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Integrative Comparative Biology ICB-55(5)Cover.qxd 10/13/15 5:46 PM Page 1 Integrative Integrative ISSN 1540-7063 (PRINT) Integrative ISSN 1557-7023 (ONLINE) &Comparative Biology & Volume 55 Number 5 November 2015 Biology Comparative CONTENTS Linking Insects with Crustacea: Comparative Physiology of the Pancrustacea Organized by Sherry L. Tamone and Jon F. Harrison 765 Linking Insects with Crustacea: Physiology of the Pancrustacea: An Introduction to the Symposium Sherry L.Tamone and Jon F. Harrison 55Volume Number 5 2015 November 771 Exoskeletons across the Pancrustacea: Comparative Morphology, Physiology, Biochemistry and Genetics Robert Roer, Shai Abehsera and Amir Sagi 792 Evolution of Respiratory Proteins across the Pancrustacea Thorsten Burmester 802 Handling and Use of Oxygen by Pancrustaceans: Conserved Patterns and the Evolution of Respiratory Structures Jon F. Harrison 816 Links between Osmoregulation and Nitrogen-Excretion in Insects and Crustaceans Dirk Weihrauch and Michael J. O’Donnell 830 The Dynamic Evolutionary History of Pancrustacean Eyes and Opsins Miriam J. Henze and Todd H. Oakley 843 Integrated Immune and Cardiovascular Function in Pancrustacea: Lessons from the Insects Julián F. Hillyer 856 Respiratory and Metabolic Impacts of Crustacean Immunity: Are there Implications for the Insects? Karen G. Burnett and Louis E. Burnett 869 Morphological, Molecular, and Hormonal Basis of Limb Regeneration across Pancrustacea Sunetra Das 878 Evolution of Ecdysis and Metamorphosis in Arthropods:The Rise of Regulation of Juvenile Hormone Sam P. S. Cheong, Juan Huang, William G. Bendena, Stephen S. Tobe and Jerome H. L. Hui 891 Neocaridina denticulata: A Decapod Crustacean Model for Functional Genomics Donald L. Mykles and Jerome H. L. Hui Leading Students and Faculty to Quantitative Biology Through Active Learning Organized by Lindsay D. Waldrop and Laura A. Miller 898 Introduction to the Symposium ‘‘Leading Students and Faculty to Quantitative Biology through Active Learning’’ Lindsay D. Waldrop and Laura A. Miller 901 A Mathematical Model and MATLAB Code for Muscle–Fluid–Structure Simulations Nicholas A. Battista, Austin J. Baird and Laura A. Miller 912 Interdisciplinary Laboratory Course Facilitating Knowledge Integration, Mutualistic Teaming, and Original Discovery Robert J. Full, Robert Dudley, M. A. R. Koehl, Thomas Libby and Cheryl Schwab 926 Using Technology to Expand the Classroom in Time, Space, and Diversity Joshua Drew 933 Using Active Learning to Teach Concepts and Methods in Quantitative Biology Lindsay D. Waldrop, Stephen C. Adolph, Cecilia G. Diniz Behn, Emily Braley, Joshua A. Drew, Robert J. Full, Louis J. Gross, John A. Jungck, Brynja Kohler, Jennifer C. Prairie, Blerta Shtylla and Laura A. Miller Integrative &Comparative Biology Volume 55 Number 5 November 2015 www.icb.oxfordjournals.org Integrative and Comparative Biology www.icb.oxfordjournals.org Society for Integrative and Comparative Biology Editor-in-Chief Executive Officers, Society for Integrative and Harold Heatwole, North Carolina State University, Raleigh, Comparative Biology NC, USA and University of New England, Armidale, NSW, President Australia Peter Wainwright (2017) President-Elect Assistant Editors Louis Burnett (2017) Suzanne C. Miller, North Carolina State University Past President Billie Swalla (2016) Editorial Board Secretary Kathy Dickson (2018) Divisional Representatives Program Officer Animal Behavior (DAB) Sherry Tamone (2016) Matthew Grober (2018), Georgia State University Program Officer Elect Comparative Biomechanics (DCB) Richard Blob (2016) Anna Ahn (2017), Harvey Mudd College Treasurer Comparative Endocrinology (DCE) Karen Martin (2019) Henry John-Alder (2018), Rutgers University Members-At-Large Comparative Physiology and Biochemistry (DCPB) Cheryl Wilga (2016) Dane Crossley (2016), University of North Dakota L. Patricia Hernandez (2017) Ecoimmunology and Disease Ecology (DEDE) Jennifer Bunaford (2018) Ken Field (2020), Bucknell University Divisional Chairs Ecology and Evolution (DEE) DAB Chair: Diana K. Hews (2016) Michael Sears (2017), Clemson University DCB Chair: Melina Hale (2017) Evolutionary Developmental Biology (DEDB) DCE Chair: Mary Mendonca (2016) Robert Zeller (2018), San Diego State University DCPB Chair: Stephen Secor (2016) Invertebrate Zoology (DIZ) DEDB Chair: Sally Leys (2016) Bruno Pernet (2020), California State University, DEDE Chair: Lynn Martin (2017) Long Beach DEE Chair: Michael Sears (2017) Neurobiology (DNB) DIZ Chair: John Zardus (2018) Richard A. Satterlie (2018), University of North DNB Chair: Paul Moore (2018) Carolina at Wilmington DPCB Chair: Michael E. Alfaro (2016) Phylogenetics and Comparative Biology (DPCB) DVM Chair: Callum Ross (2017) Lars