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Roberts, K., Steward, R. A., Süess, P., Lehmann, P. & Wheat, C. W. (2025). A time course analysis through diapause reveals dynamic temporal patterns of microRNAs associated with endocrine regulation in the butterfly Pieris napi. Molecular Ecology, 34(15), Article ID e17348.
Open this publication in new window or tab >>A time course analysis through diapause reveals dynamic temporal patterns of microRNAs associated with endocrine regulation in the butterfly Pieris napi
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2025 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 34, no 15, article id e17348Article in journal (Refereed) Published
Abstract [en]

Organisms inhabiting highly seasonal environments must cope with a wide range of environmentally induced challenges. Many seasonal challenges require extensive physiological modification to survive. In winter, to survive extreme cold and limited resources, insects commonly enter diapause, which is an endogenously derived dormant state associated with minimized cellular processes and low energetic expenditure. Due to the high degree of complexity involved in diapause, substantial cellular regulation is required, of which our understanding primarily derives from the transcriptome via messenger RNA expression dynamics. Here we aim to advance our understanding of diapause by investigating microRNA (miRNA) expression in diapausing and direct developing pupae of the butterfly Pieris napi. We identified coordinated patterns of miRNA expression throughout diapause in both head and abdomen tissues of pupae, and via miRNA target identification, found several expression patterns to be enriched for relevant diapause-related physiological processes. We also identified two candidate miRNAs, miR-14-5p and miR-2a-3p, that are likely involved in diapause progression through their activity in the ecdysone pathway, a critical regulator of diapause termination. miR-14-5p targets phantom, a gene in the ecdysone synthesis pathway, and is upregulated early in diapause. miR-2a-3p has been found to be expressed in response to ecdysone, and is upregulated during diapause termination. Together, the expression patterns of these two miRNAs match our current understanding of the timing of hormonal regulation of diapause in P. napi and provide interesting candidates to further explore the mechanistic role of microRNAs in diapause regulation.

Keywords
diapause, ecdysone, Lepidoptera, microRNA
National Category
Molecular Biology
Identifiers
urn:nbn:se:su:diva-228587 (URN)10.1111/mec.17348 (DOI)001199665900001 ()38597329 (PubMedID)2-s2.0-85190474261 (Scopus ID)
Available from: 2024-04-23 Created: 2024-04-23 Last updated: 2025-09-08Bibliographically approved
Roberts, K., Bosua, H. J. & Lehmann, P. (2025). Flexibility of metabolic rate to temperature coincides with diapause strategy. Biology Letters, 21(8), Article ID 20250192.
Open this publication in new window or tab >>Flexibility of metabolic rate to temperature coincides with diapause strategy
2025 (English)In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 21, no 8, article id 20250192Article in journal (Refereed) Published
Abstract [en]

During dormancy, insects operate on a fixed energy budget and suppress metabolic rate to extend the duration that their energy reserves last. Extending energy stores to last an entire winter can pose a significant challenge, as some habitats have winters that last most of the year. There are cases where insects enter dormancy in mid-summer and remain until the following spring. This multi-season dormancy should pose an even more significant energetic challenge, since these insects must conserve energy during winter, as well as the warmest period of summer. We compared metabolic rate-temperature curves of two related species of pierid butterflies: Pieris napi, which is dormant through winter, and Anthocharis cardamines, which exhibits a multi-season dormancy. This comparison was conducted at several time points under 18°C and 2°C acclimation conditions. We found that A. cardamines can maintain considerable metabolic suppression when acclimated to high temperatures, which is only maintained until they are exposed to low temperatures. Overall P. napi exhibits much lower levels of metabolic plasticity. Metabolic suppression exhibited in A. cardamines is enough to prevent increased rates of mass loss at high temperatures. Together, this provides evidence that both environment and life history timing of dormancy can shape metabolic plasticity.

