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  • 1. Boratynski, Zbyszek
    et al.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. University of Jyvaskyla, Finland.
    Mappes, Tapio
    Mousseau, Timothy A.
    Moller, Anders Pape
    Increased radiation from Chernobyl decreases the expression of red colouration in natural populations of bank voles (Myodes glareolus)2014In: Scientific Reports, E-ISSN 2045-2322, Vol. 4, p. 7141-Article in journal (Refereed)
    Abstract [en]

    Pheomelanin is a pink to red version of melanin pigment deposited in skin and hair. Due to its bright colour, pheomelanin plays a crucial function in signalling, in particular sexual signalling. However, production of pheomelanin, as opposed to its dark alternative, eumelanin, bears costs in terms of consumption of antioxidants important for protection of DNA against naturally produced reactive oxidative species. Therefore, decreased expression of pheomelanin is expected in organisms exposed to severe oxidative stress such as that caused by exposure to chronic ionizing radiation. We tested if variable exposure to radiation among natural populations of bank voles Myodes glareolus in Chernobyl affected expression of red colouration in their dorsal fur. The relative redness of dorsal fur was positively correlated with weight, but also negatively correlated with the level of background radiation. These results suggest that the development of the natural red colouration in adult bank voles is affected by ionizing background radiation, and potentially causing elevated levels of oxidative stress. Reduced production of pheomelanin allows more antioxidants to mitigate the oxidative stress caused by radiation. However, changing natural animal colouration for physiological reasons can have ecological costs, if e.g. it causes mismatch with habitat colouration and conspicuousness for predators.

  • 2.
    Emami, S. Noushin
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. Swedish University of Agricultural Sciences, Sweden.
    Lindberg, Bo G.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Hua, Susanna
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Hill, Sharon R.
    Mozuraitis, Raimondas
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Birgersson, Göran
    Borg-Karlson, Anna-Karin
    Ignell, Rickard
    Faye, Ingrid
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    A key malaria metabolite modulates vector blood seeking, feeding, and susceptibility to infection2017In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 355, no 6329Article in journal (Refereed)
    Abstract [en]

    Malaria infection renders humans more attractive to Anopheles gambiae sensu lato mosquitoes than uninfected people. The mechanisms remain unknown. We found that an isoprenoid precursor produced by Plasmodium falciparum, (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate (HMBPP), affects A. gambiae s. l. blood meal seeking and feeding behaviors as well as susceptibility to infection. HMBPP acts indirectly by triggering human red blood cells to increase the release of CO2, aldehydes, and monoterpenes, which together enhance vector attraction and stimulate vector feeding. When offered in a blood meal, HMBPP modulates neural, antimalarial, and oogenic gene transcription without affecting mosquito survival or fecundity; in a P. falciparum-infected blood meal, sporogony is increased.

  • 3. Friberg, Magne
    et al.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. Stockholm University, Faculty of Science, The Bolin Centre for Climate Research (together with KTH & SMHI). University of Greifswald, Greifswald, Germany.
    Wiklund, Christer
    Stockholm University, Faculty of Science, Department of Zoology. Stockholm University, Faculty of Science, The Bolin Centre for Climate Research (together with KTH & SMHI).
    Autumn mass change and winter mass loss differ between migratory and nonmigratory butterflies2023In: Animal Behaviour, ISSN 0003-3472, E-ISSN 1095-8282, Vol. 204, p. 67-75Article in journal (Refereed)
    Abstract [en]

    Poikilotherms have two major alternative strategies to deal with the inhospitable conditions of temperate winters: hibernation or migration. The vast majority of insects spend winter in a speciesspecific diapause resting stage, while others remain reproductively active after having migrated to more hospitable environments in the autumn. The butterfly clade Nymphalini offers an interesting possibility for comparisons among species adopting different strategies. Whereas most genera in this clade have evolved adult diapause, species in the genus Vanessa engage in an annual multigeneration migration cycle, leaving northern latitudes during autumn. Here, we compared two species of diapausing Aglais butterflies, A. io and A. urtica, two species of the migratory genus Vanessa, V. atalanta and V. cardui, and two morphs of Polygonia c-album, the diapausing winter morph and the direct developing hutchinsoni morph. We tested how these different species differ in resource acquisition strategy during early adult life, how the acquisition of resources affects survival in cold winter conditions and how A. io, Aglais urticae and V. atalanta differ in resting metabolism under cold conditions. The butterflies set for adult diapause (1) acquired more mass during early adult life and (2) lost less mass and had a lower resting metabolism under cold conditions. In addition, (3) the life span under cold conditions was positively related to the weight increase during early adult life in the diapausing species, but not in the migratory species. Our laboratory results demonstrate how different developmental pathways, such as diapause or direct development, can be studied by measuring mass change in living butterflies. Our expectation that migratory species would increase in mass like species set for overwintering were not met, perhaps because such studies should ideally be performed under natural conditions. (c) 2023 The Author(s). Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour. This is an open access article under the CC BY license (http://creativecommons.org/licenses/ by/4.0/).

  • 4.
    Greiser, Caroline
    et al.
    Stockholm University, Faculty of Science, Department of Physical Geography.
    von Schmalensee, Loke
    Stockholm University, Faculty of Science, Department of Zoology.
    Lindestad, Olle
    Stockholm University, Faculty of Science, Department of Zoology.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. University of Greifswald, Germany.
    Microclimatic variation affects developmental phenology, synchrony and voltinism in an insect population2022In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 36, no 12, p. 3036-3048Article in journal (Refereed)
    Abstract [en]
    1. Temperature influences the rate of most biological processes. Nonlinearities in the thermal reaction norms of such processes complicate intuitive predictions of how ectothermic organisms respond to naturally fluctuating temperatures, and by extension, to climate warming. Additionally, organisms developing close to the ground experience a highly variable microclimate landscape that often is poorly captured by coarse standard climate data.
    2. Using a butterfly population in central Sweden as a model, we quantified the consequences of small-scale temperature variation on phenology, emergence synchrony and number of annual reproductive cycles (voltinism). By combining empirical microclimate and thermal performance data, we project development of individual green-veined white butterflies (Pieris napi) across 110 sites in an exceptionally high-resolved natural microclimate landscape.
    3. We demonstrate that differences among microclimates just meters apart can have large impacts on the rate of development and emergence synchrony of neighbouring butterflies. However, when considering the full development from egg to adult, these temporal differences were reduced in some scenarios, due to negative correlations in development times among life stages. The negative correlations were caused by temperatures at some sites beginning to exceed the optimum for development as the season progressed. Indeed, which sites were optimal for fast development could change across the lifetimes of individual butterflies, that is, ‘fast’ sites could become ‘slow’ sites. Thus, from a thermal point of view, there seem to be no consistently optimal microsites. Importantly, the fast sites were not always the warmest sites. We showed that such unintuitive effects could play an important role in the regulation of phenological synchrony and voltinism in insects, as most sites consistently favoured two generations. The results were generally robust across years and three different egg-laying dates.
    4. Using high-resolved empirical climate data on organism-relevant temporal and spatial scales and considering nonlinear responses to temperature, we demonstrated the large and unintuitive population-level consequences of locally and temporarily high temperatures. We suggest to—whenever possible—incorporate species- and life stage-specific nonlinear responses to temperature when studying the effects of natural microclimate variation and climate change on organisms.
  • 5. Harvey, Jeffrey A.
    et al.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. University of Greifswald, Germany.
    Chown, Steven L.
    Scientists' warning on climate change and insects2023In: Ecological Monographs, ISSN 0012-9615, E-ISSN 1557-7015, Vol. 93, no 1, article id e1553Article, review/survey (Refereed)
    Abstract [en]

    Climate warming is considered to be among the most serious of anthropogenic stresses to the environment, because it not only has direct effects on biodiversity, but it also exacerbates the harmful effects of other human-mediated threats. The associated consequences are potentially severe, particularly in terms of threats to species preservation, as well as in the preservation of an array of ecosystem services provided by biodiversity. Among the most affected groups of animals are insects—central components of many ecosystems—for which climate change has pervasive effects from individuals to communities. In this contribution to the scientists' warning series, we summarize the effect of the gradual global surface temperature increase on insects, in terms of physiology, behavior, phenology, distribution, and species interactions, as well as the effect of increased frequency and duration of extreme events such as hot and cold spells, fires, droughts, and floods on these parameters. We warn that, if no action is taken to better understand and reduce the action of climate change on insects, we will drastically reduce our ability to build a sustainable future based on healthy, functional ecosystems. We discuss perspectives on relevant ways to conserve insects in the face of climate change, and we offer several key recommendations on management approaches that can be adopted, on policies that should be pursued, and on the involvement of the general public in the protection effort.

  • 6. Hedlund, Johanna
    et al.
    Ehrnsten, Eva
    Stockholm University, Faculty of Science, Stockholm University Baltic Sea Centre. University of Helsinki, Finland.
    Hayward, Christina
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Hayward, Alex
    New records of the Paleotropical migrant Hemianax ephippiger in the Caribbean and a review of its status in the Neotropics2020In: International journal of odonatology, ISSN 1388-7890, Vol. 23, no 4, p. 315-325Article, review/survey (Refereed)
    Abstract [en]

    Tropical America is currently experiencing the establishment of a new apex insect predator, the Paleotropical dragonfly Hemianax ephippiger (Odonata: Aeshnidae). H. ephippiger is migratory and is suggested to have colonised the eastern Neotropics by chance Trans-Atlantic displacement. We report the discovery of H. ephippiger at three new locations in the Caribbean, the islands of Bonaire, Isla de Coche (Venezuela), and Martinique, and we review its reported distribution across the Neotropics. We discuss the establishment of H. ephippiger as a new apex insect predator in the Americas, both in terms of ecological implications and the possible provision of ecosystem services. We also provide an additional new species record for Bonaire, Pantala hymenaea (Odonata: Libellulidae).

