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April 30, 2019 u vol. 116 u no. 18

From the Cover

8919 Hyena alliances and social rank 8824 Early taro cultivation in Polynesia 8846 Same-sex marriage and antigay bias 8966 Peanut-allergen inhibitor 9030 Multiple sclerosis and cell senescence

Contents

THIS WEEK IN PNAS Cover image: Pictured is a coalition of 8635 In This Issue young spotted hyenas (Crocuta crocuta) eliciting a submissive response from a larger group-mate. Eli D. Strauss INNER WORKINGS—An over-the-shoulder look at scientists at work and Kay E. Holekamp studied the 8638 Genomics blazes a trail to improved cannabis cultivation interactions of five generations of Elie Dolgin spotted hyenas in Kenya and found that female hyenas were more likely to defeat and outrank a higher-ranking PROFILE opponent when they garnered support 8641 Profile of Zhisheng An from other female hyenas. Further, rank Jennifer Viegas differences between female hyenas See Inaugural Article on page 8657 were amplified over generations due to demographic changes. The findings provide insight into mechanisms leading COMMENTARIES to changes in social rank. See the article 8644 Hyena politics: The dynamics of dynasties by Strauss and Holekamp on pages Joan B. Silk 8919–8924. Image courtesy of Kate See companion article on page 8919 Yoshida (Las Vegas Natural History Museum, Las Vegas). 8646 New age for progressive multiple sclerosis Jaime Imitola See companion article on page 9030

LETTERS 8649 Time domain versus energy domain neutron scattering analysis of protein dynamics Wolfgang Doster 8651 Reply to Doster: Franck–Condon and Van Hove formulation of quasielastic neutron scattering from complex systems Gerald R. Kneller 8653 Phototransduction gain at the G-protein, transducin, and effector protein, phosphodiesterase-6, stages in retinal rods Martin Heck, Klaus Peter Hofmann, Timothy W. Kraft, and Trevor D. Lamb 8655 Reply to Heck et al.: Signal amplification at the rhodopsin-to-transducin·phosphodiesterase step in rod phototransduction K.-W. Yau, W. W. S. Yue, and D. Silverman

Free online through the PNAS open access option. PNAS u April 30, 2019 u vol. 116 u no. 18 u iii–vii Downloaded by guest on October 2, 2021 INAUGURAL ARTICLE EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES 8657 Severe haze in northern China: A synergy of 8657 Severe haze in northern China: A synergy of anthropogenic emissions and atmospheric processes anthropogenic emissions and atmospheric processes Zhisheng An, Ru-Jin Huang, Renyi Zhang, Xuexi Tie, Guohui Li, Zhisheng An, Ru-Jin Huang, Renyi Zhang, Xuexi Tie, Guohui Li, Junji Cao, Weijian Zhou, Zhengguo Shi, Yongming Han, Junji Cao, Weijian Zhou, Zhengguo Shi, Yongming Han, Zhaolin Gu, and Yuemeng Ji Zhaolin Gu, and Yuemeng Ji See Profile on page 8641 See Profile on page 8641 8728 Climate models can correctly simulate the continuum of global-average temperature variability PHYSICAL SCIENCES Feng Zhu, Julien Emile-Geay, Nicholas P. McKay, Gregory J. Hakim, Deborah Khider, Toby R. Ault, Eric J. Steig, Sylvia Dee, APPLIED PHYSICAL SCIENCES and James W. Kirchner 8667 Deep learning in turbulent convection networks 8734 Anthropogenic strath terrace formation caused by Enrico Fonda, Ambrish Pandey, Jo¨rg Schumacher, reduced sediment retention and Katepalli R. Sreenivasan Sarah A. Schanz, David R. Montgomery, and Brian D. Collins 8673 Scale-free resilience of real traffic jams 8740 K isotopes as a tracer for continental weathering and Limiao Zhang, Guanwen Zeng, Daqing Li, Hai-Jun Huang, geological K cycling H. Eugene Stanley, and Shlomo Havlin Shilei Li (李石磊), Weiqiang Li, Brian L. Beard, Maureen E. 8679 Shock growth of ice crystal near equilibrium melting Raymo, Xiaomin Wang (王小敏), Yang Chen (陈旸), and Jun Chen pressure under dynamic compression 8746 Neoproterozoic to early Phanerozoic rise in island arc Yong-Jae Kim, Yun-Hee Lee, Sooheyong Lee, Hiroki Nada, redox state due to deep ocean oxygenation and and Geun Woo Lee increased marine sulfate levels Daniel A. Stolper and Claire E. Bucholz BIOPHYSICS AND COMPUTATIONAL BIOLOGY 8685 A diecast mineralization process forms the tough ENGINEERING mantis shrimp dactyl club 8756 Disconnection description of triple-junction motion Shahrouz Amini, Maryam Tadayon, Jun Jie Loke, Akshita Spencer L. Thomas, Chaozhen Wei, Jian Han, Yang Xiang, Kumar, Deepankumar Kanagavel, Hortense Le Ferrand, Martial and David J. Srolovitz Duchamp, Manfred Raida, Radoslaw M. Sobota, Liyan Chen, Shawn Hoon, and Ali Miserez 8766 Macromolecular relaxation, strain, and extensibility determine elastocapillary thinning and extensional 8693 Unified energetics analysis unravels SpCas9 cleavage viscosity of polymer solutions activity for optimal gRNA design Jelena Dinic and Vivek Sharma Dong Zhang, Travis Hurst, Dongsheng Duan, and Shi-Jie Chen 9002 Rapid screening of engineered microbial therapies in 8699 Structural dynamics and transient lipid binding of a 3D multicellular model synaptobrevin-2 tune SNARE assembly and membrane fusion Tetsuhiro Harimoto, Zakary S. Singer, Oscar S. Velazquez, Joanna Zhang, Samuel Castro, Taylor E. Hinchliffe, William Nils-Alexander Lakomek, Halenur Yavuz, Reinhard Jahn, Mather, and Tal Danino and A´ngel Pe´rez-Lara

