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The Genome of Drosophila innubila Reveals Lineage-Specific Patterns of Selection in Immune Genes

Hill, T, BS Koseva, and RL Unckless. 2018. The Genome of Drosophila innubila Reveals Lineage-Specific Patterns of Selection in Immune Genes. In press at Molecular Biology and Evolution.

Pathogenic microbes can exert extraordinary evolutionary pressure on their hosts. They can spread rapidly and sicken or even kill their host to promote their own proliferation. Because of this strong selective pressure, immune genes are some of the fastest evolving genes across metazoans, as highlighted in mammals and insects. Drosophila melanogaster serves as a powerful model for studying host/pathogen evolution. While Drosophila melanogaster are frequently exposed to various pathogens, little is known about D. melanogaster’s ecology, or if they are representative of other Drosophila species in terms of pathogen pressure. Here, we characterize the genome of Drosophila innubila, a mushroom-feeding species highly diverged from D. melanogaster and investigate the evolution of the immune system. We find substantial differences in the rates of evolution of immune pathways between D. innubila and D. melanogaster. Contrasting what was previously found for D. melanogaster, we find little evidence of rapid evolution of the antiviral RNAi genes and high rates of evolution in the Toll pathway. This suggests that, while immune genes tend to be rapidly evolving in most species, the specific genes that are fastest evolving may depend either on the pathogens faced by the host and/or divergence in the basic architecture of the host’s immune system.

PREPRINTS

  • Beonmar, S, KC Evans, RL Unckless and JR Chandler. 2019. Efflux pumps in Chromobacterium species and their involvement in antibiotic tolerance and survival in a co-culture competition model. BioRxiv. doi:10.1101/562140. PDF

  • Hill, T, BS Koseva, and RL Unckless. 2018. Antiviral genes are not fast evolving in Drosophila innubila. BioRxiv. doi: 10.1101/383877. PDF

  • Chapman, JR, T Hill and RL Unckless. 2018. Balancing selection drives the maintenance of genetic variation in Drosophila antimicrobial peptides. BioRxiv. doi:10.1101/298893. PDF

Prior publications

2019

  • Duxbury, EML, JP Day, DM Vespasiani, Y Thuringer, I Tolosana, SCL Smtih, L Tagliaferri, A KAacioglu, I Lindsley, L Love, RL Unckless, FM Jiggins and B Longdon. 2019. Host-pathogen coevolution increases genetic variation in susceptibility to infection. eLife 8: e46440. doi:10.7554/eLife.46440.

2018

  • Pieper, KM, RL Unckless and KA Dyer. 2018. A fast-evolving X-linked duplicate of importin-a2 is overexpressed in sex-ratio drive in Drosophila neotestacea. Molecular ecology 27(24): 5165-5179. doi:10.1111/mec.14928.

  • Smith, BR and RL Unckless. 2018. Draft genome of Lysinibacillus fusiformis Strain Juneja, a laboratory-derived pathogen of Drosophila melanogaster. Genome Announcements 6(5), e01571-17. doi:10.1128/genomeA.01571-17.

  • Hill, T and R.L. Unckless. 2018. The dynamic evolution of the Drosophila innubila Nudivirus. Infection, Genetics and Evolution 57: 151-157. doi:10.1016/j.meegid.2017.11.013.

2017

  • Hill, T. and R.L. Unckless. 2017. 2017. Baculovirus molecular evolution via gene turnover and recurrent positive selection of key genes. Journal of Virology 91: e01319-17. doi: 10.1128/JVI.01319-17.

  • Ahmed-Braimah, Y.H., R.L. Unckless and A.G. Clark. 2017. Evolutionary dynamics of male reproductive genes in the Drosophila virilis subgroup. G3: Genes, Genomes, Genetics 2017;7(9):3145-55. doi:10.1534/g3.117.1136.

2016

  • Akhund-Zade, J., A.O. Bergland and R.L. Unckless. 2016. The genetic basis of natural variation in virgin egg retention in Drosophila melanogaster (Diptera: Drosophilidae). Journal of Insect Science 17(1). doi:10.1093/jisesa/iew094.

  • Lindholm, AK, … RL Unckless, et al. (22 authors). 2016. The ecology and evolutionary dynamics of meiotic drive. Trends in Ecology and Evolution 31:315-326. doi:10.1016/j.tree.2016.02.001.

