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The consequences of surviving infection across the metamorphic boundary: tradeoff insights from RNAseq and life history measures
Stockholm University, Faculty of Science, Department of Zoology, Population Genetics.ORCID iD: 0000-0002-8782-3477
Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. Biology Centre CAS, Czech Republic.ORCID iD: 0000-0002-6382-4467
Stockholm University, Faculty of Science, Department of Zoology, Animal Ecology.ORCID iD: 0000-0003-4195-8920
Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.ORCID iD: 0000-0002-1009-8254
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(English)Manuscript (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.

National Category
Evolutionary Biology
Research subject
Population Genetics
Identifiers
URN: urn:nbn:se:su:diva-175461DOI: 10.1101/792176OAI: oai:DiVA.org:su-175461DiVA, id: diva2:1366238
Available from: 2019-10-28 Created: 2019-10-28 Last updated: 2019-11-01
In thesis
1. Immunity & the butterfly: A functional genomic study of natural variation in immunity
Open this publication in new window or tab >>Immunity & the butterfly: A functional genomic study of natural variation in immunity
2019 (English)Doctoral 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.

 

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm, 2019. p. 31
Keywords
eco-immunology, functional genomics, transcriptomics, innate immunity, selection dynamics, melanization, phagocytosis, population genetics, Pieris napi
National Category
Evolutionary Biology Genetics Zoology
Research subject
Population Genetics
Identifiers
urn:nbn:se:su:diva-175465 (URN)978-91-7797-825-1 (ISBN)978-91-7797-826-8 (ISBN)
Public defence
2019-12-13, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 2: Manuscript. Paper 3: Manuscript. Paper 4: Manuscript.

Available from: 2019-11-20 Created: 2019-10-28 Last updated: 2019-11-11Bibliographically approved

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Keehnen, Naomi L. P.Kučerova, LucieNylin, SörenTheopold, UlrichWheat, Christopher W.
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