8889 Commonly used FRET fluorophores promote collapse ENVIRONMENTAL SCIENCES of an otherwise disordered protein 8775 Fine-scale damage estimates of particulate matter air Joshua A. Riback, Micayla A. Bowman, Adam M. Zmyslowski, pollution reveal opportunities for location-specific Kevin W. Plaxco, Patricia L. Clark, and Tobin R. Sosnick mitigation of emissions Andrew L. Goodkind, Christopher W. Tessum, Jay S. Coggins, CHEMISTRY Jason D. Hill, and Julian D. Marshall 8709 Intrinsically cell-penetrating multivalent and 8781 Dating glacier ice of the last millennium by multitargeting ligands for myotonic dystrophy type 1 quantum technology JuYeon Lee, Yugang Bai, Ullas V. Chembazhi, Shaohong Peng, Zhongyi Feng, Pascal Bohleber, Sven Ebser, Lisa Ringena, Kevin Yum, Long M. Luu, Lauren D. Hagler, Julio F. Serrano, Maximilian Schmidt, Arne Kersting, Philip Hopkins, H. Y. Edwin Chan, Auinash Kalsotra, and Steven C. Zimmerman Helene Hoffmann, Andrea Fischer, Werner Aeschbach, 8715 Correlated interfacial water transport and proton and Markus K. Oberthaler conductivity in perfluorosulfonic acid membranes Xiao Ling, Mischa Bonn, Katrin F. Domke, and Sapun H. Parekh MATHEMATICS – – 8721 Modular, stereocontrolled Cβ H/Cα C activation of 8787 Counterexamples in scale calculus alkyl carboxylic acids Benjamin Filippenko, Zhengyi Zhou, and Katrin Wehrheim Ming Shang, Karla S. Feu, Julien C. Vantourout, Lisa M. Barton, Heather L. Osswald, Nobutaka Kato, Kerstin Gagaring, Case W. McNamara, Gang Chen, Liang Hu, Shengyang Ni, PHYSICS Paula Ferna´ndez-Canelas, Miao Chen, Rohan R. Merchant, 8798 Giant nonvolatile resistive switching in a Mott oxide Tian Qin, Stuart L. Schreiber, Bruno Melillo, Jin-Quan Yu, and ferroelectric hybrid and Phil S. Baran Pavel Salev, Javier del Valle, Yoav Kalcheim, and Ivan K. Schuller COMPUTER SCIENCES 8803 Strain-induced spontaneous Hall effect in an epitaxial 8852 Machine learning-assisted directed protein evolution thin film of a Luttinger semimetal with combinatorial libraries Takumi Ohtsuki, Zhaoming Tian, Akira Endo, Mario Halim, Zachary Wu, S. B. Jennifer Kan, Russell D. Lewis, Bruce J. Shingo Katsumoto, Yoshimitsu Kohama, Koichi Kindo, Mikk Wittmann, and Frances H. Arnold Lippmaa, and Satoru Nakatsuji