Keywords
diapause, metabolic rate, metabolic suppression, thermal acclimation, thermal sensitivity
National Category
Zoology
Identifiers
urn:nbn:se:su:diva-246692 (URN)10.1098/rsbl.2025.0192 (DOI)001552490400003 ()40829647 (PubMedID)2-s2.0-105013688061 (Scopus ID)
Available from: 2025-09-10 Created: 2025-09-10 Last updated: 2025-09-10Bibliographically approved
Boratyński, Z., Lavrinienko, A., Lehmann, P., Mousseau, T. A., Tukalenko, E., Vasylenko, A., . . . Nowick, K. (2025). Linking bioenergetics and radiation dose in Chornobyl rodents. Journal of Experimental Biology, 228(18), Article ID jeb250829.
Open this publication in new window or tab >>Linking bioenergetics and radiation dose in Chornobyl rodents
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2025 (English)In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 228, no 18, article id jeb250829Article in journal (Refereed) Published
Abstract [en]

High metabolic rate may provide fitness benefits for individuals. But high metabolic rates incur energetic costs and the need to ingest more food, increasing the risks of ingesting harmful substances from the environment. How organisms respond to elevated ionizing radiation is an important question in the light of pollution from nuclear accidents and waste, and reliance on radiation for medical treatments. Within and around the Chornobyl exclusion zone, we investigated how the bioenergetics of wild rodents inhabiting a gradient of radioactive contamination from ‘clean’ (<15.4 μGy day−1) to contaminated (50–2400 μGy day−1) affects their biological burden of radionuclides. We found that the biological radiation dose negatively correlates with aerobic metabolic scope (high self-maintenance and low aerobic capacity) in adults but positively correlates with metabolic scope (high aerobic capacity) in subadults. These findings suggest that metabolic downregulation may contribute to protection against radionuclide exposure, but that it is constrained by developmental obligations. The results also suggest detrimental effects of radiation on animal physiology. Understanding the physiological mechanisms underlying these relationships will be key for risk assessment of environmental contamination, radiotherapies and space exploration, and may help to rectify discordant opinions concerning the effects of radiation on organismal ecology.

Keywords
137Cs, BMR, Dose rate, Maximum metabolic rate, Pace of life, Translational ecophysiology
National Category
Ecology
Identifiers
urn:nbn:se:su:diva-247294 (URN)10.1242/jeb.250829 (DOI)40931986 (PubMedID)2-s2.0-105016024905 (Scopus ID)
Available from: 2025-09-23 Created: 2025-09-23 Last updated: 2025-09-23Bibliographically approved
Halali, S., Yapar, E., Wheat, C. W., Wahlberg, N., Gotthard, K., Chazot, N., . . . Lehmann, P. (2025). Tempo and mode of winter diapause evolution in butterflies. Evolution Letters, 9(1), 125-136
Open this publication in new window or tab >>Tempo and mode of winter diapause evolution in butterflies
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2025 (English)In: Evolution Letters, E-ISSN 2056-3744, Vol. 9, no 1, p. 125-136Article in journal (Refereed) Published
Abstract [en]

Quantifying the tempo and mode via modern phylogenetic comparative methods can provide key insights into how selection and constraints shape trait evolution on a macroevolutionary time scale. Here, we elucidate the evolution of hibernation (winter) diapause, a complex and defining life-history trait that allows temporal escape from harsh winters in temperate regions for many insects, including our model system, butterflies. Butterflies can diapause in all major life stages, and the availability of global-scale phylogenies makes them an ideal model system for studying diapause evolution. First, using a thorough literature survey, we scored the developmental stage of hibernation diapause (egg, larva, pupa, adult) vs. absence of diapause. We find that larval diapause is most common, while pupal, egg, and adult diapause are relatively rare. Next, we determined that the loss of diapause occurred at a much higher rate and that gains primarily occurred from the non-diapause state. While ancestral state estimation at deeper nodes remained uncertain, we found consistent patterns for some families and strong evidence for extensive convergence in diapause evolution. Contrary to expectations, we find no support for increased gain of diapause during the Eocene–Oligocene glaciation (~35 million years ago). Overall, the evolution of diapause in butterflies has a complex history, has evolved convergently, and has likely predated the major glaciation event consistent with the deep history of diapause evolution in insects. This study advances our understanding of the evolution of a complex and important life-history trait and establishes a macroevolutionary foundation for future studies on the ultimate and proximate basis of diapause evolution.

