Intra and inter-specific communication in Heliconius

Las mariposas del género Heliconius son un excelente ejemplo de mimetismo Mülleriano, donde especies filogenéticamente distantes convergen en un fenotipo alar casi idéntico cuando se encuentran en simpatría. Sin embargo, pocos estudios han abordado de manera integral la precisión del mimetismo y la...

Full description

Autores:

Tipo de recurso:

Fecha de publicación:: 2021

Institución:: Universidad del Rosario

Repositorio:: Repositorio EdocUR - U. Rosario

Idioma:: eng

id	EDOCUR2_febb7b5274f26b04151428a4e05eebbc
oai_identifier_str	oai:repository.urosario.edu.co:10336/30934
network_acronym_str	EDOCUR2
network_name_str	Repositorio EdocUR - U. Rosario
repository_id_str
dc.title.spa.fl_str_mv	Intra and inter-specific communication in Heliconius
dc.title.TranslatedTitle.eng.fl_str_mv	Comunicación intra e inter-específica en Heliconius
title	Intra and inter-specific communication in Heliconius
spellingShingle	Intra and inter-specific communication in Heliconius Mariposas del género Heliconius Análisis del mimetismo batesiano y mülleriano de los Heliconius Sistema de identificación entre mariposas comimeticas Identificación de señales químicas distintivas entre especies distintas de Heliconius Invertebrados Butterflies of the genus Heliconius Analysis of the Batesian and Müllerian mimicry of the Heliconius Identification system between comimetic butterflies Identification of distinctive chemical signals between species other than Heliconius
title_short	Intra and inter-specific communication in Heliconius
title_full	Intra and inter-specific communication in Heliconius
title_fullStr	Intra and inter-specific communication in Heliconius
title_full_unstemmed	Intra and inter-specific communication in Heliconius
title_sort	Intra and inter-specific communication in Heliconius
dc.contributor.advisor.none.fl_str_mv	Salazar, Camilo Pardo Díaz, Geimy Carolina
dc.subject.spa.fl_str_mv	Mariposas del género Heliconius Análisis del mimetismo batesiano y mülleriano de los Heliconius Sistema de identificación entre mariposas comimeticas Identificación de señales químicas distintivas entre especies distintas de Heliconius
topic	Mariposas del género Heliconius Análisis del mimetismo batesiano y mülleriano de los Heliconius Sistema de identificación entre mariposas comimeticas Identificación de señales químicas distintivas entre especies distintas de Heliconius Invertebrados Butterflies of the genus Heliconius Analysis of the Batesian and Müllerian mimicry of the Heliconius Identification system between comimetic butterflies Identification of distinctive chemical signals between species other than Heliconius
dc.subject.ddc.spa.fl_str_mv	Invertebrados
dc.subject.keyword.spa.fl_str_mv	Butterflies of the genus Heliconius Analysis of the Batesian and Müllerian mimicry of the Heliconius Identification system between comimetic butterflies Identification of distinctive chemical signals between species other than Heliconius
description	Las mariposas del género Heliconius son un excelente ejemplo de mimetismo Mülleriano, donde especies filogenéticamente distantes convergen en un fenotipo alar casi idéntico cuando se encuentran en simpatría. Sin embargo, pocos estudios han abordado de manera integral la precisión del mimetismo y la variación que existe en las señales miméticas a lo largo del fitness landscape (que puede comprender múltiples picos óptimos). En este estudio, haciendo uso de análisis de cuantificación del color, tamaño y forma de las alas, investigué el grado de semejanza fenotípica entre especies co-miméticas en múltiples anillos de mariposas del género Heliconius. Encontré que el tamaño y la forma de las alas no contribuyen al mimetismo. Por el contrario, el color es el principal contribuyente, pero algunos fenotipos son más precisos entre co-miméticos que otros. Esto sugiere la presencia de múltiples picos adaptativos dentro de un mismo anillo mimético. En estas mariposas, el patrón de coloración se reconoce como la principal señal para el reconocimiento de pareja entre especies que están filogenéticamente cercanas, pero cuando esta señal se ve comprometida, las señales alternativas de apareamiento deben evolucionar para asegurar el aislamiento reproductivo y la integridad de la especie. Las especies estrechamente relacionadas H. melpomene malleti y H. timareta florencia se encuentran en la misma región geográfica y, a pesar de exhibir patrones de coloración casi idénticos, presentan un fuerte aislamiento reproductivo. En esta tesis, examiné cuales señales difieren entre especies y potencialmente contribuyen al aislamiento reproductivo. El patrón de coloración alar es indistinguible entre las dos especies, mientras que el perfil químico de la androconia y los genitales de los machos exhiben marcadas diferencias. Por otra parte, realicé experimentos de comportamiento para estudiar la importancia del color y las señales químicas en el reconocimiento de pareja por parte de las hembras. Encontré que los perfiles químicos y no el patrón de coloración alar impulsan la preferencia de las hembras por machos conespecíficos. Además, los experimentos con machos y hembras híbridos sugirieron un compuesto genético importante tanto para la producción química como para la preferencia, lo que sugiere que los productos químicos son la principal barrera reproductiva que se opone al flujo de genes entre estas dos especies hermanas y co-miméticas. En conjunto, estos resultados concuerdan con la idea de que la adaptación por mimetismo es un proceso complejo y dinámico que se ve afectado por más de un factor y que una combinación efectiva de estas señales (visuales y químicas) es esencial para los procesos de comunicación intra e interespecífica en mariposas.
publishDate	2021
dc.date.accessioned.none.fl_str_mv	2021-02-18T03:40:13Z
dc.date.available.none.fl_str_mv	2021-02-18T03:40:13Z
dc.date.created.none.fl_str_mv	2021-01-20
dc.type.eng.fl_str_mv	doctoralThesis
dc.type.coar.fl_str_mv	http://purl.org/coar/resource_type/c_db06
dc.type.document.spa.fl_str_mv	Monografía
dc.type.spa.spa.fl_str_mv	Tesis de doctorado
dc.identifier.doi.none.fl_str_mv	https://doi.org/10.48713/10336_30934
dc.identifier.uri.none.fl_str_mv	https://repository.urosario.edu.co/handle/10336/30934
url	https://doi.org/10.48713/10336_30934 https://repository.urosario.edu.co/handle/10336/30934
dc.language.iso.spa.fl_str_mv	eng
language	eng
dc.rights.spa.fl_str_mv	Atribución-SinDerivadas 2.5 Colombia
dc.rights.coar.fl_str_mv	http://purl.org/coar/access_right/c_abf2
dc.rights.acceso.spa.fl_str_mv	Abierto (Texto Completo)
dc.rights.uri.none.fl_str_mv	http://creativecommons.org/licenses/by-nd/2.5/co/
rights_invalid_str_mv	Atribución-SinDerivadas 2.5 Colombia Abierto (Texto Completo) http://creativecommons.org/licenses/by-nd/2.5/co/ http://purl.org/coar/access_right/c_abf2
dc.format.mimetype.none.fl_str_mv	application/pdf
dc.publisher.spa.fl_str_mv	Universidad del Rosario
dc.publisher.department.spa.fl_str_mv	Facultad de Ciencias Naturales y Matemáticas
dc.publisher.program.spa.fl_str_mv	Doctorado en Ciencias Biomédicas y Biológicas
institution	Universidad del Rosario
dc.source.bibliographicCitation.spa.fl_str_mv	Córdoba-Aguilar A, González-Tokman D, González-Santoyo I. Insect behavior: from mechanisms to ecological and evolutionary consequences. First Edit. Oxford, UK: Oxford University Press; 2018. 414 p. Uetz GW, Roberts JA, Taylor PW. Multimodal communication and mate choice in wolf spiders: female response to multimodal versus unimodal signals. Anim Behav [Internet]. 2009;78:299–305. Available from: http://dx.doi.org/10.1016/j.anbehav.2009.04.023 Candolin U. The use of multiple cues in mate choice. Biol Rev Camb Philos Soc [Internet]. 2003;78:575–95. Available from: http://www.ncbi.nlm.nih.gov/pubmed/14700392 Chenoweth SF, Blows MW. Dissecting the complex genetic basis of mate choice. Nat Rev Genet [Internet]. 2006;7(9):681–92. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16921346 Bímová B, Albrecht T, Macholán M, Piálek J. Signalling components of the house mouse mate recognition system. Behav Processes. 2009;80(1):20–7. Wyatt TD. Pheromones and animal behaviour: communication by smell and taste. Cambridge: Cambridge University Press; 2003. Greenspan RJ, Ferveur JF. Courtship in Drosophila. Annu Rev Genet. 2000;34:205–32. Conner WE. “Un chant d’appel amoureux”: Acoustic communication in moths. J Exp Biol. 1999;202(13):1711–23. Weller SJ, Jacobson NL, Conner WE. The evolution of chemical defences and mating systems in tiger moths (Lepidoptera: Arctiidae). Biol J Linn Soc. 1999;68(4):557–78. Boppré M. Chemical communication, plant relationships, and mimicry in the evolution of Danaid butterflies. Entomol Exp Appl. 1978;24(3):64–77. Eisner T, Meinwald J. The chemistry of sexual selection. Proc Natl Acad Sci U S A. 1995;92:50–5. Jiggins CD, Naisbit RE, Coe RL, Mallet J. Reproductive isolation caused by colour pattern mimicry. Nature. 2001;411:302–305. Nosil P, Crespi BJ, Sandoval CP. Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature. 2002;417(6887):440–3. Estrada C, Jiggins CD. Interspecific sexual attraction because of convergence in warning colouration: Is there a conflict between natural and sexual selection in mimetic species? J Evol Biol. 2008;21:749–60. Buellesbach J, Vetter SG, Schmitt T. Differences in the reliance on cuticular hydrocarbons as sexual signaling and species discrimination cues in parasitoid wasps. Front Zool. 2018;15(22):1–11. Dalbosco Dell’Aglio D, Troscianko J, McMillan WO, Stevens M, Jiggins CD. The appearance of mimetic Heliconius butterflies to predators and conspecifics. Evolution (N Y). 2018;72(10):2156–66. Finkbeiner SD, Briscoe AD, Reed RD. Warning signals are seductive: Relative contributions of color and pattern to predator avoidance and mate attraction in Heliconius butterflies. Evolution (N Y). 2014;68(12):3410–20. Endler. Natural selection on color patterns in Poecilia reticulata. Evolution (N Y). 1980;34:76–91. Ruxton GD, Sherratt TN, Speed MP. Avoiding attack: The evolutionary ecology of crypsis, warning signals and mimicry. Vol. 17, Oxford biology. New York: Oxford University Press Inc.; 2004. 249 p. Sherratt TN. The evolution of Müllerian mimicry. Naturwissenschaften. 2008;95:681–95. Kapan DD. Three-butterfly system provides a field test of Müllerian mimicry. 2001;409:338–40. Elias M, Gompert Z, Jiggins C, Willmott K. Mutualistic interactions drive ecological niche convergence in a diverse butterfly community. PLoS Biol [Internet]. 2008;6(12):2642–9. Available from: http://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.0060300 Joron M. Polymorphic mimicry, microhabitat use, and sex-specific behaviour. J Evol Biol. 2005;18(3):547–56. Rojas B, Burdfield-Steel E, De Pasqual C, Gordon S, Hernández L, Mappes J, et al. Multimodal aposematic signals and their emerging role in mate attraction. Front Ecol Evol. 2018;6(93). De Bruyne M, Baker TC. Odor detection in insects: Volatile codes. J Chem Ecol. 2008;34(7):882–97. Missbach C, Dweck HKM, Vogel H, Vilcinskas A, Stensmyr MC, Hansson BS, et al. Evolution of insect olfactory receptors. Elife. 2014;3(e02115):1–22. Greenfield M. Signalers and receivers: mechanisms and evolution of arthropod communication. New York, USA: Oxford University Press; 2002. Ehman KD, Scott ME. Urinary odour preferences of MHC congenic female mice, Mus domesticus: Implications for kin recognition and detection of parasitized males. Anim Behav. 2001;62(4):781–9. Kavaliers M, Colwell DD, Braun WJ, Choleris E. Brief exposure to the odour of a parasitized male alters the subsequent mate odour responses of female mice. Anim Behav. 2003;65(1):59–68. Kavaliers M, Choleris E, Ågmo A, Pfaff DW. Olfactory-mediated parasite recognition and avoidance: Linking genes to behavior. Horm Behav. 2004;46(3):272–83. Kavaliers M, Choleris E, Ågmo A, Muglia LJ, Ogawa S, Pfaff DW. Involvement of the oxytocin gene in the recognition and avoidance of parasitized males by female mice. Anim Behav. 2005;70(3):693–702. Rich TJ, Hurst JL. The competing countermarks hypothesis: Reliable assessment of competitive ability by potential mates. Anim Behav. 1999;58(5):1027–37. Beynon RJ, Hurst JL. Multiple roles of major urinary proteins in the house mouse, Mus domesticus. Biochem Soc Trans. 2003;31(1):142–6. Czaczkes TJ, Grüter C, Ratnieks FLW. Trail pheromones: An integrative view of their role in social insect colony organization. Annu Rev Entomol. 2015;60(1):581–99. Estrada C, Schulz S, Yildizhan S, Gilbert LE. Sexual selection drives the evolution of antiaphrodisiac pheromones in butterflies. Evolution (N Y). 2011;65(10):2843–54. Schulz S, Estrada C, Yildizhan S, Boppré M, Gilbert LE. An antiaphrodisiac in Heliconius melpomene butterflies. J Chem Ecol. 2008;34(1):82–93. Nieberding CM, de Vos H, Schneider M V., Lassance J-M, Estramil N, Andersson J, et al. The male sex pheromone of the butterfly Bicyclus anynana: Towards an evolutionary analysis. PLoS One. 2008;3(7):e2751. Nieberding CM, Fischer K, Saastamoinen M, Allen CE, Wallin EA, Hedenström E, et al. Cracking the olfactory code of a butterfly: The scent of ageing. Ecol Lett. 2012;15(5):415–24. Dussourd DE, Harvis CA, Meinwald J, Eisner T. Pheromonal advertisement of a nuptial gift by a male moth (Utetheisa ornatrix). Proc Natl Acad Sci U S A [Internet]. 1991;88:9224–7. Available from: http://www.pnas.org/content/88/20/9224 Shine R, Phillips B, Waye HL, LeMaster MP, Mason RT. Chemosensory cues allow courting male garter snakes to assess body length and body condition of potential mates. Behav Ecol. 2003;54:162–6. Moore PJ, Reagan-Wallin NL, Haynes KF, Moore AJ. Odour conveys status on cockroaches. Nature [Internet]. 1997;25–6. Available from: http://www.nature.com/nature/journal/v389/n6646/full/389025a0.html Smith BH. Recognition of female kin by male bees through olfactory signals. Proc Natl Acad Sci USA [Internet]. 1983;80:4551–4553. Available from: http://www.pnas.org/content/80/14/4551.full.pdf Mas F, Jallon J-M. Sexual isolation and cuticular hydrocarbon differences between Drosophila santomea and Drosophila yakuba. J Chem Ecol. 2005;31(11):2747–52. Pardy JA, Rundle HD, Bernards MA, Moehring AJ. The genetic basis of female pheromone differences between Drosophila melanogaster and D. simulans. Heredity (Edinb) [Internet]. 2018;1. Available from: http://www.nature.com/articles/s41437-018-0080-3 Linn C, Feder JL, Nojima S, Dambroski HR, Berlocher SH, Roelofs W. Fruit odor discrimination and sympatric host race formation in Rhagoletis. Proc Natl Acad Sci U S A. 2003;100(20):11490–3. Olsson SB, Linn CEJ, Feder JL, Michel A, Dambroski HR, Berlocher SH, et al. Comparing peripheral olfactory coding with host preference in the Rhagoletis species complex. Chem Senses. 2009;34:37–48. Tregenza T, Pritchard VL, Butlin RK. Patterns of trait divergence between populations of the meadow grasshopper, Chorthippus parallelus. Evolution (N Y). 2000;54(2):574–85. Schwander T, Arbuthnott D, Gries R, Gries G, Nosil P, Crespi BJ. Hydrocarbon divergence and reproductive isolation in Timema stick Insects. BMC Evol Biol [Internet]. 2013;13. Available from: BMC Evolutionary Biology Liu Y, Hu Y, Bi J, Kong X, Long G, Zheng Y, et al. Odorant-binding proteins involved in sex pheromone and host-plant recognition of the sugarcane borer Chilo infuscatellus (Lepidoptera: Crambidae). Pest Manag Sci. 2020;10.1002/ps.5961. Pelozuelo L, Malosse C, Genestier G, Guenego H, Frerot B. Host-plant specialization in pheromone strains of the European corn borer Ostrinia nubilalis in France. J Chem Ecol. 2004;30(2):335–52. Ômura H, Yotsuzuka S. Male‐specific epicuticular compounds of the sulfur butterfly Colias erate poliographus (Lepidoptera: Pieridae). Appl Entomol Zool. 2015; Saveer AM, Becher PG, Birgersson G, Hansson BS, Witzgall P, Bengtsson M. Mate recognition and reproductive isolation in the sibling species Spodoptera littoralis and Spodoptera litura. Front Ecol Evol [Internet]. 