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Evolutionary History of Chemosensory-Related Gene Families Across the Arthropoda Seong-Il Eyun University of Nebraska - Lincoln, [email protected]

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Evolutionary History of Chemosensory-Related Gene Families Across the Arthropoda Seong-Il Eyun University of Nebraska - Lincoln, Seyun2@Unl.Edu University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Papers from the Nebraska Center for Biotechnology Biotechnology, Center for 2017 Evolutionary History of Chemosensory-Related Gene Families across the Arthropoda Seong-il Eyun University of Nebraska - Lincoln, [email protected] Ho Young Soh Chonnam National University Marijan Posavi University of Wisconsin-Madison, [email protected] James B. Munro University of Maryland School of Medicine Daniel S.T. Hughes Baylor College of Medicine See next page for additional authors Follow this and additional works at: https://digitalcommons.unl.edu/biotechpapers Part of the Biotechnology Commons, and the Molecular, Cellular, and Tissue Engineering Commons Eyun, Seong-il; Soh, Ho Young; Posavi, Marijan; Munro, James B.; Hughes, Daniel S.T.; Murali, Shwetha C.; Qu, Jiaxin; Dugan, Shannon; Lee, Sandra L.; Chao, Hsu; Dinh, Huyen; Han, Yi; Doddapaneni, HarshaVardhan; Worley, Kim C.; Muzny, Donna M.; Park, Eun-Ok; Silva, Joana C.; Gibbs, Richard A.; Richards, Stephen; and Lee, Carol Eunmi, "Evolutionary History of Chemosensory- Related Gene Families across the Arthropoda" (2017). Papers from the Nebraska Center for Biotechnology. 14. https://digitalcommons.unl.edu/biotechpapers/14 This Article is brought to you for free and open access by the Biotechnology, Center for at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Papers from the Nebraska Center for Biotechnology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Seong-il Eyun, Ho Young Soh, Marijan Posavi, James B. Munro, Daniel S.T. Hughes, Shwetha C. Murali, Jiaxin Qu, Shannon Dugan, Sandra L. Lee, Hsu Chao, Huyen Dinh, Yi Han, HarshaVardhan Doddapaneni, Kim C. Worley, Donna M. Muzny, Eun-Ok Park, Joana C. Silva, Richard A. Gibbs, Stephen Richards, and Carol Eunmi Lee This article is available at DigitalCommons@University of Nebraska - Lincoln: https://digitalcommons.unl.edu/biotechpapers/14 Evolutionary History of Chemosensory-Related Gene Families across the Arthropoda Seong-il Eyun,†,1 Ho Young Soh,2 Marijan Posavi,3 James B. Munro,4 Daniel S.T. Hughes,5 Shwetha C. Murali,5 Jiaxin Qu,5 Shannon Dugan,5 Sandra L. Lee,5 Hsu Chao,5 Huyen Dinh,5 Yi Han,5 HarshaVardhan Doddapaneni,5 Kim C. Worley,5 Donna M. Muzny,5 Eun-Ok Park,6 Joana C. Silva,4 Richard A. Gibbs,5 Stephen Richards,5 and Carol Eunmi Lee*,3 1Center for Biotechnology, University of Nebraska-Lincoln, Lincoln, NE 2Faculty of Marine Technology, Chonnam National University, Yeosu, Korea 3Center of Rapid Evolution (CORE) and Department of Integrative Biology, University of Wisconsin, Madison, WI 4Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD 5Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX 6Fisheries Science Institute, Chonnam National University, Yeosu, Korea †Present address: Department of Life Science, Chung-Ang University, Seoul, Korea *Corresponding author: E-mail: [email protected]. Associate editor: Takashi Gojobori Abstract Chemosensory-related gene (CRG) families have been studied extensively in insects, but their evolutionary history across the Arthropoda had remained relatively unexplored. Here, we address current hypotheses and prior conclusions on CRG family evolution using a more comprehensive data set. In particular, odorant receptors were hypothesized to have proliferated during terrestrial colonization by insects (hexapods), but their association with other pancrustacean clades and with independent terrestrial colonizations in other arthropod subphyla have been unclear. We also examine hy- potheses on which arthropod CRG family is most ancient. Thus, we reconstructed phylogenies of CRGs, including those from new arthropod genomes and transcriptomes, and mapped CRG gains and losses across arthropod lineages. Our analysis was strengthened by including crustaceans, especially copepods, which reside outside the hexapod/branchiopod clade within the subphylum Pancrustacea. We generated the first high-resolution genome sequence of the copepod Eurytemora affinis and annotated its CRGs. We found odorant receptors and odorant binding proteins present only in hexapods (insects) and absent from all other arthropod lineages, indicating that they are not universal adaptations to land. Gustatory receptors likely represent the oldest chemosensory receptors among CRGs, dating back to the