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 DRCLAS - David Rockefeller Center for Latin American Studies Lemann Foundation-Brazil Harvard University CNPq - Conselho Nacional de Desenvolvimento Científico e Tecnológico ICMBio - Instituto Chico Mendes de Conservação da Biodiversidade NSF - National Science Foundation
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).
Eliot JN,. 1973 The higher classification of the Lycaenidae (Lepidoptera): a tentative arrangement. Bull. Br. Mus. Nat. Hist. 28, 371-505. (doi:10.5962/bhl.part.11171)
Robbins RK,. 1982 How many butterflies species? News Lepid. Soc. 24, 40-41.
Robbins RK,. 2004 Introduction to the checklist of Eumaeini (Lycaenidae). In Atlas of neotropical lepidoptera (ed. G Lamas,). Gainsville, FL: Scientific Publishers.
Robbins RK,. 2000 The New World hairstreak genus Arawacus Kaye (Lepidoptera: Lycaenidae: Theclinae: Eumaeini). Proc. Entomol. Soc. Wash. 102, 162-169.
Martins ARP, Duarte M, Robbins RK,. 2019 Phylogenetic classification of the Atlides section of the Eumaeini (Lepidoptera, Lycaenidae). Zootaxa 4563, 119. (doi:10.11646/zootaxa.4563.1.6)
Duarte M, Robbins RK,. 2010 Description and phylogenetic analysis of the Calycopidina (Lepidoptera, Lycaenidae, Theclinae, Eumaeini): a subtribe of detritivores. Rev. Bras. Entomol. 54, 45-65. (doi:10.1590/S0085-56262010000100006)
Bálint ZS, Lorenc-Brudecka J, Pyrcz T,. 2016 New distribution data for two species of the Neotropical genus Lathecla Robbins, 2004 (Lepidoptera, Lycaenidae, Eumaeini). Opusc. Zool. 47, 151-154. (doi:10.18348/opzool.2016.2.151)
Rothschild M, Nash RJ, Bell EA,. 1986 Cycasin in the endangered butterfly Eumaeus atala florida. Phytochemistry 25, 1853-1854. (doi:10.1016/S0031-9422(00)81161-9)
Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J, Rand DB, Travassos MA,. 2002 The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annu. Rev. Entomol. 47, 733-771. (doi:10.1146/annurev.ento.47.091201.145257)
Valencia-Montoya WA, Tuberquia D, Guzmán PA, Cardona-Duque J,. 2017 Pollination of the cycad Zamia incognita A. Lindstr. & Idárraga by Pharaxonotha beetles in the Magdalena Medio Valley, Colombia: a mutualism dependent on a specific pollinator and its significance for conservation. Arthropod-Plant Interact. 11, 717-729. (doi:10.1007/s11829-017-9511-y)
Whitaker MRL, Salzman S,. 2020 Ecology and evolution of cycad-feeding Lepidoptera. Ecol. Lett. 23, 1862-1877. (doi:10.1111/ele.13581)
Robbins RK, et al,. 2021 A switch to feeding on cycads generates parallel accelerated evolution of toxin tolerance in two clades of Eumaeus caterpillars (Lepidoptera: Lycaenidae). Proc. Natl Acad. Sci. 118,. e2018965118. (doi:10.1073/pnas.2018965118)
Martins AR, Duarte M, Robbins RK,. 2019 Hairstreak butterflies (Lepidoptera, Lycaenidae) and evolution of their male secondary sexual organs. Cladistics 35, 173-197. (doi:10.1111/cla.12355)
Robbins RK, Martins ARP, Busby RC, Duarte M,. 2012. Loss of male secondary sexual structures in allopatry in the Neotropical butterfly genus Arcas (Lycaenidae: Theclinae: Eumaeini). (doi:10.1163/187631212X626195)
Robbins R, Heredia MD, Busby RC,. 2015 Male secondary sexual structures and the systematics of the Thereus oppia species group (Lepidoptera, Lycaenidae, Eumaeini). ZooKeys 520, 109-130. (doi:10.3897/zookeys.520.10134)
Tsai C-C, Childers RA, Nan Shi N, Ren C, Pelaez JN, Bernard GD, Pierce NE, Yu N,. 2020 Physical and behavioral adaptations to prevent overheating of the living wings of butterflies. Nat. Commun. 11, 551. (doi:10.1038/s41467-020-14408-8)
Bacquet PMB, Brattström O, Wang H-L, Allen CE, Löfstedt C, Brakefield PM, Nieberding CM,. 2015 Selection on male sex pheromone composition contributes to butterfly reproductive isolation. Proc. R. Soc. B 282, 20142734. (doi:10.1098/rspb.2014.2734)