  • Unckless, RL and BP Lazzaro. 2016. The potential for adaptive maintenance of diversity in insect antimicrobial peptides. Philisophical Transactions of the Royal Society B 371:20150291. doi: 10.1098/rstb.2015.0291.

  • Unckless, RL, VM Howick and BP Lazzaro. 2016. Convergent balancing selection on an antimicrobial peptide in Drosophila. Current Biology 26:257-262. Doi: 10.1016/j.cub.2015.11.063

2015

  • Unckless, RL and AG Clark. 2015. Driven to extinction: on the probability of evolutionary rescue from sex-ratio meiotic drive. bioRxiv doi: http://dx.doi.org/10.1101/018820.

  • Unckless, RL, PW Messer T Connallon and AG Clark. 2015. Modeling the Manipulation of Natural Populations by the Mutagenic Chain Reaction. Genetics 201:425-431. doi: 10.1534/genetics.115.177592 (Highlighted article).

  • Unckless, RL, SM Rottschaefer and BP Lazzaro. 2015. The Complex Contributions of Genetics and Nutrition to Immunity in Drosophila melanogaster. PLoS Genet 11: e1005030. doi:10.1371/journal.pgen.1005030

  • Unckless, RL, SM Rottschaefer and BP Lazzaro. 2015. A genome-wide association study for nutritional indices in Drosophila. Genes, Genomes and Genetics 5:417-425. doi: 10.1534/g3.114.016477.

  • Unckless, RL, AM Larracuente and AG Clark. 2015. Sex-ratio meiotic drive and Y-linked resistance in Drosophila affinis. Genetics 199:831-840. doi:10.1534/genetics.114.173948.

2014

  • Orr, HA and RL Unckless. 2014. The population genetics of evolutionary rescue. PLoS Genetics 10(8): e104551.

  • Unckless, RL and AG Clark. 2014. Sex-ratio meiotic drive and interspecific competition. Journal of Evolutionary Biology 27(8): 1513-1521.

Prior to 2014

  • Unckless, RL and J Jaenike. 2012. Maintenance of a male-killing Wolbachia in Drosophila innubila by male-killing dependent and male-killing independent mechanisms. Evolution 66(3):678-689.

  • Unckless, RL. 2011. The potential role of the X chromosome in the emergence of male-killing from mutualistic endosymbionts. Journal of Theoretical Biology 291: 99-104.

  • Unckless, RL. 2011. A DNA virus of Drosophila. PLoS ONE 6: e26564.

  • Jaenike J, RL Unckless, SN Cockburn, LM Boelio, and SJ Perlman. 2010. Adaptive evolution via symbiosis: recent spread of a defensive symbiont in Drosophila. Science 329: 212-215.

  • Unckless, RL and HA Orr. 2009. The population genetics of adaptation: multiple substitutions on a smooth fitness landscape. Genetics 183: 1079-1086.

  • Jaenike J, JK Stahlhut, LM Boelio and RL Unckless. 2009. Association between Wolbachia and Spiroplasma within Drosophila neotestacea: an emerging symbiotic mutualism. Molecular Ecology 19: 414-425.

  • Unckless, RL and JK Herren. 2009. Population genetics of sexually antagonistic mitochondrial mutants under inbreeding. Journal of Theoretical Biology 260: 132-136.

  • Unckless, RL, LM Boelio, JK Herren and J Jaenike. 2009. Wolbachia as populations within individual insects: causes and consequences of density variation in natural populations. Proceedings of the Royal Society B 276: 2805-2811.

  • Unckless, RL, LM Boelio, C Cornish and KA Dyer. 2008. Isolation and characterization of 30 polymorphic microsatellite loci from the mycophagous fly Drosophila innubila. Molecular Ecology Research 8: 939-942.

  • Unckless, RL and HA Orr. 2009. Dobzhansky-Muller incompatibilities and adaptation to a shared environment. Heredity 102: 214-217.

  • Orr, HA and RL Unckless. 2008. Population extinction and the genetics of adaptation. American Naturalist 172: 160-169.

  • Unckless, RL and J Makarewicz. 2007. The impact of nutrient loading from Canada Geese (Branta canadensis) on water quality, a mesocosm approach. Hydrobiologia 586: 391-401.