Physical and behavioral adaptations to prevent overheating of the living wings of butterflies

Tsai, Cheng‐Chia; Childers, Richard A.; Shi, Norman Nan; Ren, Crystal; Peláez, Julianne; Bernard, Gary D.; Pierce, Naomi E.; Yu, Nanfang

doi:10.1038/s41467-020-14408-8

Cited by 129 publications

(146 citation statements)

References 76 publications

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“…Even though strategies of endothermic thermoregulation are more commonly observed in moths and dragonflies ( May, 1979 ), wing movements in preparation for flight, such as wing vibration or shivering ( Heinrich, 1974 ), have been also described in diurnal Lepidoptera ( Kammer, 1968 ; Krough & Zeuthen, 1941 ). Moreover, recent work, using living Vanessa cardui , Satyrium caryaevorus and Parrhasius m-album butterflies, has unveiled the mechanisms through which haemolymph flow and androconial glands support heat transfer across the wing and has confirmed the importance of basking behaviours in thermoregulation ( Tsai et al., 2020 ). Indeed, physiological and behavioural strategies supposedly go hand in hand and are mutually adopted by thermoregulating insects.…”

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confidence: 95%

Beyond thermal melanism: association of wing melanization with fitness and flight behaviour in a butterfly

Elena

Saastamoinen

2020

Animal Behaviour

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Cold developmental conditions can greatly affect adult life history of ectotherms in seasonal habitats. Such effects are mostly negative, but sometimes adaptive. Here, we tested how cold conditions experienced during pupal development affect adult wing melanization of an insect ectotherm, the Glanville fritillary butterfly, Melitaea cinxia . We also assessed how in turn previous cold exposure and increased melanization can shape adult behaviour and fitness, by monitoring individuals in a seminatural set-up. We found that, despite pupal cold exposure inducing more melanization, wing melanization was not linked to adult thermoregulation preceding flight, under the conditions tested. Conversely, wing-vibrating behaviour had a major role in producing heat preceding flight. Moreover, more melanized individuals were more mobile across the experimental set-up. This may be caused by a direct impact of melanization on flight ability or a more indirect impact of coloration on behaviours such as mate search strategies and/or eagerness to disperse to more suitable mating habitats. We also found that more melanized individuals of both sexes had reduced mating success and produced fewer offspring, which suggests a clear fitness cost of melanization. Whether the reduced mating success is dictated by impaired mate search behaviour, reduced physical condition leading to a lower dominance status or weakened visual signalling remains unknown. In conclusion, while there was no clear role of melanization in providing a thermal advantage under our seminatural conditions, we found a fitness cost of being more melanized, which potentially impacted adult space use behaviour.

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confidence: 95%

Beyond thermal melanism: association of wing melanization with fitness and flight behaviour in a butterfly

Elena

Saastamoinen

2020

Animal Behaviour

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“…While we do not know the developmental mechanisms underlying this pattern formation, one can guess at the adaptive significance of such stability: since the spectrum of palatability is wide in this aposematic species, with some of the individuals being mimics of the others ( Alonso-Mejia & Brower, 1994 ), deviation from the established pattern would be detrimental to the population as a whole. Additionally, the migratory strategy employed by many populations of monarchs may have a stabilizing effect on the wing pattern: wing-related thermoregulation (e .g., Tsai et al , 2020 ) and communal behavior at overwintering colonies have undoubtedly contributed to shaping the wing pattern.…”

Section: Resultsmentioning

confidence: 99%

Emperors, admirals and giants, zebras, tigers and woolly bears: casting a broader net in exploring heparin effects on Lepidoptera wing patterns

Sourakov

2020

F1000Res

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Background: Studies of heparin effects on Lepidoptera wing patterns have been restricted to a small number of species. I report observations from experiments on a broader range of taxa, including first results from swallowtails, tiger moths and microlepidoptera. Methods: Heparin injections were made in prepupae and pupae of Junonia coenia (common buckeyes), Agraulis vanillae (gulf fritillaries), Heliconius charithonia (zebra longwings), Asterocampa clyton (tawny emperors), Danaus plexippus (monarchs), Vanessa atalanta (red admirals); Heraclides cresphontes (giant swallowtails), Pterourus troilus (spicebush swallowtails), Protographium marcellus (zebra swallowtails), Battus polydamas (polydamas swallowtails); Hypercompe scribonia (giant leopard moths), Estigmene acrea (acrea moths), Hyphantria cunea (fall webworm moths), Utetheisa ornatrix (ornate bella moths); Glyphodes sibillalis (mulberry leaftier). Results: Heparin sometimes altered the entire pattern in a dramatic way, sometimes caused changes locally. In buckeyes, the previous heparin study conducted on pupae was compared to injections made at a prepupal stage. In gulf fritillaries, zebra longwings and tawny emperors, the dramatic changes occurred throughout their wings, while in monarchs, changes were restricted to wing margins. Changes achieved in red admirals, show that heparin action is unrelated to the original color. In swallowtails, transformations were restricted to border system, indicating higher levels of stability and compartmentalization of wing patterns. In mulberry leaftier, changes were restricted to the marginal bands. In tiger moths, elongation of black markings led to merging of spots; in the ornate bella moth, it was accompanied by an expansion of the surrounding white bands, and results were compared to the effects of colder temperatures. Conclusions: Using pharmaceutical intervention demonstrates that there are many similarities and some very significant differences in the ways wing patterns are formed in different Lepidoptera lineages. By creating a range of variation one can demonstrate how one pattern can easily evolve into another, aiding in understanding of speciation and adaptation processes.

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“…In recent years, RS has been applied in various disciplines of biology 21,22 . Several papers in entomology involving visible (VIS) and near-infrared (NIR) spectroscopy applications coupled with numerical methods have been recently reported (see: Johnson and Naiker 19 for a comprehensive list).…”

Section: Introductionmentioning

confidence: 99%

How Spectral Properties and Machine Learning Can Categorize Twin Species - Based on Diachrysia Genus

Dyba

Wąsala

Piekarczyk

et al. 2021

Preprint

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Confirmation of distinctiveness or taxonomic affinity awaits new evidence in many twin species. In our work we used noninvasive point reflectance spectroscopy in the range from 400 to 2100 nm coupled with machine learning to study scales on the brown and golden iridescent areas on the dorsal side of the forewing of Diachrysia chrysitis and D. stenochrysis. The basis for the study a statistically significant collection of 95 specimens gathered during 23 years in Poland. The numerical part of an experiment included two independent discriminant analyses: stochastic and deterministic. The more sensitive stochastic approach achieved average compliance with the species classification made by entomologists at the level of 99-100%. It demonstrated high stability against the different configurations of training and validation sets, hence strong predictors of Diachrysia siblings distinctiveness. Both methods resulted in the same small set of relevant features, where minimal fully discriminating subsets of wavelengths were three for glass scales on the golden area and four for the brown. The differences between species in scales primarily concern their major components and ultrastructure. In melanin-absent glass scales, this is mainly chitin configuration, while in melanin-present brown scales, melanin reveals as an additional factor.

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Physical and behavioral adaptations to prevent overheating of the living wings of butterflies

Cited by 129 publications

References 76 publications

Beyond thermal melanism: association of wing melanization with fitness and flight behaviour in a butterfly

Beyond thermal melanism: association of wing melanization with fitness and flight behaviour in a butterfly

Emperors, admirals and giants, zebras, tigers and woolly bears: casting a broader net in exploring heparin effects on Lepidoptera wing patterns

How Spectral Properties and Machine Learning Can Categorize Twin Species - Based on Diachrysia Genus

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