Badyaev AV, Hill GE, Weckworth BV,. 2002 Species divergence in sexually selected traits: increase in song elaboration is related to decrease in plumage ornamentation in finches. Evolution 56, 412-419. (doi:10.1554/0014-3820(2002)056[0412:SDISST]2.0.CO;2)
Wiens JJ, Tuschhoff E,. 2020 Songs versus colours versus horns: what explains the diversity of sexually selected traits? Biol. Rev. 95, 847-864. (doi:10.1111/brv.12593)
Wiens JJ,. 2001 Widespread loss of sexually selected traits: how the peacock lost its spots. Trends Ecol. Evol. 16, 517-523. (doi:10.1016/S0169-5347(01)02217-0)
Schluter D, Price T,. 1993 Honesty, perception and population divergence in sexually selected traits. Proc. R. Soc. Lond. B 253, 117-122. (doi:10.1098/rspb.1993.0089)
Shutler D,. 2010 Sexual selection: when to expect trade-offs. Biol. Lett. 7, 101-104. (doi:10.1098/rsbl.2010.0531)
Andersson S, Pryke SR, Örnborg J, Lawes MJ, Andersson M,. 2002 Multiple receivers, multiple ornaments, and a trade-off between agonistic and epigamic signaling in a widowbird. Am. Nat. 160, 683-691. (doi:10.1086/342817)
Simmons LW, Lüpold S, Fitzpatrick JL,. 2017 Evolutionary trade-off between secondary sexual traits and ejaculates. Trends Ecol. Evol. 32, 964-976. (doi:10.1016/j.tree.2017.09.011)
Espeland M, et al,. 2018 A comprehensive and dated phylogenomic analysis of butterflies. Curr. Biol. 28, 770-778. (doi:10.1016/j.cub.2018.01.061)
Kawahara AY, et al,. 2018 Phylogenetics of moth-like butterflies (Papilionoidea: Hedylidae) based on a new 13-locus target capture probe set. Mol. Phylogenet. Evol. 127, 600-605. (doi:10.1016/j.ympev.2018.06.002)
Katoh K, Standley DM,. 2013 MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. (doi:10.1093/molbev/mst010)
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS., 2017 ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587-589. (doi:10.1038/nmeth.4285)
Lanfear R, Calcott B, Ho SYW, Guindon S,. 2012 PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29, 1695-1701. (doi:10.1093/molbev/mss020)
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R., 2020 IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era.. Mol. Biol. Evol. 37, 1530-1534. (doi:10.1093/molbev/msaa015)
Cho S, Mitchell A, Regier JC, Mitter C, Poole RW, Friedlander TP, Zhao S,. 1995 A highly conserved nuclear gene for low-level phylogenetics: elongation factor-1 alpha recovers morphology-based tree for heliothine moths. Mol. Biol. Evol. 12, 650-656. (doi:10.1093/oxfordjournals.molbev.a040244)
Mirarab S, Warnow T,. 2015 ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31, i44-i52. (doi:10.1093/bioinformatics/btv234)
Persons NW, Hosner PA, Meiklejohn KA, Braun EL, Kimball RT,. 2016 Sorting out relationships among the grouse and ptarmigan using intron, mitochondrial, and ultra-conserved element sequences. Mol. Phylogenet. Evol. 98, 123-132. (doi:10.1016/j.ympev.2016.02.003)
Yang Z,. 2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591. (doi:10.1093/molbev/msm088)
Kawahara AY, et al,. 2019 Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths. Proc. Natl Acad. Sci. USA 116, 22 657-22 663. (doi:10.1073/pnas.1907847116)
Matzke N,. 2013. BioGeoBEARS: bioGeography with Bayesian (and Likelihood) evolutionary analysis in R Scripts version 0.2.1 from CRAN.. See https://rdrr.io/cran/BioGeoBEARS/.
Revell LJ,. 2012 phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217-223. (doi:10.1111/j.2041-210X.2011.00169.x)
Pagel M,. 1994 Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. R. Soc. Lond. B 255, 37-45. (doi:10.1098/rspb.1994.0006)
Pagel M, Meade A,. 2006 Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am. Nat. 167, 808-825. (doi:10.1086/503444)
Plummer M, Best N, Cowles K, Vines K,. 2006 CODA: convergence diagnosis and output analysis for MCMC. R News 6, 7-11.