iv u www.pnas.org Contents Downloaded by guest on October 2, 2021 8809 Phase-conjugate mirror for water waves driven by the 8709 Intrinsically cell-penetrating multivalent and Faraday instability multitargeting ligands for myotonic dystrophy type 1 Vincent Bacot, Guillaume Durey, Antonin Eddi, Mathias Fink, JuYeon Lee, Yugang Bai, Ullas V. Chembazhi, Shaohong Peng, and Emmanuel Fort Kevin Yum, Long M. Luu, Lauren D. Hagler, Julio F. Serrano, 8815 How a well-adapting immune system remembers H. Y. Edwin Chan, Auinash Kalsotra, and Steven C. Zimmerman Andreas Mayer, Vijay Balasubramanian, Aleksandra M. 8859 Interaction between p53 N terminus and core domain Walczak, and Thierry Mora regulates specific and nonspecific DNA binding Fan He, Wade Borcherds, Tanjing Song, Xi Wei, Mousumi Das, Lihong Chen, Gary W. Daughdrill, SOCIAL SCIENCES and Jiandong Chen

ANTHROPOLOGY 8869 Structural insight into TRPV5 channel function and modulation 8824 Early tropical crop production in marginal subtropical and temperate Polynesia Shangyu Dang, Mark K. van Goor, Daniel Asarnow, YongQiang Wang, David Julius, Yifan Cheng, Matthew Prebble, Atholl J. Anderson, Paul Augustinus, Joshua and Jenny van der Wijst Emmitt, Stewart J. Fallon, Louise L. Furey, Simon J. Holdaway, Alex Jorgensen, Thegn N. Ladefoged, Peter J. Matthews, 8879 Cytosolic Fe-superoxide dismutase safeguards Jean-, Rebecca Phillipps, Rod Wallace, Trypanosoma cruzi from macrophage-derived and Nicholas Porch superoxide radical Alejandra Martı´nez, Carolina Prolo, Damia´n Estrada, ECONOMIC SCIENCES Natalia Rios, Marı´a Noel Alvarez, Marı´a Dolores Pin˜eyro, 8834 Evolution of social norms and correlated equilibria Carlos Robello, Rafael Radi, and Lucı´a Piacenza Bryce Morsky and Erol Akc¸ay BIOPHYSICS AND COMPUTATIONAL BIOLOGY ENVIRONMENTAL SCIENCES 8889 Commonly used FRET fluorophores promote collapse 8840 Climate change and educational attainment in the of an otherwise disordered protein global tropics Joshua A. Riback, Micayla A. Bowman, Adam M. Zmyslowski, Heather Randell and Clark Gray Kevin W. Plaxco, Patricia L. Clark, and Tobin R. Sosnick 8895 α-Sheet secondary structure in amyloid β-peptide PSYCHOLOGICAL AND COGNITIVE SCIENCES drives aggregation and toxicity in 8846 Same-sex marriage legalization associated with Alzheimer’s disease reduced implicit and explicit antigay bias Dylan Shea, Cheng-Chieh Hsu, Timothy M. Bi, Natasha Eugene K. Ofosu, Michelle K. Chambers, Jacqueline M. Chen, Paranjapye, Matthew Carter Childers, Joshua Cochran, and Eric Hehman Colson P. Tomberlin, Libo Wang, Daniel Paris, Jeffrey 9050 Functional connectomics of affective and Zonderman, Gabriele Varani, Christopher D. Link, Mike Mullan, and Valerie Daggett psychotic pathology Justin T. Baker, Daniel G. Dillon, Lauren M. Patrick, Joshua L. 8901 Coherent directed movement toward food modeled Roffman, Roscoe O. Brady Jr., Diego A. Pizzagalli, Dost O¨ ngu¨r, in Trichoplax, a ciliated animal lacking a and Avram J. Holmes nervous system Carolyn L. Smith, Thomas S. Reese, Tzipe Govezensky, SUSTAINABILITY SCIENCE and Rafael A. Barrio 8775 Fine-scale damage estimates of particulate matter air pollution reveal opportunities for location-specific CELL BIOLOGY mitigation of emissions 8909 Distinct segregation patterns of yeast cell-peripheral Andrew L. Goodkind, Christopher W. Tessum, Jay S. Coggins, Jason D. Hill, and Julian D. Marshall proteins uncovered by a method for protein segregatome analysis 8840 Climate change and educational attainment in the Shinju Sugiyama and Motomasa Tanaka global tropics Heather Randell and Clark Gray ECOLOGY BIOLOGICAL SCIENCES 8824 Early tropical crop production in marginal subtropical and temperate Polynesia APPLIED BIOLOGICAL SCIENCES Matthew Prebble, Atholl J. Anderson, Paul Augustinus, Joshua 8852 Machine learning-assisted directed protein evolution Emmitt, Stewart J. Fallon, Louise L. Furey, Simon J. Holdaway, Alex Jorgensen, Thegn N. Ladefoged, Peter J. Matthews, with combinatorial libraries Jean-Yves Meyer, Rebecca Phillipps, Rod Wallace, Zachary Wu, S. B. Jennifer Kan, Russell D. Lewis, Bruce J. and Nicholas Porch Wittmann, and Frances H. Arnold 8919 Social alliances improve rank and fitness in convention-based societies Eli D. Strauss and Kay E. Holekamp 8685 A diecast mineralization process forms the tough See Commentary on page 8644 mantis shrimp dactyl club Shahrouz Amini, Maryam Tadayon, Jun Jie Loke, Akshita 8925 Predators attacking virtual prey reveal the costs and Kumar, Deepankumar Kanagavel, Hortense Le Ferrand, Martial benefits of leadership Duchamp, Manfred Raida, Radoslaw M. Sobota, Liyan Chen, Christos C. Ioannou, Florence Rocque, James E. Herbert-Read, Shawn Hoon, and Ali Miserez Callum Duffield, and Josh A. Firth