  • 7. Hedlund, Johanna S. U.
    et al.
    Lv, Hua
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. University of Greifswald, Germany.
    Hu, Gao
    Anderson, R. Charles
    Chapman, Jason W.
    Unraveling the World's Longest Non-stop Migration: The Indian Ocean Crossing of the Globe Skimmer Dragonfly2021In: Frontiers in Ecology and Evolution, E-ISSN 2296-701X, Vol. 9, article id 698128Article in journal (Refereed)
    Abstract [en]

    Insect migration redistributes enormous quantities of biomass, nutrients and species globally. A subset of insect migrants perform extreme long-distance journeys, requiring specialized morphological, physiological and behavioral adaptations. The migratory globe skimmer dragonfly (Pantala flavescens) is hypothesized to migrate from India across the Indian Ocean to East Africa in the autumn, with a subsequent generation thought to return to India from East Africa the following spring. Using an energetic flight model and wind trajectory analysis, we evaluate the dynamics of this proposed transoceanic migration, which is considered to be the longest regular non-stop migratory flight when accounting for body size. The energetic flight model suggests that a mixed strategy of gliding and active flapping would allow a globe skimmer to stay airborne for up to 230–286 h, assuming that the metabolic rate of gliding flight is close to that of resting. If engaged in continuous active flapping flight only, the flight time is severely reduced to ∼4 h. Relying only on self-powered flight (combining active flapping and gliding), a globe skimmer could cross the Indian Ocean, but the migration would have to occur where the ocean crossing is shortest, at an exceptionally fast gliding speed and with little headwind. Consequently, we deem this scenario unlikely and suggest that wind assistance is essential for the crossing. The wind trajectory analysis reveals intra- and inter-seasonal differences in availability of favorable tailwinds, with only 15.2% of simulated migration trajectories successfully reaching land in autumn but 40.9% in spring, taking on average 127 and 55 h respectively. Thus, there is a pronounced requirement on dragonflies to be able to select favorable winds, especially in autumn. In conclusion, a multi-generational, migratory circuit of the Indian Ocean by the globe skimmer is shown to be achievable, provided that advanced adaptations in physiological endurance, behavior and wind selection ability are present. Given that migration over the Indian Ocean would be heavily dependent on the assistance of favorable winds, occurring during a relatively narrow time window, the proposed flyway is potentially susceptible to disruption, if wind system patterns were to be affected by climatic change.

  • 8.
    Ittonen, Mats
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. Stockholm University, Faculty of Science, The Bolin Centre for Climate Research (together with KTH & SMHI).
    Roberts, Kevin T.
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. Stockholm University, Faculty of Science, The Bolin Centre for Climate Research (together with KTH & SMHI). University of Greifswald, Germany.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology. Stockholm University, Faculty of Science, The Bolin Centre for Climate Research (together with KTH & SMHI).
    A range-expanding butterfly is susceptible to cold and long winters but shows no signs of local adaptation to winter conditions2023In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 37, no 12, p. 3064-3078Article in journal (Refereed)
    Abstract [en]
    1. Numerous species shift or expand their ranges poleward in response to climate change. Even when expanding species follow their climatic niches, expanding range margin populations are likely to face unfamiliar environmental conditions and thus natural selection for local adaptation.
    2. The wall brown butterfly (Lasiommata megera) has expanded northward in Sweden in the years 2000–2020, most likely as a result of climate change, and has previously been shown to have evolved local adaptations to northern daylength conditions. This evolution has occurred despite hypothesised genetic constraints to adaptation at range margins.
    3. We studied local adaptation to winter conditions in four of the previously-studied L. megera populations, using a common garden laboratory experiment with a warm and short, an intermediate, and a cold and long winter treatment. We compared the winter and post-winter survival of caterpillars from two southern core range and two northern range margin populations in Sweden.
    4. During the experiment, we measured metabolic rates of a subset of diapausing caterpillars to test whether populations differ in metabolic suppression during diapause. Further, we measured supercooling points, which reflect lower lethal temperature in L. megera, of the same subset of caterpillars. We also compared supercooling points between L. megera and three closely related species with more northern distributions.
    5. Few individuals survived the coldest treatment all the way to successful adult emergence, so L. megera seems susceptible to cold winters. Individuals of northern descent did not survive cold winters any better than individuals from southern populations. Similarly, there were no signs of local adaptation in metabolic rates or supercooling points. The comparison among species did not reveal any clear relationship between geographical distribution and supercooling point.
    6. Although northern winters probably exert strong selection on L. megera, we provide comprehensive evidence for the lack of local adaptation to winter conditions. This contrasts with the previous finding of quickly evolved local adaptation in diapause timing, highlighting the need to consider how traits associated with different seasons differ in how they may evolve and facilitate climate change-induced range expansions.
  • 9. Jaitly, Rahul
    et al.
    Ehrnsten, Eva
    Stockholm University, Faculty of Science, Stockholm University Baltic Sea Centre.
    Hedlund, Johanna
    Cant, Michael
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. University of Greifswald, Germany.
    Hayward, Alexander
    The evolution of predator avoidance in cephalopods: A case of brain over brawn?2022In: Frontiers in Marine Science, E-ISSN 2296-7745, Vol. 9, article id 909192Article, review/survey (Refereed)
    Abstract [en]

    Predation is a major evolutionary driver of animal adaptation. However, understanding of anti-predator evolution is biased toward vertebrate taxa. Cephalopoda, a class in the invertebrate phylum Mollusca, are known for their diverse anti-predator strategies, characterised by their behavioural flexibility. While ancestral cephalopods were protected by a hard outer shell, extant cephalopods have greatly reduced their reliance on physical defences. Instead, cephalopods have evolved highly developed senses to identify potential threats, cryptic skin patterns to avoid detection, startle responses to deter attack, and elaborate means of escape. While cephalopod anti-predator repertoires are relatively well described, their evolution, and the selective pressures that shaped them, have received much less attention. This is despite their potential relevance, in turn, to elucidate evolution of the remarkable cognitive abilities of cephalopods. Here, we review cephalopod anti-predator evolution, considering four key aspects: (i) shell reduction and loss; (ii) the skin patterning system; (iii) the ecological context accompanying the evolution of advanced cognit.ive abilities; (iv) why the evolutionary trajectory taken by cephalopods is so unique among invertebrates. In doing so, we consider the unique physiology of cephalopods and discuss how this may have constrained or aided the development of their anti-predator repertoire. In particular, cephalopods are poorly equipped to defend themselves physically and escape predation by fish, due to a lack of comparable weaponry or musculature. We argue that this may have selected for alternative forms of defence, driving an evolutionary trajectory favouring crypsis and complex behaviours, and the promotion of sensory and cognitive adaptations. Unravelling the complexities of cephalopod anti-predator evolution remains challenging. However, recent technological developments available for cephalopod field and laboratory studies, coupled with new genomic data and analysis approaches, offer great scope to generate novel insights.

  • 10. Javal, Marion
    et al.
    Thomas, Saskia
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. Stellenbosch University, South Africa.
    Barton, Madeleine G.
    Conlong, Desmond E.
    Du Plessis, Anton
    Terblanche, John S.
    The Effect of Oxygen Limitation on a Xylophagous Insect's Heat Tolerance Is Influenced by Life-Stage Through Variation in Aerobic Scope and Respiratory Anatomy2019In: Frontiers in Physiology, E-ISSN 1664-042X, Vol. 10, article id 1426Article in journal (Refereed)
    Abstract [en]

    Temperature has a profound impact on insect fitness and performance via metabolic, enzymatic or chemical reaction rate effects. However, oxygen availability can interact with these thermal responses in complex and often poorly understood ways, especially in hypoxia-adapted species. Here we test the hypothesis that thermal limits are reduced under low oxygen availability - such as might happen when key life-stages reside within plants - but also extend this test to attempt to explain that the magnitude of the effect of hypoxia depends on variation in key respiration-related parameters such as aerobic scope and respiratory morphology. Using two life-stages of a xylophagous cerambycid beetle, Cacosceles (Zelogenes) newmannii we assessed oxygen-limitation effects on metabolic performance and thermal limits. We complement these physiological assessments with high-resolution 3D (micro-computed tomography scan) morphometry in both life-stages. Results showed that although larvae and adults have similar critical thermal maxima (CTmax) under normoxia, hypoxia reduces metabolic rate in adults to a greater extent than it does in larvae, thus reducing aerobic scope in the former far more markedly. In separate experiments, we also show that adults defend a tracheal oxygen (critical) setpoint more consistently than do larvae, indicated by switching between discontinuous gas exchange cycles (DGC) and continuous respiratory patterns under experimentally manipulated oxygen levels. These effects can be explained by the fact that the volume of respiratory anatomy is positively correlated with body mass in adults but is apparently size-invariant in larvae. Thus, the two life-stages of C. newmannii display key differences in respiratory structure and function that can explain the magnitude of the effect of hypoxia on upper thermal limits.

  • 11. Kenning, Matthes
    et al.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. University of Jyväskylä, Finland.
    Lindström, Magnus
    Harzsch, Steffen
    Heading which way? Y-maze chemical assays: not all crustaceans are alike2015In: Helgoland Marine Research, ISSN 1438-387X, E-ISSN 1438-3888, Vol. 69, no 3, p. 305-311Article in journal (Refereed)
    Abstract [en]

    In a world full of chemicals, many crustaceans rely on elaborate olfactory systems to guide behaviors related to finding food or to assess the presence of conspecifics and predators. We analyzed the responses of the isopod Saduria entomon to a range of stimuli by which the animal is likely to encounter in its natural habitat using a Y-maze bioassay. In order to document the efficiency of the experimental design, the same bioassay was used to test the behavior of the crayfish Procambarus fallax whose ability to track odors is well documented. The crayfish performed well in the Y-maze and were able to locate the source of a food-related odor with high fidelity. The isopod S. entomon reacted indifferently or with aversion to most of the stimuli applied. In 1800 trials, only four out of 15 different stimuli yielded statistically significant results, and only one odorant was found to be significantly attractive. The findings raise several questions whether the stimuli presented and/or the experimental setup used represents an ecologically relevant situation for S. entomon. In each instance, our experiments illustrate that established methods cannot be readily transferred from one species to another.

  • 12.
    Kivela, Sami M.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Do respiratory limitations affect metabolism of insect larvae before moulting? An empirical test at the individual level2016In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 219, no 19, p. 3061-3071Article in journal (Refereed)
    Abstract [en]

    Recent data suggest that oxygen limitation may induce moulting in larval insects. This oxygen-dependent induction of moulting (ODIM) hypothesis stems from the fact that the tracheal respiratory system of insects grows primarily at moults, whereas tissue mass increases massively between moults. This may result in a mismatch between oxygen supply and demand at the end of each larval instar because oxygen demand of growing tissues exceeds the relatively fixed supply capacity of the respiratory system. The ODIM hypothesis predicts that, within larval instars, respiration and metabolic rates of an individual larva first increase with increasing body mass but eventually level off once the supply capacity of the tracheal system starts to constrain metabolism. Here, we provide the first individual-level test of this key prediction of the ODIM hypothesis. We use a novel methodology where we repeatedly measure respiration and metabolic rates throughout the penultimate- and final-instar larvae in the butterfly Pieris napi. In the penultimate instar, respiration and metabolic rates gradually decelerated along with growth, supporting the ODIM hypothesis. However, respiration and metabolic rates increased linearly during growth in the final instar, contradicting the prediction. Moreover, our data suggest considerable variation among individuals in the association between respiration rate and mass in the final instar. Overall, the results provide partial support for the ODIM hypothesis and suggest that oxygen limitation may emerge gradually within a larval instar. The results also suggest that there may be different moult induction mechanisms in larva-to-larva moults compared with the final metamorphic moult.

