[en] Although phylogenetically nested within the moths, butterflies have diverged extensively in a number of life history traits. Whereas moths rely greatly on chemical signals, visual advertisement is the hallmark of mate finding in butterflies. In the context of courtship, however, male chemical signals are widespread in both groups although they likely have multiple evolutionary origins. Here, we report that in males of the butterfly Bicyclus anynana, courtship scents are produced de novo via biosynthetic pathways shared with females of many moth species. We show that two of the pheromone components that play a major role in mate choice, namely the (Z)-9-tetradecenol and hexadecanal, are produced through the activity of a fatty acyl Delta11-desaturase and two specialized alcohol-forming fatty acyl reductases. Our study provides the first evidence of conservation and sharing of ancestral genetic modules for the production of FA-derived pheromones over a long evolutionary timeframe thereby reconciling mate communication in moths and butterflies.
Disciplines :
Life sciences: Multidisciplinary, general & others
Author, co-author :
Lienard, Marjorie ; Université de Liège - ULiège > GIGA > GIGA Molecular Biology of Diseases ; Université de Liège - ULiège > Département des sciences de la vie
Wang, Hong-Lei; Department of Biology, Pheromone Group, Lund University, Lund SE-22362,
Lassance, Jean-Marc ✱; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA) > Génomique animale ; 1] Department of Biology, Pheromone Group, Lund University, Lund
Lofstedt, Christer ✱; 1] Department of Biology, Pheromone Group, Lund University, Lund
✱ These authors have contributed equally to this work.
Language :
English
Title :
Sex pheromone biosynthetic pathways are conserved between moths and the butterfly Bicyclus anynana.
Nieukerken, E. J. v. et al. in Animal Biodiversity: An Outline Of Higher-Level Classification And Survey Of Taxonomic Richness. (ed. Zhang, Z.-Q.) Vol. 3148, 212-221 (Zootaxa, 2011).
Wahlberg, N., Wheat, C. & Pena, C. Timing and patterns in the taxonomic diversification of Lepidoptera (butterflies and moths). PLoS ONE 8, e80875 (2013).
Grimaldi, D. & Engel, M. Evolution of the insects (Cambridge University Press, 2005).
Heikkila ̈, M., Kaila, L., Mutanen, M., Pena, C. & Wahlberg, N. Cretaceous origin and repeated tertiary diversification of the redefined butterflies. Proc. R. Soc. Lond. Ser. B Biol. Sci 279, 1093-1099 (2012).
Scoble, M. The Lepidoptera: Form, Function and Diversity (Oxford University Press, 1992).
Greenfield, M. D. Senders and Receivers (Oxford University Press, 2002).
Boppre , M. in The Biology of Butterflies. (eds Vanewright, R. I. & Ackey, P. R.) 259-275 (Academic Press, 1984).
Vane-Wright, R. & Boppre, M. Visual and chemical signalling in butterflies: functional and phylogenetic perspectives. Proc. R. Soc. B Biol. Sci. 340, 197-205 (1993).
Dasmahapatra, K. et al. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487, 94-98 (2012).
Heinze, S. Sun. Compass integration of skylight cues in migratory monarch butterflies. Neuron 69, 345-358 (2011).
Carlsson, M. A., Scha ̈pers, A., Näsel, D. R. & Janz, N. Organization of the olfactory system of Nymphalidae butterflies. Chem. Senses 38, 355-367 (2013).
Andersson, J., Borg-Karlson, A.-K., Vongvanich, N. & Wiklund, C. Male sex pheromone release and female mate choice in a butterfly. J. Exp. Biol. 210, 964-970 (2007). (Pubitemid 46650600)
Nieberding, C. et al. Cracking the olfactory code of a butterfly: the scent of ageing. Ecol. Lett. 15, 415-424 (2012).
Birch, M. & Poppy, G. Scents and eversible scent structures of male moths. Annu. Rev. Entomol. 35, 25-58 (1990). (Pubitemid 120024483)
Nishida, R. et al. Male sex pheromone of a giant danaine butterfly, Idea leuconoe. J. Chem. Ecol. 22, 949-972 (1996). (Pubitemid 26344319)
Pliske, T. & Eisner, T. Sex pheromone of the queen butterfly: biology. Science 164, 1170-1172 (1969).
