 5 Green and brown substrates generally promoted formation of cryptic green and brown pupae although rearing conditions modified pupal colour response to substrate colour and larval pupation site choice.
• 6 Warm temperatures and long days increased the production of brown pupae. Short photoperiods increased the tendency of larvae to pupate on narrow twig-like substrates and to form green pupae.
• 7 Green pupae show less tendency to diapause than brown pupae. The difference between percentage diapause in the two colour forms increases under conditions favouring progressively more continuous development.

     

Convergent evolution of neuroendocrine control of phenotypic plasticity in pupal colour in butterflies

Phenotypic plasticity in pupal colour occurs in three families of butterflies (the Nymphalidae, Papilionidae and Pieridae), typically in species whose pupation sites vary unpredictably in colour. In all species studied to date, larvae ready for pupation respond to environmental cues associated with the colour of their pupation sites and moult into cryptic light (yellow–green) or dark (brown–black) pupae. In nymphalids and pierids, pupal colour is controlled by a neuroendocrine factor, pupal melanization-reducing factor (PMRF), the release of which inhibits the melanization of the pupal cuticle resulting in light pupae. In contrast, the neuroendocrine factor controlling pupal colour in papilionid butterflies results in the production of brown pupae. PMRF was extracted from the ventral nerve chains of the peacock butterfly Inachis io (Nymphalidae) and black swallowtail butterfly Papilio polyxenes (Papilionidae). When injected into pre-pupae, the extracts resulted in yellow pupae in I. io but brown pupae in P. polyxenes. These results suggest that the same neuroendocrine factor controls the plasticity in pupal colour, but that plasticity in pupal colour in these species has evolved independently (convergently).     

Environmental control of pupal colour in swallowtail butterflies (Lepidoptera: Papilioninae): Battus philenor (L.) and Papilio polyxenes Fabr.

Abstract. 1. Some swallowtail butterflies produce both green and brown pupae. The phenotypes result from the joint action of genotype and environment and usually make the pupae cryptic in their habitats.
2. The major environmental cues influencing pupal colour in two swallowtail species were determined to be textural and optical.
3. Differences in the usage of these kinds of cues in the two species are thought to have evolved because of major differences in the pupation habitats. P.polyxenes , which usually pupates on slender stems amidst vegetation, responds more strongly to optical cues. B.philenor , which usually pupates on exposed surfaces of tree trunks and cliffs, responds more strongly to textural cues.
4. Differences in the overall tendency to produce brown pupae ('sensitivity': Hazel, 1977) are thought to be related to the frequency of brown pupation sites utilized by these two species: high average sensitivity in philenor , which often uses brown sites, and lower average sensitivity in polyxenes , which often uses green sites.     

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.     

Pupation site preference and environmentally cued pupal colour dimorphism in the swallowtail butterfly Papilio polyxenes Fabr. (Lepidoptera: Papilionidae)

Environmentally cued polymorphisms are hypothesized to evolve when the environment is coarsegrained and different genotypes are unable to choose the habitats in which they are most fit. In Papilio polyxenes , which has an environmentally cued pupal colour dimorphism, there is genetic variation in both tendency to produce brown or green pupae and preference for green- or brown-inducing pupation sites, but the two traits are not correlated.     

Interactions of environmental factors influencing pupal coloration in swallowtail butterfly Papilio xuthus

The swallowtail butterfly Papilio xuthus Linné [Lepidoptera: Papilionidae] exhibits pupal protective color polyphenism. Interactions of various environmental factors on pupal coloration were analyzed in non-diapausing individuals. Under sufficient light (200lux), most pupating larvae became green pupae when the surface of the pupation site was smooth, while they became brown when the surface was rough. Tactile signals are the positive environmental factors causing induction of the brown pupal coloration. In dark boxes, the induction of the brown pupal coloration was easily induced even on a smooth surface, suggesting that light suppresses induction of brown coloration. Different colors of pupation sites did not affect pupal coloration under sufficient light. Environmental factors received during a critical period both before girdling and after girdling affected pupal coloration. When tactile signals received from rough surfaces reach threshold levels during pupation, brown pupal coloration is determined. Larvae reared under a daily periodicity of natural light formed a girdle at midnight, subsequently, the prepupae received strong daylight the following day. Under natural light most larvae produced brown pupae on rough surfaces and green pupae on smooth surfaces.     

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.     