  • 13. Kivelä, Sami M.
    et al.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Developmental plasticity in metabolism but not in energy reserve accumulation in a seasonally polyphenic butterfly2019In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 222, no 13, article id jeb202150Article in journal (Refereed)
    Abstract [en]

    The evolution of seasonal polyphenisms (discrete phenotypes in different annual generations) associated with alternative developmental pathways of diapause (overwintering) and direct development is favoured in temperate insects. Seasonal life history polyphenisms are common and include faster growth and development under direct development than in diapause. However, the physiological underpinnings of this difference remain poorly known despite its significance for understanding the evolution of polyphenisms. We measured respiration and metabolic rates through the penultimate and final larval instars in the butterfly Pieris napi and show that directly developing larvae grew and developed faster and had a higher metabolic rate than larvae entering pupal diapause. The metabolic divergence appeared only in the final instar, that is, after induction of the developmental pathway that takes place in the penultimate instar in P. napi. The accumulation of fat reserves during the final larval instar was similar under diapause and direct development, which was unexpected as diapause is predicted to select for exaggerated reserve accumulation. This suggests that overwinter survival in diapause does not require larger energy reserves than direct development, likely because of metabolic suppression in diapause pupae. The results, nevertheless, demonstrate that physiological changes coincide with the divergence of life histories between the alternative developmental pathways, thus elucidating the proximate basis of seasonal life history polyphenisms.

  • 14. Kivisaari, Kati
    et al.
    Boratyński, Zbyszek
    Lavrinienko, Anton
    Kesäniemi, Jenni
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Mappes, Tapio
    The effect of chronic low-dose environmental radiation on organ mass of bank voles in the Chernobyl exclusion zone2020In: International Journal of Radiation Biology, ISSN 0955-3002, E-ISSN 1362-3095, Vol. 96, no 10, p. 1254-1262Article in journal (Refereed)
    Abstract [en]

    Purpose: Animals are exposed to environmental ionizing radiation (IR) externally through proximity to contaminated soil and internally through ingestion and inhalation of radionuclides. Internal organs can respond to radioactive contamination through physiological stress. Chronic stress can compromise the size of physiologically active organs, but studies on wild mammal populations are scarce. The effects of environmental IR contamination on organ masses were studied by using a wild rodent inhabiting the Chernobyl exclusion zone (CEZ).

    Material and methods: The masses of brain, heart, kidney, spleen, liver and lung were assessed from bank voles (Myodes glareolus) captured from areas across radioactive contamination gradient within the CEZ. Relative organ masses were used to correct for the body mass of an individual.

    Results: Results showed a significant negative correlation between IR level in the environment and relative brain and kidney mass. A significant positive correlation between IR and relative heart mass was also found. Principal component analysis (PCA) also suggested positive relationship between IR and relative spleen mass; however, this relationship was not significant when spleen was analyzed separately. There was no apparent relationship between IR and relative liver or lung mass.

    Conclusions: Results suggest that in the wild populations even low but chronic doses of IR can lead to changes in relative organ mass. The novelty of these result is showing that exposure to low doses can affect the organ masses in similar fashion as previously shown on high, acute, radiation doses. These data support the hypothesis that wildlife might be more sensitive to IR than animals used in laboratory studies. However, more research is needed to rule out the other indirect effects such as radiosensitivity of the food sources or possible combined stress effects from e.g. infections.

  • 15. Kivisaari, Kati
    et al.
    Calhim, Sara
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. University of Jyväskylä, Finland; University of Greifswald, Germany.
    Boratyński, Zbyszek
    Mousseau, Timothy A.
    Møller, Anders P.
    Mappes, Tapio
    Chronic Background Radiation Correlates With Sperm Swimming Endurance in Bank Voles From Chernobyl2022In: Frontiers in Ecology and Evolution, E-ISSN 2296-701X, Vol. 9, article id 736389Article in journal (Refereed)
    Abstract [en]

    Sperm quantity and quality are key features explaining intra- and interspecific variation in male reproductive success. Spermatogenesis is sensitive to ionizing radiation and laboratory studies investigating acute effects of ionizing radiation have indeed found negative effects of radiation on sperm quantity and quality. In nature, levels of natural background radiation vary dramatically, and chronic effects of low-level background radiation exposure on spermatogenesis are poorly understood. The Chernobyl region offers a unique research opportunity for investigating effects of chronic low-level ionizing radiation on reproductive properties of wild organisms. We captured male bank voles (Myodes glareolus) from 24 locations in the Chernobyl exclusion zone in 2011 and 2015 and collected information on sperm morphology and kinetics. The dataset is limited in size and there overall was a relatively weak correlation between background radiation and sperm quality. Still, some correlations are worth discussing. First, mid-piece segments of spermatozoa tended to be smaller in bank vole males from areas with elevated background radiation levels. Second, we demonstrated a significant positive relationship between background radiation dose rates and the proportion of static spermatozoa among males within and among study locations after 10 as well as 60 min of incubation. Our results provide novel evidence of damaging effects of low dose ionizing radiation on sperm performance in wild rodent populations, and highlight that this topic requires further study across the natural gradients of background radiation that exist in nature.

  • 16.
    Lehmann, Philipp
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. University of Jyväskylä, Finland; Stellenbosch University, South Africa.
    Ammunét, Tea
    Barton, Madeleine
    Battisti, Andrea
    Eigenbrode, Sanford D.
    Jepsen, Jane Uhd
    Kalinkat, Gregor
    Neuvonen, Seppo
    Niemelä, Pekka
    Terblanche, John S.
    Økland, Bjørn
    Björkman, Christer
    Complex responses of global insect pests to climate warming2020In: Frontiers in Ecology and the Environment, ISSN 1540-9295, E-ISSN 1540-9309, Vol. 18, no 3, p. 141-150Article, review/survey (Refereed)
    Abstract [en]

    Although it is well known that insects are sensitive to temperature, how they will be affected by ongoing global warming remains uncertain because these responses are multifaceted and ecologically complex. We reviewed the effects of climate warming on 31 globally important phytophagous (plant-eating) insect pests to determine whether general trends in their responses to warming were detectable. We included four response categories (range expansion, life history, population dynamics, and trophic interactions) in this assessment. For the majority of these species, we identified at least one response to warming that affects the severity of the threat they pose as pests. Among these insect species, 41% showed responses expected to lead to increased pest damage, whereas only 4% exhibited responses consistent with reduced effects; notably, most of these species (55%) demonstrated mixed responses. This means that the severity of a given insect pest may both increase and decrease with ongoing climate warming. Overall, our analysis indicated that anticipating the effects of climate warming on phytophagous insect pests is far from straightforward. Rather, efforts to mitigate the undesirable effects of warming on insect pests must include a better understanding of how individual species will respond, and the complex ecological mechanisms underlying their responses.

  • 17.
    Lehmann, Philipp
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. University of Jyväskylä, Finland.
    Boratynski, Zbyszek
    Mappes, Tapio
    Mousseau, Timothy A.
    Møller, Anders P.
    Fitness costs of increased cataract frequency and cumulative radiation dose in natural mammalian populations from Chernobyl2016In: Scientific Reports, E-ISSN 2045-2322, Vol. 6, article id 19974Article in journal (Refereed)
    Abstract [en]

    A cataract is a clouding of the lens that reduces light transmission to the retina, and it decreases the visual acuity of the bearer. The prevalence of cataracts in natural populations of mammals, and their potential ecological significance, is poorly known. Cataracts have been reported to arise from high levels of oxidative stress and a major cause of oxidative stress is ionizing radiation. We investigated whether elevated frequencies of cataracts are found in eyes of bank voles Myodes glareolus collected from natural populations in areas with varying levels of background radiation in Chernobyl. We found high frequencies of cataracts in voles collected from different areas in Chernobyl. The frequency of cataracts was positively correlated with age, and in females also with the accumulated radiation dose. Furthermore, the number of offspring in female voles was negatively correlated with cataract severity. The results suggest that cataracts primarily develop as a function of ionizing background radiation, most likely as a plastic response to high levels of oxidative stress. It is therefore possible that the elevated levels of background radiation in Chernobyl affect the ecology and fitness of local mammals both directly through, for instance, reduced fertility and indirectly, through increased cataractogenesis.

  • 18.
    Lehmann, Philipp
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. Stellenbosch University, South Africa.
    Javal, Marion
    Du Plessis, Anton
    Terblanche, John S.
    Using μCT in live larvae of a large wood-boring beetle to study tracheal oxygen supply during development2021In: Journal of insect physiology, ISSN 0022-1910, E-ISSN 1879-1611, Vol. 130, article id 104199Article in journal (Refereed)
    Abstract [en]

    How respiratory structures vary with, or are constrained by, an animal’s environment is of central importance to diverse evolutionary and comparative physiology hypotheses. To date, quantifying insect respiratory structures and their variation has remained challenging due to their microscopic size, hence only a handful of species have been examined. Several methods for imaging insect respiratory systems are available, in many cases however, the analytical process is lethal, destructive, time consuming and labour intensive. Here, we explore and test a different approach to measuring tracheal volume using X-ray micro-tomography (μCT) scanning (at 15 μm resolution) on living, sedated larvae of the cerambycid beetle Cacosceles newmannii across a range of body sizes at two points in development. We provide novel data on resistance of the larvae to the radiation dose absorbed during μCT scanning, repeatability of imaging analyses both within and between time-points and, structural tracheal trait differences provided by different image segmentation methods. By comparing how tracheal dimension (reflecting metabolic supply) and basal metabolic rate (reflecting metabolic demand) increase with mass, we show that tracheal oxygen supply capacity increases during development at a comparable, or even higher rate than metabolic demand. Given that abundant gas delivery capacity in the insect respiratory system may be costly (due to e.g. oxygen toxicity or space restrictions), there are probably balancing factors requiring such a capacity that are not linked to direct tissue oxygen demand and that have not been thoroughly elucidated to date, including CO2 efflux. Our study provides methodological insights and novel biological data on key issues in rapidly quantifying insect respiratory anatomy on live insects.  