Ree RH, Smith SA,. 2008 Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst. Biol. 57, 4-14. (doi:10.1080/10635150701883881)
Ree RH, Sanmartín I,. 2018 Conceptual and statistical problems with the DEC + J model of founder-event speciation and its comparison with DEC via model selection. J. Biogeogr. 45, 741-749. (doi:10.1111/jbi.13173)
Zhang J, Cong Q, Shen J, Opler PA, Grishin NV,. 2019. Genomics of a complete butterfly continent. bioRxiv, 829887. (doi:10.1101/829887)
Robbins RK,. 1991 Evolution, comparative morphology, and identification of the Eumaeine butterfly genus Rekoa Kaye (Lycaenidae: Theclinae). Smithson Contrib. Zool. 498,. 1-64. (doi:10.5479/si.00810282.498)
Robbins RK, Nicolay SS,. 2001 An overview of Strymon Huebner (Lycaenidae: Theclinae: Eumaeini). J. Lepidopterists Soc. 55, 85-100.
Farris DW, et al,. 2011 Fracturing of the Panamanian Isthmus during initial collision with South America. Geology 39, 1007-1010. (doi:10.1130/G32237.1)
Hoorn C, et al,. 2010 Amazonia through time: andean uplift, climate change, landscape evolution, and biodiversity. Science 330, 927-931. (doi:10.1126/science.1194585)
Capitanio FA, Faccenna C, Zlotnik S, Stegman DR,. 2011 Subduction dynamics and the origin of Andean orogeny and the Bolivian orocline. Nature 480, 83-86. (doi:10.1038/nature10596)
Kimball RT, Mary CMS, Braun EL,. 2011 A macroevolutionary perspective on multiple sexual traits in the Phasianidae (Galliformes). Int. J. Evol. Biol. 2011, 423938. (doi:10.4061/2011/423938)
Emlen DJ, Warren IA, Johns A, Dworkin I, Lavine LC,. 2012 A mechanism of extreme growth and reliable signaling in sexually selected ornaments and weapons. Science 337, 860-864. (doi:10.1126/science.1224286)
Gould SJ,. 1970 Dollo on Dollo's law: irreversibility and the status of evolutionary laws. J. Hist. Biol. 3, 189-212. (doi:10.1007/BF00137351)
Miles MC, Fuxjager MJ,. 2019 Phenotypic diversity arises from secondary signal loss in the elaborate visual displays of toucans and barbets. Am. Nat. 194, 152-167. (doi:10.1086/704088)
Liman ER, Innan H,. 2003 Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proc. Natl Acad. Sci. USA 100, 3328-3332. (doi:10.1073/pnas.0636123100)
Parzer HF, Moczek AP,. 2008 Rapid antagonistic coevolution between primary and secondary sexual characters in horned beetles. Evolution 62, 2423-2428. (doi:10.1111/j.1558-5646.2008.00448.x)
Liu X, Hayashi F, Lavine LC, Yang D,. 2015 Is diversification in male reproductive traits driven by evolutionary trade-offs between weapons and nuptial gifts? Proc. R. Soc. B 282, 20150247. (doi:10.1098/rspb.2015.0247)
Darragh K, et al,. 2020 Species specificity and intraspecific variation in the chemical profiles of Heliconius butterflies across a large geographic range. Ecol. Evol. 10, 3895-3918. (doi:10.1002/ece3.6079)
Darragh K, et al,. 2021 A novel terpene synthase controls differences in anti-aphrodisiac pheromone production between closely related Heliconius butterflies. PLoS Biol. 19, e3001022. (doi:10.1371/journal.pbio.3001022)
González-Rojas MF, Darragh K, Robles J, Linares M, Schulz S, McMillan WO, Jiggins CD, Pardo-Diaz C, Salazar C,. 2020 Chemical signals act as the main reproductive barrier between sister and mimetic Heliconius butterflies. Proc. R. Soc. B 287, 20200587. (doi:10.1098/rspb.2020.0587)
Darragh K, et al,. 2017 Male sex pheromone components in Heliconius butterflies released by the androconia affect female choice. PeerJ 5, e3953. (doi:10.7717/peerj.3953)
Prakash A, Monteiro A,. 2020 Doublesex mediates the development of sex-specific pheromone organs in Bicyclus butterflies via multiple mechanisms. Mol. Biol. Evol. 37, 1694-1707. (doi:10.1093/molbev/msaa039)
Hall JPW, Harvey DJ,. 2002 A survey of androconial organs in the Riodinidae (Lepidoptera). Zool. J. Linn. Soc. 136, 171-197. (doi:10.1046/j.1096-3642.2002.00003.x)
Valencia-Montoya WA, et al. 2021 Data from: Evolutionary trade-offs between male secondary sexual traits revealed by a phylogeny of the hyperdiverse tribe Eumaeini (Lepidoptera: Lycaenidae). Dryad Digital Repository. (doi:10.5061/dryad.tqjq2bvz9)
