Rapid seasonal evolution in innate immunity of wild <em>Drosophila melanogaster</em>

Emily Behrman

Virginia Howick

Martin Kapun

Fabian Staubach

Figure S1:

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Figure S2:

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Supplementary methods:

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^{Department of Biology, University of Pennsylvania, 433 S. University Ave., Philadelphia, PA 19104, USA}

^{Department of Entomology, Cornell University, 3125 Comstock Hall, Ithaca, NY 14853, USA}

^{Department of Ecology and Evolution, University of Lausanne, Lausanne 1015, Switzerland}

^{Department of Biology, Stanford University, 371 Serra St, Stanford, CA 94305-5020, USA}

^{Albert-Ludwigs University, Freiburg, Germany}

^{Department of Biology, University of Virginia, 409 McCormic Rd, Charlottesville, VA 22904, USA}

e-mail: ude.nnepu.sas@ylimeb

^{Present address: Janelia Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive Ashburn, VA 20147, USA.}

^{Present address: Wellcome Trust Sanger Institute, Hinxton, University of Cambridgeshire, Cambridge CB10 1AS, UK.}

Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9.figshare.c.3959995.

Received 2017 Nov 23; Accepted 2017 Dec 5.

Abstract

Understanding the rate of evolutionary change and the genetic architecture that facilitates rapid adaptation is a current challenge in evolutionary biology. Comparative studies show that genes with immune function are among the most rapidly evolving genes across a range of taxa. Here, we use immune defence in natural populations of Drosophila melanogaster to understand the rate of evolution in natural populations and the genetics underlying rapid change. We probed the immune system using the natural pathogens Enterococcus faecalis and Providencia rettgeri to measure post-infection survival and bacterial load of wild D. melanogaster populations collected across seasonal time along a latitudinal transect along eastern North America (Massachusetts, Pennsylvania and Virginia). There are pronounced and repeatable changes in the immune response over the approximately 10 generations between spring and autumn collections, with a significant but less distinct difference observed among geographical locations. Genes with known immune function are not enriched among alleles that cycle with seasonal time, but the immune function of a subset of seasonally cycling alleles in immune genes was tested using reconstructed outbred populations. We find that flies containing seasonal alleles in Thioester-containing protein 3 (Tep3) have different functional responses to infection and that epistatic interactions among seasonal Tep3 and Drosomycin-like 6 (Dro6) alleles underlie the immune phenotypes observed in natural populations. This rapid, cyclic response to seasonal environmental pressure broadens our understanding of the complex ecological and genetic interactions determining the evolution of immune defence in natural populations.

Keywords: rapid adaptation, innate immunity, Drosophila melanogaster, Thioester-containing protein 3, Drosomycin-like 6, epistasis

Abstract

Acknowledgements

We thank Robert Unckless and two anonymous reviewers for constructive feedback on the manuscript.

Acknowledgements

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