  • 19.
    Lehmann, Philipp
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. Stellenbosch University, South Africa .
    Javal, Marion
    Terblanche, John S.
    Oxygen limitation is not the cause of death during lethal heat exposure in an insect2019In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 15, no 1, article id 20180701Article in journal (Refereed)
    Abstract [en]

    Oxygen- and capacity-limited thermal tolerance (OCLTT) is a controversial hypothesis claiming to explain variation in, and mechanistically determine, animal thermal limits. The lack of support from Insecta is typically argued to be a consequence of their high-performance respiratory systems. However, no studies have reported internal body oxygen levels during thermal ramping so it is unclear if changes in ambient gas are partially or fully offset by a compensatory respiratory system. Here we provide such an assessment by simultaneously recording haemolymph oxygen (pO(2)) levels-as an approximation of tissue oxygenation-while experimentally manipulating ambient oxygen and subjecting organisms to thermal extremes in a series of thermolimit respirometry experiments using pupae of the butterfly Pieris napi. The main results are that while P. napi undergo large changes in haemolymph pO(2) that are positively correlated with experimental oxygen levels, haemolymph pO(2) is similar pre-and post-death during thermal assays. OCLTT predicts that reduction in body oxygen level should lead to a reduction in CTmax. Despite finding the former, there was no change in CTmax across a wide range of body oxygen levels. Thus, we argue that oxygen availability is not a functional determinant of the upper thermal limits in pupae of P. napi.

  • 20.
    Lehmann, Philipp
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. University of Jyväskylä, Finland.
    Kaunisto, Sirpa
    Kostal, Vladimir
    Margus, Aigi
    Zahradnickova, Helena
    Lindström, Leena
    Comparative Ecophysiology of Cold-Tolerance-Related Traits: Assessing Range Expansion Potential for an Invasive Insect at High Latitude2015In: Physiological and Biochemical Zoology, ISSN 1522-2152, E-ISSN 1537-5293, Vol. 88, no 3, p. 254-265Article in journal (Refereed)
    Abstract [en]

    Survival at high latitude requires the capability to cope with seasonally imposed stress, such as low winter temperatures or large temperature fluctuations. The Colorado potato beetle, Leptinotarsa decemlineata, is an invasive pest of potato that has rapidly spread from low latitudes to higher latitudes. During the last 30 years, a decrease in range expansion speed is apparent in Europe. We use a comparative approach to assess whether this could be due to an inability of L. decemlineata to cope with the harsher winters encountered at high latitude, when compared to two native northern chrysomelid beetles with similar overwintering ecology. We investigated several cold-tolerance-related physiological traits at different time points during winter. Cold tolerance followed a latitudinal pattern; the northern species were more tolerant to short-term subzero temperatures than the invasive L. decemlineata. The other northern species, the knotgrass leaf beetle, Chrysolina polita, was found to tolerate internal freezing. Interestingly, the pattern for overwinter survival at 5 degrees C was the opposite and higher in L. decemlineata than the northern species and could be related to behavioral differences between species in overwintering location selection and a potential physiological trade-off between tolerance to cold shock and to chronic cold exposure. Furthermore, while the northern species accumulated large amounts of different sugars and polyols with probable cryoprotectant functions, none were detected in L. decemlineata at high concentrations. This lack of cryoprotectant accumulation could explain the difference in cold tolerance between the species and also suggests that a lack of physiological capacity to tolerate low temperatures could slow further latitudinal range expansion of L. decemlineata.

  • 21.
    Lehmann, Philipp
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. University of Jyväskylä, Finland.
    Lyytinen, Anne
    Piiroinen, Saija
    Lindström, Leena
    Is a change in juvenile hormone sensitivity involved in range expansion in an invasive beetle?2015In: Frontiers in Zoology, E-ISSN 1742-9994, Vol. 12, article id 20Article in journal (Refereed)
    Abstract [en]

    Introduction: It has been suggested that rapid range expansion could proceed through evolution in the endocrinological machinery controlling life-history switches. Based on this we tested whether the Colorado potato beetle, Leptinotarsa decemlineata, which has rapidly expanded its range across latitudinal regions in Europe, and shows photoperiodic adaptation in overwintering initiation, has different sensitivities to juvenile hormone (JH) manipulation along a latitudinal gradient. Results: A factorial experiment where beetles were reared either under a long or short day photoperiod was performed. Hormone levels were manipulated by topical applications. An allatostatin mimic, H17, was used to decrease and a juvenile hormone III analogue, pyriproxyfen, was used to increase the hormone levels. The effects of photoperiod and hormone manipulations on fecundity and overwintering related burrowing were monitored. Application of H17 decreased fecundity but did not induce overwintering related burrowing. Manipulation with pyriproxyfen increased fecundity and delayed burrowing. While small population-dependent differences in responsiveness to the topical application treatments were observed in fecundity, none were seen in overwintering related burrowing. Conclusions: The results indicate that the rapid photoperiodic adaptation manifested in several life-history and physiological traits in L. decemlineata in Europe is unlikely a result of population dependent differences in JH III sensitivity. While other endocrine factors cannot be ruled out, more likely mechanisms could be genetic changes in upstream elements, such as the photoperiodic clock or the insulin signaling pathway.

  • 22.
    Lehmann, Philipp
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. University of Jyväskylä, Finland.
    Lyytinen, Anne
    Piiroinen, Saija
    Lindström, Leena
    Latitudinal differences in diapause related photoperiodic responses of European Colorado potato beetles (Leptinotarsa decemlineata)2015In: Evolutionary Ecology, ISSN 0269-7653, E-ISSN 1573-8477, Vol. 29, no 2, p. 269-282Article in journal (Refereed)
    Abstract [en]

    Many organisms use photoperiodic cues to assess seasonal progression and pace their phenology. As photoperiod correlates with latitude, range expansions in seasonal environments may require re-synchronization of phenology and life-history traits with novel season length. Adaptive resynchronization takes time, and hence might be one factor explaining why range expansion to higher latitudes often is slow. Studies investigating latitudinal clines in photoperiodic traits often focus on species or populations which are well established. However, studying organisms which are in the process of expanding their range can provide valuable information on the evolutionary ecological mechanisms driving the adaptive synchronization to seasonal environments. The Colorado potato beetle, Leptinotarsa decemlineata, is a pest of potato, which rapidly has spread towards higher latitudes. We studied whether beetles from six European populations along a latitudinal axis are synchronized with their local photoperiodic environmental conditions. Variation in critical photoperiod (when 50 % of individuals make the decision to overwinter), diapause incidence, burrowing age for diapause and resurfacing behaviour were investigated by maintaining beetles under six photoperiods. The beetles showed a clear latitudinal pattern in diapause incidence and burrowing age for diapause but not in critical photoperiod. Resurfacing behaviour of burrowed beetles increased with the length of the photoperiod, which through unsynchronized overwintering behaviour could lead to high overwintering mortality. Thus, while synchronization of diapause preparation with local photoperiodic conditions can be one reason explaining the success of L. decemlineata in expanding to higher latitudes, further northward range expansion could be constrained by inherent difficulties to initiate overwintering under very long photoperiods.

  • 23.
    Lehmann, Philipp
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. University of Jyväskylä, Finland.
    Margus, Aigi
    Lindström, Leena
    Inheritance patterns of photoperiodic diapause induction in Leptinotarsa decemlineata2016In: Physiological entomology (Print), ISSN 0307-6962, E-ISSN 1365-3032, Vol. 41, no 3, p. 218-223Article in journal (Refereed)
    Abstract [en]

    Photoperiod is a reliable indicator of season and an important cue that many insects use for phenological synchronization. Undergoing range expansion insects can face a change in the local photoperiod to which they need to resynchronize. Rapid range expansion can be associated with rapid photoperiodic adaptation, which can be associated with intense selection on strongly heritable polygenic traits. Alternatively, it is proposed that, in insects with an XO sex-determination system, genes with large effect residing on the sex chromosome could drive photoperiodic adaptation because the gene or genes are exposed to selection in the sex carrying only a single X-chromosome. The present study seeks to understand which of these alternatives more likely explains the rapid photoperiodic adaptation in European Colorado potato beetles Leptinotarsa decemlineata Say. Diapause induction is assessed in beetles from a northern and a southern population, as well as from reciprocal hybrid crosses between the northern and southern population, when reared at an intermediate length photoperiod. The crosses within population display the expected responses, with the northern and southern populations showing high and low diapause propensity, respectively. The hybrids show intermediate responses in all studied traits. No clear difference in the responses in hybrids depending on the latitudinal origin of their father or mother is detected, even though partial paternal line dominance is seen in the responses of male beetles in one hybrid cross. These results therefore indicate that, in L. decemlineata, photoperiodic diapause induction is strongly heritable, and has an additive polygenic autosomal background.

  • 24.
    Lehmann, Philipp
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Carlsson, Mikael A.
    Stockholm University, Faculty of Science, Department of Zoology.
    Idiosyncratic development of sensory structures in brains of diapausing butterfly pupae: implications for information processing2017In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 284, no 1858, article id 20170897Article in journal (Refereed)
    Abstract [en]

    Diapause is an important escape mechanism from seasonal stress in many insects. A certain minimum amount of time in diapause is generally needed in order for it to terminate. The mechanisms of time-keeping in diapause are poorly understood, but it can be hypothesized that a well-developed neural system is required. However, because neural tissue is metabolically costly to maintain, there might exist conflicting selective pressures on overall brain development during diapause, on the one hand to save energy and on the other hand to provide reliable information processing during diapause. We performed the first ever investigation of neural development during diapause and non-diapause (direct) development in pupae of the butterfly Pieris napi from a population whose diapause duration is known. The brain grew in size similarly in pupae of both pathways up to 3 days after pupation, when development in the diapause brain was arrested. While development in the brain of direct pupae continued steadily after this point, no further development occurred during diapause until temperatures increased far after diapause termination. Interestingly, sensory structures related to vision were remarkably well developed in pupae from both pathways, in contrast with neuropils related to olfaction, which only developed in direct pupae. The results suggest that a well-developed visual system might be important for normal diapause development.

  • 25.
    Lehmann, Philipp
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. University of Jyväskylä, Finland.
    Piiroinen, Saija
    Lyytinen, Anne
    Lindstroem, Leena
    Responses in metabolic rate to changes in temperature in diapausing Colorado potato beetle Leptinotarsa decemlineata from three European populations2015In: Physiological entomology (Print), ISSN 0307-6962, E-ISSN 1365-3032, Vol. 40, no 2, p. 123-130Article in journal (Refereed)
    Abstract [en]

    Many insects survive adverse periods in seasonal environments by entering diapause, a deep resting stage, during which energy consumption is typically low and gas exchange is in the form of a discontinuous gas exchange cycle (DGC). Because insects in high-latitude environments are severely time constrained during summer, an effective diapause termination with careful regulation of metabolic rate is important. The present study examines whether diapausing Colorado potato beetles Leptinotarsa decemlineataSay originating from three latitudinally different regions in Europe differ in their quantitative or qualitative gas exchange patterns in response to an increasing temperature. Overall production of gaseous CO2, as well as qualitative patterns relating to the DGC, are measured at a late stage of diapause at four different temperatures in increasing order from 13, 18, 23 to 28 degrees C. Overall CO2 production is found to be lower in the two northern populations (61 degrees 49N and 55 degrees 75N) compared with the southernmost population (45 degrees 48N) but increases as a function of temperature in all populations in a similar way. However, in the northern populations, raising the temperature increases the amount of CO2 discharged during single DGC peaks, whereas the DGC frequency remains relatively unchanged. By contrast, in the southernmost population, the amount of CO2 discharged during individual DGC peaks remains relatively unchanged, whereas the DGC frequency increases as a function of temperature. The observed differences may relate to water retention benefits or, alternatively, energetic benefits relating to heightened gas exchange efficiency in hypoxic or hypercapnic environments. Overall, the results suggest that, although populations of L. decemlineata may have similar thermal sensitivities, they have different qualitative strategies to regulate metabolic re-activation at diapause termination.

