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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.
    Keehnen, Naomi
    et al.
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.
    Fors, Lisa
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.
    Integrating immune cell expression with signatures of selection suggests novel targets in melanin trafficking for geographic differences in melanin-related immune performanceManuscript (preprint) (Other academic)
  • 3.
    Keehnen, Naomi
    et al.
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.
    Fors, Lisa
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.
    Järver, Peter
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Spetz, Anna-Lena
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology, Animal Ecology.
    Theopold, Ulrich
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Wheat, Christopher
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.
    Geographic variation in hemocyte diversity and phagocytic propensity shows a diffuse genomic signature in the green veined white butterflyManuscript (preprint) (Other academic)
    Abstract [en]

    Insects rely on their innate immune system to successfully mediate complex interactions with their internal microbiota, as well as the microbes present in the environment. Given the variation in microbes across habitats, the challenges to respond to them is likely to result in local adaptation in the immune system. Here we focus upon phagocytosis, a mechanism by which pathogens and foreign particles are engulfed in order to be contained, killed and processed for antigen presentation. We investigated the phenotypic and genetic variation related to phagocytosis, in two allopatric populations of the butterfly Pieris napi. We found that the populations differ in their hemocyte composition, and overall phagocytic capability, driven by the increased phagocytic propensity of each cell type. However, no evidence for divergence in phagocytosis-related genes was observed, though an enrichment of genes involved in glutamine metabolism was found, which have recently been linked to immune cell differentiation in mammals.

  • 4.
    Keehnen, Naomi L. P.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Hill, Jason
    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.
    Microevolutionary selection dynamics acting on immune genes of the green-veined white butterfly, Pieris napi2018In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 27, no 13, p. 2807-2822Article in journal (Refereed)
    Abstract [en]

    Insects rely on their innate immune system to successfully mediate complex interactions with their microbiota, as well as the microbes present in the environment. Previous work has shown that components of the canonical immune gene repertoire evolve rapidly and have evolutionary characteristics originating from interactions with fast-evolving microorganisms. Although these interactions are likely to vary among populations, there is a poor understanding of the microevolutionary dynamics of immune genes, especially in non-Dipteran insects. Here, we use the full set of canonical insect immune genes to investigate microevolutionary dynamics acting on these genes between and among populations by comparing three allopatric populations of the green-veined white butterfly, Pieris napi (Linne; Lepidoptera, Pieridae). Immune genes showed increased genetic diversity compared to genes from the rest of the genome and various functional categories exhibited different types of signatures of selection, at different evolutionary scales, presenting a complex pattern of selection dynamics. Signatures of balancing selection were identified in 10 genes, and 17 genes appear to be under positive selection. Genes involved with the cellular arm of the immune response as well as the Toll pathway appear to be enriched among our outlier loci, regardless of functional category. This suggests that the targets of selection might focus upon an entire pathway, rather than functional subsets across pathways. Our microevolutionary results are similar to previously observed macroevolutionary patterns from diverse taxa, suggesting that either the immune system is robust to dramatic differences in life history and microbial communities, or that diverse microbes exert similar selection pressures.

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  • 5.
    Keehnen, Naomi L. P.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.
    Kučerova, Lucie
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. Biology Centre CAS, Czech Republic.
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology, Animal Ecology.
    Theopold, Ulrich
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.
    The consequences of surviving infection across the metamorphic boundary: tradeoff insights from RNAseq and life history measuresManuscript (preprint) (Other academic)
    Abstract [en]

    The broad diversity of insect life has been shaped, in part, by pathogen pressure, yet the influence of injury and infection during critical periods of development is understudied. During development, insects undergo metamorphosis, wherein the organism experiences a dramatic shift in their overall morphology, and physiology. In temperate zones, metamorphosis is often directly followed by a developmental arrest called diapause, for which the insect needs to acquire enough energy reserves before the onset of winter. We investigated the long-term effects of injury and infection using two bacteria in the butterfly Pieris napi, revealing that the negative consequences of bacterial infection carry across the metamorphic boundary. Initial direct effects of infection were weight loss and slower development, as well as an increased mortality at higher infection levels. The detrimental effects were stronger in the gram-positive Micrococcus luteus compared to gram-negative Escherichia coli. Transcriptome-wide differences between the two bacteria were already observed in the gene expression profile of the first 24 hours after infection. Larvae infected with M. luteus showed a strong suppression of all non-immunity related processes, with several types of immune responses being activated. The impact of these transcriptomic changes, a tradeoff between homeostasis and immune response, were visible in the life history data, wherein individuals infected with M. luteus had the highest mortality rate, along with the lowest pupal weight, developmental rate and adult weight of all the treatments. Overall, we find that the cost of infection and wounding in the final larval instar carries over the metamorphic boundary, and is expected to negatively affect their lifetime fitness.

