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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, ISSN 2045-2322, 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. 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.

  • 4.
    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.

  • 5. 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.

  • 6.
    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, ISSN 2045-2322, 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.

  • 7.
    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.

  • 8.
    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.

  • 9.
    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, ISSN 1742-9994, 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.

  • 10.
    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.

  • 11.
    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.

  • 12.
    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.

  • 13.
    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.

  • 14.
    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.

  • 15.
    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.

  • 16.
    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.

  • 17. 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, ISSN 2045-2322, 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.

  • 18.
    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.

  • 19. 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.

  • 20. 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.

  • 21. 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.

  • 22.
    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, ISSN 2045-7758, 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.

  • 23. 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.

  • 24.
    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.

  • 25.
    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)
  • 26.
    Woronik, Alyssa
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Stefanescu, Constanti
    Kakela, Reijo
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Physiological differences between female limited, alternative life history strategies: The Alba phenotype in the butterfly Colias croceus2018In: Journal of insect physiology, ISSN 0022-1910, E-ISSN 1879-1611, Vol. 107, p. 257-264Article in journal (Refereed)
    Abstract [en]

    Across a wide range of taxa, individuals within populations exhibit alternative life history strategies (ALHS) where their phenotypes dramatically differ due to divergent investments in growth, reproduction and survivorship, with the resulting trade-offs directly impacting Darwinian fitness. Though the maintenance of ALHS within populations is fairly well understood, little is known regarding the physiological mechanisms that underlie ALHS and how environmental conditions can affect the evolution and expression of these phenotypes. One such ALHS, known as Alba, exists within females of many species in the butterfly genus Colias. Previous works in New World species not only found that female morphs differ in their wing color due to a reallocation of resources away from the synthesis of wing pigments to other areas of development, but also that temperature played an important role in these trade-offs. Here we build on previous work conducted in New World species by measuring life history traits and conducting lipidomics on individuals reared at hot and cold temperatures in the Old World species Colias croceus. Results suggest that the fitness of Alba and orange morphs likely varies with rearing temperature, where Alba females have higher fitness in cold conditions and orange in warm. Additionally shared traits between Old and New World species suggest the Alba mechanism is likely conserved across the genus. Finally, in the cold treatment we observe an intermediate yellow morph that may have decreased fitness due to slower larval development. This cost may manifest as disruptive selection in the field, thereby favoring the maintenance of the two discrete morphs. Taken together these results add insights into the evolution of, and the selection on, the Alba ALHS.

  • 27.
    Woronik, Alyssa
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Stefanescu, Constanti
    Käkelä, Reijo
    Wheat, Christopher
    Stockholm University, Faculty of Science, Department of Zoology.
    Lehmann, Philipp
    Stockholm University, Faculty of Science, Department of Zoology.
    Physiological differences between female limited, alternative life history strategies: the Alba phenotype in the butterfly Colias croceusManuscript (preprint) (Other academic)
1 - 27 of 27
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