Schmitz (2019), W.M. Keck Science Department of Editor-in-Chief, ICB: Harold F. Heatwole (2016) Claremont McKenna, Pitzer, and Scripps Colleges SPDAC Chair: Sean Lema (2016) Vertebrate Morphology (DVM) Ed. Council Chair: Bram Lutton (2018) Lara Ferry (2016), Arizona State University BPC Chair: Michele Nishiguchi (2016) Executive Director: Brett J. Burk Associates Dominique Adriaens (2016), University of Ghent, Ghent, Belgium Christopher R. Bridges (2016), Heinrich-Heine Universita´t, Dusselforf, Germany Berry Pinshow (2016), Ben Gurion University of the Negev, Israel Julia Sigwart (2018), Queen’s University Belfast Cover image: Mating blue-tailed damselflies (Ischnura elegans). Insects like these damselflies are derived crustaceans, but they have been historically ranked as different taxonomic classes within arthropods and studied separately. In this issue, articles from the symposium ‘‘Linking Insects with Crustacea: Comparative Physiology of the Pancrustacea’’ develop synergies based on our new evolutionary understanding of the group. Photo by Miriam J. Henze. Integrative and Comparative Biology Advance Access published August 28, 2015 Integrative and Comparative Biology Integrative and Comparative Biology, pp. 1–13 doi:10.1093/icb/icv100 Society for Integrative and Comparative Biology SYMPOSIUM TheDynamicEvolutionaryHistoryofPancrustaceanEyesandOpsins Miriam J. Henze* and Todd H. Oakley1,† *Department of Biology, Lund University, Lund, Sweden; †Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA, USA From the symposium ‘‘Linking Insects with Crustacea: Comparative Physiology of the Pancrustacea’’ presented at the Downloaded from annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2015 at West Palm Beach, Florida. 1E-mail: [email protected] Synopsis Pancrustacea (Hexapoda plus Crustacea) display an enormous diversity of eye designs, including multiple types http://icb.oxfordjournals.org/ of compound eyes and single-chambered eyes, often with color vision and/or polarization vision. Although the eyes of some pancrustaceans are well-studied, there is still much to learn about the evolutionary paths to this amazing visual diversity. Here, we examine the evolutionary history of eyes and opsins across the principle groups of Pancrustacea. First, we review the distribution of lateral and median eyes, which are found in all major pancrustacean clades (Oligostraca, Multicrustacea, and Allotriocarida). At the same time, each of those three clades has taxa that lack lateral and/or median eyes. We then compile data on the expression of visual r-opsins (rhabdomeric opsins) in lateral and median eyes across Pancrustacea and find no evidence for ancient opsin clades expressed in only one type of eye. Instead, opsin clades with at University of California, Santa Barbara on August 31, 2015 eye-specific expression are products of recent gene duplications, indicating a dynamic past, during which opsins often changed expression from one type of eye to another. We also investigate the evolutionary history of peropsins and r-opsins, which are both known to be expressed in eyes of arthropods. By searching published transcriptomes, we discover for the first time crustacean peropsins and suggest that previously reported odonate opsins may also be peropsins. Finally, from analyzing a reconciled, phylogenetic tree of arthropod r-opsins, we infer that the ancestral pancrustacean had four visual opsin genes, which we call LW2, MW1, MW2, and SW. These are the progenitors of opsin clades that later were variously duplicated or lost during pancrustacean evolution. Together, our results reveal a particularly dynamic history, with losses of eyes, duplication and loss of opsin genes, and changes in opsin expression between types of eyes. Introduction Here, we review the presence and absence of the With color vision, polarization vision, multiple types two main types of arthropod eyes across major pan- of eyes, and more optical diversity than in any other crustacean groups, we summarize data on gene ex- phylum (Land and Nilsson 2012), pancrustacean eyes pression in those eyes, and we infer phylogenetic are of particular interest to evolutionary biologists. histories of two kinds of pancrustacean opsins, How the diversity and exquisite functionality of visual r-opsins (rhabdomeric opsins) and peropsins. those eyes evolved are enduring questions. While From their last common ancestor, pancrustaceans some species, like Drosophila, are well studied inherited two fundamentally different types of ce- (Buschbeck and Friedrich 2008; Wernet et al. phalic visual organs (Paulus 1979, 2000; Bitsch and 2015), we know far less about groups other than Bitsch 2005; Nilsson and Kelber 2007): lateral and winged insects. In recent years,
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