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  • 1.
    Hill, Jason
    et al.
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics. Uppsala University, Sweden.
    Rastas, Pasi
    Hornett, Emily A.
    Neethiraj, Ramprasad
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.
    Clark, Nathan
    Morehouse, Nathan
    de la Paz Celorio-Mancera, Maria
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.
    Carnicer Cols, Jofre
    Dircksen, Heinrich
    Stockholm University, Faculty of Science, Department of Zoology, Functional Morphology.
    Meslin, Camille
    Keehnen, Naomi
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.
    Pruisscher, Peter
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.
    Sikkink, Kristin
    Vives, Maria
    Vogel, Heiko
    Wiklund, Christer
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.
    Woronik, Alyssa
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics. New York University, USA.
    Boggs, Carol L.
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.
    Unprecedented reorganization of holocentric chromosomes provides insights into the enigma of lepidopteran chromosome evolution2019In: Science Advances, E-ISSN 2375-2548, Vol. 5, no 6, article id eaau3648Article in journal (Refereed)
    Abstract [en]

    Chromosome evolution presents an enigma in the mega-diverse Lepidoptera. Most species exhibit constrained chromosome evolution with nearly identical haploid chromosome counts and chromosome-level gene collinearity among species more than 140 million years divergent. However, a few species possess radically inflated chromosomal counts due to extensive fission and fusion events. To address this enigma of constraint in the face of an exceptional ability to change, we investigated an unprecedented reorganization of the standard lepidopteran chromosome structure in the green-veined white butterfly (Pieris napi). We find that gene content in P. napi has been extensively rearranged in large collinear blocks, which until now have been masked by a haploid chromosome number close to the lepidopteran average. We observe that ancient chromosome ends have been maintained and collinear blocks are enriched for functionally related genes suggesting both a mechanism and a possible role for selection in determining the boundaries of these genome-wide rearrangements.

  • 2.
    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.

  • 3.
    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.

  • 4.
    Neethiraj, Ramprasad
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Pruisscher, Peter
    Stockholm University, Faculty of Science, Department of Zoology.
    Pruisscher Keehnen, Naomi
    Stockholm University, Faculty of Science, Department of Zoology.
    Woronik, Alyssa
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology.
    Wheat, Christopher
    Stockholm University, Faculty of Science, Department of Zoology.
    A dark melanic morph of Pieris napi shares its origins with other dark morphs of LepidopteraManuscript (preprint) (Other academic)
  • 5.
    Pruisscher, Peter
    Stockholm University, Faculty of Science, Department of Zoology.
    Functional genomics of diapause in two temperate butterflies2019Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Natural selection will act on a given phenotype to maximize fitness in a particular environment, even if this would result in reduced fitness in other environments. In insects some of the strongest selection pressures act on timing life cycles to seasonal variation in environmental conditions, in order to maximize growth, reproduction, and to anticipate the onset of winter. Many temperate insects survive winter by entering a pre-programmed state of developmental arrest, called diapause. The decision to induce diapause is predominantly based on measuring day length. Populations have adapted to latitudinal variation in photoperiod, thereby synchronizing with local seasonal variation. However, there is no general understanding of the genetic basis for controlling diapause induction, maintenance and termination. In this thesis I aimed to gain a better understanding of the genetic basis underlying variation in the induction decision, as well as to gain insights into gene expression changes during diapause in temperate butterflies.

     

    I started by revealing local adaptation in the photoperiodic response of two divergent populations of Pieris napi (Paper I). I found that variation in diapause induction among populations of both P. napi and Pararge aegeria showed strong sex-linked inheritance in inter-population crosses (Paper I and II). The genome-wide variation across populations was relatively low in both species. However, there was strong divergence in genomic regions containing the circadian clock genes timeless and period in P. aegeria, and period, cycle, and clock in P. napi. The genetic variation in these specific regions segregated between diapausing and direct developing individuals of inter-population crosses, showing that allelic variation at few genes with known functions in the circadian clock correlated to variation in diapause induction (Paper II and III).

     

    Furthermore, I investigated the transcriptional dynamics in two tissues (head and abdomen) during diapause (Paper IV). Already at the first day of pupal development there are on average 409 differentially expressed genes (DEG) each up and down regulated between the direct development and diapause pathways, and this increases dramatically across these formative stages to an average of 2695. Moreover, gene expression is highly dynamic during diapause, showing more than 2600 DEG’s in the first month of diapause development, but only 20 DEG’s in the third month. Moreover, gene expression is independent of environmental conditions, revealing a pre-programmed transcriptional landscape that is active during the winter. Still, adults emerging from either the direct or diapause pathways do not show large transcriptomic differences, suggesting the adult phenotype is strongly canalized.