  • 26.
    Lehmann, Philipp
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Pruisscher, Peter
    Stockholm University, Faculty of Science, Department of Zoology.
    Kostal, Vladimir
    Moos, Martin
    Simek, Petr
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology.
    Agren, Rasmus
    Varemo, Leif
    Wiklund, Christer
    Stockholm University, Faculty of Science, Department of Zoology.
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Metabolome dynamics of diapause in the butterfly Pieris napi: distinguishing maintenance, termination and post-diapause phases2018In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 221, no 2, article id UNSP jeb169508Article in journal (Refereed)
    Abstract [en]

    Diapause is a deep resting stage facilitating temporal avoidance of unfavourable environmental conditions, and is used by many insects to adapt their life cycle to seasonal variation. Although considerable work has been invested in trying to understand each of the major diapause stages (induction, maintenance and termination), we know very little about the transitions between stages, especially diapause termination. Understanding diapause termination is crucial for modelling and predicting spring emergence and winter physiology of insects, including many pest insects. In order to gain these insights, we investigated metabolome dynamics across diapause development in pupae of the butterfly Pieris napi, which exhibits adaptive latitudinal variation in the length of endogenous diapause that is uniquely well characterized. By employing a time-series experiment, we show that the whole-body metabolome is highly dynamic throughout diapause and differs between pupae kept at a diapause-terminating (low) temperature and those kept at a diapause-maintaining (high) temperature. We showmajor physiological transitions through diapause, separate temperature-dependent from temperature-independent processes and identify significant patterns of metabolite accumulation and degradation. Together, the data show that although the general diapause phenotype (suppressed metabolism, increased cold tolerance) is established in a temperature-independent fashion, diapause termination is temperature dependent and requires a cold signal. This revealed several metabolites that are only accumulated under diapause-terminating conditions and degraded in a temperature-unrelated fashion during diapause termination. In conclusion, our findings indicate that some metabolites, in addition to functioning as cryoprotectants, for example, are candidates for having regulatory roles as metabolic clocks or time-keepers during diapause.

  • 27.
    Lehmann, Philipp
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Pruisscher, Peter
    Stockholm University, Faculty of Science, Department of Zoology.
    Posledovich, Diana
    Stockholm University, Faculty of Science, Department of Zoology.
    Carlsson, Mikael
    Stockholm University, Faculty of Science, Department of Zoology.
    Käkelä, Reijo
    Tang, Patrik
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology.
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology.
    Wiklund, Christer
    Stockholm University, Faculty of Science, Department of Zoology.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Energy and lipid metabolism during direct and diapause development in a pierid butterfly2016In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 219, no 19, p. 3049-3060Article in journal (Refereed)
    Abstract [en]

    Diapause is a fundamental component of the life-cycle in the majority of insects living in environments characterized by strong seasonality. The present study addresses poorly understood associations and trade-offs between endogenous diapause duration, thermal sensitivity of development, energetic cost of development and cold tolerance. Diapause intensity, metabolic rate trajectories and lipid profiles of directly developing and diapausing animals were studied using pupae and adults of Pieris napi butterflies from a population for which endogenous diapause is well studied. Endogenous diapause was terminated after 3 months and termination required chilling. Metabolic and postdiapause development rates increased with diapause duration, while the metabolic cost of postdiapause development decreased, indicating that once diapause is terminated development proceeds at a low rate even at low temperature. Diapausing pupae had larger lipid stores than the directly developing pupae and lipids constituted the primary energy source during diapause. However, during diapause lipid stores did not decrease. Thus, despite lipid catabolism meeting the low energy costs of the diapausing pupae, primary lipid store utilization did not occur until the onset of growth and metamorphosis in spring. In line with this finding, diapausing pupae contained low amounts of mitochondria-derived cardiolipins, which suggests a low capacity for fatty acid β-oxidation. While ontogenic development had a large effect on lipid and fatty acid profiles, only small changes in these were seen during diapause. The data therefore indicate that the diapause lipidomic phenotype is built early, when pupae are still at high temperature, and retained until diapause post-diapause development.

  • 28.
    Lehmann, Philipp
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Van der Bijl, Wouter
    Stockholm University, Faculty of Science, Department of Zoology.
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology.
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Timing of diapause termination in relation to variation in winter climate2017In: Physiological entomology (Print), ISSN 0307-6962, E-ISSN 1365-3032, Vol. 42, no 3, p. 232-238Article in journal (Refereed)
    Abstract [en]

    In temperate insects, winters are typically endured by entering diapause, which comprises a deep resting stage. Correct timing of diapause termination is vital for synchronization of emergence with conspecifics and for mobilizing resources when conditions for growth and reproduction become favourable. Although critical to survival, the intrinsic and extrinsic drivers of diapause termination timing are poorly understood. In the present study, we investigate diapause development under a range of durations (10-24weeks) spent at different temperatures (-2 to 10 degrees C) in the pupal diapausing butterfly Pieris napi Linnaeus (Lepidoptera: Pieridae). We determine: (i) the maximum cold temperature for diapause development; (ii) if pupae in diapause count cold days or cold sums; and (iii) whether diapause termination is distinct or gradual. The results indicate large and idiosyncratic effects of high and low nonlethal temperatures on diapause development in P. napi. Although all temperatures tested lead to diapause termination, a thermal optimum between 2 and 4 degrees C is observed. Lower temperatures lead to decreased eclosion propensity, whereas higher temperatures slow down development and increase emergence desynchronization. These data suggest that, rather than a simple cold-summing process with a distinct diapause termination point, there are trade-offs between time and temperature at the low and high end of the thermal range, resulting in a nonlinear thermal landscape showing a ridge of increasing eclosion propensity at moderate temperatures. The present study suggests that the effects of temperature on diapause development should be included in projections on post-winter phenology models of insects, including pest species.

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  • 29.
    Lehmann, Philipp
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. University of Jyväskylä, Finland.
    Westberg, Melissa
    Tang, Patrik
    Lindström, Leena
    Käkelä, Reijo
    The Diapause Lipidomes of Three Closely Related Beetle Species Reveal Mechanisms for Tolerating Energetic and Cold Stress in High-Latitude Seasonal Environments2020In: Frontiers in Physiology, E-ISSN 1664-042X, Vol. 11, article id 576617Article in journal (Refereed)
    Abstract [en]

    During winter insects face energetic stress driven by lack of food, and thermal stress due to sub-optimal and even lethal temperatures. To survive, most insects living in seasonal environments such as high latitudes, enter diapause, a deep resting stage characterized by a cessation of development, metabolic suppression and increased stress tolerance. The current study explores physiological adaptations related to diapause in three beetle species at high latitudes in Europe. From an ecological perspective, the comparison is interesting since one species (Leptinotarsa decemlineata) is an invasive pest that has recently expanded its range into northern Europe, where a retardation in range expansion is seen. By comparing its physiological toolkit to that of two closely related native beetles (Agelastica alni and Chrysolina polita) with similar overwintering ecology and collected from similar latitude, we can study if harsh winters might be constraining further expansion. Our results suggest all species suppress metabolism during diapause and build large lipid stores before diapause, which then are used sparingly. In all species diapause is associated with temporal shifts in storage and membrane lipid profiles, mostly in accordance with the homeoviscous adaptation hypothesis, stating that low temperatures necessitate acclimation responses that increase fluidity of storage lipids, allowing their enzymatic hydrolysis, and ensure integral protein functions. Overall, the two native species had similar lipidomic profiles when compared to the invasive species, but all species showed specific shifts in their lipid profiles after entering diapause. Taken together, all three species show adaptations that improve energy saving and storage and membrane lipid fluidity during overwintering diapause. While the three species differed in the specific strategies used to increase lipid viscosity, the two native beetle species showed a more canalized lipidomic response, than the recent invader. Since close relatives with similar winter ecology can have different winter ecophysiology, extrapolations among species should be done with care. Still, range expansion of the recent invader into high latitude habitats might indeed be retarded by lack of physiological tools to manage especially thermal stress during winter, but conversely species adapted to long cold winters may face these stressors as a consequence of ongoing climate warming.

  • 30.
    Liao, Sifang
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Post, Stephanie
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Veenstra, Jan A.
    Tatar, Marc
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology.
    Regulatory Roles of Drosophila Insulin-Like Peptide 1 (DILP1) in Metabolism Differ in Pupal and Adult Stages2020In: Frontiers in Endocrinology, E-ISSN 1664-2392, Vol. 11, article id 180Article in journal (Refereed)
    Abstract [en]

    The insulin/IGF-signaling pathway is central in control of nutrient-dependent growth during development, and in adult physiology and longevity. Eight insulin-like peptides (DILP1-8) have been identified in Drosophila, and several of these are known to regulate growth, metabolism, reproduction, stress responses, and lifespan. However, the functional role of DILP1 is far from understood. Previous work has shown that dilp1/DILP1 is transiently expressed mainly during the pupal stage and the first days of adult life. Here, we study the role of dilp1 in the pupa, as well as in the first week of adult life, and make some comparisons to dilp6 that displays a similar pupal expression profile, but is expressed in fat body rather than brain neurosecretory cells. We show that mutation of dilp1 diminishes organismal weight during pupal development, whereas overexpression increases it, similar to dilp6 manipulations. No growth effects of dilp1 or dilp6 manipulations were detected during larval development. We next show that dilp1 and dilp6 increase metabolic rate in the late pupa and promote lipids as the primary source of catabolic energy. Effects of dilp1 manipulations can also be seen in the adult fly. In newly eclosed female flies, survival during starvation is strongly diminished in dilp1 mutants, but not in dilp2 and dilp1/dilp2 mutants, whereas in older flies, only the double mutants display reduced starvation resistance. Starvation resistance is not affected in male dilp1 mutant flies, suggesting a sex dimorphism in dilp1 function. Overexpression of dilp1 also decreases survival during starvation in female flies and increases egg laying and decreases egg to pupal viability. In conclusion, dilp1 and dilp6 overexpression promotes metabolism and growth of adult tissues during the pupal stage, likely by utilization of stored lipids. Some of the effects of the dilp1 manipulations may carry over from the pupa to affect physiology in young adults, but our data also suggest that dilp1 signaling is important in metabolism and stress resistance in the adult stage.

