brush organ; insect phylogenetics; scent pad; scent patch; sexual selection; Pheromones; Animals; Biological Evolution; Male; Phenotype; Phylogeny; Butterflies; Biochemistry, Genetics and Molecular Biology (all); Immunology and Microbiology (all); Environmental Science (all); Agricultural and Biological Sciences (all); General Agricultural and Biological Sciences; General Environmental Science; General Immunology and Microbiology; General Biochemistry, Genetics and Molecular Biology; General Medicine
Abstract :
[en] Male butterflies in the hyperdiverse tribe Eumaeini possess an unusually complex and diverse repertoire of secondary sexual characteristics involved in pheromone production and dissemination. Maintaining multiple sexually selected traits is likely to be metabolically costly, potentially resulting in trade-offs in the evolution of male signals. However, a phylogenetic framework to test hypotheses regarding the evolution and maintenance of male sexual traits in Eumaeini has been lacking. Here, we infer a comprehensive, time-calibrated phylogeny from 379 loci for 187 species representing 91% of the 87 described genera. Eumaeini is a monophyletic group that originated in the late Oligocene and underwent rapid radiation in the Neotropics. We examined specimens of 818 of the 1096 described species (75%) and found that secondary sexual traits are present in males of 91% of the surveyed species. Scent pads and scent patches on the wings and brush organs associated with the genitalia were probably present in the common ancestor of Eumaeini and are widespread throughout the tribe. Brush organs and scent pads are negatively correlated across the phylogeny, exhibiting a trade-off in which lineages with brush organs are unlikely to regain scent pads and vice versa. In contrast, scent patches seem to facilitate the evolution of scent pads, although they are readily lost once scent pads have evolved. Our results illustrate the complex interplay between natural and sexual selection in the origin and maintenance of multiple male secondary sexual characteristics and highlight the potential role of sexual selection spurring diversification in this lineage.
Disciplines :
Genetics & genetic processes
Author, co-author :
Valencia-Montoya, Wendy A ; Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA
Quental, Tiago B; Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA ; Instituto de Biociências, Universidade de São Paulo, Brazil
Tonini, João Filipe R ; Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA
Talavera, Gerard ; Institut Botànic de Barcelona (IBB, CSIC-Ajuntament de Barcelona), 08038 Barcelona, Catalonia, Spain
Crall, James D; Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA
Lamas, Gerardo ; Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima, Peru
Busby, Robert C; 9275 Hollow Pine Drive, Estero, FL 34135, USA
Carvalho, Ana Paula S; McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA
Morais, Ana B; Departamento de Ecologia e Evolução, CCNE, Universidade Federal de Santa Maria, Santa Maria, RS, Brasil
Oliveira Mega, Nicolás; Departamento de Zoologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS 91501970, Brazil
Romanowski, Helena Piccoli; Departamento de Zoologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS 91501970, Brazil
Lienard, Marjorie ; Université de Liège - ULiège > GIGA > GIGA Molecular Biology of Diseases ; Department of Biology, Lund University, Lund, Sweden
Salzman, Shayla ; School of Integrative Plant Sciences, Cornell University, Ithaca, NY 14853, USA
Whitaker, Melissa R L; Entomological Collection, Department of Environmental Systems Science, ETH Zürich, Zürich, Switzerland
Kawahara, Akito Y; McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA
Lohman, David J ; Biology Department, City College of New York, City University of New York, New York, NY 10031, USA ; PhD Program in Biology, Graduate Center, City University of New York, New York, NY 10016, USA ; Entomology Section, Zoology Division, Philippine National Museum of Natural History, Manila 1000, Philippines
Robbins, Robert K ; Department of Entomology, Smithsonian Institution, Washington, DC 20013-7012, USA
Pierce, Naomi E ; Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA
“Ramón y Cajal” programme of the Spanish Ministry of Science and Innovation
Funders :
ICMBio - Instituto Chico Mendes de Conservação da Biodiversidade [BR] DRCLAS - David Rockefeller Center for Latin American Studies [US-MA] Lemann Foundation-Brazil [BR] Harvard University [US-MA] CNPq - Conselho Nacional de Desenvolvimento Científico e Tecnológico [BR] ICMBio - Instituto Chico Mendes de Conservação da Biodiversidade [BR] NSF - National Science Foundation [US-VA]
Funding text :
Data accessibility. Research data associated with this study are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.tqjq2bvz9 [63], and NCBI Bioproject PRJNA714105, Biosamples: SAMN18315678– SAMN18315893 and SAMN18322226–SAMN18322244. Authors’ contributions. All authors gave final approval for publication and agreed to be held accountable for the work performed therein. Competing interests. We declare we have no competing interests. Funding. This study was supported by Instituto Chico Mendes de Con-servação da Biodiversidade (grant no. 11990-1), David Rockefeller Center for Latin American Studies (DRCLAS), Society for Systematic Biology (SSB-Mini-PEET), DRCLAS and Lemann Foundation, “Ramón y Cajal” programme of the Spanish Ministry of Science and Innovation (grant no. RYC2018-025335-I), Putnam Expeditionary Fund, Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology (OEB) at Harvard University, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (grantnos. 200814/2015-0 and 304273/2014-7), Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) (Collecting license (11990-1) and Collecting license (20395-1)) and NSF (grant nos. 1906333, DEB-0447244, DEB-1541500, DEB-1541557 and DEB-1541560). Acknowledgements. We thank Michael F. Braby, Dana Campbell, James Coleman, Mark Cornwall, Alexandre Danchenko, Kelvyn Dunn, Rod Eastwood, Alan Heath, Nikolai Kandul, Norbert G. Kondla, N. Mega, Carlos Pena, Jon Sanders, Art Shapiro, Man Wah Tan,This study was supported by Instituto Chico Mendes de Conserva??o da Biodiversidade (grant no. 11990-1), David Rockefeller Center for Latin American Studies (DRCLAS), Society for Systematic Biology (SSB- Mini-PEET), DRCLAS and Lemann Foundation, ?Ram?n y Cajal? programme of the Spanish Ministry of Science and Innovation (grant no. RYC2018-025335-I), Putnam Expeditionary Fund, Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology (OEB) at Harvard University, Conselho Nacional de Desenvolvimento Cient?fico e Tecnol?gico (CNPq) (grant nos. 200814/2015-0 and 304273/2014-7), Instituto Chico Mendes de Conserva??o da Biodiversidade (ICMBio) (Collecting license (11990-1) and Collecting license (20395-1)) and NSF (grant nos. 1906333, DEB-0447244, DEB-1541500, DEB-1541557 and DEB-1541560).
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