     

    Thus, by integrating whole-genome scans with targeted genotyping and bulk-segregant analyses in population crosses, I demonstrate that adaptive variation in seasonal life cycle regulation in the two butterflies P. napi and P. aegeria both converge on genes of the circadian clock, suggesting convergent evolution in these distantly related butterflies.

    Moreover, the diapause program is a dynamic process with a distinct transcriptional profile in comparison to direct development, showing that on a transcriptome level diapause development and direct development are two distinct developmental strategies.

  • 6.
    Pruisscher, Peter
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Larsdotter-Mellström, Helena
    Stockholm University, Faculty of Science, Department of Zoology. The University of Western Australia, Australia.
    Stefanescu, Constantí
    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.
    Sex-linked inheritance of diapause induction in the butterfly Pieris napi2017In: Physiological entomology (Print), ISSN 0307-6962, E-ISSN 1365-3032, Vol. 42, no 3, p. 257-265Article in journal (Refereed)
    Abstract [en]

    Many temperate insects survive harsh environmental conditions, such as winter, by entering a state of developmental arrest. This diapause state is predominantly induced by photoperiod. The photoperiod varies with latitude and has led to local adaptation in the photoperiodic induction of diapause in many insects. To understand the rapid evolution of the photoperiodic threshold, it is important to investigate and understand the underlying genetic mechanisms. In the present study, the genetic basis of photoperiodic diapause induction is investigated in the green-veined white butterfly Pieris napi (Lepidoptera, Pieridae) by assaying diapause induction in a range of conditions for a Swedish and Spanish population. Furthermore, the inheritance of diapause induction is assessed in reciprocal F1 hybrids and backcrosses between the two populations. The southern population shows a clear photoperiodic threshold determining diapause or direct development, whereas the northern populations show a high incidence of diapause, regardless of photoperiod. The hybrid crosses reveal that the inheritance of diapause induction is strongly sex-linked, and that diapause incidence in the genetic crosses is highly dependent on photoperiod. This emphasizes the importance of assaying a range of conditions in diapause inheritance studies. The results indicate a strongly heritable diapause induction with a major component on the Z-chromosome, as well as a minor effect of the autosomal background.

  • 7.
    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.

  • 8.
    Pruisscher, Peter
    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.
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology.
    Genetic variation underlying local adaptation of diapause induction along a cline in a butterfly2018In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 27, no 18, p. 3613-3626Article in journal (Refereed)
    Abstract [en]

    Diapause is a life history strategy allowing individuals to arrest development until favourable conditions return, and it is commonly induced by shortened day length that is latitude specific for local populations. Although understanding the evolutionary dynamics of a threshold trait like diapause induction provides insights into the adaptive process and adaptive potential of populations, the genetic mechanism of variation in photoperiodic induction of diapause is not well understood. Here, we investigate genetic variation underlying latitudinal variation in diapause induction and the selection dynamics acting upon it. Using a genomewide scan for divergent regions between two populations of the butterfly Pararge aegeria that differ strongly in their induction thresholds, we identified and investigated the patterns of variation in those regions. We then tested the association of these regions with diapause induction using between-population crosses, finding significant SNP associations in four genes present in two chromosomal regions, one with the gene period, and the other with the genes kinesin, carnitine O-acetyltransferase and timeless. Patterns of allele frequencies in these two regions in population samples along a latitudinal cline suggest strong selection against heterozygotes at two genes within these loci (period, timeless). Evidence for additional loci modifying the diapause decision was found in patterns of allelic change in relation to induction thresholds over the cline, as well as in backcross analyses. Taken together, population-specific adaptations of diapause induction appear to be due to a combination of alleles of larger and smaller effect size, consistent with an exponential distribution of effect sizes involved in local adaption.

  • 9.
    Pruisscher, Peter
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology.
    Wheat, Christopher
    Stockholm University, Faculty of Science, Department of Zoology.
    Gotthard, Karl
    Stockholm University, Faculty of Science, Department of Zoology.
    A chromosomal block containing clock genes associates with variation in diapause inductionManuscript (preprint) (Other academic)
    Abstract [en]

    Developmental plasticity describes the capacity of individuals with the same genotype to induce permanent change in a phenotype depending on a specific external input. One well-studied example of adaptive developmental plasticity is the induction of facultative diapause in insects. Studies investigating the inheritance of diapause induction have suggested diverse genetic backgrounds. However, only few studies have performed unbiased genome scans to identify genes affecting the induction decision. Here we perform an unbiased whole genome scan to identify divergence between two populations that differ in their propensity to diapause, finding low divergence between these populations. We then investigate genetic differences between diapausing and directly developing siblings from backcrosses of these populations that revealed one particular region of divergence. This region is located on the Z-chromosome and contained three circadian clock genes, cyc_2, clock, and per. The results from this study help understand the genetic basis that is underlying plasticity.

  • 10.
    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.

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