  • 31.
    Lindestad, Olle
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    von Schmalensee, Loke
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Variation in butterfly diapause duration in relation to voltinism suggests adaptation to autumn warmth, not winter cold2020In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 34, no 5, p. 1029-1040Article in journal (Refereed)
    Abstract [en]

    The life cycles of animals vary in relation to local climate, as a result of both direct environmental effects and population-level variation in plastic responses. Insects often respond to the approach of winter by entering diapause, a hormonally programmed resting state where development is suspended and metabolism suppressed. Populations often differ in the duration of diapause, but the adaptive reasons for this are unclear. We performed a common-garden overwintering experiment with respirometric measurements in order to investigate the progression of diapause in the butterfly Pararge aegeria. Both the duration of diapause and the depth of metabolic suppression were shown to vary between populations. In contrast to previous results from various insects, diapause duration did not correspond to the local length of winter. Instead, the observed pattern was consistent with a scenario in which diapause duration is primarily a product of selection for suppressed metabolism during warm autumn conditions. The relationship between optimal diapause duration and the length of the warm season is complicated by variation in the number of yearly generations (voltinism). These results shed new light on variation in diapause ecophysiology, and highlight voltinism as an integrated product of selection at multiple points in the seasonal cycle. A free Plain Language Summary can be found within the Supporting Information of this article.

  • 32. Margus, Aigi
    et al.
    Piiroinen, Saija
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. University of Jyväskylä, Finland; Greifswald University, Germany.
    Grapputo, Alessandro
    Gilbert, Leona
    Chen, Yolanda H.
    Lindström, Leena
    Sequence variation and regulatory variation in acetylcholinesterase genes contribute to insecticide resistance in different populations of Leptinotarsa decemlineata2021In: Ecology and Evolution, E-ISSN 2045-7758, Vol. 11, no 22, p. 15995-16005Article in journal (Refereed)
    Abstract [en]

    Although insect herbivores are known to evolve resistance to insecticides through multiple genetic mechanisms, resistance in individual species has been assumed to follow the same mechanism. While both mutations in the target site insensitivity and increased amplification are known to contribute to insecticide resistance, little is known about the degree to which geographic populations of the same species differ at the target site in a response to insecticides. We tested structural (e.g., mutation profiles) and regulatory (e.g., the gene expression of Ldace1 and Ldace2, AChE activity) differences between two populations (Vermont, USA and Belchow, Poland) of the Colorado potato beetle, Leptinotarsa decemlineata in their resistance to two commonly used groups of insecticides, organophosphates, and carbamates. We established that Vermont beetles were more resistant to azinphos-methyl and carbaryl insecticides than Belchow beetles, despite a similar frequency of resistance-associated alleles (i.e., S291G) in the Ldace2 gene. However, the Vermont population had two additional amino acid replacements (G192S and F402Y) in the Ldace1 gene, which were absent in the Belchow population. Moreover, the Vermont population showed higher expression of Ldace1 and was less sensitive to AChE inhibition by azinphos-methyl oxon than the Belchow population. Therefore, the two populations have evolved different genetic mechanisms to adapt to organophosphate and carbamate insecticides.

  • 33. Margus, Aigi
    et al.
    Piiroinen, Saija
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. University of Jyväskylä, Finland.
    Tikka, Santtu
    Karvanen, Juha
    Lindström, Leena
    Sublethal Pyrethroid Insecticide Exposure Carries Positive Fitness Effects Over Generations in a Pest Insect2019In: Scientific Reports, E-ISSN 2045-2322, Vol. 9, article id 11320Article in journal (Refereed)
    Abstract [en]

    Stress tolerance and adaptation to stress are known to facilitate species invasions. Many invasive species are also pests and insecticides are used to control them, which could shape their overall tolerance to stress. It is well-known that heavy insecticide usage leads to selection of resistant genotypes but less is known about potential effects of mild sublethal insecticide usage. We studied whether stressful, sublethal pyrethroid insecticide exposure has within-generational and/or maternal transgenerational effects on fitness-related traits in the Colorado potato beetle (Leptinotarsa decemlineata) and whether maternal insecticide exposure affects insecticide tolerance of offspring. Sublethal insecticide stress exposure had positive within-and transgenerational effects. Insecticide-stressed larvae had higher adult survival and higher adult body mass than those not exposed to stress. Furthermore, offspring whose mothers were exposed to insecticide stress had higher larval and pupal survival and were heavier as adults (only females) than those descending from control mothers. Maternal insecticide stress did not explain differences in lipid content of the offspring. To conclude, stressful insecticide exposure has positive transgenerational fitness effects in the offspring. Therefore, unsuccessful insecticide control of invasive pest species may lead to undesired side effects since survival and higher body mass are known to facilitate population growth and invasion success.

  • 34.
    Nielsen, Matthew E.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. Greifswald University, Germany.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Longer and warmer prewinter periods reduce post-winter fitness in a diapausing insect2022In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 36, no 5, p. 1151-1162Article in journal (Refereed)
    Abstract [en]
    1. Diapause is considered an important adaptation for survival of winter; however, insects often enter diapause long before its onset. Thus, diapausing insects must also be able to survive these prewinter conditions which warm temperatures could make quite energetically taxing despite relative inactivity.
    2. We tested for both immediate and delayed fitness effects of prewinter conditions in diapausing Pieris napi butterfly pupae, experimentally exposing them to different prewinter treatments in a factorial design. We placed diapausing pupae at one of three temperatures (15, 20 and 25°C) for 1 to 16 weeks, followed by the same standardized winter for all individuals.
    3. We monitored survival of pupae at multiple points during the experiment, including after winter, as well as their change in mass. For a subset of individuals, we also made repeated metabolic measurements.
    4. We found substantial weight loss during prewinter warm periods, greater during longer prewinter treatments at higher temperatures. This weight loss was associated with elevated metabolic rates at higher temperatures which increased over the duration of the prewinter treatment.
    5. Although we found little prewinter mortality associated with these conditions, mortality was much greater post-winter for individuals in long, warm prewinter treatments and the dry mass of adults that did survive these conditions was lower, highlighting the need to understand chronic or delayed effects of stress on fitness.
    6. Ultimately, we found substantial fitness consequences of prewinter conditions for a diapausing insect. Given that climate change will make these prewinter periods both longer and more intense, it will be important to understand how dormant organisms tolerate or reduce the length of these dormant, inactive periods.
  • 35.
    Pruisscher, Peter
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    de la Paz Celorio-Mancera, Maria
    Stockholm University, Faculty of Science, Department of Zoology.
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Wheat, Christopher
    Stockholm University, Faculty of Science, Department of Zoology.
    Transcriptomic profiling of pupal diapause in the butterfly Pieris napiManuscript (preprint) (Other academic)
    Abstract [en]

    Diapause is a common means of overwintering among insects that is characterized by arrested development and increased tolerance to stress and cold. Diapause is a vital aspect of life cycle timing, and while the expression of specific candidate genes during diapause have been investigated, there is no general understanding of the dynamics of the transcriptional landscape as a whole during the extended diapause phenotype. Here we performed a time-course experiment using RNA-Seq on the head and abdomen in the butterfly Pieris napi. In both body parts, comparing diapause and directly developing siblings, differentially expressed genes are detected from the first day of pupal development and onwards, varying dramatically across these formative stages. During diapause there are strong gene expression dynamics independent of environmental conditions, revealing a pre-programmed transcriptional landscape that is active during the winter. Different biological processes appear to be active in the two body parts. Still, adults emerging from either the direct or diapause pathways do not show large transcriptomic differences, suggesting the adult phenotype is strongly canalized.

  • 36.
    Pruisscher, Peter
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology.
    Extensive transcriptomic profiling of pupal diapause in a butterfly reveals a dynamic phenotype2022In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 31, no 4, p. 1269-1280Article in journal (Refereed)
    Abstract [en]

    Diapause is a common adaptation for overwintering in insects that is characterized by arrested development and increased tolerance to stress and cold. While the expression of specific candidate genes during diapause have been investigated, there is no general understanding of the dynamics of the transcriptional landscape as a whole during the extended diapause phenotype. Such a detailed temporal insight is important as diapause is a vital aspect of life cycle timing. Here, we performed a time-course experiment using RNA-Seq on the head and abdomen in the butterfly Pieris napi. In both body parts, comparing diapausing and nondiapausing siblings, differentially expressed genes are detected from the first day of pupal development and onwards, varying dramatically across these formative stages. During diapause there are strong gene expression dynamics present, revealing a preprogrammed transcriptional landscape that is active during the winter. Different biological processes appear to be active in the two body parts. Finally, adults emerging from either the direct or diapause pathways do not show large transcriptomic differences, suggesting the adult phenotype is strongly canalized. 

  • 37. Rainio, Miia J.
    et al.
    Margus, Aigi
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. University of Jyväskylä, Finland.
    Helander, Marjo
    Lindstrom, Leena
    Effects of a glyphosate-based herbicide on survival and oxidative status of a non-target herbivore, the Colorado potato beetle (Leptinotarsa decenilineata)2019In: Comparative Biochemistry and Physiology - Part C: Toxicology & Pharmacology, ISSN 1532-0456, E-ISSN 1878-1659, Vol. 215, p. 47-55Article in journal (Refereed)
    Abstract [en]

    Glyphosate is the globally most used herbicide against a wide range of weeds. Glyphosate has been considered safe to animals as it mainly targets physiological pathways in plants. However, recent toxicological studies have revealed that glyphosate can cause various toxic effects also on animals. In this study, we investigated the direct toxic effects of a glyphosate-based herbicide (GBH, Roundup (R) Bio) on 1) survival and 2) oxidative status of a non-target herbivore by using Colorado potato beetles (Leptinotarsa decemlineata), originating from Poland and USA, as model species. Larvae were randomly divided into three groups: 1) high concentration (100% Roundup Bio, 360 g/l), 2) low concentration (1.5% Roundup Bio) and 3) control group (water). Larvae were exposed to Roundup for different time periods: 2 h, 24 h, 48 h, 72 h and 96 h. Larval survival decreased in the group treated with high concentration of GBH compared to controls, whereas the low concentration group did not differ from the control group. GBH treatment had no association with oxidative status biomarkers (i.e. catalase, superoxide dismutase, glutathione-S-transferase, glutathione and glutathione related enzymes), but increased lipid hydro-peroxide levels after 2h exposure, suggesting increased oxidative damage soon after the exposure. Larvae of different origin also differed in their oxidative status, indicating population-dependent differences in antioxidant defence system. Environmentally relevant concentrations of GBH are not likely to affect larval survival, but high concentrations can reduce survival and increase oxidative damage of non-target herbivores. Also, populations of different origin and pesticide usage history can differ in their tolerance to GBH.