2014;2(18):1–7. Available from: http://journal.frontiersin.org/article/10.3389/fevo.2014.00018/abstract Sheck AL, Groot AT, Ward CM, Gemeno C, Wang J, Brownie C, et al. Genetics of sex pheromone blend differences between Heliothis virescens and Heliothis subflexa: A chromosome mapping approach. J Evol Biol. 2006;19(2):600–17. Marco A, Chivers DP, Kiesecker JM, Blaustein AR. Mate choice by chemical cues in Western Redback (Plethodon vehiculum) and Dunn’s (P. dunni) salamanders. Ethology [Internet]. 1998;104:781–8. Available from: http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0310.1998.tb00111.x/abstract Martín J, López P. Chemoreception, symmetry and mate choice in lizards. Proc R Soc B Biol Sci [Internet]. 2000;267:1265–9. Available from: http://rspb.royalsocietypublishing.org/content/267/1450/1265 Novotny MV. Pheromones, binding proteins and receptor responses in rodents. Biochem Soc. 2003;117–22. Wyatt TD. Pheromones and animal behavior: chemical signals and signatures. Cambridge: Cambridge University Press; 2014. Phelan PL, Baker TC. Evolution of male pheromones in moths: repoductive isolation through sexual selection? Science (80- ). 1987;235:205–7. Löfstedt C, Herrebout WM, Menken SBJ. Sex pheromones and their potential role in the evolution of reproductive isolation in small ermine moths (Yponomeutidae). Chemoecology [Internet]. 1991;2:20–8. Available from: http://link.springer.com/article/10.1007/BF01240662 VN - readcube.com Costanzo K, Monteiro A. A The use of chemical and visual cues in female choice in the butterfly Bicyclus anynana. Proc R Soc B Biol Sci. 2007;274:845–51. Bigiani A, Mucignat-Caretta C, Montani G, Tirindelli R. Pheromone reception in mammals. Rev Physiol Biochem Pharmacol. 2005;155:1–35. Glover TJ, Tang XH, Roelofs WL. Sex-pheromone blend discrimination by male moths from E and Z-strains of European corn-borer. J Chem Ecol. 1987;13(1):143–51. Eltz T, Zimmermann Y, Pfeiffer C, Ramirez Pech J, Twele R, Francke W, et al. An olfactory shift is associated with male perfume differentiation and species divergence in orchid bees. Curr Biol [Internet]. 2008;18:1844– 8. Available from: http://dx.doi.org/10.1016/j.cub.2008.10.049 Symonds MRE, Elgar MA. The evolution of pheromonal diversity. Trends Ecol Evol. 2008;23:220-228. Tanigaki T, Yamaoka R, Sota T. The role of cuticular hydrocarbons in mating and conspecific recognition in the closely related Longicorn beetles Pidonia grallatrix and P. takechii. Zoolog Sci. 2007;24(1):39–45. Geiselhardt S, Otte T, Hilker M. Looking for a similar partner: host plants shape mating preferences of herbivorous insects by altering their contact pheromones. Ecol Lett. 2012;15(9):971–7. Peterson MA, Dobler S, Larson EL, Juárez D, Schlarbaum T, Monsen KJ, et al. Profiles of cuticular hydrocarbons mediate male mate choice and sexual isolation between hybridising Chrysochus (Coleoptera: Chrysomelidae). Chemoecology. 2007;17(2):87–96. Xue HJ, Wei JN, Magalhães S, Zhang B, Song KQ, Liu J, et al. Contact pheromones of 2 sympatric beetles are modified by the host plant and affect mate choice. Behav Ecol. 2016;27(3):895–902. South A, LeVan K, Leombruni L, Orians CM, Lewis SM. Examining the role of cuticular hydrocarbons in Firefly species recognition. Ethology. 2008;114(9):916–24. Hay-Roe MM, Lamas G, Nation JL. Pre- and postzygotic isolation and Haldane rule effects in reciprocal crosses of Danaus erippus and Danaus plexippus (Lepidoptera: Danainae), supported by differentiation of cuticular hydrocarbons, establish their status as separate species. Biol J Linn Soc. 2007;91(3):445–53. Syvertsen TC, Jackson LL, Blomquist GJ, Vinson SB. Alkadienes mediating courtship in the parasitoid Cardiochiles nigriceps (Hymenoptera: Braconidae). J Chem Ecol. 1995;21(12):1971–89. Howard RW. Comparative analysis of cuticular hydrocarbons from the Ectoparasitoids Cephalonomia waterstoni and Laelius utilis (Hymenoptera: Bethylidae) and their respective hosts, Cryptolestes ferrugineus (Coleoptera: Cucujidae) and <i>Trogoderm. Ann Entomol Soc Am. 1992;85(3):317–25. Merrill RM, Dasmahapatra KK, Davey JW, Dell’Aglio DD, Hanly JJ, Huber B, et al. The diversification Heliconius butterflies: What have we learned in 150 years? J Evol Biol. 2015;28(8):1417–38. Jiggins CD. Ecological speciation in mimetic butterflies. Bioscience [Internet]. 2008;58(6):541–8. Available from: http://bioscience.oxfordjournals.org/cgi/doi/10.1641/B580610 Mérot C. Speciation in Heliconius butterflies: the balance between mimicry convergence and ecological divergence. Muséum National d ́Histoire Naturelle, Paris.; 2014. Brower LP, Brower JVZ, Collins CT. Experimental studies of mimicry. 7. Relative palatability and Mullerian mimicry among neotropical butterflies of the subfamily Heliconiinae. Zool Sci Contrib New York Zool Soc. 1963;48(7):65–84. Chai P, Srygley RB. Predation and the flight, morphology, and temperature of Neotropical rain-forest butterflies. Am Nat. 1990;135(6):748–65. Darragh K. Pheromones in Heliconius butterflies: Chemical ecology, genetics, and behaviour. University of Cambridge; 2019. Arias M, Davey JW, Martin S, Jiggins C, Nadeau N, Joron M, et al. How do predators generalize warning signals in simple and complex prey communities? Insights from a videogame. Proc R Soc B Biol Sci. 2020;287:e20200014. Merrill RM, Van Schooten B, Scott JA, Jiggins CD. Pervasive genetic associations between traits causing reproductive isolation in Heliconius butterflies. Proc R Soc B. 2011;278:511–8. Darragh K, Vanjari S, Mann F, González-Rojas MF, Morrison CR, Salazar C, et al. Male sex pheromone components in Heliconius butterflies released by the androconia affect female choice. PeerJ [Internet]. 2017;5:e3953. Available from: https://peerj.com/articles/3953 Rutowski R. The evolution of male mate-locating behavior in butterflies. Am Nat. 1991;138(5):1121–39. Mavárez J, Salazar CA, Bermingham E, Salcedo C, Jiggins CD, Linares M. Speciation by hybridization in Heliconius butterflies. Nature. 2006;441(7095):868–71. Jiggins CD, Estrada C, Rodrigues A. Mimicry and the evolution of premating isolation in Heliconius melpomene Linnaeus. J Evol Biol. 2004;17:680–91. Merrill RM, Rastas P, Martin SH, Melo MC, Barker S, Davey J, et al. Genetic dissection of assortative mating behavior. PLoS Biol. 2019;17(2):1–21. Boppré M. Chemically mediated interactions between butterflies. The biology of butterflies. Vane-Wright R, Ackery P, editors. Academic Press, London; 1984. 259–275 p. Pinheiro de Castro ÉC, Zagrobelny M, Zurano JP, Zikan Cardoso M, Feyereisen R, Bak S. Sequestration and biosynthesis of cyanogenic glucosides in passion vine butterflies and consequences for the diversification of their host plants. Ecol Evol. 2019;9:5079–93. Sculfort O, de Castro ECP, Kozak KM, Bak S, Elias M, Nay B, et al. Variation of chemical compounds in wild Heliconiini reveals ecological factors involved in the evolution of chemical defenses in mimetic butterflies. Ecol Evol. 2020;(November 2019):1–18. Darragh K, Byers KJRP, Merrill RM, McMillan WO, Schulz S, Jiggins CD. Male pheromone composition depends on larval but not adult diet in Heliconius melpomene. Ecol Entomol. 2019;44(3):397–405. de Castro ÉCP, Musgrove J, Bak S, McMillan WO, Jiggins CD. Phenotypic plasticity in chemical defence allows butterflies to diversify host use strategies. bioRxiv Prepr. 2020; Langham GM. Specialized avian predators repeatedly attack novel color morphs of Heliconius butterflies. Evolution (N Y). 2004;58(12):2783–7. Finkbeiner SD, Fishman DA, Osorio D, Briscoe AD. Ultraviolet and yellow reflectance but not fluorescence is important for visual discrimination of conspecifics by Heliconius erato. J Exp Biol [Internet]. 2017;220(7):1267–76. Available from: http://jeb.biologists.org/lookup/doi/10.1242/jeb.153593 Mallet J, Barton NH. Strong natural selection in a warning-color hybrid zone. Evolution (N Y). 1989;43(2):421– 31. Kapan DD. Divergent natural selection and Müllerian mimicry in polymorphic Heliconius cydno (Lepidoptera:Nymphalidae). The University of British Columbia; 1998. Kronforst MR, Papa R. The functional basis of wing patterning in Heliconius butterflies: The molecules behind mimicry. Genetics. 2015;200:1–19. Linares M. The ghost of mimicry past: laboratory reconstitution of an extinct butterfly “race.” Heredity (Edinb). 1997;78:628–35. Mallet J. Shift happens! Shifting balance and the evolution of diversity in warning colour and mimicry. Ecol Entomol. 2010;35(SUPPL. 1):90–104. Fisher R. The genetical theory of natural selection. Oxford, U.K.: Oxford Univ. Press; 1930. Chouteau M, Angers B. Wright’s shifting balance theory and the diversification of aposematic signals. PLoS One. 2012;7(3):e34028. Márquez R, Linderoth TP, Mejía-Vargas D, Nielsen R, Amézquita A, Kronforst MR. Divergence, gene flow, and the origin of leapfrog geographic distributions: The history of colour pattern variation in Phyllobates poison- dart frogs. Mol Ecol. 2020;29:3702–19. Chouteau M, Llaurens V, Piron-Prunier F, Joron M. Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures. Proc Natl Acad Sci [Internet]. 2017;114(31):8325–9. Available from: http://www.pnas.org/lookup/doi/10.1073/pnas.1702482114 Jamie GA, Meier JI. The persistence of polymorphisms across species radiations. Trends Ecol Evol [Internet]. 2020;35(9):795–808. Available from: https://doi.org/10.1016/j.tree.2020.04.007 Nadeau NJ. Genes controlling mimetic colour pattern variation in butterflies. Curr Opin Insect Sci [Internet]. 2016;17:24–31. Available from: http://dx.doi.org/10.1016/j.cois.2016.05.013 Lewis JJ, Reed RD. Genome-wide regulatory adaptation shapes population-level genomic landscapes in Heliconius. Mol Biol Evol. 2018;36(1):159–73. Orteu A, Jiggins CD. The genomics of coloration provides insights into adaptive evolution. Nat Rev Genet [Internet]. 2020;21(8):461–75. Available from: http://dx.doi.org/10.1038/s41576-020-0234-z Morris J, Hanly JJ, Martin SH, Van Belleghem SM, Salazar CA, Jiggins CD, et al. Deep convergence, shared ancestry, and evolutionary novelty in the genetic architecture of Heliconius mimicry. Genetics. 2020;216:765–80. Merrill RM, Wallbank RWR, Bull V, Salazar PCA, Mallet J, Stevens M, et al. Disruptive ecological selection on a mating cue. Proc R Soc B. 2012;279:4907–13. Mérot C, Frérot B, Leppik E, Joron M. Beyond magic traits: Multimodal mating cues in Heliconius butterflies. Evolution (N Y). 2015;69(11):2891–904. Rossi M, Hausmann AE, Thurman TJ, Montgomery SH, Papa R, Jiggins CD, et al. Visual mate preference evolution during butterfly speciation is linked to neural processing genes. Nat Commun [Internet]. 2020;11(4763). Available from: http://dx.doi.org/10.1038/s41467-020-18609-z Armstrong EA. The ethology of bird display and behavior. New York, NY: Dover Publications.; 1965. Gilliard ET. Birds of paradise and bower birds. Press NH, editor. Garden City, NY; 1969. Jones TM, Hamilton JGC. A role for pheromones in mate choice in a lekking sandfly. Anim Behav. 1998;56:891–8. Kotiaho JS. Testing the assumptions of conditional handicap theory: costs and condition dependence of a sexually selected trait. Behav Ecol Sociobiol. 2000;48:188–94. Milinski M, Bakker TCM. Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature. 1990;344:330–3. Pivnick KA, Lavoir-Dornik J, McNeil J. The role of the androconia in the mating behaviour of the European skipper, Thymelicus lineola, and evidence for a male sex pheromone. Physiol Entomol. 1992;17(October):260–8. Snedden WA, Sakaluk SK. Acoustic signalling and its relation to male mating success in sagebrush crickets. Anim Behav. 1992;44(4):633–9. Wing L. Drumming flight in the blue grouse and courtship characters of the Tetraonidae. Condor. 1946;48:154–7. Wertheim B, van Baalen E-JA, Dicke M, Vet LEM. Pheromone mediated aggregation in nonsocial arthropods: An evolutionary ecological perspective. Annu Rev Entomol. 2005;50(1):321–46. Schiestl FP. The evolution of floral scent and insect chemical communication. Ecol Lett. 2010;13(5):643–56. Ali MF, Morgan ED. Chemical communication in insect communities: a guide to insect pheromones with special emphasis on social insects. Biol Rev. 1990;65:227–247. Butenandt VA, Beckmann R, Stamm D, Hecker E. Über den sexual-lockstoff des seidenspinners Bombyx mori. Reindarstellung und Konstitution. Z Naturforsch. 1959;14b:283–4. Löfstedt C. Moth pheromone genetics and evolution. Philos Trans Biol Sci. 1993;340(1292):167–77. Smadja C, Butlin RK. On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity (Edinb). 2009;102:77–97. Wicker-Thomas C. Evolution of insect pheromones and their role in reproductive isolation and speciation. Ann la Soc Entomol Fr [Internet]. 2011;47(1–2):55–62. Available from: http://www.scopus.com/inward/record.url?eid=2-s2.0-80053962352&partnerID=tZOtx3y1 Grillet M, Everaerts C, Houot B, Ritchie MG, Cobb M, Ferveur JF. Incipient speciation in Drosophila melanogaster involves chemical signals. Sci Rep. 2012;2(i):1–11. Vane-Wright RI, Boppré M. Visual and chemical signalling in butterflies: functional and phylogenetic perspectives. Philos Trans R Soc L B Biol Sci. 1993;340:197–205. Jiggins CD. The Ecology and Evolution of Heliconius Butterflies. Oxford University Press; 2017. 330 p. Rothschild M, Moore BP, Brown W V. Pyrazines as warning odour components in the Monarch butterfly, Danaus plexippus, and in moth of the genera Zygaena and Amata (Lepidoptera). Biol J Linn Soc. 1984;23:375–380. Müller F. The scent-scales of the male “Maracujá butterflies.” In: Longstaff GB, editor. Butterfly hunting in many lands. New York, NY: Longmans, Green & Co; 1912. p. 655–659. Eltringham H. On the abdominal glands in Heliconius (Lepidoptera). Trans R Entomol Soc Lond. 1925;73:269– 275. Barth R. Os órgäos odoriferos masculinos de alguns Heliconiinae do Brasil. Mem Inst Oswaldo Cruz. 1952;50:335–86. Klein AL, de Araújo AM. Courtship behavior of Heliconius erato phyllis (Lepidoptera, Nymphalidae) towards virgin and mated females: Conflict between attraction and repulsion signals? J Ethol. 2010;28(3):409–20. Crane J. Imaginal behaviour of a Trinidad butterfly, Heliconius erato hydara Hewitson, with special reference to the social use of color. Zool N Y. 1955;40:167–196. Estrada C, Yildizhan S, Schulz S, Gilbert LE. Sex-specific chemical cues from immatures facilitate the evolution of mate guarding in Heliconius butterflies. Proc R Soc B Biol Sci [Internet]. 2010;277:407–13. Available from: http://rspb.royalsocietypublishing.org/cgi/doi/10.1098/rspb.2009.1476 Gilbert LE. Postmating female odor in Heliconius butterflies: A male-contributed antiaphrodisia? Science (80- ). 1976;193(4251):419–20. Malouines C. Counter-perfume: using pheromones to prevent female remating. Biol Rev. 2016;92(3):1570– 81. Mann F, Vanjari S, Rosser N, Mann S, Dasmahapatra KK, Corbin C, et al. The scent chemistry of Heliconius wing androconia. J Chem Ecol. 2017;43(9):843–57. Liénard MA, Wang H-L, Lassance J-M, Löfstedt C. Sex pheromone biosynthetic pathways are conserved between moths and the butterfly Bicyclus anynana. Nat Commun [Internet]. 2014;5:3957. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4050330&tool=pmcentrez&rendertype=abstr act Yildizhan S, Van Loon J, Sramkova A, Ayasse M, Arsene C, ten Broeke C, et al. Aphrodisiac pheromones from the wings of the small cabbage white and large cabbage white butterflies, Pieris rapae and Pieris brassicae. ChemBioChem. 2009;10:1666–77. Andersson J, Borg-Karlson A-K, Vongvanich N, Wiklund C. Male sex pheromone release and female mate choice in a butterfly. J Exp Biol. 2007;210:964–70. Nishida R, Schulz S, Kim CS, Fukami H, Kuwahara Y, Honda K, et al. Male sex pheromone of a giant danaine butterfly, Idea leuconoe. J Chem Ecol [Internet]. 