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Evolutionary Developmental Biology (Evo-Devo) Research in Latin America SYLVAIN MARCELLINI1, FAVIO GONZÁLEZ2, ANDRES F

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Evolutionary Developmental Biology (Evo-Devo) Research in Latin America SYLVAIN MARCELLINI1, FAVIO GONZÁLEZ2, ANDRES F REVIEW Evolutionary Developmental Biology (Evo-Devo) Research in Latin America SYLVAIN MARCELLINI1, FAVIO GONZÁLEZ2, ANDRES F. SARRAZIN3, NATALIA PABÓN-MORA4, MARIANA BENÍTEZ5, ALMA PIÑEYRO-NELSON6, GUSTAVO L. REZENDE7, ERNESTO MALDONADO8, PATRICIA NEIVA SCHNEIDER9, MARIANA B. GRIZANTE10,RODRIGONUNES DA FONSECA11 , FRANCISCO VERGARA-SILVA12, VANESSA SUAZA-GAVIRIA4, CECILIA ZUMAJO-CARDONA4, EDUARDOE.ZATTARA13, SOFIA CASASA13, 4 14∗ HAROLD SUÁREZ-BARON , AND FEDERICO D. BROWN 1Laboratorio de Desarrollo y Evolución, Departamento de Biología Celular, Facultad de Ciencias Biológicas, Universidad de Concepción, Concepción, Chile 2Facultad de Ciencias, Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá, Colombia 3Instituto de Química, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile 4Instituto de Biología, Universidad de Antioquia, Medellín, Colombia 5Laboratorio Nacional de Ciencias de la Sostenibilidad, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad de México, México 6Departamento de Producción Agrícola y Animal, Universidad Autónoma Metropolitana, Xochimilco, Ciudad de México, México 7Universidade Estadual do Norte Fluminense, CBB, LQFPP, Campos dos Goytacazes, RJ, Brazil 8EvoDevo Lab, Unidad de Sistemas Arrecifales, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Puerto Morelos, Quintana Roo, México 9Instituto de Ciências Biológicas, Universidade Federal do Pará, Belem, PA, Brazil 10School of Life Sciences, Arizona State University, Tempe, AZ, USA 11 Núcleo em Ecologia e Desenvolvimento SócioAmbiental de Macaé (NUPEM), Campus Macaé, Universidade Federal do Rio de Janeiro, Macae, RJ, Brazil 12Instituto de Biología, Universidad Nacional Autónoma de Mexico, Ciudad de México, México 13Department of Biology, Indiana University, Bloomington, IN, USA 14Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brazil ABSTRACT Famous for its blind cavefish and Darwin’s finches, Latin America is home to some of the richest biodiversity hotspots of our planet. The Latin American fauna and flora inspired and captivated naturalists from the nineteenth and twentieth centuries, including such notable pioneers such as Fritz Müller, Florentino Ameghino, and Léon Croizat who made a significant contribution to the ∗Correspondence to: Federico D. Brown, Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão. Travessa 14. No. 101. Cidade Universitária, São Paulo, SP 05508-090. Brazil. E-mail: [email protected] Received 24 March 2016; Revised 16 June 2016; Accepted 20 June 2016 DOI: 10.1002/jez.b.22687 Published online in Wiley Online Library (wileyonlinelibrary.com). C 2016 WILEY PERIODICALS, INC. 2 MARCELLINI ET AL. study of embryology and evolutionary thinking. But, what are the historical and present contribu- tions of the Latin American scientific community to Evo-Devo? Here, we provide the first compre- hensive overview of the Evo-Devo laboratories based in Latin America and describe current lines of research based on endemic species, focusing on body plans and patterning, systematics, physiol- ogy, computational modeling approaches, ecology, and domestication. Literature searches reveal that Evo-Devo in Latin America is still in its early days; while showing encouraging indicators of productivity, it has not stabilized yet, because it relies on few and sparsely distributed labo- ratories. Coping with the rapid changes in national scientific policies and contributing to solve social and health issues specific to each region are among the main challenges faced by Latin American researchers. The 2015 inaugural meeting of the Pan-American Society for Evolution- ary Developmental Biology played a pivotal role in bringing together Latin American researchers eager to initiate and consolidate regional and worldwide collaborative networks. Such networks will undoubtedly advance research on the extremely high genetic and phenotypic biodiversity of Latin America, bound to be an almost infinite source of amazement and fascinating findings for the Evo-Devo community. J. Exp. Zool. (Mol. Dev. Evol.) 00:1–36, 2016. C 2016 Wiley Periodicals, Inc. How to cite this article: Marcellini S, González FA, Sarrazin AF, Pabón-Mora N, Benítez M, Piñeyro-Nelson A, Rezende GL, Maldonado E, Schneider PN, Grizante MB, Da Fonseca RN, J. Exp. Zool. (Mol. Dev. Evol.) Vergara-Silva F, Suaza-Gaviria V, Zumajo-Cardona C, Zattara EE, Casasa S, Suárez-Baron H, 00:1–36, Brown FD. 2016. Evolutionary developmental biology (Evo-Devo) research in latin america. J. 2016 Exp. Zool. (Mol. Dev. Evol.) 00:1–36. “Evolutionism in general from