Phelan, P. L. in The Evolution of Mating Systems in Insects and Arachnids. (eds Choe, J. C. & Crespi, B. J.) 240-256 (Cambridge University Press, 1997).
Nieberding, C. M. et al. The male sex pheromone of the butterfly Bicyclus anynana: towards an evolutionary analysis. PLoS ONE 3, 7 (2008).
Costanzo, K. & Monteiro, A. The use of chemical and visual cues in female choice in the butterfly Bicyclus anynana. Proc. Biol. Sci 274, 845-851 (2007). (Pubitemid 47056765)
El-Sayed, A. M. The Pherobase: Database of Insect pheromones and semiochemicals http://www.pherobase.com (2010).
Ando, T., Inomata, S.-I. & Yamamoto, M. Lepidopteran sex pheromones. Top. Curr. Chem. 239, 51-96 (2004).
Shanklin, J. & Cahoon, E. B. Desaturation and related modifications of fatty acids. Ann. Rev. Plant Physiol. Mol. Biol. 49, 611-641 (1998).
Dallerac, R. et al. A D9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 97, 9449-9454 (2000). (Pubitemid 30650795)
Chertemps, T., Duportets, L., Labeur, C., Ueyama, M. & Wicker-Thomas, C. A female-specific desaturase gene responsible for diene hydrocarbon biosynthesis and courtship behaviour in Drosophila melanogaster. Insect Mol. Biol. 15, 465-473 (2006). (Pubitemid 44166568)
Buček, A. et al. The role of desaturases in the biosynthesis of marking pheromones in bumblebee males. Insect Biochem. Mol. Biol. 43, 724-731 (2013).
Knipple, D. C., Rosenfield, C.-L., Nielsen, R., You, K. M. & Jeong, S. E. Evolution of the integral membrane desaturase gene family in moths and flies. Genetics 162, 1737-1752 (2002). (Pubitemid 36114659)
Roelofs, W. L. & Rooney, A. P. Molecular genetics and evolution of pheromone biosynthesis in Lepidoptera. Proc. Natl Acad. Sci. USA 100, 9179-9184 (2003). (Pubitemid 37033903)
Lie & acute;nard, M. A., Strandh, M., Hedenstrom, E., Johansson, T. & Löfstedt, C. Key biosynthetic gene subfamily recruited for pheromone production prior to the extensive radiation of Lepidoptera. BMC Evol. Biol. 8, 270 (2008).
Tillman, J. A., Seybold, S. J., Jurenka, R. A. & Blomquist, G. J. Insect pheromones-an overview of biosynthesis and endocrine regulation. Insect Biochem. Mol. Biol. 29, 481-514 (1999). (Pubitemid 29297127)
Blomquist, G. J., Jurenka, R. A., Schal, C. & Tittiger, C. in Comprehensive Molecular Insect Science Vol. 3 (eds Gilbert, L. I., Iatrou, K. & Gill, S.) 705-751 (Elsevier Academic Press, 2005).
Roelofs, W. L. et al. Evolution of moth sex pheromones via ancestral genes. Proc. Natl Acad. Sci. USA 99, 13621-13626 (2002). (Pubitemid 35215430)
Wang, H.-L., Lie & acute;nard, M. A., Zhao, C.-H., Wang, C.-Z. & Lo & dir;;fstedt, C. Neofunctionalization in an ancestral insect desaturase lineage led to rare D6 pheromone signals in the Chinese tussah silkworm. Insect Biochem. Mol. Biol. 40, 742-751 (2010).