1996;22(5):949–72. Available from: http://dx.doi.org/10.1007/BF02029947 Zhang YN, Xia YH, Zhu JY, Li SY, Dong SL. Putative pathway of sex pheromone biosynthesis and degradation by expression patterns of genes identified from female pheromone gland and adult antenna of Sesamia inferens (Walker). J Chem Ecol. 2014;40:439–51. Zhang YN, Xia YH, Zhu JY, Li SY, Dong SL. Putative pathway of sex pheromone biosynthesis and degradation by expression patterns of genes identified from female pheromone gland and adult antenna of Sesamia inferens (Walker). J Chem Ecol. 2014;40:439–51. He P, Zhang Y-F, Hong D-Y, Wang J, Wang X-L, Zuo L-H, et al. A reference gene set for sex pheromone biosynthesis and degradation genes from the diamondback moth, Plutella xylostella, based on genome and transcriptome digital gene expression analyses. BMC Genomics [Internet]. 2017;18(219). Available from: http://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-017-3592-y Jurenka R. Insect pheromone biosynthesis. Top Curr Chem. 2004;239:97–131. Ando T, Inomata S, Yamamoto M. Lepidopteran Sex Pheromones. Top Curr Chem. 2004;239:51–96. Groot AT, Dekker T, Heckel DG. The genetic basis of pheromone evolution in moths. Annu Rev Entomol [Internet]. 2016;61:99–117. Available from: http://www.annualreviews.org/doi/10.1146/annurev-ento- 010715-023638 Leary GP, Allen JE, Bunger PL, Luginbill JB, Linn CE, Macallister IE, et al. Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species. Proc Natl Acad Sci U S A. 2012;109(35):14081–6. Miura N, Nakagawa T, Touhara K, Ishikawa Y. Broadly and narrowly tuned odorant receptors are involved in female sex pheromone reception in Ostrinia moths. Insect Biochem Mol Biol [Internet]. 2010;40(1):64–73. Available from: http://dx.doi.org/10.1016/j.ibmb.2009.12.011 Leal WS. Odorant reception in insects: Roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol. 2012;58:373–91. Corcoran JA, Jordan MD, Thrimawithana AH, Crowhurst RN, Newcomb RD. The peripheral olfactory repertoire of the lightbrown apple moth, Epiphyas postvittana. PLoS One. 2015;10(5):e0128596. Walker III WB, Gonzalez F, Garczynski SF, Witzgall P. The chemosensory receptors of codling moth Cydia pomonella – expression in larvae and adults. Sci Rep. 2016;6:23518. De Fouchier A, Walker WB, Montagné N, Steiner C, Binyameen M, Schlyter F, et al. Functional evolution of Lepidoptera olfactory receptors revealed by deorphanization of a moth repertoire. Nat Commun. 2017;8(15709). Zhang Y-N, Zhang L-W, Chen D-S, Liang S, Zhao-Qun L, Ye Z-F, et al. Molecular identification of differential expression genes associated with sex pheromone biosynthesis in Spodoptera exigua. Mol Genet Genomics. 2017; Groot AT, Staudacher H, Barthel A, Inglis O, Schöfl G, Santangelo RG, et al. One quantitative trait locus for intra- and interspecific variation in a sex pheromone. Mol Ecol. 2013;22:1065–80. Koutroumpa FA, Jacquin-Joly E. Sex in the night : Fatty acid-derived sex pheromones and corresponding membrane pheromone receptors in insects. Biochimie [Internet]. 2014;1–7. Available from: http://dx.doi.org/10.1016/j.biochi.2014.07.018 Liu Y, Gu S, Zhang Y, Guo Y, Wang G. Candidate olfaction genes identified within the Helicoverpa armigera antennal transcriptome. PLoS One. 2012;7(10):e48260. Gu SH, Wu KM, Guo YY, Pickett JA, Field LM, Zhou JJ, et al. Identification of genes expressed in the sex pheromone gland of the black cutworm Agrotis ipsilon with putative roles in sex pheromone biosynthesis and transport. BMC Genomics [Internet]. 2013;14(636). Available from: BMC Genomics Jung CR, Kim Y. Comparative transcriptome analysis of sex pheromone glands of two sympatric lepidopteran congener species. Genomics [Internet]. 2014;103(4):308–15. Available from: http://dx.doi.org/10.1016/j.ygeno.2014.02.009 Li RT, Ning C, Huang LQ, Dong JF, Li X, Wang CZ. Expressional divergences of two desaturase genes determine the opposite ratios of two sex pheromone components in Helicoverpa armigera and Helicoverpa assulta. Insect Biochem Mol Biol [Internet]. 2017;90:90–100. Available from: https://doi.org/10.1016/j.ibmb.2017.09.016 Vogel H, Heidel AJ, Heckel DG, Groot AT. Transcriptome analysis of the sex pheromone gland of the noctuid moth Heliothis virescens. BMC Genomics. 2010;11(29):16–8. Xia YH, Zhang YN, Hou XQ, Li F, Dong SL. Large number of putative chemoreception and pheromone biosynthesis genes revealed by analyzing transcriptome from ovipositor-pheromone glands of Chilo suppressalis. Sci Rep. 2015;5:1–12. Svensson M. Sexual selection in moths: the role of chemical communication. Biol Rev [Internet]. 1996;71:113–35. Available from: http://onlinelibrary.wiley.com/doi/10.1111/j.1469- 185X.1996.tb00743.x/full Yildizhan S, van Loon J, Sramkova A, Ayasse M, Arsene C, ten Broeke C, et al. Aphrodisiac pheromones from the wings of the small cabbage white and large cabbage white butterflies, Pieris rapae and Pieris brassicae. ChemBioChem. 2009;10(10):1666–77. Mann F, Szczerbowski D, Silva L De, Mcclure M, Elias M, Schulz S. 3-Acetoxy-fatty acid isoprenyl esters from androconia of the ithomiine butterfly Ithomia salapia. Beilstein J Org Chem. 2020;16:2776–87. Wang HL, Brattström O, Brakefield PM, Francke W, Löfstedt C. Identification and biosynthesis of novel male specific esters in the wings of the tropical butterfly, Bicyclus martius sanaos. J Chem Ecol. 2014;40(6):549–59. Ozaki K, Utoguchi A, Yamada A, Yoshikawa H. Identification and genomic structure of chemosensory proteins (CSP) and odorant binding proteins (OBP) genes expressed in foreleg tarsi of the swallowtail butterfly Papilio xuthus. Insect Biochem Mol Biol [Internet]. 2008;38(11):969–76. Available from: http://dx.doi.org/10.1016/j.ibmb.2008.07.010 Byers KJRP, Darragh K, Garza SF, Almeida DA, Warren IA, Rastas PMA, et al. Clusteing of loci controlling species differences in male chemical bouquets of sympatric Heliconius butterflies. bioRxiv Prepr. 2020; Beatty CD, Beirinckx K, Sherratt TN. The evolution of Müllerian mimicry in multispecies communities. Nature [Internet]. 2004;431(7004):63–66. Available from: http://www.nature.com/nature/journal/v431/n7004/abs/nature02818.html Beatty CD, Beirinckx K, Sherratt TN. The evolution of Müllerian mimicry in multispecies communities. Nature [Internet]. 2004;431(7004):63–66. Available from: http://www.nature.com/nature/journal/v431/n7004/abs/nature02818.html Gavrilets S, Hastings A. Coevolutionary chase in two-species systems with applications to mimicry. J Theor Biol. 1998;191:415–27. Huheey JE. Studies in warning coloration and mimicry. VII. Evolutionary consequences of a Batesian- Müllerian spectrum: A model for Müllerian mimicry. Evolution (N Y) [Internet]. 1976;30(1):86–93. Available from: http://www.jstor.org/stable/2407675%5Cnhttp://www.jstor.org/stable/pdfplus/2407675.pdf?acceptTC=tr ue Mérot C, Le Poul Y, Théry M, Joron M. Refining mimicry: phenotypic variation tracks the local optimum. J Anim Ecol. 2016;85(4):1056–69. Sheppard PM, Turner JRG. The existence of Müllerian Mimicry. Evolution (N Y). 1974;31:452–3. Joron M, Iwasa Y. The evolution of a Müllerian mimic in a spatially distributed community. J Theor Biol. 2005;237(1):87–103. Joron M. Mimicry. In: Cardé RT, Resh VH, editors. Encyclopedia of Insects. 2nd Editio. New York: Academic Press, New York.; 2009. p. 633–43. Joron M, Mallet JLB. Diversity in mimicry: Paradox or paradigm? Trends Ecol Evol. 1998;13(11):461–6. Mallet J, Joron M. Evolution of diversity in warning color and mimicry: Polymorphisms, shifting balance, and speciation. Annu Rev Ecol Syst [Internet]. 1999;30:201–33. Available from: http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.30.1.201 Ihalainen E, Lindström L, Mappes J, Puolakkainen S. Can experienced birds select for Müllerian mimicry? Behav Ecol. 2008;19(2):362–8. Ihalainen E, Lindström L, Mappes J, Puolakkainen S. Can experienced birds select for Müllerian mimicry? Behav Ecol. 2008;19(2):362–8. Langham GM. Rufous-tailed jacamars and aposematic butterflies: Do older birds attack novel prey? Behav Ecol. 2006;17(2):285–90. Ihalainen E, Rowland HM, Speed MP, Ruxton GD, Mappes J. Prey community structure affects how predators select for Müllerian mimicry. Proc R Soc B Biol Sci [Internet]. 2012;279(1736):2099–105. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3321702&tool=pmcentrez&rendertype=abstr act Benson WW. Natural Selection for Müllerian mimicry in Heliconius erato in Costa Rica. Science (80- ). 1972;176(4037):936–9. Chouteau M, Angers B. The role of predators in maintaining the geographic organization of aposematic signals. Am Nat. 2011;178(6):810–7. Owen DF, Smith DAS, Gordon IJ, Owixy AM. Polymorphic Müllerian mimicry in a group of African butterflies: a re-assessment of the relationship between Danaus chrysippus, Acraea encedon and Acraea encedana (Lepidoptera: Nymphalidae). J Zool. 1994;232(1):93–108. Gordon IJ, Smith DAS. Diversity in mimicry. Trends Ecol Evol. 1999;14(4):150–1. Chouteau M, Arias M, Joron M. Warning signals are under positive frequency-dependent selection in nature. Proc Natl Acad Sci [Internet]. 2016;113(8):2164–9. Available from: http://www.pnas.org/lookup/doi/10.1073/pnas.1519216113 Mallet J, McMillan WO, Jiggins CD. Mimicry and warning colour at the boundary between races and species. In: Howard D, Berlocher S, editors. Endless forms Species and speciation [Internet]. Oxford, UK: Oxford University Press; 1998. p. 390–403. Available from: http://discovery.ucl.ac.uk/67729/ Brower AVZ. A new mimetic species of Heliconius (Lepidoptera: Nymphalidae), from southeastern Colombia, revealed by cladistic analysis of mitochondrial DNA sequences. Zool J Linn Soc. 1996;116:317–32. Giraldo N, Salazar C, Jiggins CD, Bermingham E, Linares M. Two sisters in the same dress: Heliconius cryptic species. BMC Evol Biol. 2008;8(324). Mérot C, Mavárez J, Evin A, Dasmahapatra KK, Mallet J, Lamas G, et al. Genetic differentiation without mimicry shift in a pair of hybridizing Heliconius species (Lepidoptera: Nymphalidae). Biol J Linn Soc. 2013;109:830–47. Nadeau NJ, Ruiz M, Salazar P, Counterman B, Medina JA, Ortiz-Zuazaga H, et al. Population genomics of parallel hybrid zones in the mimetic butterflies, H. melpomene and H. erato. Genome Res [Internet]. 2014;24:1316–33. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24823669 Rossato DO, Boligon D, Fornel R, Kronforst MR, Gonçalves GL, Moreira GRP. Subtle variation in size and shape of the whole forewing and the red band among co-mimics revealed by geometric morphometric analysis in Heliconius butterflies. Ecol Evol [Internet]. 2018;1–16. Available from: http://doi.wiley.com/10.1002/ece3.3916 Van Belleghem SM, Alicea Roman PA, Carbia Gutierrez H, Counterman BA, Papa R. Perfect mimicry between Heliconius butterflies is constrained by genetics and development. Proc R Soc B Biol Sci [Internet]. 2020;287:20201267. Available from: https://royalsocietypublishing.org/doi/10.1098/rspb.2020.1267 Rosser N. Speciation and biogeography of Heliconnine butterflies. 2012. de Castro ÉCP, Zagrobelny M, Cardoso MZ, Bak S. The arms race between heliconiine butterflies and Passiflora plants - new insights on an ancient subject. Biol Rev [Internet]. 2017; Available from: http://doi.wiley.com/10.1111/brv.12357 Rohlf FJ. TPSDig. Stony Brook, NY: Department of Ecology and Evolution, State University of NY at Stony Brook; 2010. Adams D, Collyer M, Kaliontzopoulou A, Sherratt E. Geometric morphometric analyses of 2D/3D landmark data. https://cran.r-project.org/package=geomorph.; 2017. Bookstein F. Morphometrics tools for landmark data: Geometry and biology. New York, NY: Cambridge University Press; 1991. Zelditch ML, Swiderski DL, Sheets HD, Fink WL. Geometric morphometrics for biologist: a primer. San Diego, LA: Elsevier Academic Press; 2004. Hijmans RJ, Williams E, Vennes C. Package ‘geosphere.’ 2019. Friendly M, Fox J. Candisc: visualizing generalized canonical discriminant and canonical correlation analysis [Internet]. 2017. Available from: https://cran.r-project.org/package=candisc Van Belleghem SM, Papa R, Ortiz-Zuazaga H, Hendrickx F, Jiggins CD, McMillan WO, et al. Patternize : An R package for quantifying color pattern variation. Methods Ecol Evol. 2018;9:390–8. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;11(7):671–5. Müller F. Ituna and Thyridia: a remarkable case of mimicry in butterflies. Trans Entomol Soc London. 1879;1879:20–29. Sbordoni V, Bullini L, Scarpelli G, Forestiero S, Rampini M. Mimicry in the burnet moth Zygaena ephialtes: population studies and evidence of a Batesian—Müllerian situation. Ecol Entomol. 1979;4:83–93. Niehuis O, Hofmann A, Naumann CM, Misof B. Evolutionary history of the burnet moth genus Zygaena Fabricius, 1775 (Lepidoptera: Zygaenidae) inferred from nuclear and mitochondrial sequence data: phylogeny, host-plant association, wing pattern evolution and historical biogeography. Biol J Linn Soc. 2007;92:501–20. Plowright RC, Owen RE. The evolutionary significance of bumble bee color patterns: a mimetic interpretation. Evolution (N Y). 1980;34(4):622–37. Williams P. The distribution of bumblebee colour patterns worldwide: possible significance for thermoregulation, crypsis, and warning mimicry. Biol J Linn Soc. 2007;92:97–118. Zrzavý J, Nedvěd O. Evolution of mimicry in the New World Dysdercus (Hemiptera: Pyrrhocoridae). J Evol Biol. 1999;12:956–69. Symula R, Schulte R, Summers K. Molecular phylogenetic evidence for a mimetic radiation in Peruvian poison frogs supports a Müllerian mimicry hypothesis. Proc R Soc B Biol Sci. 2001;268:2415–21. Chiari Y, Vences M, Vieites DR, Rabemananjara F, Bora P, Ramilijaona Ravoahangimalala O, et al. New evidence for parallel evolution of colour patterns in Malagasy poison frogs (Mantella). Mol Ecol. 2004;13:3763–74. Sanders KL, Malhotra A, Thorpe RS. Evidence for a Müllerian mimetic radiation in Asian pitvipers. Proc R Soc B Biol Sci. 2006;273:1135–41. Springer VG, Smith-Vaniz WF. Mimetic relationships involving fishes of the family Blenniidae. Smithson Contrib to Zool. 1972;(112):1–36. Dumbacher JP, Fleischer RC. Phylogenetic evidence for colour pattern convergence in toxic pitohuis: Müllerian mimicry in birds? Proc R Soc B Biol Sci. 2001;268:1971–6. Chittka L. Bee color vision is optimal for coding flower color, but flower colors are not optimal for being coded—why? Isr J Plant Sci. 1997;45:115–27. Roy BA, Widmer A. Floral mimicry: a fascinating yet poorly understood phenomenon. Trends Plant Sci. 1999;4(8):325–30. Benitez-Vieyra S, Hempel De Ibarra N, Wertlen AM, Cocucci AA. How to look like a mallow: Evidence of floral mimicry between Turneraceae and Malvaceae. Proc R Soc B Biol Sci. 2007;274:2239–48. Jones RT, Le Poul Y, Whibley AC, Mèrot C, Ffrench-Constant RH, Joron M. Wing shape variation associated with mimicry in butterflies. Evolution (N Y). 2013;67(8):2323–34. Montejo-Kovacevich G, Smith JE, Meier JI, Bacquet CN, Whiltshire-Romero E, Nadeau NJ, et al. Altitude and life-history shape the evolution of Heliconius wings. Evolution (N Y). 2019;73(12):2436–50. Mena S, Kozak KM, Cárdenas RE, Checa MF. Forest stratification shapes allometry and flight morphology of tropical butterflies. Proc R Soc B Biol Sci [Internet]. 2020;287:20201071. Available from: https://royalsocietypublishing.org/doi/10.1098/rspb.2020.1071 Chazot N, Panara S, Zilbermann N, Blandin P, Le Poul Y, Cornette R, et al. Morpho morphometrics: Shared ancestry and selection drive the evolution of wing size and shape in Morpho butterflies. Evolution (N Y). 2015;70(1):181–94. Cespedes A, Penz CM, DeVries PJ. Cruising the rain forest floor: Butterfly wing shape evolution and gliding in ground effect. J Anim Ecol. 2015;84(3):808–16. Mendoza-Cuenca L, Macías-Ordóñez R. Foraging polymorphism in Heliconius charitonia (Lepidoptera: Nymphalidae): morphological constraints and behavioural compensation. J Trop Ecol. 2005;21:407–15. Mallet JLB, Jackson DA. The ecology and social behaviour of the Neotropical butterfly Heliconius xanthocles Bates in Colombia. Zool J Linn Soc. 1980;70:1–13. Reed RD, Papa R, Martin A, Hines HM, Counterman BA, Pardo-Diaz GC, et al. <i>Optix</> drives the repeated convergent evolution of butterfly wing pattern mimicry. Science (80- ). 