Keywords
convergent evolution, Eocene–Oligocene glacial maximum, life-history trait, Mk models, phylogenetic comparative methods, seasonality
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:su:diva-239886 (URN)10.1093/evlett/qrae054 (DOI)001337040500001 ()2-s2.0-85217016573 (Scopus ID)
Available from: 2025-02-27 Created: 2025-02-27 Last updated: 2025-02-27Bibliographically approved
von Schmalensee, L., Süess, P., Roberts, K., Gotthard, K. & Lehmann, P. (2024). A quantitative model of temperature-dependent diapause progression. Proceedings of the National Academy of Sciences of the United States of America, 121(36), Article ID e2407057121.
Open this publication in new window or tab >>A quantitative model of temperature-dependent diapause progression
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2024 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 121, no 36, article id e2407057121Article in journal (Refereed) Published
Abstract [en]

Winter diapause in insects is commonly terminated through cold exposure, which, like vernalization in plants, prevents development before spring arrives. Currently, quantitative understanding of the temperature dependence of diapause termination is limited, likely because diapause phenotypes are generally cryptic to human eyes. We introduce a methodology to tackle this challenge. By consecutively moving butterfly pupae of the species Pieris napi from several different cold conditions to 20 °C, we show that diapause termination proceeds as a temperature-dependent rate process, with maximal rates at relatively cold temperatures and low rates at warm and extremely cold temperatures. Further, we show that the resulting thermal reaction norm can predict P. napi diapause termination timing under variable temperatures. Last, we show that once diapause is terminated in P. napi, subsequent development follows a typical thermal performance curve, with a maximal development rate at around 31 °C and a minimum at around 2 °C. The sequence of these thermally distinct processes (diapause termination and postdiapause development) facilitates synchronous spring eclosion in nature; cold microclimates where diapause progresses quickly do not promote fast postdiapause development, allowing individuals in warmer winter microclimates to catch up, and vice versa. The unveiling of diapause termination as one temperature-dependent rate process among others promotes a parsimonious, quantitative, and predictive model, wherein winter diapause functions both as an adaptation against premature development during fall and winter and for synchrony in spring.

Keywords
diapause, diapause termination, ecological predictions, insect, thermal performance curve
National Category
Zoology
Identifiers
urn:nbn:se:su:diva-237787 (URN)10.1073/pnas.2407057121 (DOI)001440979900007 ()39196619 (PubMedID)2-s2.0-85202738541 (Scopus ID)
Available from: 2025-01-14 Created: 2025-01-14 Last updated: 2025-10-03Bibliographically approved
Sepúlveda-Rodríguez, G., Roberts, K. T., Araújo, P., Lehmann, P. & Baird, E. (2024). Bumblebee thermoregulation at increasing temperatures is affected by behavioral state. Journal of Thermal Biology, 121, Article ID 103830.
Open this publication in new window or tab >>Bumblebee thermoregulation at increasing temperatures is affected by behavioral state
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2024 (English)In: Journal of Thermal Biology, ISSN 0306-4565, E-ISSN 1879-0992, Vol. 121, article id 103830Article in journal (Refereed) Published
Abstract [en]

Over the past decades, increasing environmental temperatures have been identified as one of the causes of major insect population declines and biodiversity loss. However, it is unclear how these rising temperatures affect endoheterothermic insects, like bumblebees, that have evolved thermoregulatory capacities to exploit cold and temperate habitats. To investigate this, we measured head, thoracic, and abdominal temperature of bumblebee (Bombus terrestris) workers across a range of temperatures (24 °C–32 °C) during three distinct behaviors. In resting bumblebees, the head, abdomen, and thorax conformed to the environmental temperature. In pre-flight bumblebees, the head and abdominal temperatures were elevated with respect to the environmental temperature, while the thoracic temperature was maintained, indicating a pre-flight muscle warming stage. In post-flight bumblebees, abdominal temperature increased at the same rate as environmental temperature, but the head and the thoracic temperature did not. By calculating the excess temperature ratio, we show that thermoregulation in bumblebees during flight is partially achieved by the active transfer of heat produced in the thorax to the abdomen, where it can more easily be dissipated. These results provide the first indication that the thermoregulatory abilities of bumblebees are plastic and behavior dependent. We also show that the flight speed and number of workers foraging increase with increasing temperature, suggesting that bees do not avoid flying at these temperatures despite its impact on behavioral performance.