Natural pupation sites of swallowtail butterflies (Lepidoptera: Papilioninae): Papilio polyxenes Fabr., P.glaucus L. and Battus philenor (L.)

Abstract. 1. Natural pupation sites have been found in Papilio polyxenes and P.glaucus by releasing prepupal larvae marked with UV-fluorescent paint and locating them at night with a UV lamp, and in Battus philenor by searching a forest habitat where the larval foodplant is abundant.
2. P.polyxenes , a species of weedy habitats, pupates off the ground on a variety of substrates including grasses, weed stalks, posts, etc. The pupae may be green or brown, resembling the substrate.
3. P.glaucus , a species of forest habitats, pupates very close to the ground in the litter and has monomorphic brown pupae.
4. B.philenor , also a forest species, pupates on exposed surfaces (chiefly tree-trunks or cliffs) well off the ground. Its pupae may be brown or green, but the latter were found only on the slenderest twigs.
5. The results for polyxenes and glaucus support the generalization of Clarke & Sheppard (1972) that species of stable habitats are likely to have monomorphic pupae, while those of habitats in which available sites may not be so similar from one generation to the next will be dimorphic.
6. B.philenor is more problematical, but its tendency towards pupal monomorphism (brown) is logical in relation to its common pupation sites.     

Two different sensory mechanisms for the control of pupal protective coloration in butterflies

The butterflies Graphium sarpedon nipponum Fruhstorfer and Papilio xuthus Linné show pupal protective color polymorphism, but the two species appear to have different sensory mechanisms for determining pupal coloration. When light was of sufficient illumination, the larvae of Graphium sarpedon became bright yellowish green pupae on white pupation boards and reddish brown pupae on black pupation boards. The pupal coloration thus strongly depended on the brightness of the pupation site. In addition, larvae became bright yellowish green pupae in complete darkness. From these results, measurement of the illumination suggested that pupal color is determined by the illuminant difference between incidence light from the dorsal direction and ventral light from a paper board; i.e., the sum of the reflected light of the board plus the penetrated light passing through the board. The illuminant difference required for reddish brown coloration was 40 lux or more. The optical signals received through the stemmata during a critical period before formation of the thorax garter (band string) were important for coloration. By contrast, in Papilio xuthus, successive tactile signals from a rough surfaced pupation site during a critical period before and after formation of the garter were important for determining brown pupal coloration.     

The effect of larval photoperiod on pupal colour and diapause in swallowtail butterflies

ABSTRACT.

• 1 There are significant differences in the effects of larval photo-period on diapause and pupal colour among the species Papilio polyxenes Fabr., P.troilus L., Battus philenor (L.) and Eurytides marcellus (Cramer).
• 2 Diapause and pupal colour in P.polyxenes and P.troilus are strongly influenced by larval photoperiod, short photophase eliciting brown diapausing pupae. Photoperiods of 15L:9D permit the expression of the green and brown pupal colour alternatives.
• 3 Pupal colour in B.philenor and E.marcellus is not affected by larval photoperiod, but short photophase induces diapause in these species.
• 4 All species except B.philenor show an association between brown pupal colour and diapause: Emarcellus when reared on long (midsummer) photophase, P.polyxenes and P.troilus when reared on short (autumnal) photophase.
• 5 In P.polyxenes, short photophase can affect pupal colour responses directly, whether the individual enters diapause or not.
• 6 Differences among the species are related to differences in the ecology of their natural pupation sites.

     

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.     

Pupal colour polymorphism in Papilio machaon L. and the survival in the field of cryptic versus non-cryptic pupae

• 1 A field experiment was carried out in a natural habitat of Papilio machaon L. in southern Sweden to assess the evolutionary significance of pupal colour polymorphism.
• 2 Cryptic and non-cryptic pupae were planted in pairs in the vegetation, and exposed to predators.
• 3 The protective coloration conferred a selective advantage approximating 1.5 on the cryptic pupae of the summer generation. In the overwintering generation no difference could be detected between the predation of cryptic and non-cryptic pupae.
• 4 The adaptive fitness of protective coloration, as determined by the different rates of elimination of the colour morphs, was greater for the green pupae than for the brown ones.
• 5 Natural selection favours the evolution of a seasonal difference in the proportion of green and brown pupae in the summer and hibernating generations of P.machaon.