2011;333(6046):1137–41. Lewis JJ, Van Belleghem SM. Mechanisms of change: a population-based perspective on the roles of modularity and pleiotropy in diversification. Front Ecol Evol. 2020;8:1–12. Wallbank RWR, Baxter SW, Pardo-Diaz C, Hanly JJ, Martin SH, Mallet J, et al. Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling. PLoS Biol. 2016;14(1):1–16. McMillan WO, Livraghi L, Concha C, Hanly JJ. From patterning genes to process: unraveling the gene regulatory networks that pattern Heliconius wings. Front Ecol Evol. 2020;8(221):1–15. Nadeau NJ, Pardo-Diaz GC, Whibley A, Supple MA, Saenko S V., Wallbank RWR, et al. The gene cortex controls mimicry and crypsis in butterflies and moths. Nature [Internet]. 2016;534(7605):106–10. Available from: http://dx.doi.org/10.1038/nature17961 Martin A, Papa R, Nadeau NJ, Hill RI, Counterman BA, Halder G, et al. Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand. Proc Natl Acad Sci [Internet]. 2012;109(31):12632–7. Available from: http://www.pnas.org/cgi/doi/10.1073/pnas.1204800109 Lewis JJ, Van Belleghem SM, Riccardo P, Danko CG, Reed RD. Many functionally connected loci foster adaptive diversification along a neotropical hybrid zone. Sci Adv. 2020;6:eabb8617. Moest M, Van Belleghem SM, James JE, Salazar C, Martin SH, Barker SL, et al. Selective sweeps on novel and introgressed variation shape mimicry loci in a butterfly adaptive radiation. Vol. 18, PLOS Biology. 2020. e3000597 p. Morris J, Navarro N, Rastas P, Rawlins LD, Sammy J, Mallet J, et al. The genetic architecture of adaptation: convergence and pleiotropy in Heliconius wing pattern evolution. Heredity (Edinb) [Internet]. 2019;123(2):138–52. Available from: http://dx.doi.org/10.1038/s41437-018-0180-0 Papa R, Kapan DD, Counterman BA, Maldonado K, Lindstrom DP, Reed RD, et al. Multi-Allelic Major Effect Genes Interact with Minor Effect QTLs to Control Adaptive Color Pattern Variation in Heliconius erato. PLoS One. 2013;8(3):e57033. Concha C, Wallbank RWR, Hanly JJ, Fenner J, Livraghi L, Rivera ES, et al. Interplay between developmental flexibility and determinism in the evolution of mimetic Heliconius wing patterns. Curr Biol [Internet]. 2019;29:1–14. Available from: https://doi.org/10.1016/j.cub.2019.10.010 Rowe C, Lindström L, Lyytinen A. The importance of pattern similarity between Müllerian mimics in predator avoidance learning. Proc R Soc B Biol Sci. 2004;271(1537):407–13. Ihalainen E, Lindström L, Mappes J. Investigating Müllerian mimicry: Predator learning and variation in prey defences. J Evol Biol. 2007;20(2):780–91. Rowland HM, Ihalainen E, Lindström L, Mappes J, Speed MP. Co-mimics have a mutualistic relationship despite unequal defences. Nature. 2007;448(7149):64–7. Finkbeiner SD, Briscoe AD, Mullen SP. Complex dynamics underlie the evolution of imperfect wing pattern convergence in butterflies. Evolution (N Y). 2017;71(4):949–59. Rutowski RL, Nahm AC, Macedonia JM. Iridescent hindwing patches in the Pipevine Swallowtail: Differences in dorsal and ventral surfaces relate to signal function and context. Funct Ecol. 2010;24(4):767–75. Su S, Lim M, Kunte K. Prey from the eyes of predators: Color discriminability of aposematic and mimetic butterflies from an avian visual perspective. Evolution (N Y). 2015;69(11):2985–94. Oliver JC, Robertson KA, Monteiro A. Accommodating natural and sexual selection in butterfly wing pattern evolution. Proc R Soc B Biol Sci. 2009;276(1666):2369–75. Robertson KA, Monteiro A. Female Bicyclus anynana butterflies choose males on the basis of their dorsal UV-reflective eyespot pupils. Proc R Soc B Biol Sci. 2005;272(1572):1541–6. De Bona S, Valkonen JK, López-Sepulcre A, Mappes J. Predator mimicry, not conspicuousness, explains the efficacy of butterfly eyespots. Proc R Soc B Biol Sci. 2015;282:20150202. DeVries PJ, Penz CM, Hill RI. Vertical distribution, flight behaviour and evolution of wing morphology in Morpho butterflies. J Anim Ecol. 2010;79:1077–85. Finkbeiner SD. Communal roosting in Heliconius butterflies (Nymphalidae): roost recruitment, establishment, fidelity, and resource use trends based on age and sex. J Lepid Soc. 2014;68(1):10–6. Willmott KR, Willmott JCR, Elias M, Jiggins CD. Maintaining mimicry diversity: optimal warning colour patterns differ among microhabitats in Amazonian clearwing butterflies. Proc R Soc B. 2017;284:20170744. Cuthill IC, Allen WL, Arbuckle K, Caspers B, Chaplin G, Hauber ME, et al. The biology of color. Science (80- ). 2017;357(6350):eaan0221. Arias M, Meichanetzoglou A, Elias M, Rosser N, De-Silva DL, Nay B, et al. Variation in cyanogenic compounds concentration within a Heliconius butterfly community: does mimicry explain everything? BMC Evol Biol [Internet]. 2016;16(272):1–10. Available from: http://dx.doi.org/10.1186/s12862-016-0843-5 Coyne J., Orr H. Speciation. Sunderland, Massachusets: Sinauer Associates Inc, Sunderland, MA, USA.; 2004. 545 p. Wang L, Anderson DJ. Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature [Internet]. 2010;463(7278):227–31. Available from: http://www.nature.com/doifinder/10.1038/nature08678 Hartlieb E, Anderson P. Olfactory-released behaviours. In: B.S. H, editor. Insect Olfaction. Berlin, Heidelberg: Springer; 1999. p. 315–49. Alves H, Rouault JD, Kondoh Y, Nakano Y, Yamamoto D, Kim YK, et al. Evolution of cuticular hydrocarbons of hawaiian Drosophilidae. Behav Genet. 2010;40(5):694–705. Estrada C, Gilbert LE. Host plants and immatures as mate-searching cues in Heliconius butterflies. Anim Behav [Internet]. 2010;80(2):231–9. Available from: http://dx.doi.org/10.1016/j.anbehav.2010.04.023 Mérot C, Salazar C, Merrill RM, Jiggins CD, Joron M. What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies. Proc R Soc B Biol Sci. 2017;284:20170335. Darragh K, Montejo-Kovacevich G, Kozak KM, Morrison CR, Figueiredo CME, Ready JS, et al. Species specificity and intraspecific variation in the chemical profiles of Heliconius butterflies across a large geographic range. Ecol Evol Press [Internet]. 2019;00:1–25. Available from: https://www.biorxiv.org/content/10.1101/573469v1 Merrill RM, Chia A, Nadeau NJ. Divergent warning patterns contribute to assortative mating between incipient Heliconius species. Ecol Evol. 2014;4(7):911–7. Kozak KM, Wahlberg N, Neild AFE, Dasmahapatra KK, Mallet J, Jiggins CD. Multilocus Species Trees Show the Recent Adaptive Radiation of the Mimetic Heliconius Butterflies. Syst Biol. 2015;64(3):505–24. Brower AVZ. Parallel race formation and the evolution of mimicry in Heliconius butterflies : A phylogenetic hypothesis from mitochondrial DNA sequences. Evolution (N Y). 1996;50(1):195–221. Jiggins CD, Linares M, Naisbit RE, Salazar C, Yang ZH, Mallet J. Sex-linked hybrid sterility in a butterfly. Evolution (N Y). 2001;55(8):1631–8. Sanchez AP, Pardo-Diaz GC, Enciso-Romero J, Muñoz A, Jiggins CD, Salazar C, et al. An introgressed wing pattern acts as a mating cues. Evolution (N Y). 2015;69(6):1619–29. Vanjari S, Mann F, Merrill R, Schulz S, Jiggins C. Male sex pheromone components in the butterfly Heliconius melpomene. bioRxiv. 2015; R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2016. Bates D, Maechler M, Bolker B, Walker S, Bojesen Christensen RH, Singmann H, et al. Linear Mixed-Effects Models using “Eigen” and S4. Journal of Statistical Software. 2015. p. 1–48. Wickham H. ggplot2 - Elegant Graphics for Data Analysis. 2nd ed. New York, NY: Springer-Verlag; 2009. 260 p. Fox J, Weisberg S. An R companion to applied regression. 2nd ed. Sage, editor. Thousand Oaks, CA; 2011. 449 p. Dorai-Raj S. binom: Binomial confidence intervals for several parameterizations [Internet]. 2014. Available from: http://cran.r-project.org/package=binom Hench K, Vargas M, Höppner MP, McMillan WO, Puebla O. Inter-chromosomal coupling between vision and pigmentation genes during genomic divergence. Nat Ecol Evol. 2019;3(4):657–67. Bay RA, Arnegard ME, Conte GL, Best J, Bedford NL, McCann SR, et al. Genetic coupling of female mate choice with polygenic ecological divergence facilitates Stickleback speciation. Curr Biol. 2017;27(21):3344-3349.e4. Shahandeh MP, Pischedda A, Turner TL. Male mate choice via cuticular hydrocarbon pheromones drives reproductive isolation between Drosophila species. Evolution (N Y). 2017;72(1):123–35. Keller-Costa T, Canário AVM, Hubbard PC. Chemical communication in cichlids: A mini-review. Gen Comp Endocrinol [Internet]. 2015;221:64–74. Available from: http://dx.doi.org/10.1016/j.ygcen.2015.01.001 Merrill RM, Gompert Z, Dembeck LM, Kronforst MR, McMillan WO, Jiggins CD. Mate preference across the speciation continuum in a clade of mimetic butterflies. Evolution (N Y). 2011;65(5):1489–500. Muñoz AG, Salazar C, Castaño J, Jiggins CD, Linares M. Multiple sources of reproductive isolation in a bimodal butterfly hybrid zone. J Evol Biol. 2010;23(6):1312–20. Southcott L, Kronforst M. Female mate choice is a reproductive isolating barrier in Heliconius butterflies : Ethology. 2018;124:862–8659. Larsdotter-Mellström H, Eriksson K, Liblikas I, Wiklund C, Borg-Karlson AK, Nylin S, et al. It’s all in the mix: Blend-specific behavioral response to a sexual pheromone in a butterfly. Front Physiol. 2016;7(68):1–10. Snellings Y, Herrera B, Wildemann B, Beelen M, Zwarts L, Wenseleers T, et al. The role of cuticular hydrocarbons in mate recognition in Drosophila suzukii. Sci Rep [Internet]. 2018;8(4996):1–11. Available from: http://dx.doi.org/10.1038/s41598-018-23189-6 Rundle HD, Chenoweth SF, Doughty P, Blows MW. Divergent selection and the evolution of signal traits and mating preferences. PLoS Biol. 2005;3(11):1988–95. Grula J, McChesney J, Taylor O. Aphrodisiac pheromones of the sulfur butterflies Colias eurytheme and C. philodice (Lepidoptera, Pieridae). J Chem Ecol. 1980;6:241–56. Wago H. Studies on the Mating Behavior of the Pale Grass Blue, Zizeeria maha argia (Lepidoptera : Lycaenidae) III. Olfactory Cues in Sexual Discrimination by Males. Appl Ent Zool. 1978;13:283–9. Koutroumpa FA, Monsempes C, François M-C, de Cian A, Royer C, Concordet J-P, et al. Heritable genome editing with CRISPR/Cas9 induces anosmia in a crop pest moth. Sci Rep. 2016;6:29620. Counterman BA, Araujo-Perez F, Hines HM, Baxter SW, Morrison CM, Lindstrom DP, et al. Genomic hotspots for adaptation: The population genetics of Müllerian mimicry in Heliconius erato. PLoS Genet. 2010;6(2):e1000796. Counterman BA, Araujo-Perez F, Hines HM, Baxter SW, Morrison CM, Lindstrom DP, et al. Genomic hotspots for adaptation: The population genetics of Müllerian mimicry in Heliconius erato. PLoS Genet. 2010;6(2):e1000796. Hillier NK, Vickers NJ. The role of Heliothine hairpencil compounds in female Heliothis virescens (Lepidoptera: Noctuidae) behavior and mate acceptance. Chem Senses. 2004;29(6):499–511. Schulz S, Nishida R. The pheromone system of the male danaine butterfly, Idea leuconoe. Bioorg Med Chem. 1996;4(3):341–9. Albre J, Steinwender B, Newcomb RD. The evolution of desaturase gene regulation involved in sex pheromone production in Leafroller Moths of the genus Planotortrix. J Hered. 2013;104(5):627–38. Dopman EB, Robbins PS, Seaman A. Components of reproductive isolation between North American pheromone strains of the European corn borer. Evolution (N Y). 2010;64(4):881–902. Naisbit RE, Jiggins CD, Linares M, Salazar C, Mallet J. Hybrid sterility, Haldane’s rule and speciation in Heliconius cydno and H. melpomene. Genet Soc Am. 2002;161:1517–26. Edwards AWF. Likelihood. Cambridge University Press; 1972. Hummel HE, Miller T. Techniques in pheromone research. Springer Science and Business Media; 2012. 464 p. Hammer Ø, Harper DAT, Ryan PD. PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron [Internet]. 2001;4(1)(1):1–9. Available from: http://palaeo- electronica.org/2001_1/past/issue1_01.htm Burdfield-Steel E, Pakkanen H, Rojas B, Galarza JA, Mappes J. De novo synthesis of chemical defenses in an aposematic moth. J Insect Sci. 2018;18(2):1–4. Moore BP, Brown WV, Rothschild M. Methylalkylpyrazines in aposematic insects, their hostplants and mimics. Chemoecology. 1990;1(2):43–51. Kaye H, Mackintosch NJ, Rothschild M, Moore BP. Odour of pyrazine potentiates an association between environmental cues and unpalatable taste. Anim Behav. 1989;37:1–6. Coyne J, Orr H. Speciation. Sinauer Associates Inc, Sunderland, MA, USA.; 2004. Brand P, Hinojosa-Díaz IA, Ayala R, Daigle M, Yurrita Obiols CL, Eltz T, et al. The evolution of sexual signaling is linked to odorant receptor tuning in perfume-collecting orchid bees. Nat Commun [Internet]. 2020;11. Available from: http://dx.doi.org/10.1038/s41467-019-14162-6 Löfstedt C, Wahlberg N, Millar JG. Evolutionary Patterns of Pheromone Diversity in Lepidoptera. In: Berkeley ed. JARC, editor. Pheromone Communication in Moths : Evolution, Behavior and Application. University of California Press; 2016. p. 43-78. Byers KJRP, Darragh K, Musgrove J, Abondano Almeida D, Garza SF, Warren IA, et al. A major locus controls a biologically active pheromone component in Heliconius melpomene. Evolution (N Y). 2020;1–16. Conner W, Iyengar V. Male pheromones in moths. In pheromone communication. In: Allison J, Ring C, editors. Evolution, Behavior and Application. Berkeley: University of California Press; 2016. p. 191–208. Aldrich JR, Blum MS, Duffey SS, Fales HM. Male specific natural products in the bug, Leptoglossus phyllopus: Chemistry and possible function. J Insect Physiol. 1976;22(9):1201–6. Morgan ED. Biosynthesis in insects: advanced edition. Royal Society of Chemistry, editor. RSC Publishing; 2010. 362 p. Meyer HJ, Norris DM. Vanillin and Syringaldehyde as attractants (Coleoptera: Scolytidae). Ann Entomol Soc Am. 1967;60(4):858–9. Seenivasagan T, Sharma KR, Sekhar K, Ganesan K, Prakash S, Vijayaraghavan R. Electroantennogram, flight orientation, and oviposition responses of Aedes aegypti to the oviposition pheromone n-heneicosane. Parasitol Res. 2009;104:827–33. Simmons LW, Alcock J, Reeder A. The role of cuticular hydrocarbons in male attraction and repulsion by female Dawson’s burrowing bee, Amegilla dawsoni. Anim Behav. 2003;66:677–85. Combs PA, Krupp JJ, Khosla NM, Bua D, Petrov DA, Levine JD, et al. Tissue-specific cis-regulatory divergence implicates eloF in inhibiting interspecies mating in Drosophila. Curr Biol. 2018;28(24):3969-3975.e3. Kost S, Heckel DG, Yoshido A, Groot AT. A Z-linked sterility locus causes sexual abstinence in hybrid females and facilitates speciation in Spodoptera frugiperda. Evolution (N Y). 2016;70(6):1418–27. Smadja CM, Butlin RK. A framework for comparing processes of speciation in the presence of gene flow. Mol Ecol. 2011;20(24):5123–40. Seehausen O, Takimoto G, Roy D, Jokela J. Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol Ecol. 2008;17:30 – 44. Southcott L, Kronforst M. Female mate choice is a reproductive isolating barrier in Heliconius butterflies. Ethology. 2018;124:862–8659. Gleason JM, James RA, Wicker-Thomas C, Ritchie MG. Identification of quantitative trait loci function through analysis of multiple cuticular hydrocarbons differing between Drosophila simulans and Drosophila sechellia females. Heredity (Edinb) [internet] 2009, 103(5):416-24. Available from: http:dx.doi.org/10.1038/hdy.2009.79 Teal PEA, Tumlinson JH. Effects of interspecific hybridization between Heliothis virescens and H. subflexa on the sex pheromone communication system. Insect Physol. 1997;41:519–25. Constantino LM, Salazar JA. Natural hybridization of Heliconius cydno Doubleday from Western Colombia (Lepidoptera: Nymphalidae: Heliconiinae). Bol Cient del Mus Hist Nat Univ Caldas. 1998;2(June):41–5.