Keywords
Bombus, Thermoregulation, Climate warming, Behavior, Flight speed
National Category
Zoology
Identifiers
urn:nbn:se:su:diva-231190 (URN)10.1016/j.jtherbio.2024.103830 (DOI)001227780200001 ()38604117 (PubMedID)2-s2.0-85189887173 (Scopus ID)
Available from: 2024-06-24 Created: 2024-06-24 Last updated: 2025-08-07Bibliographically approved
Terblanche, J. S., Clusella-Trullas, S. & Lehmann, P. (2024). How climate change might impact insect movement via physiological mechanisms. One Earth (4), 608-622
Open this publication in new window or tab >>How climate change might impact insect movement via physiological mechanisms
2024 (English)In: One Earth, ISSN 2590-3330, E-ISSN 2590-3322, no 4, p. 608-622Article, review/survey (Refereed) Published
Abstract [en]

Climate change is altering the abundance and geographic distributions of insects, with potential consequences for human health, sustainable agriculture, and ecosystem function. How insects will be affected during their routine movements by climate-change-associated warming remains poorly understood. Here, we therefore review the potential impacts of, and mechanisms involved in coping with, heat stress during movement from an ecophysiological perspective. Within a movement ecology framework, we propose key ecophysiology attributes that support insect movement with warming conditions. By identifying major knowledge gaps and focusing on movement-related traits discussed here, future studies can further strengthen mechanistic links between functional traits and insect redistribution under climate change and, therefore, provide more robust forecasting tools.

National Category
Climate Science
Identifiers
urn:nbn:se:su:diva-235935 (URN)10.1016/j.oneear.2024.03.008 (DOI)001246088900001 ()2-s2.0-85189987692 (Scopus ID)
Available from: 2024-11-26 Created: 2024-11-26 Last updated: 2025-02-07Bibliographically approved
Siemers, I., von Schmalensee, L., Ziesemer, S., Gotthard, K. & Lehmann, P. (2024). Predictable local adaptation in butterfly photoperiodism but not thermal performance along a latitudinal cline. Ecosphere, 15(5), Article ID e4842.
Open this publication in new window or tab >>Predictable local adaptation in butterfly photoperiodism but not thermal performance along a latitudinal cline
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2024 (English)In: Ecosphere, Vol. 15, no 5, article id e4842Article in journal (Refereed) Published
Abstract [en]

In seasonal environments, organisms must synchronize their life cycles to conditions favorable for growth and reproduction. Because season length varies geographically, local adaptation should arise in traits that regulate phenological responses. Geographic photoperiodism clines are well known, but comparable studies on thermal performance are equivocal and often overlook nonlinear responses. Therefore, we examined local adaptation in plastic responses to both photoperiod and temperature along a 752-km latitudinal cline, by comparing four Swedish populations of the butterfly Pieris napi. Using a common garden design, we estimated (1) photoperiod response curves for diapause induction and (2) thermal performance curves for development and growth rates. We show that differences in photoperiodism follow the expected geographical pattern, where diapause is induced at longer daylengths in northern populations (where growth seasons are short and summer days long). However, population differences in thermal performance curves were small and seemingly idiosyncratic, without clear clinal patterns. Photoperiodic responses appear to evolve more readily than thermal responses, highlighting photoperiodism as a key driver of local life cycle synchronization.

Keywords
evolutionary ecology, Lepidoptera, local adaptation, phenology, phenotypic plasticity, photoperiodism, seasonality, temperature, thermal adaptation, thermal performance
National Category
Zoology
Identifiers
urn:nbn:se:su:diva-235909 (URN)10.1002/ecs2.4842 (DOI)001220807000001 ()2-s2.0-85192892499 (Scopus ID)
Available from: 2024-11-26 Created: 2024-11-26 Last updated: 2024-11-26Bibliographically approved
Brown, I., Ghaly, M., Greiser, C., Lam, N. & Lehmann, P. (2024). Seasonal optimisation of drone-based photogrammetry in a heterogeneous boreal landscape. Applied Vegetation Science, 27(3), Article ID e12797.
Open this publication in new window or tab >>Seasonal optimisation of drone-based photogrammetry in a heterogeneous boreal landscape
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2024 (English)In: Applied Vegetation Science, ISSN 1402-2001, E-ISSN 1654-109X, Vol. 27, no 3, article id e12797Article in journal (Refereed) Published
Abstract [en]