Contents PNAS u April 30, 2019 u vol. 116 u no. 18 u v Downloaded by guest on October 2, 2021 ENVIRONMENTAL SCIENCES 9014 Single-cell whole-genome sequencing reveals the 8931 Environmental DNA for improved detection and functional landscape of somatic mutations in B environmental surveillance of schistosomiasis lymphocytes across the human lifespan Mita E. Sengupta, Micaela Hellstro¨m, Henry C. Kariuki, Lei Zhang, Xiao Dong, Moonsook Lee, Alexander Y. Maslov, Annette Olsen, Philip F. Thomsen, Helena Mejer, Eske Tao Wang, and Jan Vijg Willerslev, Mariam T. Mwanje, Henry Madsen, Thomas K. 9020 Cancer stemness, intratumoral heterogeneity, and Kristensen, Anna-Sofie Stensgaard, and Birgitte J. Vennervald immune response across cancers Alex Miranda, Phineas T. Hamilton, Allen W. Zhang, Swetansu EVOLUTION Pattnaik, Etienne Becht, Artur Mezheyeuski, Jarle Bruun, 8834 Evolution of social norms and correlated equilibria Patrick Micke, Aure´lien de Reynies, and Brad H. Nelson Bryce Morsky and Erol Akc¸ay 9030 Cellular senescence in progenitor cells contributes to 8941 Testing the role of trait reversal in evolutionary diminished remyelination potential in progressive diversification using song loss in wild crickets multiple sclerosis Nathan W. Bailey, Sonia Pascoal, and Fernando Montealegre-Z Alexandra M. Nicaise, Laura J. Wagstaff, Cory M. Willis, Carolyn Paisie, Harshpreet Chandok, Paul Robson, Valentina 8950 Exaggeration and cooption of innate immunity for Fossati, Anna Williams, and Stephen J. Crocker social defense See Commentary on page 8646 Mayako Kutsukake, Minoru Moriyama, Shuji Shigenobu, Xian-Ying Meng, Naruo Nikoh, Chiyo Noda, Satoru Kobayashi, and Takema Fukatsu MICROBIOLOGY 9040 Mutations in the HIV-1 envelope glycoprotein can broadly rescue blocks at multiple steps in the GENETICS virus replication cycle 8960 Functional characterization of 3D protein structures Rachel Van Duyne, Lillian S. Kuo, Phuong Pham, Ken Fujii, informed by human genetic diversity and Eric O. Freed Michael Hicks, Istvan Bartha, Julia di Iulio, J. , and Amalio Telenti 9050 Functional connectomics of affective and IMMUNOLOGY AND INFLAMMATION psychotic pathology 8966 Designer covalent heterobivalent inhibitors prevent Justin T. Baker, Daniel G. Dillon, Lauren M. Patrick, Joshua L. IgE-dependent responses to peanut allergen Roffman, Roscoe O. Brady Jr., Diego A. Pizzagalli, Dost O¨ ngu¨r, Peter E. Deak, Baksun Kim, Amina Abdul Qayum, Jaeho Shin, and Avram J. Holmes Girish Vitalpur, Kirsten M. Kloepfer, Matthew J. Turner, Neal 9060 Causal inference accounts for heading perception in Smith, Wayne G. Shreffler, Tanyel Kiziltepe, Mark H. Kaplan, and Basar Bilgicer the presence of object motion + Kalpana Dokka, Hyeshin Park, Michael Jansen, Gregory C. 8975 Hypoxia-inducible factors in CD4 T cells promote DeAngelis, and Dora E. Angelaki metabolism, switch cytokine secretion, and T cell help in humoral immunity 9066 Compulsive drug use is