dc.source.instname.none.fl_str_mv	instname:Universidad del Rosario
dc.source.reponame.none.fl_str_mv	reponame:Repositorio Institucional EdocUR
bitstream.url.fl_str_mv	https://repository.urosario.edu.co/bitstreams/c4db6bfa-15cc-4456-9fe7-f3407e861f75/download https://repository.urosario.edu.co/bitstreams/027db425-1871-42e8-a1cf-d5c8550b5391/download https://repository.urosario.edu.co/bitstreams/9c5c507a-af9a-487a-b52f-8b3856bc5f72/download https://repository.urosario.edu.co/bitstreams/e6627ea9-3326-4bef-81c0-87cc57643ead/download https://repository.urosario.edu.co/bitstreams/83a4f96f-a336-4ae1-b827-8045fc3d9175/download
bitstream.checksum.fl_str_mv	7979f5f07dac7271904e62107ed6a361 dab767be7a093b539031785b3bf95490 fab9d9ed61d64f6ac005dee3306ae77e d6d4c54dbc7dfc587573ccf4995282f1 2ed63ca5c588c28325926468d7d5e6cd
bitstream.checksumAlgorithm.fl_str_mv	MD5 MD5 MD5 MD5 MD5
repository.name.fl_str_mv	Repositorio institucional EdocUR
repository.mail.fl_str_mv	edocur@urosario.edu.co
_version_	1818106433583972352
spelling	Salazar, Camilo79873757600Pardo Díaz, Geimy Carolina53107311600González-Rojas, María FernandaDoctor en Ciencias Biomédicas y BiológicasFull timefb2fd4e5-b8b2-43d3-8369-ddc6e025b0366002021-02-18T03:40:13Z2021-02-18T03:40:13Z2021-01-20Las mariposas del género Heliconius son un excelente ejemplo de mimetismo Mülleriano, donde especies filogenéticamente distantes convergen en un fenotipo alar casi idéntico cuando se encuentran en simpatría. Sin embargo, pocos estudios han abordado de manera integral la precisión del mimetismo y la variación que existe en las señales miméticas a lo largo del fitness landscape (que puede comprender múltiples picos óptimos). En este estudio, haciendo uso de análisis de cuantificación del color, tamaño y forma de las alas, investigué el grado de semejanza fenotípica entre especies co-miméticas en múltiples anillos de mariposas del género Heliconius. Encontré que el tamaño y la forma de las alas no contribuyen al mimetismo. Por el contrario, el color es el principal contribuyente, pero algunos fenotipos son más precisos entre co-miméticos que otros. Esto sugiere la presencia de múltiples picos adaptativos dentro de un mismo anillo mimético. En estas mariposas, el patrón de coloración se reconoce como la principal señal para el reconocimiento de pareja entre especies que están filogenéticamente cercanas, pero cuando esta señal se ve comprometida, las señales alternativas de apareamiento deben evolucionar para asegurar el aislamiento reproductivo y la integridad de la especie. Las especies estrechamente relacionadas H. melpomene malleti y H. timareta florencia se encuentran en la misma región geográfica y, a pesar de exhibir patrones de coloración casi idénticos, presentan un fuerte aislamiento reproductivo. En esta tesis, examiné cuales señales difieren entre especies y potencialmente contribuyen al aislamiento reproductivo. El patrón de coloración alar es indistinguible entre las dos especies, mientras que el perfil químico de la androconia y los genitales de los machos exhiben marcadas diferencias. Por otra parte, realicé experimentos de comportamiento para estudiar la importancia del color y las señales químicas en el reconocimiento de pareja por parte de las hembras. Encontré que los perfiles químicos y no el patrón de coloración alar impulsan la preferencia de las hembras por machos conespecíficos. Además, los experimentos con machos y hembras híbridos sugirieron un compuesto genético importante tanto para la producción química como para la preferencia, lo que sugiere que los productos químicos son la principal barrera reproductiva que se opone al flujo de genes entre estas dos especies hermanas y co-miméticas. En conjunto, estos resultados concuerdan con la idea de que la adaptación por mimetismo es un proceso complejo y dinámico que se ve afectado por más de un factor y que una combinación efectiva de estas señales (visuales y químicas) es esencial para los procesos de comunicación intra e interespecífica en mariposas.Heliconius butterflies are an excellent example of Müllerian mimicry, where phylogenetically distant species converge to nearly identical wing phenotype when occurring in sympatry. However, few studies have comprehensively addressed mimicry accuracy and variation in mimicry signals across the fitness landscape (which may comprise multiple fitness peaks). In this study, using analysis of colour quantification, wing size and shape, I investigate the extent of phenotypic resemblance between co- mimic species in multiple Heliconius mimicry rings. I found that wing size and shape do not contribute to mimicry. In contrast, colour phenotype is the main contributor, but some phenotypes are more accurate between co-mimics than others. This suggests the presence of multiple adaptive peaks within the same mimetic ring. In these butterflies, colour pattern is recognised as the main cue for mate recognition between species that are phylogenetically close, but when this cue is compromised alternative mating signals must evolve to ensure reproductive isolation and species integrity. The closely related species H. melpomene malleti and H. timareta florencia occur in the same geographical region, and despite being co-mimics, they display strong reproductive isolation. Here, I tested which cues differ between species, and potentially contribute to reproductive isolation. Wing colour pattern was indistinguishable between the two species, while the chemical profile of the males’ androconia and genitalia showed marked differences. Finally, I conducted behavioural experiments to study the importance of colour and chemical signals in mate recognition by females. I found that chemical blends and not wing colour pattern drive the preference of females for conspecific males. Also, experiments with hybrid males and females suggested an important genetic compound for both chemical production and preference suggesting that chemicals are the major reproductive barrier opposing gene flow between these two sister and co-mimic species. Altogether, these results agree with the idea that mimicry adaptation is a complex and dynamic process affected by more than one factor and that an effective combination of these signals (visual and chemical) is essential for intra- and interspecific communication processes in butterflies.application/pdfhttps://doi.org/10.48713/10336_30934 https://repository.urosario.edu.co/handle/10336/30934engUniversidad del RosarioFacultad de Ciencias Naturales y MatemáticasDoctorado en Ciencias Biomédicas y BiológicasAtribución-SinDerivadas 2.5 ColombiaAbierto (Texto Completo)PARGRAFO: En caso de presentarse cualquier reclamación o acción por parte de un tercero en cuanto a los derechos de autor sobre la obra en cuestión, EL AUTOR, asumirá toda la responsabilidad, y saldrá en defensa de los derechos aquí autorizados; para todos los efectos la universidad actúa como un tercero de buena fe.http://creativecommons.org/licenses/by-nd/2.5/co/http://purl.org/coar/access_right/c_abf2Córdoba-Aguilar A, González-Tokman D, González-Santoyo I. Insect behavior: from mechanisms to ecological and evolutionary consequences. First Edit. Oxford, UK: Oxford University Press; 2018. 414 p.Uetz GW, Roberts JA, Taylor PW. Multimodal communication and mate choice in wolf spiders: female response to multimodal versus unimodal signals. Anim Behav [Internet]. 2009;78:299–305. Available from: http://dx.doi.org/10.1016/j.anbehav.2009.04.023Candolin U. The use of multiple cues in mate choice. Biol Rev Camb Philos Soc [Internet]. 2003;78:575–95. Available from: http://www.ncbi.nlm.nih.gov/pubmed/14700392Chenoweth SF, Blows MW. Dissecting the complex genetic basis of mate choice. Nat Rev Genet [Internet]. 2006;7(9):681–92. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16921346Bímová B, Albrecht T, Macholán M, Piálek J. Signalling components of the house mouse mate recognition system. Behav Processes. 2009;80(1):20–7.Wyatt TD. Pheromones and animal behaviour: communication by smell and taste. Cambridge: Cambridge University Press; 2003.Greenspan RJ, Ferveur JF. Courtship in Drosophila. Annu Rev Genet. 2000;34:205–32.Conner WE. “Un chant d’appel amoureux”: Acoustic communication in moths. J Exp Biol. 1999;202(13):1711–23.Weller SJ, Jacobson NL, Conner WE. The evolution of chemical defences and mating systems in tiger moths (Lepidoptera: Arctiidae). Biol J Linn Soc. 1999;68(4):557–78.Boppré M. Chemical communication, plant relationships, and mimicry in the evolution of Danaid butterflies. Entomol Exp Appl. 1978;24(3):64–77.Eisner T, Meinwald J. The chemistry of sexual selection. Proc Natl Acad Sci U S A. 1995;92:50–5.Jiggins CD, Naisbit RE, Coe RL, Mallet J. Reproductive isolation caused by colour pattern mimicry. Nature. 2001;411:302–305.Nosil P, Crespi BJ, Sandoval CP. Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature. 2002;417(6887):440–3.Estrada C, Jiggins CD. Interspecific sexual attraction because of convergence in warning colouration: Is there a conflict between natural and sexual selection in mimetic species? J Evol Biol. 2008;21:749–60.Buellesbach J, Vetter SG, Schmitt T. Differences in the reliance on cuticular hydrocarbons as sexual signaling and species discrimination cues in parasitoid wasps. Front Zool. 2018;15(22):1–11.Dalbosco Dell’Aglio D, Troscianko J, McMillan WO, Stevens M, Jiggins CD. The appearance of mimetic Heliconius butterflies to predators and conspecifics. Evolution (N Y). 2018;72(10):2156–66.Finkbeiner SD, Briscoe AD, Reed RD. Warning signals are seductive: Relative contributions of color and pattern to predator avoidance and mate attraction in Heliconius butterflies. Evolution (N Y). 2014;68(12):3410–20.Endler. Natural selection on color patterns in Poecilia reticulata. Evolution (N Y). 1980;34:76–91.Ruxton GD, Sherratt TN, Speed MP. Avoiding attack: The evolutionary ecology of crypsis, warning signals and mimicry. Vol. 17, Oxford biology. New York: Oxford University Press Inc.; 2004. 249 p.Sherratt TN. The evolution of Müllerian mimicry. Naturwissenschaften. 2008;95:681–95.Kapan DD. Three-butterfly system provides a field test of Müllerian mimicry. 2001;409:338–40.Elias M, Gompert Z, Jiggins C, Willmott K. Mutualistic interactions drive ecological niche convergence in a diverse butterfly community. PLoS Biol [Internet]. 2008;6(12):2642–9. Available from: http://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.0060300Joron M. Polymorphic mimicry, microhabitat use, and sex-specific behaviour. J Evol Biol. 2005;18(3):547–56.Rojas B, Burdfield-Steel E, De Pasqual C, Gordon S, Hernández L, Mappes J, et al. Multimodal aposematic signals and their emerging role in mate attraction. Front Ecol Evol. 2018;6(93).De Bruyne M, Baker TC. Odor detection in insects: Volatile codes. J Chem Ecol. 2008;34(7):882–97.Missbach C, Dweck HKM, Vogel H, Vilcinskas A, Stensmyr MC, Hansson BS, et al. Evolution of insect olfactory receptors. Elife. 2014;3(e02115):1–22.Greenfield M. Signalers and receivers: mechanisms and evolution of arthropod communication. New York, USA: Oxford University Press; 2002.Ehman KD, Scott ME. Urinary odour preferences of MHC congenic female mice, Mus domesticus: Implications for kin recognition and detection of parasitized males. Anim Behav. 2001;62(4):781–9.Kavaliers M, Colwell DD, Braun WJ, Choleris E. Brief exposure to the odour of a parasitized male alters the subsequent mate odour responses of female mice. Anim Behav. 2003;65(1):59–68.Kavaliers M, Choleris E, Ågmo A, Pfaff DW. Olfactory-mediated parasite recognition and avoidance: Linking genes to behavior. Horm Behav. 2004;46(3):272–83.Kavaliers M, Choleris E, Ågmo A, Muglia LJ, Ogawa S, Pfaff DW. Involvement of the oxytocin gene in the recognition and avoidance of parasitized males by female mice. Anim Behav. 2005;70(3):693–702.Rich TJ, Hurst JL. The competing countermarks hypothesis: Reliable assessment of competitive ability by potential mates. Anim Behav. 1999;58(5):1027–37.Beynon RJ, Hurst JL. Multiple roles of major urinary proteins in the house mouse, Mus domesticus. Biochem Soc Trans. 2003;31(1):142–6.Czaczkes TJ, Grüter C, Ratnieks FLW. Trail pheromones: An integrative view of their role in social insect colony organization. Annu Rev Entomol. 2015;60(1):581–99.Estrada C, Schulz S, Yildizhan S, Gilbert LE. Sexual selection drives the evolution of antiaphrodisiac pheromones in butterflies. Evolution (N Y). 2011;65(10):2843–54.Schulz S, Estrada C, Yildizhan S, Boppré M, Gilbert LE. An antiaphrodisiac in Heliconius melpomene butterflies. J Chem Ecol. 2008;34(1):82–93.Nieberding CM, de Vos H, Schneider M V., Lassance J-M, Estramil N, Andersson J, et al. The male sex pheromone of the butterfly Bicyclus anynana: Towards an evolutionary analysis. PLoS One. 2008;3(7):e2751.Nieberding CM, Fischer K, Saastamoinen M, Allen CE, Wallin EA, Hedenström E, et al. Cracking the olfactory code of a butterfly: The scent of ageing. Ecol Lett. 2012;15(5):415–24.Dussourd DE, Harvis CA, Meinwald J, Eisner T. Pheromonal advertisement of a nuptial gift by a male moth (Utetheisa ornatrix). Proc Natl Acad Sci U S A [Internet]. 1991;88:9224–7. Available from: http://www.pnas.org/content/88/20/9224Shine R, Phillips B, Waye HL, LeMaster MP, Mason RT. Chemosensory cues allow courting male garter snakes to assess body length and body condition of potential mates. Behav Ecol. 2003;54:162–6.Moore PJ, Reagan-Wallin NL, Haynes KF, Moore AJ. Odour conveys status on cockroaches. Nature [Internet]. 1997;25–6. Available from: http://www.nature.com/nature/journal/v389/n6646/full/389025a0.htmlSmith BH. Recognition of female kin by male bees through olfactory signals. Proc Natl Acad Sci USA [Internet]. 1983;80:4551–4553. Available from: http://www.pnas.org/content/80/14/4551.full.pdfMas F, Jallon J-M. Sexual isolation and cuticular hydrocarbon differences between Drosophila santomea and Drosophila yakuba. J Chem Ecol. 2005;31(11):2747–52.Pardy JA, Rundle HD, Bernards MA, Moehring AJ. The genetic basis of female pheromone differences between Drosophila melanogaster and D. simulans. Heredity (Edinb) [Internet]. 2018;1. Available from: http://www.nature.com/articles/s41437-018-0080-3Linn C, Feder JL, Nojima S, Dambroski HR, Berlocher SH, Roelofs W. Fruit odor discrimination and sympatric host race formation in Rhagoletis. Proc Natl Acad Sci U S A. 2003;100(20):11490–3.Olsson SB, Linn CEJ, Feder JL, Michel A, Dambroski HR, Berlocher SH, et al. Comparing peripheral olfactory coding with host preference in the Rhagoletis species complex. Chem Senses. 2009;34:37–48.Tregenza T, Pritchard VL, Butlin RK. Patterns of trait divergence between populations of the meadow grasshopper, Chorthippus parallelus. Evolution (N Y). 2000;54(2):574–85.Schwander T, Arbuthnott D, Gries R, Gries G, Nosil P, Crespi BJ. Hydrocarbon divergence and reproductive isolation in Timema stick Insects. BMC Evol Biol [Internet]. 2013;13. Available from: BMC Evolutionary BiologyLiu Y, Hu Y, Bi J, Kong X, Long G, Zheng Y, et al. Odorant-binding proteins involved in sex pheromone and host-plant recognition of the sugarcane borer Chilo infuscatellus (Lepidoptera: Crambidae). Pest Manag Sci. 2020;10.1002/ps.5961.Pelozuelo L, Malosse C, Genestier G, Guenego H, Frerot B. Host-plant specialization in pheromone strains of the European corn borer Ostrinia nubilalis in France. J Chem Ecol. 2004;30(2):335–52.Ômura H, Yotsuzuka S. Male‐specific epicuticular compounds of the sulfur butterfly Colias erate poliographus (Lepidoptera: Pieridae). Appl Entomol Zool. 2015;Saveer AM, Becher PG, Birgersson G, Hansson BS, Witzgall P, Bengtsson M. Mate recognition and reproductive isolation in the sibling species Spodoptera littoralis and Spodoptera litura. Front Ecol Evol [Internet]. 2014;2(18):1–7. Available from: http://journal.frontiersin.org/article/10.3389/fevo.2014.00018/abstractSheck AL, Groot AT, Ward CM, Gemeno C, Wang J, Brownie C, et al. Genetics of sex pheromone blend differences between Heliothis virescens and Heliothis subflexa: A chromosome mapping approach. J Evol Biol. 2006;19(2):600–17.Marco A, Chivers DP, Kiesecker JM, Blaustein AR. Mate choice by chemical cues in Western Redback (Plethodon vehiculum) and Dunn’s (P. dunni) salamanders. Ethology [Internet]. 