Aims: Uncrewed aerial vehicles (UAV), or drones, have become more affordable and easier to use, resulting in increased UAV applications in ecology and conservation. However, solar illumination, vegetation phenology and prevailing weather conditions will impact the quality of the derived products to differing degrees. In this study, we investigate how seasonal differences in solar illumination, tree foliage and weather conditions impact the accuracy of digital elevation models (DEM) and canopy height models (CHM) in a heterogeneous boreal landscape. Methods: We compared DEMs and CHMs derived from drone photogrammetry with DEMs and CHMs produced from a drone-mounted laser scanner across three seasons with different solar illumination, tree foliage and weather conditions during leaf-off and leaf-on seasons. Photogrammetric height models were evaluated across three land-cover classes consisting of open areas, sparse-forest and forest. The most accurate CHM for sparse-forest was produced during summer under overcast conditions, whereas for the forest class, summer under clear skies was best. Results: Structure from motion (SfM) photogrammetry performed well against the LiDAR survey in most cases with correlations between sampled points of up to R2 = 0.995. Root mean square errors (RMSEs) were <1.5 m in all DEMs and as low as 0.31 m in autumn clear-sky data over open terrain. CHM RMSEs were somewhat higher in all cases except under winter overcast conditions when the RMSE for sparse-forest reached 6.03 m. Conclusions: We have shown that SfM photogrammetry is surprisingly robust to variations in vegetation type, tree phenology and weather, and performs well in comparison with a reference LiDAR data set. Our results show that, in boreal forests, autumn is the preferred season under clear-sky conditions for DEM generation from SfM photogrammetry across all land-cover classes, whereas summer is preferred for CHM modelling with a small trade-off between overcast and clear-sky conditions over different vegetation types. These results can help potential SfM users in ecology and forestry plan missions and review the quality of products derived from drone photogrammetry products.

Keywords
forest canopy, phenology, photogrammetry, structure from motion, UAV
National Category
Earth Observation
Identifiers
urn:nbn:se:su:diva-238462 (URN)10.1111/avsc.12797 (DOI)001274457800001 ()2-s2.0-85199344735 (Scopus ID)
Available from: 2025-01-27 Created: 2025-01-27 Last updated: 2025-01-27Bibliographically approved
Schebeck, M., Lehmann, P., Laparie, M., Bentz, B. J., Ragland, G. J., Battisti, A. & Hahn, D. A. (2024). Seasonality of forest insects: why diapause matters. Trends in Ecology & Evolution (8), 757-770
Open this publication in new window or tab >>Seasonality of forest insects: why diapause matters
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2024 (English)In: Trends in Ecology & Evolution, ISSN 0169-5347, no 8, p. 757-770Article, review/survey (Refereed) Published
Abstract [en]

Insects have major impacts on forest ecosystems, from herbivory and soil-nutrient cycling to killing trees at a large scale. Forest insects from temperate, tropical, and subtropical regions have evolved strategies to respond to seasonality; for example, by entering diapause, to mitigate adversity and to synchronize lifecycles with favorable periods. Here, we show that distinct functional groups of forest insects; that is, canopy dwellers, trunk-associated species, and soil/litter-inhabiting insects, express a variety of diapause strategies, but do not show systematic differences in diapause strategy depending on functional group. Due to the overall similarities in diapause strategies, we can better estimate the impacts of anthropogenic change on forest insect populations and, consequently, on key ecosystems.

Keywords
climate change, dormancy, lifecycle regulation, overwintering, phenology
National Category
Ecology Forest Science
Identifiers
urn:nbn:se:su:diva-235589 (URN)10.1016/j.tree.2024.04.010 (DOI)001290555300001 ()38777634 (PubMedID)2-s2.0-85193725684 (Scopus ID)
Available from: 2024-11-15 Created: 2024-11-15 Last updated: 2024-11-15Bibliographically approved
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Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0001-8344-6830

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