associated with imbalance of orbitofrontal- and prelimbic-striatal circuits in Sung Hoon Cho, Ariel L. Raybuck, Julianna Blagih, Edna Kemboi, Volker H. Haase, Russell G. Jones, punishment-resistant individuals 胡玉正 and Mark R. Boothby Yuzheng Hu ( ), Betty Jo Salmeron, Irina N. Krasnova, + Hong Gu, Hanbing Lu, Antonello Bonci, Jean L. Cadet, 8985 DNA threads released by activated CD4 T Elliot A. Stein, and Yihong Yang lymphocytes provide autocrine costimulation 9072 Modulation of fear generalization by the zona incerta Massimo Costanza, Pietro L. Poliani, Paola Portararo, Barbara Cappetti, Silvia Musio, Francesca Pagani, Archana Venkataraman, Natalia Brody, Preethi Reddi, Jidong Lawrence Steinman, Mario P. Colombo, Rosetta Pedotti, Guo, Donald Gordon Rainnie, and Brian George Dias and Sabina Sangaletti 9078 Reduced default mode network functional + 8995 Select sequencing of clonally expanded CD8 T cells connectivity in patients with recurrent reveals limits to clonal expansion major depressive disorder Huang Huang, Michael J. Sikora, Saiful Islam, Roshni Roy Chao-Gan Yan, Xiao Chen, Le Li, Francisco Xavier Castellanos, Chowdhury, Yueh-hsiu Chien, Thomas J. Scriba, Mark M. Davis, Tong-Jian Bai, Qi-Jing Bo, Jun Cao, Guan-Mao Chen, and Lars M. Steinmetz Ning-Xuan Chen, Wei Chen, Chang Cheng, Yu-Qi Cheng, Xi-Long Cui, Jia Duan, Yi-Ru Fang, Qi-Yong Gong, Wen-Bin Guo, Zheng-Hua Hou, Lan Hu, Li Kuang, Feng Li, Kai-Ming Li, MEDICAL SCIENCES Tao Li, Yan-Song Liu, Zhe-Ning Liu, Yi-Cheng Long, Qing-Hua 9002 Rapid screening of engineered microbial therapies in Luo, Hua-Qing Meng, Dai-Hui Peng, Hai-Tang Qiu, Jiang Qiu, a 3D multicellular model Yue-Di Shen, Yu-Shu Shi, Chuan-Yue Wang, Fei Wang, Kai Tetsuhiro Harimoto, Zakary S. Singer, Oscar S. Velazquez, Wang, Li Wang, Xiang Wang, Ying Wang, Xiao-Ping Wu, Joanna Zhang, Samuel Castro, Taylor E. Hinchliffe, William Xin-Ran Wu, Chun-Ming Xie, Guang-Rong Xie, Hai-Yan Xie, Mather, and Tal Danino Peng Xie, Xiu-Feng Xu, Hong Yang, Jian Yang, Jia-Shu Yao, Shu-Qiao Yao, Ying-Ying Yin, Yong-Gui Yuan, Ai-Xia Zhang, 9008 Inherited predisposition to malignant mesothelioma Hong Zhang, Ke-Rang Zhang, Lei Zhang, Zhi-Jun Zhang, Ru-Bai and overall survival following platinum chemotherapy Zhou, Yi-Ting Zhou, Jun-Juan Zhu, Chao-Jie Zou, Tian-Mei Si, Raffit Hassan, Betsy Morrow, Anish Thomas, Tom Walsh, Xi-Nian Zuo, Jing-Ping Zhao, and Yu-Feng Zang Ming K. Lee, Suleyman Gulsuner, Meghana Gadiraju, Vasiliki Panou, Shaojian Gao, Idrees Mian, Javed Khan, Mark Raffeld, 9084 Intrinsic planar polarity mechanisms influence the Snehal Patel, Liqiang Xi, Jun S. Wei, Mary Hesdorffer, Jingli position-dependent regulation of synapse Zhang, Kathleen Calzone, Arpita Desai, Emerson Padiernos, properties in inner hair cells Christine Alewine, David S. Schrump, Seth M. Steinberg, Philippe Jean, O¨ zge Demet O¨ zc¸ete, Basile Tarchini, Hedy L. Kindler, Mary-Claire King, and Jane E. Churpek and Tobias Moser