1998;104:781–8. Available from: http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0310.1998.tb00111.x/abstractMartín J, López P. Chemoreception, symmetry and mate choice in lizards. Proc R Soc B Biol Sci [Internet]. 2000;267:1265–9. Available from: http://rspb.royalsocietypublishing.org/content/267/1450/1265Novotny MV. Pheromones, binding proteins and receptor responses in rodents. Biochem Soc. 2003;117–22.Wyatt TD. Pheromones and animal behavior: chemical signals and signatures. Cambridge: Cambridge University Press; 2014.Phelan PL, Baker TC. Evolution of male pheromones in moths: repoductive isolation through sexual selection? Science (80- ). 1987;235:205–7.Löfstedt C, Herrebout WM, Menken SBJ. Sex pheromones and their potential role in the evolution of reproductive isolation in small ermine moths (Yponomeutidae). Chemoecology [Internet]. 1991;2:20–8. Available from: http://link.springer.com/article/10.1007/BF01240662 VN - readcube.comCostanzo K, Monteiro A. A The use of chemical and visual cues in female choice in the butterfly Bicyclus anynana. Proc R Soc B Biol Sci. 2007;274:845–51.Bigiani A, Mucignat-Caretta C, Montani G, Tirindelli R. Pheromone reception in mammals. Rev Physiol Biochem Pharmacol. 2005;155:1–35.Glover TJ, Tang XH, Roelofs WL. Sex-pheromone blend discrimination by male moths from E and Z-strains of European corn-borer. J Chem Ecol. 1987;13(1):143–51.Eltz T, Zimmermann Y, Pfeiffer C, Ramirez Pech J, Twele R, Francke W, et al. An olfactory shift is associated with male perfume differentiation and species divergence in orchid bees. Curr Biol [Internet]. 2008;18:1844– 8. Available from: http://dx.doi.org/10.1016/j.cub.2008.10.049Symonds MRE, Elgar MA. The evolution of pheromonal diversity. Trends Ecol Evol. 2008;23:220-228.Tanigaki T, Yamaoka R, Sota T. The role of cuticular hydrocarbons in mating and conspecific recognition in the closely related Longicorn beetles Pidonia grallatrix and P. takechii. Zoolog Sci. 2007;24(1):39–45.Geiselhardt S, Otte T, Hilker M. Looking for a similar partner: host plants shape mating preferences of herbivorous insects by altering their contact pheromones. Ecol Lett. 2012;15(9):971–7.Peterson MA, Dobler S, Larson EL, Juárez D, Schlarbaum T, Monsen KJ, et al. Profiles of cuticular hydrocarbons mediate male mate choice and sexual isolation between hybridising Chrysochus (Coleoptera: Chrysomelidae). Chemoecology. 2007;17(2):87–96.Xue HJ, Wei JN, Magalhães S, Zhang B, Song KQ, Liu J, et al. Contact pheromones of 2 sympatric beetles are modified by the host plant and affect mate choice. Behav Ecol. 2016;27(3):895–902.South A, LeVan K, Leombruni L, Orians CM, Lewis SM. Examining the role of cuticular hydrocarbons in Firefly species recognition. Ethology. 2008;114(9):916–24.Hay-Roe MM, Lamas G, Nation JL. Pre- and postzygotic isolation and Haldane rule effects in reciprocal crosses of Danaus erippus and Danaus plexippus (Lepidoptera: Danainae), supported by differentiation of cuticular hydrocarbons, establish their status as separate species. Biol J Linn Soc. 2007;91(3):445–53.Syvertsen TC, Jackson LL, Blomquist GJ, Vinson SB. Alkadienes mediating courtship in the parasitoid Cardiochiles nigriceps (Hymenoptera: Braconidae). J Chem Ecol. 1995;21(12):1971–89.Howard RW. Comparative analysis of cuticular hydrocarbons from the Ectoparasitoids Cephalonomia waterstoni and Laelius utilis (Hymenoptera: Bethylidae) and their respective hosts, Cryptolestes ferrugineus (Coleoptera: Cucujidae) and <i>Trogoderm. Ann Entomol Soc Am. 1992;85(3):317–25.Merrill RM, Dasmahapatra KK, Davey JW, Dell’Aglio DD, Hanly JJ, Huber B, et al. The diversification Heliconius butterflies: What have we learned in 150 years? J Evol Biol. 2015;28(8):1417–38.Jiggins CD. Ecological speciation in mimetic butterflies. Bioscience [Internet]. 2008;58(6):541–8. Available from: http://bioscience.oxfordjournals.org/cgi/doi/10.1641/B580610Mérot C. Speciation in Heliconius butterflies: the balance between mimicry convergence and ecological divergence. Muséum National d ́Histoire Naturelle, Paris.; 2014.Brower LP, Brower JVZ, Collins CT. Experimental studies of mimicry. 7. Relative palatability and Mullerian mimicry among neotropical butterflies of the subfamily Heliconiinae. Zool Sci Contrib New York Zool Soc. 1963;48(7):65–84.Chai P, Srygley RB. Predation and the flight, morphology, and temperature of Neotropical rain-forest butterflies. Am Nat. 1990;135(6):748–65.Darragh K. Pheromones in Heliconius butterflies: Chemical ecology, genetics, and behaviour. University of Cambridge; 2019.Arias M, Davey JW, Martin S, Jiggins C, Nadeau N, Joron M, et al. How do predators generalize warning signals in simple and complex prey communities? Insights from a videogame. Proc R Soc B Biol Sci. 2020;287:e20200014.Merrill RM, Van Schooten B, Scott JA, Jiggins CD. Pervasive genetic associations between traits causing reproductive isolation in Heliconius butterflies. Proc R Soc B. 2011;278:511–8.Darragh K, Vanjari S, Mann F, González-Rojas MF, Morrison CR, Salazar C, et al. Male sex pheromone components in Heliconius butterflies released by the androconia affect female choice. PeerJ [Internet]. 2017;5:e3953. Available from: https://peerj.com/articles/3953Rutowski R. The evolution of male mate-locating behavior in butterflies. Am Nat. 1991;138(5):1121–39.Mavárez J, Salazar CA, Bermingham E, Salcedo C, Jiggins CD, Linares M. Speciation by hybridization in Heliconius butterflies. Nature. 2006;441(7095):868–71.Jiggins CD, Estrada C, Rodrigues A. Mimicry and the evolution of premating isolation in Heliconius melpomene Linnaeus. J Evol Biol. 2004;17:680–91.Merrill RM, Rastas P, Martin SH, Melo MC, Barker S, Davey J, et al. Genetic dissection of assortative mating behavior. PLoS Biol. 2019;17(2):1–21.Boppré M. Chemically mediated interactions between butterflies. The biology of butterflies. Vane-Wright R, Ackery P, editors. Academic Press, London; 1984. 259–275 p.Pinheiro de Castro ÉC, Zagrobelny M, Zurano JP, Zikan Cardoso M, Feyereisen R, Bak S. Sequestration and biosynthesis of cyanogenic glucosides in passion vine butterflies and consequences for the diversification of their host plants. Ecol Evol. 2019;9:5079–93.Sculfort O, de Castro ECP, Kozak KM, Bak S, Elias M, Nay B, et al. Variation of chemical compounds in wild Heliconiini reveals ecological factors involved in the evolution of chemical defenses in mimetic butterflies. Ecol Evol. 2020;(November 2019):1–18.Darragh K, Byers KJRP, Merrill RM, McMillan WO, Schulz S, Jiggins CD. Male pheromone composition depends on larval but not adult diet in Heliconius melpomene. Ecol Entomol. 2019;44(3):397–405.de Castro ÉCP, Musgrove J, Bak S, McMillan WO, Jiggins CD. Phenotypic plasticity in chemical defence allows butterflies to diversify host use strategies. bioRxiv Prepr. 2020;Langham GM. Specialized avian predators repeatedly attack novel color morphs of Heliconius butterflies. Evolution (N Y). 2004;58(12):2783–7.Finkbeiner SD, Fishman DA, Osorio D, Briscoe AD. Ultraviolet and yellow reflectance but not fluorescence is important for visual discrimination of conspecifics by Heliconius erato. J Exp Biol [Internet]. 2017;220(7):1267–76. Available from: http://jeb.biologists.org/lookup/doi/10.1242/jeb.153593Mallet J, Barton NH. Strong natural selection in a warning-color hybrid zone. Evolution (N Y). 1989;43(2):421– 31.Kapan DD. Divergent natural selection and Müllerian mimicry in polymorphic Heliconius cydno (Lepidoptera:Nymphalidae). The University of British Columbia; 1998.Kronforst MR, Papa R. The functional basis of wing patterning in Heliconius butterflies: The molecules behind mimicry. Genetics. 2015;200:1–19.Linares M. The ghost of mimicry past: laboratory reconstitution of an extinct butterfly “race.” Heredity (Edinb). 1997;78:628–35.Mallet J. Shift happens! Shifting balance and the evolution of diversity in warning colour and mimicry. Ecol Entomol. 2010;35(SUPPL. 1):90–104.Fisher R. The genetical theory of natural selection. Oxford, U.K.: Oxford Univ. Press; 1930.Chouteau M, Angers B. Wright’s shifting balance theory and the diversification of aposematic signals. PLoS One. 2012;7(3):e34028.Márquez R, Linderoth TP, Mejía-Vargas D, Nielsen R, Amézquita A, Kronforst MR. Divergence, gene flow, and the origin of leapfrog geographic distributions: The history of colour pattern variation in Phyllobates poison- dart frogs. Mol Ecol. 2020;29:3702–19.Chouteau M, Llaurens V, Piron-Prunier F, Joron M. Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures. Proc Natl Acad Sci [Internet]. 2017;114(31):8325–9. Available from: http://www.pnas.org/lookup/doi/10.1073/pnas.1702482114Jamie GA, Meier JI. The persistence of polymorphisms across species radiations. Trends Ecol Evol [Internet]. 2020;35(9):795–808. Available from: https://doi.org/10.1016/j.tree.2020.04.007Nadeau NJ. Genes controlling mimetic colour pattern variation in butterflies. Curr Opin Insect Sci [Internet]. 2016;17:24–31. Available from: http://dx.doi.org/10.1016/j.cois.2016.05.013Lewis JJ, Reed RD. Genome-wide regulatory adaptation shapes population-level genomic landscapes in Heliconius. Mol Biol Evol. 2018;36(1):159–73.Orteu A, Jiggins CD. The genomics of coloration provides insights into adaptive evolution. Nat Rev Genet [Internet]. 2020;21(8):461–75. Available from: http://dx.doi.org/10.1038/s41576-020-0234-zMorris J, Hanly JJ, Martin SH, Van Belleghem SM, Salazar CA, Jiggins CD, et al. Deep convergence, shared ancestry, and evolutionary novelty in the genetic architecture of Heliconius mimicry. Genetics. 2020;216:765–80.Merrill RM, Wallbank RWR, Bull V, Salazar PCA, Mallet J, Stevens M, et al. Disruptive ecological selection on a mating cue. Proc R Soc B. 2012;279:4907–13.Mérot C, Frérot B, Leppik E, Joron M. Beyond magic traits: Multimodal mating cues in Heliconius butterflies. Evolution (N Y). 2015;69(11):2891–904.Rossi M, Hausmann AE, Thurman TJ, Montgomery SH, Papa R, Jiggins CD, et al. Visual mate preference evolution during butterfly speciation is linked to neural processing genes. Nat Commun [Internet]. 2020;11(4763). Available from: http://dx.doi.org/10.1038/s41467-020-18609-zArmstrong EA. The ethology of bird display and behavior. New York, NY: Dover Publications.; 1965.Gilliard ET. Birds of paradise and bower birds. Press NH, editor. Garden City, NY; 1969.Jones TM, Hamilton JGC. A role for pheromones in mate choice in a lekking sandfly. Anim Behav. 1998;56:891–8.Kotiaho JS. Testing the assumptions of conditional handicap theory: costs and condition dependence of a sexually selected trait. Behav Ecol Sociobiol. 2000;48:188–94.Milinski M, Bakker TCM. Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature. 1990;344:330–3.Pivnick KA, Lavoir-Dornik J, McNeil J. The role of the androconia in the mating behaviour of the European skipper, Thymelicus lineola, and evidence for a male sex pheromone. Physiol Entomol. 1992;17(October):260–8.Snedden WA, Sakaluk SK. Acoustic signalling and its relation to male mating success in sagebrush crickets. Anim Behav. 1992;44(4):633–9.Wing L. Drumming flight in the blue grouse and courtship characters of the Tetraonidae. Condor. 1946;48:154–7.Wertheim B, van Baalen E-JA, Dicke M, Vet LEM. Pheromone mediated aggregation in nonsocial arthropods: An evolutionary ecological perspective. Annu Rev Entomol. 2005;50(1):321–46.Schiestl FP. The evolution of floral scent and insect chemical communication. Ecol Lett. 2010;13(5):643–56.Ali MF, Morgan ED. Chemical communication in insect communities: a guide to insect pheromones with special emphasis on social insects. Biol Rev. 1990;65:227–247.Butenandt VA, Beckmann R, Stamm D, Hecker E. Über den sexual-lockstoff des seidenspinners Bombyx mori. Reindarstellung und Konstitution. Z Naturforsch. 1959;14b:283–4.Löfstedt C. Moth pheromone genetics and evolution. Philos Trans Biol Sci. 1993;340(1292):167–77.Smadja C, Butlin RK. On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity (Edinb). 2009;102:77–97.Wicker-Thomas C. Evolution of insect pheromones and their role in reproductive isolation and speciation. Ann la Soc Entomol Fr [Internet]. 2011;47(1–2):55–62. Available from: http://www.scopus.com/inward/record.url?eid=2-s2.0-80053962352&partnerID=tZOtx3y1Grillet M, Everaerts C, Houot B, Ritchie MG, Cobb M, Ferveur JF. Incipient speciation in Drosophila melanogaster involves chemical signals. Sci Rep. 2012;2(i):1–11.Vane-Wright RI, Boppré M. Visual and chemical signalling in butterflies: functional and phylogenetic perspectives. Philos Trans R Soc L B Biol Sci. 1993;340:197–205.Jiggins CD. The Ecology and Evolution of Heliconius Butterflies. Oxford University Press; 2017. 330 p.Rothschild M, Moore BP, Brown W V. Pyrazines as warning odour components in the Monarch butterfly, Danaus plexippus, and in moth of the genera Zygaena and Amata (Lepidoptera). Biol J Linn Soc. 1984;23:375–380.Müller F. The scent-scales of the male “Maracujá butterflies.” In: Longstaff GB, editor. Butterfly hunting in many lands. New York, NY: Longmans, Green & Co; 1912. p. 655–659.Eltringham H. On the abdominal glands in Heliconius (Lepidoptera). Trans R Entomol Soc Lond. 1925;73:269– 275.Barth R. Os órgäos odoriferos masculinos de alguns Heliconiinae do Brasil. Mem Inst Oswaldo Cruz. 1952;50:335–86.Klein AL, de Araújo AM. Courtship behavior of Heliconius erato phyllis (Lepidoptera, Nymphalidae) towards virgin and mated females: Conflict between attraction and repulsion signals? J Ethol. 2010;28(3):409–20.Crane J. Imaginal behaviour of a Trinidad butterfly, Heliconius erato hydara Hewitson, with special reference to the social use of color. Zool N Y. 1955;40:167–196.Estrada C, Yildizhan S, Schulz S, Gilbert LE. Sex-specific chemical cues from immatures facilitate the evolution of mate guarding in Heliconius butterflies. Proc R Soc B Biol Sci [Internet]. 2010;277:407–13. Available from: http://rspb.royalsocietypublishing.org/cgi/doi/10.1098/rspb.2009.1476Gilbert LE. Postmating female odor in Heliconius butterflies: A male-contributed antiaphrodisia? Science (80- ). 1976;193(4251):419–20.Malouines C. Counter-perfume: using pheromones to prevent female remating. Biol Rev. 2016;92(3):1570– 81.Mann F, Vanjari S, Rosser N, Mann S, Dasmahapatra KK, Corbin C, et al. The scent chemistry of Heliconius wing androconia. J Chem Ecol. 2017;43(9):843–57.Liénard MA, Wang H-L, Lassance J-M, Löfstedt C. Sex pheromone biosynthetic pathways are conserved between moths and the butterfly Bicyclus anynana. Nat Commun [Internet]. 2014;5:3957. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4050330&tool=pmcentrez&rendertype=abstr actYildizhan S, Van Loon J, Sramkova A, Ayasse M, Arsene C, ten Broeke C, et al. Aphrodisiac pheromones from the wings of the small cabbage white and large cabbage white butterflies, Pieris rapae and Pieris brassicae. ChemBioChem. 2009;10:1666–77.Andersson J, Borg-Karlson A-K, Vongvanich N, Wiklund C. Male sex pheromone release and female mate choice in a butterfly. J Exp Biol. 2007;210:964–70.Nishida R, Schulz S, Kim CS, Fukami H, Kuwahara Y, Honda K, et al. Male sex pheromone of a giant danaine butterfly, Idea leuconoe. J Chem Ecol [Internet]. 1996;22(5):949–72. Available from: http://dx.doi.org/10.1007/BF02029947Zhang YN, Xia YH, Zhu JY, Li SY, Dong SL. Putative pathway of sex pheromone biosynthesis and degradation by expression patterns of genes identified from female pheromone gland and adult antenna of Sesamia inferens (Walker). J Chem Ecol. 2014;40:439–51.Zhang YN, Xia YH, Zhu JY, Li SY, Dong SL. Putative pathway of sex pheromone biosynthesis and degradation by expression patterns of genes identified from female pheromone gland and adult antenna of Sesamia inferens (Walker). J Chem Ecol. 2014;40:439–51.He P, Zhang Y-F, Hong D-Y, Wang J, Wang X-L, Zuo L-H, et al. A reference gene set for sex pheromone biosynthesis and degradation genes from the diamondback moth, Plutella xylostella, based on genome and transcriptome digital gene expression analyses. BMC Genomics [Internet]. 2017;18(219). Available from: http://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-017-3592-yJurenka R. Insect pheromone biosynthesis. Top Curr Chem. 2004;239:97–131.Ando T, Inomata S, Yamamoto M. Lepidopteran Sex Pheromones. Top Curr Chem. 2004;239:51–96.Groot AT, Dekker T, Heckel DG. The genetic basis of pheromone evolution in moths. Annu Rev Entomol [Internet]. 