1. Levels of artificial night lighting are increasing rapidly worldwide, subjecting nocturnal organisms to a major change in their environment. Many moth species are strongly attracted to sources of artificial night lighting, with potentially severe, yet poorly studied, consequences for development, reproduction and inter/intra-specific interactions.2. Here, we present results of a field-based experiment where we tested effects of various types of artificial lighting on mating in the winter moth (Operophtera brumata, Lepidoptera: Geometridae). We illuminated trunks of oak trees with green, white, red or no artificial LED light at night, and caught female O. brumata on these trunks using funnel traps. The females were dissected to check for the presence of a spermatophore, a sperm package that is delivered by males to females during mating.3. We found a strong reduction in the number of females on the illuminated trunks, indicating artificial light inhibition of activity. Furthermore, artificial light inhibited mating: 53% of females caught on non-illuminated trunks had mated, whereas only 13%, 16% and 28% of the females that were caught on green, white and red light illuminated trunks had mated respectively. 4. A second experiment showed that artificial night lighting reduced the number of males that were attracted to a synthetic O. brumata pheromone lure. This effect was strongest under red light and mildest under green light.5. This study provides, for the first time, field-based evidence that artificial night lighting disrupts reproductive behaviour of moths, and that reducing short wavelength radiation only partly mitigates these negative effects.
The winter moth (Operophtera brumata) belongs to one of the most species-rich families in Lepidoptera, the Geometridae (approximately 23,000 species). This family is of great economic importance as most species are herbivorous and capable of defoliating trees. Genome assembly of the winter moth allows the study of genes and gene families, such as the cytochrome P450 gene family, which is known to be vital in plant secondary metabolite detoxification and host-plant selection. It also enables exploration of the genomic basis for female brachyptery (wing reduction), a feature of sexual dimorphism in winter moth, and for seasonal timing, a trait extensively studied in this species. Here we present a reference genome for the winter moth, the first geometrid and largest sequenced Lepidopteran genome to date (638 Mb) including a set of 16,912 predicted protein-coding genes. This allowed us to assess the dynamics of evolution on a genome-wide scale using the P450 gene family. We also identified an expanded gene family potentially linked to female brachyptery, and annotated the genes involved in the circadian clock mechanism as main candidates for involvement in seasonal timing. The genome will contribute to Lepidopteran genomic resources and comparative genomics. In addition, the genome enhances our ability to understand the genetic and molecular basis of insect seasonal timing and thereby provides a reference for future evolutionary and population studies on the winter moth.
Animals should time activities, such as foraging, migration and reproduction, as well as seasonal physiological adaptation, in a way that maximizes fitness. The fitness outcome of such activities depends largely on their interspecific interactions; the temporal overlap with other species determines when they should be active in order to maximize their encounters with food and to minimize their encounters with predators, competitors and parasites. To cope with the constantly changing, but predictable structure of the environment, organisms have evolved internal biological clocks, which are synchronized mainly by light, the most predictable and reliable environmental cue (but which can be masked by other variables), which enable them to anticipate and prepare for predicted changes in the timing of the species they interact with, on top of responding to them directly. Here, we review examples where the internal timing system is used to predict interspecific interactions, and how these interactions affect the internal timing system and activity patterns. We then ask how plastic these mechanisms are, how this plasticity differs between and within species and how this variability in plasticity affects interspecific interactions in a changing world, in which light, the major synchronizer of the biological clock, is no longer a reliable cue owing to the rapidly changing climate, the use of artificial light and urbanization.This article is part of the themed issue 'Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals'.
In seasonal environments, organisms synchronize their life cycle with the annual cycle of environmental factors. In many insect species, this includes a diapause response: a timed dormant stage that allows to survive harsh winter conditions. Previously, we have shown that larval diapause in the parasitic wasp Nasonia vitripennis is induced by the mother upon exposure to a threshold number of short photoperiods (named switch point) and diapause response follows a latitudinal cline in natural populations. Here, we present a QTL analysis using two lines derived from the extremes of this clinal distribution: a northern line from Oulu, Finland and a southern line from Corsica, France. A genomic region on chromosome 1 and one on chromosome 5 were found to be associated with photoperiodic diapause induction. Interestingly, these regions contain the putative clock genes period, cycle (chromosome 1) and cryptochrome (chromosome 5). An analysis of period polymorphisms in seven European populations showed a clinal distribution of two main haplotypes that correlate with the latitudinal cline for diapause induction.
