Evolutionary trade-offs between male secondary sexual traits revealed by a phylogeny of the hyperdiverse tribe Eumaeini (Lepidoptera: Lycaenidae)

Wendy A. Valencia-Montoya, Tiago B. Quental, João Filipe R. Tonini, Gerard Talavera, James D. Crall, Gerardo Lamas, Robert C. Busby, Ana Paula S. Carvalho, Ana B. Morais, Nicolás Oliveira Mega, Helena Piccoli Romanowski, Marjorie A. Liénard, Shayla Salzman, Melissa R.L. Whitaker, Akito Y. Kawahara, David J. Lohman, Robert K. Robbins, Naomi E. Pierce

Research output: Contribution to journalArticlepeer-review

Abstract

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.

Original languageEnglish
Article number2020.2512
JournalProceedings of the Royal Society B: Biological Sciences
Volume288
Issue number1950
DOIs
StatePublished - 12 May 2021
Externally publishedYes

Bibliographical note

Funding Information:
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) (grant

Funding Information:
nos. 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,

Funding Information:
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).

Publisher Copyright:
© 2021 The Authors.

Keywords

  • brush organ
  • insect phylogenetics
  • scent pad
  • scent patch
  • sexual selection

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