  • 38.
    Roberts, Kevin
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. University of Greifswald, Germany.
    Steward, Rachel A.
    Stockholm University, Faculty of Science, Department of Zoology. Lund University, Sweden.
    Süess, Philip
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. Stockholm University, Faculty of Science, The Bolin Centre for Climate Research (together with KTH & SMHI). University of Greifswald, Germany.
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics. Stockholm University, Faculty of Science, Department of Zoology, Systematic Zoology.
    A time course analysis through diapause reveals dynamic temporal patterns of microRNAs associated with endocrine regulation in the butterfly Pieris napi2024In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294XArticle in journal (Refereed)
    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.

  • 39.
    Roberts, Kevin
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Szejner-Sigal, Andre
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. Stockholm University, Faculty of Science, The Bolin Centre for Climate Research (together with KTH & SMHI).
    Seasonal energetics: are insects constrained by energy during dormancy?2023In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 226, no 21, article id jeb245782Article in journal (Refereed)
    Abstract [en]

    In seasonal environments, many animals, including insects, enter dormancy, where they are limited to a fixed energy budget. The inability to replenish energetic stores during these periods suggests insects should be constrained by pre-dormancy energy stores. Over the last century, the community of researchers working on survival during dormancy has operated under the strong assumption that energy limitation is a key fitness trait driving the evolution of seasonal strategies. That is, energy use has to be minimized during dormancy because insects otherwise run out of energy and die during dormancy, or are left with too little energy to complete development, reproductive maturation or other costly post-dormancy processes such as dispersal or nest building. But if energy is so strongly constrained during dormancy, how can some insects - even within the same species and population - be dormant in very warm environments or show prolonged dormancy for many successive years? In this Commentary, we discuss major assumptions regarding dormancy energetics and outline cases where insects appear to align with our assumptions and where they do not. We then highlight several research directions that could help link organismal energy use with landscape-level changes. Overall, the optimal energetic strategy during dormancy might not be to simply minimize metabolic rate, but instead to maintain a level that matches the demands of the specific life-history strategy. Given the influence of temperature on energy use rates of insects in winter, understanding dormancy energetic strategies is critical in order to determine the potential impacts of climate change on insects in seasonal environments.

  • 40. Salman, Md Habibur R.
    et al.
    Giomi, Folco
    Laparie, Mathieu
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Pitacco, Andrea
    Battisti, Andrea
    Termination of pupal diapause in the pine processionary moth Thaumetopoea pityocampa2019In: Physiological entomology (Print), ISSN 0307-6962, E-ISSN 1365-3032, Vol. 44, no 1, p. 53-59Article in journal (Refereed)
    Abstract [en]

    Diapause development is a complex process involving several eco-physiological phases. Understanding these phases, especially diapause termination, is vital for interpreting the life history of many insect species and for developing suitable predictive models of population dynamics. The pine processionary moth is a major defoliator of pine and a vertebrate health hazard in the Mediterranean region. This species can display either univoltine or semivoltine development, with a pupal diapause extending from a few months to several years, respectively. Although the ecological and applied importance of diapause is acknowledged, its physiological regulation in either case remains obscure. In the present study, we characterize pre-termination, termination and post-termination phases of pupae developing as univoltine or remaining in prolonged diapause. Changes in metabolic activity are monitored continuously using thermocouples, comprising a novel method based on direct calorimetry, and periodically by use of O-2 respirometry. The two methods clearly detect diapause termination in both types of pupae before any visible morphological or behavioural changes can be observed. Univoltine individuals are characterized by an increase in metabolic activity from pre-termination through to termination and post-termination, ultimately resulting in emergence. Remarkably, a synchronous termination is observed in individuals that enter prolonged diapause instead of emerging; however, in these pupae, the increased metabolic activity is only transient. The present study represents a starting point toward understanding the eco-physiology of diapause development processes in the pupae of the pine processionary moth.

  • 41. Salman, Md Habibur Rahman
    et al.
    Giomi, Folco
    Laparie, Mathieu
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Battisti, Andrea
    Prepupal diapause synchronizes adult emergence in the pine processionary moth Thaumetopoea pityocampa (Lepidoptera: Notodontidae)2018In: Agricultural and Forest Entomology, ISSN 1461-9555, E-ISSN 1461-9563, Vol. 20, no 4, p. 582-588Article in journal (Refereed)
    Abstract [en]

    1 Insects with short-lived adults must synchronize their emergence to maximize fitness. 2 However, pre-imaginal development time often varies among individuals as a result of exposure to varied abiotic and biotic factors; therefore, mechanisms adjusting pre-imaginal development time are expected. 3 Larvae of the pine processionary moth feed throughout the winter and conclude their development with characteristic processions in spring, leaving the trees to pupate in soil. 4 The procession period can be as long as 2 months in some regions because of prior desynchronization of larval colonies, whereas the emergence period of the adults in summer remains short (less than 1 month). 5 Through weekly sampling of larvae leaving trees to pupate in soil and subsequent rearing under field and laboratory conditions, it was observed that early prepupae waited longer than late prepupae before moulting into pupa. 6 The differential duration of the prepupal stage was independent of temperature conditions and allowed resynchronization of colonies and overlapping emergences. 7 The prepupal phase therefore appears to be critical for understanding the regulation of adult emergence of this important pest insect.

  • 42. Smit, Chantelle
    et al.
    Javal, Marion
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Terblanche, John S.
    Metabolic responses to starvation and feeding contribute to the invasiveness of an emerging pest insect2021In: Journal of insect physiology, ISSN 0022-1910, E-ISSN 1879-1611, Vol. 128, article id 104162Article in journal (Refereed)
    Abstract [en]

    Metabolic rate, and the flexibility thereof, is a complex trait involving several inter-linked variables that can influence animal energetics, behavior, and ultimately, fitness. Metabolic traits respond readily to ambient temperature variation, in some cases increasing relative or absolute energetic costs, while in other cases, depending on the organism's metabolic and behavioral responses to changing conditions, resulting in substantial energy savings. To gain insight into the rapid recent emergence of the indigenous South African longhorn beetle Cacosceles newmannii as a crop pest in sugarcane, a better understanding of its metabolic rate, feeding response, digestion times, and aerobic scope is required, in conjunction with any behavioral responses to food availability or limitation thereof. Here, we therefore experimentally determined metabolic rate, estimated indirectly as CO2 production using flow-through respirometry, in starved, fasted, and fed C. newmannii larvae, at 20 degrees C and 30 degrees C. We estimated multiple parameters of metabolic rate (starved, standard, active, and maximum metabolic rates) as well as aerobic scope (AS), specific dynamic action (SDA), and the percentage time active during respirometry trials. Additionally, in individuals that showed cyclic or discontinuous gas exchange patterns, we compared rate, volume, and duration of cycles, and how these were influenced by temperature. Standard and active metabolic rate, and AS and SDA were significantly higher in the larvae measured at 30 degrees C than those measured at 20 degrees C. By contrast, starved and maximum metabolic rates and percentage time active were unaffected by temperature. At rest and after digestion was complete, 35% of larvae showed cyclic gas exchange at both temperatures; 5% and 15% showed continuous gas exchange at 20 degrees C and 30 degrees C respectively, and 10% and 0% showed discontinuous gas exchange at 20 degrees C and 30 degrees C respectively. We propose that the ability of C. newmannii larvae to survive extended periods of resource limitation, combined with a rapid ability to process food upon securing resources, even at cooler conditions that would normally suppress digestion in tropical insects, may have contributed to their ability to feed on diverse low energy resources typical of their host plants, and become pests of, and thrive on, a high energy host plant like sugarcane.

  • 43.
    Stålhandske, Sandra
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Pruisscher, Peter
    Stockholm University, Faculty of Science, Department of Zoology.
    Leimar, Olof
    Stockholm University, Faculty of Science, Department of Zoology.
    Effect of winter cold duration on spring phenology of the orange tip butterfly, Anthocharis cardamines 2015In: Ecology and Evolution, E-ISSN 2045-7758, Vol. 5, no 23, p. 5509-5520Article in journal (Refereed)
    Abstract [en]

    The effect of spring temperature on spring phenology is well understood in a wide range of taxa. However, studies on how winter conditions may affect spring phenology are underrepresented. Previous work on Anthocharis cardamines (orange tip butterfly) has shown population-specific reaction norms of spring development in relation to spring temperature and a speeding up of post-winter development with longer winter durations. In this experiment, we examined the effects of a greater and ecologically relevant range of winter durations on post-winter pupal development of A. cardamines of two populations from the United Kingdom and two from Sweden. By analyzing pupal weight loss and metabolic rate, we were able to separate the overall post-winter pupal development into diapause duration and post-diapause development. We found differences in the duration of cold needed to break diapause among populations, with the southern UK population requiring a shorter duration than the other populations. We also found that the overall post-winter pupal development time, following removal from winter cold, was negatively related to cold duration, through a combined effect of cold duration on diapause duration and on post-diapause development time. Longer cold durations also lead to higher population synchrony in hatching. For current winter durations in the field, the A. cardamines population of southern UK could have a reduced development rate and lower synchrony in emergence because of short winters. With future climate change, this might become an issue also for other populations. Differences in winter conditions in the field among these four populations are large enough to have driven local adaptation of characteristics controlling spring phenology in response to winter duration. The observed phenology of these populations depends on a combination of winter and spring temperatures; thus, both must be taken into account for accurate predictions of phenology.