mollusks and birds to mam- tionary and developmental approaches. Evo-Devo has proven mals: what, finally, Empedocles said and Aristotle wrote” to be a dynamic, multidisciplinary and hotly debated field title in Léon Croizat’s Space, Time, Form (’64:481) (Gilbert et al., ’96; Sommer, 2009; Parsons and Albertson, 2013; Wray et al., 2014; Moczek et al., 2015; Pieretti et al., 2015; INTRODUCTION Roux et al., 2015). It has fostered the establishment of several Evolution and development are two fields in biology that were specialized journals (e.g., Evolution & Development; Evo-Devo; considered to be associated and complementary to each other Development, Genes, and Evolution; Journal of Experimental Zo- since their conception. Just 4 years after publication of Darwin’s ology, Part B: Molecular and Developmental Evolution), journal opus magna, Fritz Müller proposed what came to be the first sections (e.g., Evolution of Developmental Control in Develop- Evo-Devo explanation of von Baer’s laws of embryology, which mental Biology; Evolutionary Developmental Biology in Fron- soon became further expanded in Ernst Haeckel’s biogenetic law tiers in Ecology and Evolution; Evolutionary Developmental Bi- (von Baer, 1828; Darwin, 1859; Haeckel, 1866; Müller, 1869). At ology in Neotropical Biodiversity), and scientific societies (Euro the end of the nineteenth century, the philosophical rift between Evo-Devo and PanAm Evo-Devo). Hence, the number of articles naturalism and experimentalism split these twin fields apart. As that mention “Evo-Devo” or equivalent terms and synonyms per a result, evolutionary biology and developmental biology re- year has been increasing steadily since the mid-1990s (Fig. 1A). mained mostly isolated from each other until the second half In Latin America, Evo-Devo is only starting to emerge when of the twentieth century, when foundational developmental ge- compared to scientific output in the rest of the world (Fig. 1A), netic experiments started rebuilding bridges between the devel- but also displays a pronounced and steady growth in its use opment and evolution of form and function (Raff and Kaufman, as a concept in the scientific literature (Fig. 1B). As part ofthe ’83). The pioneering works of Richard Goldschmidt and Stephen Latin American community, we took advantage of the inaugu- Jay Gould (Goldschmidt, ’40; Gould, ’77a, ’77b) eventually led ral meeting of the PanAmerican Society for Evo-Devo (August to 1981’s Dahlem Workshop on Evolution and Development, 5–9, 2015, in Berkeley, CA) to organize a workshop aimed at which set out an agenda to “pry open the black box [of develop- discussing the current challenges of Evo-Devo in Latin Amer- ment]” (Haag and Lenski, 2011) and became an early milestone ica (Lesoway, 2016; Specht, 2016). One of the issues identified of modern Evo-Devo. Since then, a number of highly influential in this workshop was the lack of visibility of Latin American books (e.g., Raff and Kaufman, ’83; Gerhart and Kirschner, ’97; research. In this review, we sought to highlight the work of fore- Carroll et al., 2005) have inspired researchers to combine evolu- runners of Evo-Devo research in Latin America and to comment J. Exp. Zool. (Mol. Dev. Evol.) EVO-DEVO IN LATIN AMERICA 3 LATIN AMERICA: A LIVING LABORATORY FOR EVO-DEVO RESEARCH One can only marvel at the staggering biodiversity of Latin America. Three of five leading biodiversity hotspots (Tropical Andes, Brazil’s Atlantic Forest, and Caribbean) are located in this region, which together holds nearly 12% of the world’s endemic plant species (Myers et al., 2000). This is not surprising know- ing that the Neotropics are estimated to house about 100,000 plant species (Stoll, 2012). Furthermore, in a single hectare of the Western Amazon over 300 species of trees can be found, the same number of species found in the whole of Eastern North America (Wade, 2015). If Mesoamerica is included into the bio- diversity hotspots mentioned above, these four regions alone serve as shelter to 15% of the world’s endemic vertebrate species (Myers et al., 2000). The Neotropics are estimated to have 40% (approximately 4000) of bird species in the world (Stotz et al., ’96). Similarly, South America alone contains a third (approximately 1700) of all anuran species, with nearly 96% of these being endemic to the region (Duellman, ’99; www.amphibiaweb.org). Present-day diversity is the result of millions of years of biologic, oceanographic, geologic, and climatologic changes. Present day diversity in the Neotropics is proposed to have been generated by events dating back to the early Miocene Figure 1. Usage of the word “Evo-Devo” (and all its synonyms in (15–23 Mya) when the Caribbean sea poured into South Ameri- English, Spanish, or Portuguese) expands rapidly in the world sci- can northwestern regions forming an enormous
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