     

Trade-offs between melanisation and life-history traits in Helicoverpa armigera

Abstract.  1. Previously we established a homozygous melanic strain (JBM) with 16 black pupae spontaneously occurring within a laboratory population (JBW) of Helicoverpa armigera and demonstrated that the melanisation is controlled by a single recessive autosomal gene.
2. Data obtained indicate that the melanisation is globally expressed in the pupal and adult stages (except for the body hairs of adults) but not in the egg and larval stages. No differences in body colour can be found between the melanic JBM and the wild-type JBW strains before the metamorphic pupation moult. After pupation, the JBM pupae gradually blacken, whereas the wild-type JBW pupae gradually turn brown, indicating that the biosynthetic steps leading to brown pigments are shut off in the JBM strain. In the adult stage, wings are darker and hairs on the abdomen and tergum are lighter in the melanic moths than in the wild-type individuals.
3. Life-table experiments reveal that the melanism is associated with slower development in all life stages, smaller body weight, lower mating rate and fecundity, less mating time, and accordingly, lower net reproduction rate and population trend index.
4. Single pair inbreeding and reciprocal crosses show that the mating rate is much lower in the inter-strain crosses than in the intra-strain crosses, indicating the presence of mating preference for its own colour morph and the presence to some degree of reproductive isolation between the two colour morphs.     

Patterns of pupal mortality in field populations of Hydropsyche and Cheumatopsyche (Trichoptera: Hydropsychidae)

SUMMARY. 1. Up to 40% of hydropsychid pupal cases (from three stations on the Credit and Humber Rivers, Ontario, Canada) contained insects already dead when collected; chironomid infestation accounted for up to 82% of total mortality within a taxon from any one station. The remaining mortality appeared to be due to siltation.
2. For all taxa ( Cheumatopsyche Wallengren and four species of Hydropsyche Pictet), and at all stations, prepupae suffered significantly more chironomid-related mortality than did fully-developed pupae.
3. Chironomid infestation generally affected all species of Hydropsyche equally; at some stations, Cheumatopsyche pupae appeared to suffer less chironomid-related mortality than did co-existing Hydropsyche species.
4. Chironomid infestation affected a greater proportion of pupae at the station where the density of pupal cases (per sampling quadrat) was greatest.
5. Vertical distribution of the pupation site had no apparent influence on mortality attributed to either siltation or chironomid infestation.
6. Chironomid infestation varied seasonally; it was greatest in May and July-August at an upstream station, and peaked in June at the downstream stations.
7. Mortality attributed to siltation was relatively constant for all stages and taxa, at all stations, throughout the sampling programme.     

Pupal polymorphism in the butterfly Danaus chrysippus (L.): environmental, seasonal and genetic influences

The pupae of the tropical butterfly Danaus chrysippus are either green or pink the switch being operated by a ‘greening’ hormone produced in the larval head. Both environmental and genetic cues are involved in controlling the endocrine mechanism. The environmental factors identified are of two distinct kinds: proximate factors influence pupal colour after the larva has selected its pupation site, whereas ultimate factors are effective at an earlier stage, either prompting choice of pupation site by the larva or priming pupation physiology in a particular direction. Genetic factors preadapt the larva to form a pupa which will be cryptic in the normal or average conditions, climatic or biogeographical, anticipated in its environment. The proximate factors demonstrated are background colour, darkness, light quality (wavelength) and humidity. There is some evidence that substrate texture may also be relevant. Ultimate factors are temperature, humidity and species of larval foodplant. Two closely linked gene loci which govern the phenotype of adult morphs and races either have a pleiotropic effect on pupa colour or are closely linked with other genes which do so. Moreover, the two loci interact epistatically with respect to their pupation effects. Factors producing predominantly green pupae are plant substrates, yellow background, darkness, yellow light, high humidity, high temperature, the b allele at the B locus when homozygous and, on non-plant substrates, the C allele at the C locus. High frequencies of pink pupae result on non-plant substrates, red backgrounds, in blue light, low humidity, low temperatures and in B- and cc genotypes. The C locus alleles, C and c, interact epistatically with the B alleles, their effect on choice of pupation site being determined by linkage phase. Of the two foodplants tested, Calotropis produced a high frequency of green pupae and Tylophora of pinks. The seasonal cycling of rainfall, temperature, availability or condition of foodplant, and gene frequencies are all correlated with oscillations in the frequencies of green and pink pupae. Though genotype influences pupa colour, all genotypes are capable of forming pupae of both colours. The variation can therefore be attributed to an environmental polyphenism superimposed upon a genetic polymorphism. The hormone producing green pupae emanates from the head during the prepupal period. Denied hormonal influence, the pupa is pink. Pupal colour is judged to be aposematic at close range and cryptic at distance.     