vi u www.pnas.org Contents Downloaded by guest on October 2, 2021 9094 Delta-secretase-cleaved Tau antagonizes TrkB CORRECTIONS neurotrophic signalings, mediating Alzheimer’s disease pathologies ENVIRONMENTAL SCIENCES Jie Xiang, Zhi-Hao Wang, Eun Hee Ahn, Xia Liu, Shan-Ping Yu, Fredric P. Manfredsson, Ivette M. Sandoval, Gong Ju, Shengxi 9135 Elevated levels of diesel range organic compounds in Wu, and Keqiang Ye groundwater near Marcellus gas operations are derived from surface activities 9103 Hypoxia tolerance in the Norrin-deficient retina and the Brian D. Drollette, Kathrin Hoelzer, Nathaniel R. chronically hypoxic brain studied at single-cell resolution Warner, Thomas H. Darrah, Osman Karatum, Jacob S. Heng, Amir Rattner, Genevieve L. Stein-O’Brien, Megan P. O’Connor, Robert K. Nelson, Loretta A. Briana L. Winer, Bryan W. Jones, Hilary J. Vernon, Loyal A. Fernandez, Christopher M. Reddy, Avner Goff, and Jeremy Nathans Vengosh, Robert B. Jackson, Martin Elsner, 9115 Protease-independent action of tissue plasminogen and Desiree L. Plata activator in brain plasticity and neurological recovery after ischemic stroke BIOCHEMISTRY, CHEMISTRY Hongjian Pu, Yejie Shi, Lili Zhang, Zhengyu Lu, Qing Ye, 9136 Transcriptome-wide profiling of multiple RNA Rehana K. Leak, Fei Xu, Shubei Ma, Hongfeng Mu, Zhishuo modifications simultaneously at single- Wei, Na Xu, Yuguo Xia, Xiaoming Hu, T. Kevin Hitchens, Michael V. L. Bennett, and Jun Chen base resolution Vahid Khoddami, Archana Yerra, Timothy L. Mosbruger, Aaron M. Fleming, Cynthia J. Burrows, and Bradley R. Cairns 9125 Constitutive release of CPS1 in bile and its role as ENVIRONMENTAL SCIENCES a protective cytokine during acute liver injury Min-Jung Park, Louis G. D’Alecy, Michelle A. Anderson, 9137 Light-driven growth in Amazon evergreen forests Venkatesha Basrur, Yongjia Feng, Graham F. Brady, Dong-il explained by seasonal variations of vertical Kim, Jun Wu, Alexey I. Nesvizhskii, Joerg Lahann, Nicholas W. canopy structure Lukacs, Robert J. Fontana, and M. Bishr Omary Hao Tang and Ralph Dubayah

Contents PNAS u April 30, 2019 u vol. 116 u no. 18 u vii Downloaded by guest on October 2, 2021