Philipp Lehmann

Population dependent effects of photoperiod on diapause related physiological traits in an invasive beetle (Leptinotarsa decemlineata).

Organisms undergoing latitudinal range expansion face a change in the photoperiod which can lead to a mismatch between the timing of seasonal changes in physiological and life history traits with seasonal environmental changes. This mismatch can lead to lowered survival, for example, due to unsynchronized diapause timing. Successful range expansion even in recent introductions requires that organisms which use the photoperiod for seasonal predictions should show interpopulational differences in photoperiodic responses at different latitudes, as the photoperiod is a function of latitude. We investigated among population differences in photoperiodic responses of life history and physiological traits linked to diapause in the invasive beetle Leptinotarsa decemlineata. Beetles from a northern marginal and a southern European population were reared under short day (12:12L:D) and long day (18:6L:D) photoperiods. Both populations reacted similarly to the short day photoperiod. Their abdominal total lipid content increased and water content decreased which suggests that the beetles prepared for diapause. This was also indicated by low mortality during diapause. In the long day photoperiod large interpopulational differences were found, the southern population ceased lipid accumulation after 5 days, while the northern population continued lipid accumulation as beetles in the short day photoperiod. This indicates that the northern population has a longer critical photoperiod than the southern one. Abdominal total lipid stores in 10 day old beetles were shown to be predominantly composed of neutral lipids (85%), most likely representing storage triacylglycerols. Fatty acid profiles of both the neutral lipids and the phospholipids showed large shifts during the first 10 day of adult life, predominantly in the fractions of 18:0, 18:1ω9, 18:2ω6 and 18:3ω3. Although the degree of unsaturation increased with age, it was not higher in diapausing than non-diapausing beetles. This indicates that this species does not increase diapause related cold tolerance via homeoviscous adaptation, and might have developed other means to cope with suboptimal temperatures, such as behavioral adaptations.

A key malaria metabolite modulates vector blood seeking, feeding, and susceptibility to infection

Siren molecule calls loudly to mosquitoes People infected by malaria become more attractive to the mosquito vectors of the disease, which facilitates the spread of malaria. Emami et al. found that red blood cells of the host respond to a parasite-derived isoprenoid called HMBPP by increasing the production of carbon dioxide and several monoterpenes and aldehydes. Mosquitoes fed HMBPP-spiked blood displayed malaria parasite–specific changes in gene transcription, which reinforced attractiveness for the mosquito. HMBPP also stimulates mosquito feeding and malaria parasite reproduction. Thus, the parasite manipulates its mammalian host to make it more attractive to the insect vectors and exploits the same molecule to amplify transmission. Science, this issue p. 1076 An isoprenoid released by Plasmodium-infected red blood cells has several functions in enhancing parasite transmission. 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.

Increased radiation from Chernobyl decreases the expression of red colouration in natural populations of bank voles ( Myodes glareolus )

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.

Effect of winter cold duration on spring phenology of the orange tip butterfly, Anthocharis cardamines

Abstract 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.

Photoperiodic effects on diapause-associated gene expression trajectories in European Leptinotarsa decemlineata populations

Behavioural and physiological changes during diapause, an important strategy of insects for surviving harsh seasonal conditions, have been intensively studied. The genetic and molecular mechanisms underpinning diapause development are less well known. We took a candidate gene approach to study prediapause gene expression patterns in the Colorado potato beetle (Leptinotarsa decemlineata), an invasive insect that has rapidly spread northwards to high seasonality environments. Newly eclosed beetles originating from southern (Italy) and northern (Russia) Europe were reared under short‐ [12 h light (L):12 h dark (D)] and long‐day (18L:6D) photoperiods for 10 days. This time period includes the sensitive period for the photoperiodic induction and initiation of diapause. Gene expression trajectories of 12 diapause‐related genes (regulatory, metabolic and stress‐resistance) were analysed from 0‐, 5‐ and 10‐day‐old beetles. Gene expression differences increased with age, deviating significantly between populations and photoperiods in 10‐day‐old beetles. The gene expression profiles, particularly those related to energy metabolism and stress‐resistance, indicate that beetles originating from Russia also prepare for diapause under the long‐day photoperiod and show qualitative differences in the diapausing phenotype. Our study shows that population‐dependent differences seen in behavioural and physiological traits connected with diapause in L. decemlineata are also evident in the expression trajectories of diapause‐related genes.

Comparative Ecophysiology of Cold-Tolerance-Related Traits: Assessing Range Expansion Potential for an Invasive Insect at High Latitude

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°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.

Fitness costs of increased cataract frequency and cumulative radiation dose in natural mammalian populations from Chernobyl

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.

Northward range expansion requires synchronization of both overwintering behaviour and physiology with photoperiod in the invasive Colorado potato beetle (Leptinotarsa decemlineata).

Photoperiodic phenological adaptations are prevalent in many organisms living in seasonal environments. As both photoperiod and growth season length change with latitude, species undergoing latitudinal range expansion often need to synchronize their life cycle with a changing photoperiod and growth season length. Since adaptive synchronization often involves a large number of time-consuming genetic changes, behavioural plasticity might be a faster way to adjust to novel conditions. We compared behavioural and physiological traits in overwintering (diapause) preparation in three latitudinally different European Colorado potato beetle (Leptinotarsa decemlineata) populations reared under two photoperiods. Our aim was to study whether behavioural plasticity could play a role in rapid range expansion into seasonal environments. Our results show that while burrowing into the soil occurred in the southernmost studied population also under a non-diapause-inducing long photoperiod, the storage lipid content of these beetles was very low compared to the northern populations. However, similar behavioural plasticity was not found in the northern populations. Furthermore, the strongest suppression of energy metabolism was seen in pre-diapause beetles from the northernmost population. These results could indicate accelerated diapause preparation and possibly energetic adjustments due to temporal constraints imposed by a shorter, northern, growth season. Our results indicate that behavioural plasticity in burrowing may have facilitated initial range expansion of L. decemlineata in Europe. However, long-term persistence at high latitudes has required synchronization of burrowing behaviour with physiological traits. The results underline that eco-physiological life-history traits of insects, such as diapause, should be included in studies on range expansion.

Energy and lipid metabolism during direct and diapause development in a pierid butterfly

ABSTRACT 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 in which endogenous diapause has been well studied. Endogenous diapause was terminated after 3 months and termination required chilling. Metabolic and post-diapause development rates increased with diapause duration, while the metabolic cost of post-diapause 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 developed early, when pupae are still at high temperature, and retained until post-diapause development. Summary: Diapause termination in Pieris napi requires chilling, energy is stored for post-diapause purposes and the diapause lipidome is distinct but lacks dynamics during diapause development.

Do respiratory limitations affect metabolism of insect larvae before moulting? An empirical test at the individual level

ABSTRACT 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. Summary: Respiratory limitations for metabolism appear in the penultimate larval instar but not in the last instar in growing butterfly larvae, supporting oxygen-dependent moult induction in larva-to-larva moults.