Effect of habitat type and soil moisture on pupal stage of a Mediterranean forest pest (Thaumetopoea pityocampa)

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Diapause pupal color diphenism induced by temperature and humidity conditions in Byasa alcinous (Lepidoptera: Papilionidae)

We investigated whether diapause pupae of Byasa alcinous exhibit pupal color diphenism (or polyphenism) similar to the diapause pupal color polyphenism shown by Papilio xuthus. All diapause pupae of B. alcinous observed in the field during winter showed pupal coloration of a dark-brown type. When larvae were reared and allowed to reach pupation under short-day conditions at 18 °C under a 60 ± 5% relative humidity, diapause pupae exhibited pupal color types of brown (33%), light-brown (25%), yellowish-brown (21%), diapause light-yellow (14%) and diapause yellow (7%). When mature larvae reared at 18 °C were transferred and allowed to reach pupation at 10 °C and 25 °C under a 60 ± 5% relative humidity after a gut purge, the developmental ratio of brown and light-brown, yellowish-brown, and diapause light-yellow and diapause yellow types was 91.2, 8.8 and 0.0% at 10 °C, and 12.2, 48.8 and 39.0% at 25 °C, respectively. On the other hand, when mature larvae reared at 18 °C were transferred and allowed to reach pupation at 10 °C, 18 °C and 25 °C under an over 90% relative humidity after a gut purge, the developmental ratio of brown and light-brown, yellowish-brown, and diapause light-yellow and diapause yellow types was 79.8, 16.9 and 3.3% at 10 °C, 14.5, 26.9 and 58.6% at 18 °C, and 8.3, 21.2 and 70.5% at 25 °C, respectively. These results indicate that diapause pupae of brown types are induced by lower temperature and humidity conditions, whereas yellow types are induced by higher temperature and humidity conditions. The findings of this study show that diapause pupae of B. alcinous exhibit pupal color diphenism comprising brown and diapause yellow types, and suggest that temperature and humidity experienced after a gut purge are the main factors that affect the diapause pupal coloration of B. alcinous as environmental cues.     

The proximate control of pupal color in swallowtail butterflies: implications for the evolution of environmentally cued pupal color in butterflies (Lepidoptera: Papilionidae)

The environmentally cued production of cryptic green/yellow or brown/melanized pupae is widespread in butterflies, occurring in the Nymphalidae, Pieridae, and the Papilionidae subfamily Papilioninae. The dimorphism is controlled by the hormone pupal melanization reducing factor (PMRF). In the nymphalid Inachis io dibutryl cAMP mimics PMRF, and inhibits pupal melanization. However, in the papilionid Papilio polyxenes PMRF stimulates browning, suggesting that the control of pupal color by PMRF has evolved independently in the swallowtail and nymphalid-pierid lineages. We examined this hypothesis by using ligatures to prevent hormone release in five species representing three Papilioninae tribes. One species, Papilio glaucus, produces only brown pupae. Ligatures resulted in green cuticle posterior to the ligature in all five swallowtail species, including P. glaucus, suggesting that the mode of action of PMRF is the same in the three tribes. We also found that in P. polyxenes injections of dibutryl cAMP into prepupal larvae mimic the effect of PMRF, by causing dose-dependent pupal browning. Our results support the hypothesis that the control of pupal color by PMRF has evolved independently in the two lineages. The observation that green pupal color can be induced in P. glaucus by ligature indicates that environmentally cued pupal color could evolve by facultative inhibition of PMRF release.     

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.     

Pupal colour dimorphism in swallowtail butterflies: timing of the sensitive period and environmental control

ABSTRACT. Two North American swallowtail butterflies with pupal colour dimorphism, Eurytides marcellus (Cramer) and Papilio troilus L., use chiefly the colour of the pupation substrate to determine pupal colour, and are affected hardly ( P.troilus ) or not at all ( E.marcellus ) by substrate texture. The use of colour cues in these species is in contrast to the greater importance of texture in two other sympatric swallowtails (Hazel & West, 1979). E.marcellus larvae evacuate the gut and start prepupal wandering around mid-day. If they have not reached the sensitive period for pupal colour determination by nightfall they will delay the sensitive period until the next day. Among other North American swallowtails with pupal colour dimorphism there is no tendency for those species that use textural cues for pupal colour determination to evacuate the gut later in the day than those using pupation site colour.