Placozoa. We also clarified and confirmed the evolutionary history of antennal ionotropic receptors across the Arthropoda. All Article antennal ionotropic receptors in E. affinis were expressed more highly in males than in females, suggestive of an asso- ciation with male mate-recognition behavior. This study is the most comprehensive comparative analysis to date of CRG family evolution across the largest and most speciose metazoan phylum Arthropoda. Key words: chemoreception, chemoreceptor, chemosensory receptors, gene family evolution, Copepoda, Crustacea. Introduction would have imposed novel challenges and requirements for chemosensation, as the transmission and reception of chem- Chemosensation refers to the physiological responses of sense ical stimuli become altered in diverse environments, such as organs to chemical stimuli, including taste and odor, and is in aquatic versus aerial media. Such diverse transmission me- observed across a wide range of taxa from bacteria to humans dia would impose varying evolutionary pressures on genes (Bargmann 2006; Vosshall and Stocker 2007; Nei et al. 2008; underlying chemosensory responses. Interestingly, the three Kaupp 2010). Chemosensory systems play critical roles in major subphyla within the Arthropoda, that is, the mediating behavioral responses such as feeding, mating, pred- Pancrustacea (e.g., crustaceans and insects), Myriapoda (e.g., ator avoidance, and predation. Chemosensing in the phylum centipede and millipedes), and Chelicerata (e.g., spiders, mites, Arthropoda is particularly intriguing, given the extraordinary and scorpions) have colonized freshwater and terrestrial hab- diversity of habitats and ecological niches that arthropods itats independently (Giribet et al. 2001; Regier et al. 2010; von have been able to colonize, spanning marine, brackish, hyper- Reumont et al. 2012; Oakley et al. 2013). Thus, given these saline, freshwater, terrestrial, and extremely arid environ- independent transitions to land, have chemosensing systems ments (Cloudsley-Thompson 1975; Sømme 1989; Glenner evolved through the same pathways during these parallel but et al. 2006; Kelley et al. 2014). These habitat colonizations independent colonization events? ß The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] Open Access 1838 Mol. Biol. Evol. 34(8):1838–1862 doi:10.1093/molbev/msx147 Advance Access publication April 29, 2017 Arthropod Chemosensory-Related Genes . doi:10.1093/molbev/msx147 MBE Based primarily on the study of the fruit fly Drosophila mel- ancient arthropod chemoreceptors, dating back to the origin anogaster, arthropod chemoreception has been found to be of the Protostomia (Croset et al. 2010). In contrast, more recent mediated by three different multigene families of chemosen- studies found GRs to be more ancient, originating early in the sory receptors. These include two gene families of seven trans- evolution of metazoans, given their presence in the eumeta- membrane receptors, namely the gustatory receptors (GRs) zoan phylum Placozoa (Trichoplax adhaerens)(Robertson (Clyne et al. 2000) and the more derived odorant receptors 2015; Saina et al. 2015). In addition, the analysis of evolutionary (ORs) (Clyne et al. 1999; Gao and Chess 1999; Vosshall et al. histories of IR genes has been based mostly on studies of 1999), which are unrelated to the vertebrate GRs and ORs insects, with relatively little investigation of their presence or (Gardiner et al. 2009). More recently, a third family of chemo- absence in other arthropod lineages (Croset et al. 2010). sensory receptors has been discovered in D. melanogaster, Addressing the hypotheses above, regarding patterns of namely, the ionotropic receptors (IRs), which are a class within CRG evolution across the Arthropoda, requires the analysis the ancient and highly conserved ionotropic glutamate recep- of multiple members within the subphylum Pancrustacea tor (iGluR) family of ligand-gated ion channels (Benton et al. beyond the insects (Hexapoda), the inclusion of the arthro- 2009; Croset et al. 2010; Abuin et al. 2011; Benton 2015). In pod subphyla Myriapoda (e.g., centipedes and millipedes) and addition, two soluble binding protein families, the chemosen- Chelicerata (e.g., spiders, mites, and scorpions), as well as the sory proteins (CSPs) and insect-type odorant binding proteins inclusion of outgroup phyla. However, until recently, genomic (OBPs), are known to mediate the transport of ligands to the data beyond the hexapod/branchiopod clade (e.g., insects chemosensory receptors (Pelosi et al. 2006; Laughlin et al. 2008; and Daphnia) had been lacking. Very few comparative anal- Vieira and Rozas 2011; Pelosi et
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