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  • 44.
    Süess, Philip
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Dircksen, Heinrich
    Stockholm University, Faculty of Science, Department of Zoology.
    Roberts, Kevin T.
    Stockholm University, Faculty of Science, Department of Zoology.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology.
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology.
    Carlsson, Mikael A.
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. University of Greifswald, Germany.
    Time- and temperature-dependent dynamics of prothoracicotropic hormone and ecdysone sensitivity co-regulate pupal diapause in the green-veined white butterfly Pieris napi2022In: Insect Biochemistry and Molecular Biology, ISSN 0965-1748, E-ISSN 1879-0240, Vol. 149, article id 103833Article in journal (Refereed)
    Abstract [en]

    Diapause, a general shutdown of developmental pathways, is a vital adaptation allowing insects to adjust their life cycle to adverse environmental conditions such as winter. Diapause in the pupal stage is regulated by the major developmental hormones prothoracicotropic hormone (PTTH) and ecdysone. Termination of pupal diapause in the butterfly Pieris napi depends on low temperatures; therefore, we study the temperature-dependence of PTTH secretion and ecdysone sensitivity dynamics throughout diapause, with a focus on diapause termination. While PTTH is present throughout diapause in the cell bodies of two pairs of neurosecretory cells in the brain, it is absent in the axons, and the PTTH concentration in the haemolymph is significantly lower during diapause than during post diapause development, indicating that the PTTH signaling is reduced during diapause. The sensitivity of pupae to ecdysone injections is dependent on diapause stage. While pupae are sensitive to ecdysone during early diapause initiation, they gradually lose this sensitivity and become insensitive to non-lethal concentrations of ecdysone about 30 days into diapause. At low temperatures, reflecting natural overwintering conditions, diapause termination propensity after ecdysone injection is precocious compared to controls. In stark contrast, at high temperatures reflecting late summer and early autumn conditions, sensitivity to ecdysone does not return. Thus, here we show that PTTH secretion is reduced during diapause, and additionally, that the low ecdysone sensitivity of early diapause maintenance is lost during termination in a temperature dependent manner. The link between ecdysone sensitivity and low-temperature dependence reveals a putative mechanism of how diapause termination operates in insects that is in line with adaptive expectations for diapause.

  • 45.
    Süess, Philip
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Roberts, Kevin
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. Stockholm University, Faculty of Science, The Bolin Centre for Climate Research (together with KTH & SMHI). University of Greifswald, Germany.
    Temperature dependence of gas exchange patterns shift as diapause progresses in the butterfly Pieris napi2023In: Journal of insect physiology, ISSN 0022-1910, E-ISSN 1879-1611, Vol. 151, article id 104585Article in journal (Refereed)
    Abstract [en]

    Insects have the capacity to significantly modify their metabolic rate according to environmental conditions and physiological requirement. Consequently, the respiratory patterns can range from continuous gas exchange (CGE) to discontinuous gas exchange (DGE). In the latter, spiracles are kept closed during much of the time, and gas exchange occurs only during short periods when spiracles are opened. While ultimate causes and benefits of DGE remain debated, it is often seen during insect diapause, a deep resting stage that insects induce to survive unfavourable environmental conditions, such as winter. The present study explores the shifts between CGE and DGE during diapause by performing long continuous respirometry measurements at multiple temperatures during key diapause stages in the green-veined white butterfly Pieris napi. The primary goal is to explore respiratory pattern as a non-invasive method to assess whether pupae are in diapause or have transitioned to post-diapause. Respiratory pattern can also provide insight into endogenous processes taking place during diapause, and the prolonged duration of diapause allows for the detailed study of the thermal dependence of the DGE pattern. Pupae change from CGE to DGE a few days after pupation, and this shift coincides with metabolic rate suppression during diapause initiation. Once in diapause, pupae maintain DGE even at elevated temperatures that significantly increase CO2 production. Instead of shifting respiratory pattern to CGE, pupae increase the frequency of DGE cycles. Since total CO2 released during a single open phase remains unchanged, our results suggest that P. napi pupae defend a maximum internal rho CO2 set point, even in their heavily suppressed diapause state. During post-diapause development, CO2 production increases as a function of development and changes to CGE during temperature conditions permissive for development. Taken together, the results show that respiratory patterns are highly regulated during diapause in P. napi and change predictably as diapause progresses.

  • 46. Tverin, Malin
    et al.
    Westberg, Melissa
    Kokkonen, Iiris
    Tang, Patrik
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Lundström, Karl
    Käkelä, Reijo
    Factors affecting the degree of vertical stratification of fatty acids in grey seal blubber2019In: Marine Biology, ISSN 0025-3162, E-ISSN 1432-1793, Vol. 166, no 8, article id 105Article in journal (Refereed)
    Abstract [en]

    The biochemistry of marine mammal blubber differs vertically from skin to muscle, which forms a challenge for using fatty acids (FAs) from differently sampled blubber as a proxy for dietary studies required for ecosystem-based management of coastal resources. In the blubber of some phocid seal individuals, the vertical stratification of several FAs is pronounced whereas in others the FAs distribute almost evenly through the blubber column. Using gas chromatography, we analysed the blubber vertical FA profiles of 30 adult male grey seals from the Baltic Sea, and examined which factors induced the largest vertical change of FA composition detected at the depth of 15-18mm (outer and middle blubber boundaries). It was revealed that the degree of this compositional shift did not depend on the blubber thickness. Seal age only affected the vertical distribution of the FAs 16:0 and 16:1n-7. However, the outer blubber ratio of 9-desaturated monounsaturated FAs (MUFAs) to their saturated FA (SFA) precursors was not increased by grey seal age, contrasting earlier findings for ringed seals. A major determinant of the degree of FA stratification between the outer and middle blubber was the mismatch between the individually varying FA composition of the innermost blubber, regarded to reflect the dietary FA supply the most, and the uniform FA composition of endogenously regulated MUFA-rich outer blubber. Thus, discarding a fixed-depth layer of the grey seal outermost blubber, which we here show to span 0-18mm from skin and which to a lesser extent reflects the diet of the individual, may in the case of small pinnipeds improve the sensitivity of the FA analysis in assessing spatial, temporal and individual dietary differences. When studying the outer blubber samples using only the diet-derived PUFA variables (SFAs and MUFAs omitted), the sensitivity of the analysis was better than when using this sample type with all main FA variables included.

  • 47.
    von Schmalensee, Loke
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. Stockholm University, Faculty of Science, The Bolin Centre for Climate Research (together with KTH & SMHI).
    Caillault, Pauline
    Stockholm University, Faculty of Science, Department of Zoology.
    Hulda Gunnarsdóttir, Katrín
    Stockholm University, Faculty of Science, Department of Zoology.
    Gotthard, Carl
    Stockholm University, Faculty of Science, Department of Zoology. Stockholm University, Faculty of Science, The Bolin Centre for Climate Research (together with KTH & SMHI).
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology. Stockholm University, Faculty of Science, The Bolin Centre for Climate Research (together with KTH & SMHI). University of Greifswald, Germany.
    Seasonal specialization drives divergent population dynamics in two closely related butterflies2023In: Nature Communications, E-ISSN 2041-1723, Vol. 14, article id 3663Article in journal (Refereed)
    Abstract [en]

    Seasons impose different selection pressures on organisms through contrasting environmental conditions. How such seasonal evolutionary conflict is resolved in organisms whose lives span across seasons remains underexplored. Through field experiments, laboratory work, and citizen science data analyses, we investigate this question using two closely related butterflies (Pieris rapae and P. napi). Superficially, the two butterflies appear highly ecologically similar. Yet, the citizen science data reveal that their fitness is partitioned differently across seasons. Pieris rapae have higher population growth during the summer season but lower overwintering success than do P. napi. We show that these differences correspond to the physiology and behavior of the butterflies. Pieris rapae outperform P. napi at high temperatures in several growth season traits, reflected in microclimate choice by ovipositing wild females. Instead, P. rapae have higher winter mortality than do P. napi. We conclude that the difference in population dynamics between the two butterflies is driven by seasonal specialization, manifested as strategies that maximize gains during growth seasons and minimize harm during adverse seasons, respectively.

  • 48.
    von Schmalensee, Loke
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Hulda Gunnarsdóttir, Katrin
    Stockholm University, Faculty of Science, Department of Zoology.
    Näslund, Joacim
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Thermal performance under constant temperatures can accurately predict insect development times across naturally variable microclimates2021In: Ecology Letters, ISSN 1461-023X, E-ISSN 1461-0248, Vol. 24, no 8, p. 1633-1645Article in journal (Refereed)
    Abstract [en]

    External conditions can drive biological rates in ectotherms by directly influencing body temperatures. While estimating the temperature dependence of performance traits such as growth and development rate is feasible under controlled laboratory settings, predictions in nature are difficult. One major challenge lies in translating performance under constant conditions to fluctuating environments. Using the butterfly Pieris napi as model system, we show that development rate, an important fitness trait, can be accurately predicted in the field using models parameterized under constant laboratory temperatures. Additionally, using a factorial design, we show that accurate predictions can be made across microhabitats but critically hinge on adequate consideration of non-linearity in reaction norms, spatial heterogeneity in microclimate and temporal variation in temperature. Our empirical results are also supported by a comparison of published and simulated data. Conclusively, our combined results suggest that, discounting direct effects of temperature, insect development rates are generally unaffected by thermal fluctuations.

  • 49.
    Wiklund, Christer
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Friberg, Magne
    Diapause decision in the small tortoiseshell butterfly, Aglais urticae2019In: Entomologia Experimentalis et Applicata, ISSN 0013-8703, E-ISSN 1570-7458, Vol. 167, no 5, p. 433-441Article in journal (Refereed)
    Abstract [en]

    Insects in temperate areas spend the inhospitable winter conditions in a resting stage known as diapause. In species that diapause in the larval or pupal stage, the decision whether to diapause or develop directly is customarily taken during the late instars, with long days (i.e., long light phases) and high temperatures promoting direct development. Among butterflies that overwinter as adults, data are rare and variable, but imply that the larval daylength conditions can affect the pathway decision. We studied the small tortoiseshell, Aglais urticae L. (Lepidoptera: Nymphalidae, Nymphalini), which is partially bivoltine from Central Scandinavia and southwards, and tested whether the pathway decision is taken in the larval or adult stage. We reared larvae under long-day (L22:D2) or short-day (L12:D12) photoperiods, and recorded the pathway taken by the eclosing adults by scoring their propensity to mate and produce eggs. We also tested whether the larval photoperiod influenced adult ability to diapause by assessing adult survival. The results clearly indicate that (1) there is no detectable effect of larval photoperiod treatment on the pathway decision taken by adults whether to enter diapause or to develop directly, (2) some individuals are obligately univoltine and insensitive to photoperiod during adulthood, whereas (3) other individuals can facultatively enter diapause or direct development, depending on the photoperiod experienced after adult eclosion.

  • 50.
    Woronik, Alyssa
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Neethiraj, Ramprasad
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Maria, de la Paz Celorio Mancera
    Stockholm University, Faculty of Science, Department of Zoology.
    Stefanescu, Constanti
    Hill, Jason
    Stockholm University, Faculty of Science, Department of Zoology.
    Käkelä, Reijo
    Brattstrom, Oskar
    Wheat, Christopher
    Stockholm University, Faculty of Science, Department of Zoology.
    A transposable element insertion is associated with a female-limited, alternative life history strategyManuscript (preprint) (Other academic)
12 1 - 50 of 53
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