Understanding the relationship between an insect's developmental rate and temperature is crucial to forecast insect phenology under climate change. In the winter moth Operophtera brumata timing of egg‐hatching has severe fitness consequences on growth and reproduction as egg‐hatching has to match bud burst of the host tree. In the winter moth, as in many insect species, egg development is strongly affected by ambient temperatures. Here we use laboratory experiments to show for the first time that the effect of temperature on developmental rate depends on the stage of development of the eggs. Building on this experimental finding, we present a novel physiological model to describe winter moth egg development in response to temperature. Our model, a modification of the existing Sharpe−Schoolfield biophysical model, incorporates the effect of developmental stage on developmental rate. Next we validate this model using a 13‐year data‐set from winter moth eggs kept under ambient conditions and compared this validation with a degree day model and with the Sharpe−Schoolfield model, which lacks the interaction between temperature and developmental stage on developmental rate. We show that accounting for the interaction between temperature and developmental stage improved the predictive power of the model and contributed to our understanding of annual variation in winter moth egg phenology. As climate change leads to unequal changes in temperatures throughout the year, a description of insect development in response to realistic patterns of temperature rather than an invariable degree‐day approach will help us to better predict future responses of insect phenology, and thereby insect fitness, to climate change.
Abstract1. To maximise their fitness, organisms need to synchronise their phenology with the seasonal variation in environmental conditions. Most phenological traits are affected by environmental abiotic cues such as photoperiod, temperature and rainfall. When individuals with complex life cycles fail to match one of the stages with the favourable environment, the negative conditions experienced may lead to carry-over effects and, thus, influence fitness in subsequent stages.2. In the winter moth, an herbivorous insect with an annual life cycle, timing of egghatching in spring is strongly influenced by temperature and varies from year to year. To investigate whether the phenological variation in egg-hatching date affects subsequent stages, we analysed data on egg-hatching date and adult catching date (considered here to be a proxy for adult eclosion date) from our long-term study . Furthermore, we experimentally manipulated the photoperiod experienced by newly hatched larvae and recorded the phenology of their subsequent life cycle stages.3. In the long-term field study, we found that the timing of winter moth egg-hatching in spring varied strongly from year to year. Interestingly, however, the timing of adult eclosion date in winter showed little inter-annual variation. In line with these findings, our experimental data showed that the winter moth shortened the duration of their pupal development when they experienced a late spring photoperiod as a larva, and prolonged pupal development when experiencing early spring photoperiod. The effects of the larval photoperiodic treatments persisted during egg development in the following generation.4. The results show that a phenological shift that occurs during an early life stage is partially compensated during subsequent stages and suggest that the mechanism underlying this compensation is mediated by photoperiod. Winter moths regulated their phenology in such a way that the variation in the egg-hatching stage was not carried over to the next life cycle stages. This has strong effects on fitness as it (1) ensures the synchronisation of adult eclosion during the mating period and (2) is likely to reduce potentially negative fitness consequences of phenological mismatches in egg-hatching in the following generation. Overall, these findings stress the importance of understanding phenological carry-over effects to forecast the impact of global change in species with complex life cycles.
1. Diets that maximise life span often differ from diets that maximise reproduction. Animals have therefore evolved advanced foraging strategies to acquire optimal nutrition and maximise their fitness. The free‐living adult females of parasitoid wasps (Hymenoptera) need to balance their search for hosts to reproduce and for carbohydrate resources to feed. 2. Honeydew, excreted by phloem‐feeding insects, presents a widely available carbohydrate source in nature that can benefit natural enemies of honeydew‐producing insects. However, the effects of variation in honeydew on organisms in the fourth trophic level, such as hyperparasitoids, are not yet understood. 3. This study examined how five different honeydew types influence longevity and fecundity of four hyperparasitoid taxa. Asaphes spp. (Pteromalidae) and Dendrocerus spp. (Megaspilidae) are secondary parasitoids of aphid parasitoids and are thus associated with honeydew‐producing insects. Gelis agilis and Acrolyta nens (both Ichneumonidae) are secondary parasitoids of species that do not use honeydew‐producing hosts. 4. Most honeydew types had a positive or neutral effect on life span and fecundity of hyperparasitoids compared with controls without honeydew, although negative effects were also found for both aphid hyperparasitoids. Honeydew produced by aphids feeding on sweet pepper plants was most beneficial for all hyperparasitoid taxa, which can partially be explained by the high amount of honeydew, but also by the composition of dietary sugars in these honeydew types. 5. The findings of this study underline the value of aphid honeydew as a carbohydrate resource for fourth‐trophic‐level organisms, not only those associated with honeydew‐producing insects but also ‘interlopers’ without such a natural association.
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