2016;61:99–117. Available from: http://www.annualreviews.org/doi/10.1146/annurev-ento- 010715-023638Leary GP, Allen JE, Bunger PL, Luginbill JB, Linn CE, Macallister IE, et al. Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species. Proc Natl Acad Sci U S A. 2012;109(35):14081–6.Miura N, Nakagawa T, Touhara K, Ishikawa Y. Broadly and narrowly tuned odorant receptors are involved in female sex pheromone reception in Ostrinia moths. Insect Biochem Mol Biol [Internet]. 2010;40(1):64–73. Available from: http://dx.doi.org/10.1016/j.ibmb.2009.12.011Leal WS. Odorant reception in insects: Roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol. 2012;58:373–91.Corcoran JA, Jordan MD, Thrimawithana AH, Crowhurst RN, Newcomb RD. The peripheral olfactory repertoire of the lightbrown apple moth, Epiphyas postvittana. PLoS One. 2015;10(5):e0128596.Walker III WB, Gonzalez F, Garczynski SF, Witzgall P. The chemosensory receptors of codling moth Cydia pomonella – expression in larvae and adults. Sci Rep. 2016;6:23518.De Fouchier A, Walker WB, Montagné N, Steiner C, Binyameen M, Schlyter F, et al. Functional evolution of Lepidoptera olfactory receptors revealed by deorphanization of a moth repertoire. Nat Commun. 2017;8(15709).Zhang Y-N, Zhang L-W, Chen D-S, Liang S, Zhao-Qun L, Ye Z-F, et al. Molecular identification of differential expression genes associated with sex pheromone biosynthesis in Spodoptera exigua. Mol Genet Genomics. 2017;Groot AT, Staudacher H, Barthel A, Inglis O, Schöfl G, Santangelo RG, et al. One quantitative trait locus for intra- and interspecific variation in a sex pheromone. Mol Ecol. 2013;22:1065–80.Koutroumpa FA, Jacquin-Joly E. Sex in the night : Fatty acid-derived sex pheromones and corresponding membrane pheromone receptors in insects. Biochimie [Internet]. 2014;1–7. Available from: http://dx.doi.org/10.1016/j.biochi.2014.07.018Liu Y, Gu S, Zhang Y, Guo Y, Wang G. Candidate olfaction genes identified within the Helicoverpa armigera antennal transcriptome. PLoS One. 2012;7(10):e48260.Gu SH, Wu KM, Guo YY, Pickett JA, Field LM, Zhou JJ, et al. Identification of genes expressed in the sex pheromone gland of the black cutworm Agrotis ipsilon with putative roles in sex pheromone biosynthesis and transport. BMC Genomics [Internet]. 2013;14(636). Available from: BMC GenomicsJung CR, Kim Y. Comparative transcriptome analysis of sex pheromone glands of two sympatric lepidopteran congener species. Genomics [Internet]. 2014;103(4):308–15. Available from: http://dx.doi.org/10.1016/j.ygeno.2014.02.009Li RT, Ning C, Huang LQ, Dong JF, Li X, Wang CZ. Expressional divergences of two desaturase genes determine the opposite ratios of two sex pheromone components in Helicoverpa armigera and Helicoverpa assulta. Insect Biochem Mol Biol [Internet]. 2017;90:90–100. Available from: https://doi.org/10.1016/j.ibmb.2017.09.016Vogel H, Heidel AJ, Heckel DG, Groot AT. Transcriptome analysis of the sex pheromone gland of the noctuid moth Heliothis virescens. BMC Genomics. 2010;11(29):16–8.Xia YH, Zhang YN, Hou XQ, Li F, Dong SL. Large number of putative chemoreception and pheromone biosynthesis genes revealed by analyzing transcriptome from ovipositor-pheromone glands of Chilo suppressalis. Sci Rep. 2015;5:1–12.Svensson M. Sexual selection in moths: the role of chemical communication. Biol Rev [Internet]. 1996;71:113–35. Available from: http://onlinelibrary.wiley.com/doi/10.1111/j.1469- 185X.1996.tb00743.x/fullYildizhan S, van Loon J, Sramkova A, Ayasse M, Arsene C, ten Broeke C, et al. Aphrodisiac pheromones from the wings of the small cabbage white and large cabbage white butterflies, Pieris rapae and Pieris brassicae. ChemBioChem. 2009;10(10):1666–77.Mann F, Szczerbowski D, Silva L De, Mcclure M, Elias M, Schulz S. 3-Acetoxy-fatty acid isoprenyl esters from androconia of the ithomiine butterfly Ithomia salapia. Beilstein J Org Chem. 2020;16:2776–87.Wang HL, Brattström O, Brakefield PM, Francke W, Löfstedt C. Identification and biosynthesis of novel male specific esters in the wings of the tropical butterfly, Bicyclus martius sanaos. J Chem Ecol. 2014;40(6):549–59.Ozaki K, Utoguchi A, Yamada A, Yoshikawa H. Identification and genomic structure of chemosensory proteins (CSP) and odorant binding proteins (OBP) genes expressed in foreleg tarsi of the swallowtail butterfly Papilio xuthus. Insect Biochem Mol Biol [Internet]. 2008;38(11):969–76. Available from: http://dx.doi.org/10.1016/j.ibmb.2008.07.010Byers KJRP, Darragh K, Garza SF, Almeida DA, Warren IA, Rastas PMA, et al. Clusteing of loci controlling species differences in male chemical bouquets of sympatric Heliconius butterflies. bioRxiv Prepr. 2020;Beatty CD, Beirinckx K, Sherratt TN. The evolution of Müllerian mimicry in multispecies communities. Nature [Internet]. 2004;431(7004):63–66. Available from: http://www.nature.com/nature/journal/v431/n7004/abs/nature02818.htmlBeatty CD, Beirinckx K, Sherratt TN. The evolution of Müllerian mimicry in multispecies communities. Nature [Internet]. 2004;431(7004):63–66. Available from: http://www.nature.com/nature/journal/v431/n7004/abs/nature02818.htmlGavrilets S, Hastings A. Coevolutionary chase in two-species systems with applications to mimicry. J Theor Biol. 1998;191:415–27.Huheey JE. Studies in warning coloration and mimicry. VII. Evolutionary consequences of a Batesian- Müllerian spectrum: A model for Müllerian mimicry. Evolution (N Y) [Internet]. 1976;30(1):86–93. Available from: http://www.jstor.org/stable/2407675%5Cnhttp://www.jstor.org/stable/pdfplus/2407675.pdf?acceptTC=tr ueMérot C, Le Poul Y, Théry M, Joron M. Refining mimicry: phenotypic variation tracks the local optimum. J Anim Ecol. 2016;85(4):1056–69.Sheppard PM, Turner JRG. The existence of Müllerian Mimicry. Evolution (N Y). 1974;31:452–3.Joron M, Iwasa Y. The evolution of a Müllerian mimic in a spatially distributed community. J Theor Biol. 2005;237(1):87–103.Joron M. Mimicry. In: Cardé RT, Resh VH, editors. Encyclopedia of Insects. 2nd Editio. New York: Academic Press, New York.; 2009. p. 633–43.Joron M, Mallet JLB. Diversity in mimicry: Paradox or paradigm? Trends Ecol Evol. 1998;13(11):461–6.Mallet J, Joron M. Evolution of diversity in warning color and mimicry: Polymorphisms, shifting balance, and speciation. Annu Rev Ecol Syst [Internet]. 1999;30:201–33. Available from: http://www.annualreviews.org/doi/10.1146/annurev.ecolsys.30.1.201Ihalainen E, Lindström L, Mappes J, Puolakkainen S. Can experienced birds select for Müllerian mimicry? Behav Ecol. 2008;19(2):362–8.Ihalainen E, Lindström L, Mappes J, Puolakkainen S. Can experienced birds select for Müllerian mimicry? Behav Ecol. 2008;19(2):362–8.Langham GM. Rufous-tailed jacamars and aposematic butterflies: Do older birds attack novel prey? Behav Ecol. 2006;17(2):285–90.Ihalainen E, Rowland HM, Speed MP, Ruxton GD, Mappes J. Prey community structure affects how predators select for Müllerian mimicry. Proc R Soc B Biol Sci [Internet]. 2012;279(1736):2099–105. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3321702&tool=pmcentrez&rendertype=abstr actBenson WW. Natural Selection for Müllerian mimicry in Heliconius erato in Costa Rica. Science (80- ). 1972;176(4037):936–9.Chouteau M, Angers B. The role of predators in maintaining the geographic organization of aposematic signals. Am Nat. 2011;178(6):810–7.Owen DF, Smith DAS, Gordon IJ, Owixy AM. Polymorphic Müllerian mimicry in a group of African butterflies: a re-assessment of the relationship between Danaus chrysippus, Acraea encedon and Acraea encedana (Lepidoptera: Nymphalidae). J Zool. 1994;232(1):93–108.Gordon IJ, Smith DAS. Diversity in mimicry. Trends Ecol Evol. 1999;14(4):150–1.Chouteau M, Arias M, Joron M. Warning signals are under positive frequency-dependent selection in nature. Proc Natl Acad Sci [Internet]. 2016;113(8):2164–9. Available from: http://www.pnas.org/lookup/doi/10.1073/pnas.1519216113Mallet J, McMillan WO, Jiggins CD. Mimicry and warning colour at the boundary between races and species. In: Howard D, Berlocher S, editors. Endless forms Species and speciation [Internet]. Oxford, UK: Oxford University Press; 1998. p. 390–403. Available from: http://discovery.ucl.ac.uk/67729/Brower AVZ. A new mimetic species of Heliconius (Lepidoptera: Nymphalidae), from southeastern Colombia, revealed by cladistic analysis of mitochondrial DNA sequences. Zool J Linn Soc. 1996;116:317–32.Giraldo N, Salazar C, Jiggins CD, Bermingham E, Linares M. Two sisters in the same dress: Heliconius cryptic species. BMC Evol Biol. 2008;8(324).Mérot C, Mavárez J, Evin A, Dasmahapatra KK, Mallet J, Lamas G, et al. Genetic differentiation without mimicry shift in a pair of hybridizing Heliconius species (Lepidoptera: Nymphalidae). Biol J Linn Soc. 2013;109:830–47.Nadeau NJ, Ruiz M, Salazar P, Counterman B, Medina JA, Ortiz-Zuazaga H, et al. Population genomics of parallel hybrid zones in the mimetic butterflies, H. melpomene and H. erato. Genome Res [Internet]. 2014;24:1316–33. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24823669Rossato DO, Boligon D, Fornel R, Kronforst MR, Gonçalves GL, Moreira GRP. Subtle variation in size and shape of the whole forewing and the red band among co-mimics revealed by geometric morphometric analysis in Heliconius butterflies. Ecol Evol [Internet]. 2018;1–16. Available from: http://doi.wiley.com/10.1002/ece3.3916Van Belleghem SM, Alicea Roman PA, Carbia Gutierrez H, Counterman BA, Papa R. Perfect mimicry between Heliconius butterflies is constrained by genetics and development. Proc R Soc B Biol Sci [Internet]. 2020;287:20201267. Available from: https://royalsocietypublishing.org/doi/10.1098/rspb.2020.1267Rosser N. Speciation and biogeography of Heliconnine butterflies. 2012.de Castro ÉCP, Zagrobelny M, Cardoso MZ, Bak S. The arms race between heliconiine butterflies and Passiflora plants - new insights on an ancient subject. Biol Rev [Internet]. 2017; Available from: http://doi.wiley.com/10.1111/brv.12357Rohlf FJ. TPSDig. Stony Brook, NY: Department of Ecology and Evolution, State University of NY at Stony Brook; 2010.Adams D, Collyer M, Kaliontzopoulou A, Sherratt E. Geometric morphometric analyses of 2D/3D landmark data. https://cran.r-project.org/package=geomorph.; 2017.Bookstein F. Morphometrics tools for landmark data: Geometry and biology. New York, NY: Cambridge University Press; 1991.Zelditch ML, Swiderski DL, Sheets HD, Fink WL. Geometric morphometrics for biologist: a primer. San Diego, LA: Elsevier Academic Press; 2004.Hijmans RJ, Williams E, Vennes C. Package ‘geosphere.’ 2019.Friendly M, Fox J. Candisc: visualizing generalized canonical discriminant and canonical correlation analysis [Internet]. 2017. Available from: https://cran.r-project.org/package=candiscVan Belleghem SM, Papa R, Ortiz-Zuazaga H, Hendrickx F, Jiggins CD, McMillan WO, et al. Patternize : An R package for quantifying color pattern variation. Methods Ecol Evol. 2018;9:390–8.Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;11(7):671–5.Müller F. Ituna and Thyridia: a remarkable case of mimicry in butterflies. Trans Entomol Soc London. 1879;1879:20–29.Sbordoni V, Bullini L, Scarpelli G, Forestiero S, Rampini M. Mimicry in the burnet moth Zygaena ephialtes: population studies and evidence of a Batesian—Müllerian situation. Ecol Entomol. 1979;4:83–93.Niehuis O, Hofmann A, Naumann CM, Misof B. Evolutionary history of the burnet moth genus Zygaena Fabricius, 1775 (Lepidoptera: Zygaenidae) inferred from nuclear and mitochondrial sequence data: phylogeny, host-plant association, wing pattern evolution and historical biogeography. Biol J Linn Soc. 2007;92:501–20.Plowright RC, Owen RE. The evolutionary significance of bumble bee color patterns: a mimetic interpretation. Evolution (N Y). 1980;34(4):622–37.Williams P. The distribution of bumblebee colour patterns worldwide: possible significance for thermoregulation, crypsis, and warning mimicry. Biol J Linn Soc. 2007;92:97–118.Zrzavý J, Nedvěd O. Evolution of mimicry in the New World Dysdercus (Hemiptera: Pyrrhocoridae). J Evol Biol. 1999;12:956–69.Symula R, Schulte R, Summers K. Molecular phylogenetic evidence for a mimetic radiation in Peruvian poison frogs supports a Müllerian mimicry hypothesis. Proc R Soc B Biol Sci. 2001;268:2415–21.Chiari Y, Vences M, Vieites DR, Rabemananjara F, Bora P, Ramilijaona Ravoahangimalala O, et al. New evidence for parallel evolution of colour patterns in Malagasy poison frogs (Mantella). Mol Ecol. 2004;13:3763–74.Sanders KL, Malhotra A, Thorpe RS. Evidence for a Müllerian mimetic radiation in Asian pitvipers. Proc R Soc B Biol Sci. 2006;273:1135–41.Springer VG, Smith-Vaniz WF. Mimetic relationships involving fishes of the family Blenniidae. Smithson Contrib to Zool. 1972;(112):1–36.Dumbacher JP, Fleischer RC. Phylogenetic evidence for colour pattern convergence in toxic pitohuis: Müllerian mimicry in birds? Proc R Soc B Biol Sci. 2001;268:1971–6.Chittka L. Bee color vision is optimal for coding flower color, but flower colors are not optimal for being coded—why? Isr J Plant Sci. 1997;45:115–27.Roy BA, Widmer A. Floral mimicry: a fascinating yet poorly understood phenomenon. Trends Plant Sci. 1999;4(8):325–30.Benitez-Vieyra S, Hempel De Ibarra N, Wertlen AM, Cocucci AA. How to look like a mallow: Evidence of floral mimicry between Turneraceae and Malvaceae. Proc R Soc B Biol Sci. 2007;274:2239–48.Jones RT, Le Poul Y, Whibley AC, Mèrot C, Ffrench-Constant RH, Joron M. Wing shape variation associated with mimicry in butterflies. Evolution (N Y). 2013;67(8):2323–34.Montejo-Kovacevich G, Smith JE, Meier JI, Bacquet CN, Whiltshire-Romero E, Nadeau NJ, et al. Altitude and life-history shape the evolution of Heliconius wings. Evolution (N Y). 2019;73(12):2436–50.Mena S, Kozak KM, Cárdenas RE, Checa MF. Forest stratification shapes allometry and flight morphology of tropical butterflies. Proc R Soc B Biol Sci [Internet]. 2020;287:20201071. Available from: https://royalsocietypublishing.org/doi/10.1098/rspb.2020.1071Chazot N, Panara S, Zilbermann N, Blandin P, Le Poul Y, Cornette R, et al. Morpho morphometrics: Shared ancestry and selection drive the evolution of wing size and shape in Morpho butterflies. Evolution (N Y). 2015;70(1):181–94.Cespedes A, Penz CM, DeVries PJ. Cruising the rain forest floor: Butterfly wing shape evolution and gliding in ground effect. J Anim Ecol. 2015;84(3):808–16.Mendoza-Cuenca L, Macías-Ordóñez R. Foraging polymorphism in Heliconius charitonia (Lepidoptera: Nymphalidae): morphological constraints and behavioural compensation. J Trop Ecol. 2005;21:407–15.Mallet JLB, Jackson DA. The ecology and social behaviour of the Neotropical butterfly Heliconius xanthocles Bates in Colombia. Zool J Linn Soc. 1980;70:1–13.Reed RD, Papa R, Martin A, Hines HM, Counterman BA, Pardo-Diaz GC, et al. <i>Optix</> drives the repeated convergent evolution of butterfly wing pattern mimicry. Science (80- ). 2011;333(6046):1137–41.Lewis JJ, Van Belleghem SM. Mechanisms of change: a population-based perspective on the roles of modularity and pleiotropy in diversification. Front Ecol Evol. 2020;8:1–12.Wallbank RWR, Baxter SW, Pardo-Diaz C, Hanly JJ, Martin SH, Mallet J, et al. Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling. PLoS Biol. 2016;14(1):1–16.McMillan WO, Livraghi L, Concha C, Hanly JJ. From patterning genes to process: unraveling the gene regulatory networks that pattern Heliconius wings. Front Ecol Evol. 2020;8(221):1–15.Nadeau NJ, Pardo-Diaz GC, Whibley A, Supple MA, Saenko S V., Wallbank RWR, et al. The gene cortex controls mimicry and crypsis in butterflies and moths. Nature [Internet]. 2016;534(7605):106–10. Available from: http://dx.doi.org/10.1038/nature17961Martin A, Papa R, Nadeau NJ, Hill RI, Counterman BA, Halder G, et al. Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand. Proc Natl Acad Sci [Internet]. 2012;109(31):12632–7. Available from: http://www.pnas.org/cgi/doi/10.1073/pnas.1204800109Lewis JJ, Van Belleghem SM, Riccardo P, Danko CG, Reed RD. Many functionally connected loci foster adaptive diversification along a neotropical hybrid zone. Sci Adv. 2020;6:eabb8617.Moest M, Van Belleghem SM, James JE, Salazar C, Martin SH, Barker SL, et al. Selective sweeps on novel and introgressed variation shape mimicry loci in a butterfly adaptive radiation. Vol. 18, PLOS Biology. 