  • 6.
    Keehnen, Naomi L. P.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Rolff, Jens
    Theopold, Ulrich
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology.
    Insect Antimicrobial Defences: A Brief History, Recent Findings, Biases, and a Way Forward in Evolutionary Studies2017In: Insect Immunity / [ed] Petros Ligoxygakis, London: Academic Press, 2017, p. 1-33Chapter in book (Refereed)
    Abstract [en]

    We propose that an evolutionary and phenotype-driven approach, harnessing current technological developments, has much to offer for our understanding of insect immunity. After briefly reviewing the history of the discovery of canonical immune system, the current understanding of its components is reviewed and then we argue that the current paradigm of research may be biassed due to (a) its limited taxonomic perspective, (b) the evolutionary time scale being studied, and (c) a focus primarily if not exclusively, upon the canonical, humoural gene set. For the rest of the review, we then discuss the importance of a phenotype down approach as an understudied perspective, exemplified by the need for understanding the basis of cellular responses and wounding as a source of selection on immunity in the wild. We propose that research on those topics almost certainly will provide new insights into the evolution of the insect immune system.

  • 7.
    Keehnen, Naomi L.P.
    Stockholm University, Faculty of Science, Department of Zoology.
    Immunity & the butterfly: A functional genomic study of natural variation in immunity2019Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Butterflies are ubiquitous and abundant, occurring in a wide variety of environments that contain diverse microbial communities with varied pathogenic pressures. These pathogens and parasites present a constant threat to organisms, and have led to the evolution of complex and intricate immune responses. Despite strong selection against immunological threats, organisms display great variation in their immune capabilities, both on the genetic and physiological level. Investigating this variation remains challenging, since differences in immune responses might arise from changes in the amount, size or performance of cells or organs. Disentangling these relative contributions is important, as the targets of selection are expected to differ, ranging from immune genes directly related to the phenotype to genes indirectly involved via cell proliferation. This thesis focuses on characterizing the immune system of the butterfly Pieris napi and investigating its remarkable variation across populations by using both phenotypic and genotypic measurements. By integrating RNA-seq with life history measurements, I found that the cost of infection and wounding in the final larval stage carries over the metamorphic boundary in P. napi (Paper II). Using population comparisons, I identified both the action and potential targets of natural selection in wild populations within their respective immune responses (Paper I, III & IV). The immune genes in P. napi show increased genetic variation compared to the rest of the genome, and microevolutionary selection dynamics act on these genes between and among populations (Paper I). I measured the cellular immune responses related to phagocytosis and melanization in common garden reared larvae originating from two allopatric populations (Spain, Sweden) (Paper III & IV). The two populations were found to differ in their blood cell composition, and overall phagocytic capability, driven by the increased phagocytic propensity of each cell type (Paper III). However, genome wide analysis of divergence between these populations found no excess genetic differentiation in genes annotated to phagocytic capacity, suggesting that our observed population differences might arise from genes affecting the activation or transdifferentiation of cells, which currently lack functional annotation. Interestingly, genes involved in glutamine metabolism, which have been linked to immune cell differentiation in mammals, did show divergence between the populations. In addition, the populations also differed in prophenoloxidase activity, a common method for quantifying immune related melanization in insects, along with the abundance of the cell-type (oenocytoids) related to this important immune function (Paper IV). Integrative analysis using both transcriptomic and genomic data revealed that the genes involved in this phenotype showed no significant differentiation between the populations. However, a gene involved with proper trafficking of melanogenic enzymes in vertebrates was found to be highly expressed and highly diverged between the two populations, providing an interesting candidate for future studies. This thesis demonstrates the advantages of integrating several genomic tools with lab experiments to quantify natural variation in the immune system of butterflies.

     

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  • 8.
    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)
1 - 8 of 8
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