2020. e3000597 p.Morris J, Navarro N, Rastas P, Rawlins LD, Sammy J, Mallet J, et al. The genetic architecture of adaptation: convergence and pleiotropy in Heliconius wing pattern evolution. Heredity (Edinb) [Internet]. 2019;123(2):138–52. Available from: http://dx.doi.org/10.1038/s41437-018-0180-0Papa R, Kapan DD, Counterman BA, Maldonado K, Lindstrom DP, Reed RD, et al. Multi-Allelic Major Effect Genes Interact with Minor Effect QTLs to Control Adaptive Color Pattern Variation in Heliconius erato. PLoS One. 2013;8(3):e57033.Concha C, Wallbank RWR, Hanly JJ, Fenner J, Livraghi L, Rivera ES, et al. Interplay between developmental flexibility and determinism in the evolution of mimetic Heliconius wing patterns. Curr Biol [Internet]. 2019;29:1–14. Available from: https://doi.org/10.1016/j.cub.2019.10.010Rowe C, Lindström L, Lyytinen A. The importance of pattern similarity between Müllerian mimics in predator avoidance learning. Proc R Soc B Biol Sci. 2004;271(1537):407–13.Ihalainen E, Lindström L, Mappes J. Investigating Müllerian mimicry: Predator learning and variation in prey defences. J Evol Biol. 2007;20(2):780–91.Rowland HM, Ihalainen E, Lindström L, Mappes J, Speed MP. Co-mimics have a mutualistic relationship despite unequal defences. Nature. 2007;448(7149):64–7.Finkbeiner SD, Briscoe AD, Mullen SP. Complex dynamics underlie the evolution of imperfect wing pattern convergence in butterflies. Evolution (N Y). 2017;71(4):949–59.Rutowski RL, Nahm AC, Macedonia JM. Iridescent hindwing patches in the Pipevine Swallowtail: Differences in dorsal and ventral surfaces relate to signal function and context. Funct Ecol. 2010;24(4):767–75.Su S, Lim M, Kunte K. Prey from the eyes of predators: Color discriminability of aposematic and mimetic butterflies from an avian visual perspective. Evolution (N Y). 2015;69(11):2985–94.Oliver JC, Robertson KA, Monteiro A. Accommodating natural and sexual selection in butterfly wing pattern evolution. Proc R Soc B Biol Sci. 2009;276(1666):2369–75.Robertson KA, Monteiro A. Female Bicyclus anynana butterflies choose males on the basis of their dorsal UV-reflective eyespot pupils. Proc R Soc B Biol Sci. 2005;272(1572):1541–6.De Bona S, Valkonen JK, López-Sepulcre A, Mappes J. Predator mimicry, not conspicuousness, explains the efficacy of butterfly eyespots. Proc R Soc B Biol Sci. 2015;282:20150202.DeVries PJ, Penz CM, Hill RI. Vertical distribution, flight behaviour and evolution of wing morphology in Morpho butterflies. J Anim Ecol. 2010;79:1077–85.Finkbeiner SD. Communal roosting in Heliconius butterflies (Nymphalidae): roost recruitment, establishment, fidelity, and resource use trends based on age and sex. J Lepid Soc. 2014;68(1):10–6.Willmott KR, Willmott JCR, Elias M, Jiggins CD. Maintaining mimicry diversity: optimal warning colour patterns differ among microhabitats in Amazonian clearwing butterflies. Proc R Soc B. 2017;284:20170744.Cuthill IC, Allen WL, Arbuckle K, Caspers B, Chaplin G, Hauber ME, et al. The biology of color. Science (80- ). 2017;357(6350):eaan0221.Arias M, Meichanetzoglou A, Elias M, Rosser N, De-Silva DL, Nay B, et al. Variation in cyanogenic compounds concentration within a Heliconius butterfly community: does mimicry explain everything? BMC Evol Biol [Internet]. 2016;16(272):1–10. Available from: http://dx.doi.org/10.1186/s12862-016-0843-5Coyne J., Orr H. Speciation. Sunderland, Massachusets: Sinauer Associates Inc, Sunderland, MA, USA.; 2004. 545 p.Wang L, Anderson DJ. Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature [Internet]. 2010;463(7278):227–31. Available from: http://www.nature.com/doifinder/10.1038/nature08678Hartlieb E, Anderson P. Olfactory-released behaviours. In: B.S. H, editor. Insect Olfaction. Berlin, Heidelberg: Springer; 1999. p. 315–49.Alves H, Rouault JD, Kondoh Y, Nakano Y, Yamamoto D, Kim YK, et al. Evolution of cuticular hydrocarbons of hawaiian Drosophilidae. Behav Genet. 2010;40(5):694–705.Estrada C, Gilbert LE. Host plants and immatures as mate-searching cues in Heliconius butterflies. Anim Behav [Internet]. 2010;80(2):231–9. Available from: http://dx.doi.org/10.1016/j.anbehav.2010.04.023Mérot C, Salazar C, Merrill RM, Jiggins CD, Joron M. What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies. Proc R Soc B Biol Sci. 2017;284:20170335.Darragh K, Montejo-Kovacevich G, Kozak KM, Morrison CR, Figueiredo CME, Ready JS, et al. Species specificity and intraspecific variation in the chemical profiles of Heliconius butterflies across a large geographic range. Ecol Evol Press [Internet]. 2019;00:1–25. Available from: https://www.biorxiv.org/content/10.1101/573469v1Merrill RM, Chia A, Nadeau NJ. Divergent warning patterns contribute to assortative mating between incipient Heliconius species. Ecol Evol. 2014;4(7):911–7.Kozak KM, Wahlberg N, Neild AFE, Dasmahapatra KK, Mallet J, Jiggins CD. Multilocus Species Trees Show the Recent Adaptive Radiation of the Mimetic Heliconius Butterflies. Syst Biol. 2015;64(3):505–24.Brower AVZ. Parallel race formation and the evolution of mimicry in Heliconius butterflies : A phylogenetic hypothesis from mitochondrial DNA sequences. Evolution (N Y). 1996;50(1):195–221.Jiggins CD, Linares M, Naisbit RE, Salazar C, Yang ZH, Mallet J. Sex-linked hybrid sterility in a butterfly. Evolution (N Y). 2001;55(8):1631–8.Sanchez AP, Pardo-Diaz GC, Enciso-Romero J, Muñoz A, Jiggins CD, Salazar C, et al. An introgressed wing pattern acts as a mating cues. Evolution (N Y). 2015;69(6):1619–29.Vanjari S, Mann F, Merrill R, Schulz S, Jiggins C. Male sex pheromone components in the butterfly Heliconius melpomene. bioRxiv. 2015;R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2016.Bates D, Maechler M, Bolker B, Walker S, Bojesen Christensen RH, Singmann H, et al. Linear Mixed-Effects Models using “Eigen” and S4. Journal of Statistical Software. 2015. p. 1–48.Wickham H. ggplot2 - Elegant Graphics for Data Analysis. 2nd ed. New York, NY: Springer-Verlag; 2009. 260 p.Fox J, Weisberg S. An R companion to applied regression. 2nd ed. Sage, editor. Thousand Oaks, CA; 2011. 449 p.Dorai-Raj S. binom: Binomial confidence intervals for several parameterizations [Internet]. 2014. Available from: http://cran.r-project.org/package=binomHench K, Vargas M, Höppner MP, McMillan WO, Puebla O. Inter-chromosomal coupling between vision and pigmentation genes during genomic divergence. Nat Ecol Evol. 2019;3(4):657–67.Bay RA, Arnegard ME, Conte GL, Best J, Bedford NL, McCann SR, et al. Genetic coupling of female mate choice with polygenic ecological divergence facilitates Stickleback speciation. Curr Biol. 2017;27(21):3344-3349.e4.Shahandeh MP, Pischedda A, Turner TL. Male mate choice via cuticular hydrocarbon pheromones drives reproductive isolation between Drosophila species. Evolution (N Y). 2017;72(1):123–35.Keller-Costa T, Canário AVM, Hubbard PC. Chemical communication in cichlids: A mini-review. Gen Comp Endocrinol [Internet]. 2015;221:64–74. Available from: http://dx.doi.org/10.1016/j.ygcen.2015.01.001Merrill RM, Gompert Z, Dembeck LM, Kronforst MR, McMillan WO, Jiggins CD. Mate preference across the speciation continuum in a clade of mimetic butterflies. Evolution (N Y). 2011;65(5):1489–500.Muñoz AG, Salazar C, Castaño J, Jiggins CD, Linares M. Multiple sources of reproductive isolation in a bimodal butterfly hybrid zone. J Evol Biol. 2010;23(6):1312–20.Southcott L, Kronforst M. Female mate choice is a reproductive isolating barrier in Heliconius butterflies : Ethology. 2018;124:862–8659.Larsdotter-Mellström H, Eriksson K, Liblikas I, Wiklund C, Borg-Karlson AK, Nylin S, et al. It’s all in the mix: Blend-specific behavioral response to a sexual pheromone in a butterfly. Front Physiol. 2016;7(68):1–10.Snellings Y, Herrera B, Wildemann B, Beelen M, Zwarts L, Wenseleers T, et al. The role of cuticular hydrocarbons in mate recognition in Drosophila suzukii. Sci Rep [Internet]. 2018;8(4996):1–11. Available from: http://dx.doi.org/10.1038/s41598-018-23189-6Rundle HD, Chenoweth SF, Doughty P, Blows MW. Divergent selection and the evolution of signal traits and mating preferences. PLoS Biol. 2005;3(11):1988–95.Grula J, McChesney J, Taylor O. Aphrodisiac pheromones of the sulfur butterflies Colias eurytheme and C. philodice (Lepidoptera, Pieridae). J Chem Ecol. 1980;6:241–56.Wago H. Studies on the Mating Behavior of the Pale Grass Blue, Zizeeria maha argia (Lepidoptera : Lycaenidae) III. Olfactory Cues in Sexual Discrimination by Males. Appl Ent Zool. 1978;13:283–9.Koutroumpa FA, Monsempes C, François M-C, de Cian A, Royer C, Concordet J-P, et al. Heritable genome editing with CRISPR/Cas9 induces anosmia in a crop pest moth. Sci Rep. 2016;6:29620.Counterman BA, Araujo-Perez F, Hines HM, Baxter SW, Morrison CM, Lindstrom DP, et al. Genomic hotspots for adaptation: The population genetics of Müllerian mimicry in Heliconius erato. PLoS Genet. 2010;6(2):e1000796.Counterman BA, Araujo-Perez F, Hines HM, Baxter SW, Morrison CM, Lindstrom DP, et al. Genomic hotspots for adaptation: The population genetics of Müllerian mimicry in Heliconius erato. PLoS Genet. 2010;6(2):e1000796.Hillier NK, Vickers NJ. The role of Heliothine hairpencil compounds in female Heliothis virescens (Lepidoptera: Noctuidae) behavior and mate acceptance. Chem Senses. 2004;29(6):499–511.Schulz S, Nishida R. The pheromone system of the male danaine butterfly, Idea leuconoe. Bioorg Med Chem. 1996;4(3):341–9.Albre J, Steinwender B, Newcomb RD. The evolution of desaturase gene regulation involved in sex pheromone production in Leafroller Moths of the genus Planotortrix. J Hered. 2013;104(5):627–38.Dopman EB, Robbins PS, Seaman A. Components of reproductive isolation between North American pheromone strains of the European corn borer. Evolution (N Y). 2010;64(4):881–902.Naisbit RE, Jiggins CD, Linares M, Salazar C, Mallet J. Hybrid sterility, Haldane’s rule and speciation in Heliconius cydno and H. melpomene. Genet Soc Am. 2002;161:1517–26.Edwards AWF. Likelihood. Cambridge University Press; 1972.Hummel HE, Miller T. Techniques in pheromone research. Springer Science and Business Media; 2012. 464 p.Hammer Ø, Harper DAT, Ryan PD. PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron [Internet]. 2001;4(1)(1):1–9. Available from: http://palaeo- electronica.org/2001_1/past/issue1_01.htmBurdfield-Steel E, Pakkanen H, Rojas B, Galarza JA, Mappes J. De novo synthesis of chemical defenses in an aposematic moth. J Insect Sci. 2018;18(2):1–4.Moore BP, Brown WV, Rothschild M. Methylalkylpyrazines in aposematic insects, their hostplants and mimics. Chemoecology. 1990;1(2):43–51.Kaye H, Mackintosch NJ, Rothschild M, Moore BP. Odour of pyrazine potentiates an association between environmental cues and unpalatable taste. Anim Behav. 1989;37:1–6.Coyne J, Orr H. Speciation. Sinauer Associates Inc, Sunderland, MA, USA.; 2004.Brand P, Hinojosa-Díaz IA, Ayala R, Daigle M, Yurrita Obiols CL, Eltz T, et al. The evolution of sexual signaling is linked to odorant receptor tuning in perfume-collecting orchid bees. Nat Commun [Internet]. 2020;11. Available from: http://dx.doi.org/10.1038/s41467-019-14162-6Löfstedt C, Wahlberg N, Millar JG. Evolutionary Patterns of Pheromone Diversity in Lepidoptera. In: Berkeley ed. JARC, editor. Pheromone Communication in Moths : Evolution, Behavior and Application. University of California Press; 2016. p. 43-78.Byers KJRP, Darragh K, Musgrove J, Abondano Almeida D, Garza SF, Warren IA, et al. A major locus controls a biologically active pheromone component in Heliconius melpomene. Evolution (N Y). 2020;1–16.Conner W, Iyengar V. Male pheromones in moths. In pheromone communication. In: Allison J, Ring C, editors. Evolution, Behavior and Application. Berkeley: University of California Press; 2016. p. 191–208.Aldrich JR, Blum MS, Duffey SS, Fales HM. Male specific natural products in the bug, Leptoglossus phyllopus: Chemistry and possible function. J Insect Physiol. 1976;22(9):1201–6.Morgan ED. Biosynthesis in insects: advanced edition. Royal Society of Chemistry, editor. RSC Publishing; 2010. 362 p.Meyer HJ, Norris DM. Vanillin and Syringaldehyde as attractants (Coleoptera: Scolytidae). Ann Entomol Soc Am. 1967;60(4):858–9.Seenivasagan T, Sharma KR, Sekhar K, Ganesan K, Prakash S, Vijayaraghavan R. Electroantennogram, flight orientation, and oviposition responses of Aedes aegypti to the oviposition pheromone n-heneicosane. Parasitol Res. 2009;104:827–33.Simmons LW, Alcock J, Reeder A. The role of cuticular hydrocarbons in male attraction and repulsion by female Dawson’s burrowing bee, Amegilla dawsoni. Anim Behav. 2003;66:677–85.Combs PA, Krupp JJ, Khosla NM, Bua D, Petrov DA, Levine JD, et al. Tissue-specific cis-regulatory divergence implicates eloF in inhibiting interspecies mating in Drosophila. Curr Biol. 2018;28(24):3969-3975.e3.Kost S, Heckel DG, Yoshido A, Groot AT. A Z-linked sterility locus causes sexual abstinence in hybrid females and facilitates speciation in Spodoptera frugiperda. Evolution (N Y). 2016;70(6):1418–27.Smadja CM, Butlin RK. A framework for comparing processes of speciation in the presence of gene flow. Mol Ecol. 2011;20(24):5123–40.Seehausen O, Takimoto G, Roy D, Jokela J. Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol Ecol. 2008;17:30 – 44.Southcott L, Kronforst M. Female mate choice is a reproductive isolating barrier in Heliconius butterflies. Ethology. 2018;124:862–8659.Gleason JM, James RA, Wicker-Thomas C, Ritchie MG. Identification of quantitative trait loci function through analysis of multiple cuticular hydrocarbons differing between Drosophila simulans and Drosophila sechellia females. Heredity (Edinb) [internet] 2009, 103(5):416-24. Available from: http:dx.doi.org/10.1038/hdy.2009.79Teal PEA, Tumlinson JH. Effects of interspecific hybridization between Heliothis virescens and H. subflexa on the sex pheromone communication system. Insect Physol. 1997;41:519–25.Constantino LM, Salazar JA. Natural hybridization of Heliconius cydno Doubleday from Western Colombia (Lepidoptera: Nymphalidae: Heliconiinae). Bol Cient del Mus Hist Nat Univ Caldas. 1998;2(June):41–5.instname:Universidad del Rosarioreponame:Repositorio Institucional EdocURMariposas del género HeliconiusAnálisis del mimetismo batesiano y mülleriano de los HeliconiusSistema de identificación entre mariposas comimeticasIdentificación de señales químicas distintivas entre especies distintas de HeliconiusInvertebrados592600Butterflies of the genus HeliconiusAnalysis of the Batesian and Müllerian mimicry of the HeliconiusIdentification system between comimetic butterfliesIdentification of distinctive chemical signals between species other than HeliconiusIntra and inter-specific communication in HeliconiusComunicación intra e inter-específica en HeliconiusdoctoralThesisMonografíaTesis de doctoradohttp://purl.org/coar/resource_type/c_db06Escuela de Medicina y Ciencias de la SaludORIGINALTesis_doctoral_Gonzalez.pdfTesis_doctoral_Gonzalez.pdfapplication/pdf47487378https://repository.urosario.edu.co/bitstreams/c4db6bfa-15cc-4456-9fe7-f3407e861f75/download7979f5f07dac7271904e62107ed6a361MD51CC-LICENSElicense_rdflicense_rdfapplication/rdf+xml; charset=utf-8805https://repository.urosario.edu.co/bitstreams/027db425-1871-42e8-a1cf-d5c8550b5391/downloaddab767be7a093b539031785b3bf95490MD53LICENSElicense.txtlicense.txttext/plain1475https://repository.urosario.edu.co/bitstreams/9c5c507a-af9a-487a-b52f-8b3856bc5f72/downloadfab9d9ed61d64f6ac005dee3306ae77eMD52TEXTTesis_doctoral_Gonzalez.pdf.txtTesis_doctoral_Gonzalez.pdf.txtExtracted texttext/plain437767https://repository.urosario.edu.co/bitstreams/e6627ea9-3326-4bef-81c0-87cc57643ead/downloadd6d4c54dbc7dfc587573ccf4995282f1MD54THUMBNAILTesis_doctoral_Gonzalez.pdf.jpgTesis_doctoral_Gonzalez.pdf.jpgGenerated Thumbnailimage/jpeg2288https://repository.urosario.edu.co/bitstreams/83a4f96f-a336-4ae1-b827-8045fc3d9175/download2ed63ca5c588c28325926468d7d5e6cdMD5510336/30934oai:repository.urosario.edu.co:10336/309342021-02-18 03:03:14.013http://creativecommons.org/licenses/by-nd/2.5/co/Atribución-SinDerivadas 2.5 Colombiahttps://repository.urosario.edu.coRepositorio institucional EdocURedocur@urosario.edu.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

Intra and inter-specific communication in Heliconius

Publicaciones similares