Liu, W., Rooney, A. P., Xue, B. & Roelofs, W. L. Desaturases from the spotted fireworm moth (Choristoneura parallela) shed light on the evolutionary origins of novel moth sex pheromone desaturases. Gene 342, 303-311 (2004). (Pubitemid 39452349)
Matousková, P., Pichov & acute;, I. & Svatos & coron;, A. Functional characterization of a desaturase from the tobacco hornworm moth (Manduca sexta) with bifunctional Z11- and 10,12-desaturase activity. Insect Biochem. Mol. Biol. 37, 601-610 (2007). (Pubitemid 46756316)
Moto, K. et al. Involvement of a bifunctional fatty-acyl desaturase in the biosynthesis of the silkmoth, Bombyx mori, sex pheromone. Proc. Natl Acad. Sci. USA 101, 8631-8636 (2004). (Pubitemid 38745822)
Serra, M., Pina, B., Abad, J. L., Camps, F. & Fabriás, G. A multifunctional desaturase involved in the biosynthesis of the processionary moth sex pheromone. Proc. Natl Acad. Sci. USA 104, 16444-16449 (2007). (Pubitemid 350211039)
Doan, T. T. P. et al. Functional expression of five Arabidopsis fatty acyl-CoA reductase genes in Escherichia coli. J. Plant Physiol. 166, 787-796 (2009).
Rowland, O. et al. CER4 encodes an alcohol-forming fatty acyl-coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiol. 142, 866-877 (2006). (Pubitemid 44764615)
Teerawanichpan, P. & Qiu, X. Molecular and functional analysis of three fatty acyl-CoA reductases with distinct substrate specificities in copepod Calanus finmarchicus. Mar. Biotechnol. 14, 227-236 (2012).
Teerawanichpan, P. & Qiu, X. Fatty acyl-CoA reductase and wax synthase from Euglena gracilis in the biosynthesis of medium-chain wax esters. Lipids 45, 263-273 (2010).
Teerawanichpan, P., Robertson, A. J. & Qiu, X. A fatty acyl-CoA reductase highly expressed in the head of honey bee (Apis mellifera) involves biosynthesis of a wide range of aliphatic fatty alcohols. Insect Biochem. Mol. Biol. 40, 641-649 (2010).
Moto, K. et al. Pheromone gland-specific fatty-acyl reductase of the silkmoth, Bombyx mori. Proc. Natl Acad. Sci. USA 100, 9156-9161 (2003). (Pubitemid 37033899)
Liénard, M. A., Hagstro & dir;m, A. K., Lassance, J.-M. & Löfstedt, C. Evolution of multi-component pheromone signals in small ermine moths involves a single fatty-acyl reductase gene. Proc. Natl Acad. Sci. USA 107, 10955-10960 (2010).
Lassance, J.-M. et al. Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones. Nature 466, 486-489 (2010).
Lassance, J.-M. et al. Functional consequences of sequence variation in the pheromone biosynthetic gene pgFAR for Ostrinia moths. Proc. Natl Acad. Sci. USA 110, 3967-3972 (2013).
Hagstro & die;m, A., Lie & acute;nard, M., Groot, A., Hedenstro & die;m, E. & Lo & die;fstedt, C. Semi-selective fatty acyl reductases from four heliothine moths influence the specific pheromone composition. PLoS ONE 7, e37230 (2012).
Hellenbrand, J., Biester, E.-M., Gruber, J., Hamberg, M. & Frentzen, M. Fatty acyl-CoA reductases of birds. BMC Biochem. 12, 64 (2011).
Cheng, J. B. & Russell, D. W. Mammalian wax biosynthesis. J. Biol. Chem. 279, 37789-37797 (2004).
Estrada, C., Schulz, S., Yildizhan, S. & Gilbert, L. Sexual selection drives the evolution of antiaphrodisiac pheromones in butterflies. Evolution 65, 2843-2854 (2011).
Schulz, S., Yildizhan, S. & van Loon, J. The biosynthesis of hexahydrofarnesylactone in the butterfly Pieris brassicae. J. Chem. Ecol. 37, 360-363 (2011).
Zhan, S., Merlin, C., Boore, J. & Reppert, S. The monarch butterfly genome yields insights into long-distance migration. Cell 147, 1171-1185 (2011).
Shirangi, T. R., Dufour, H. D., Williams, T. M. & Carroll, S. B. Rapid evolution of sex pheromone-producing enzyme expression in Drosophila. PLoS Biol. 7, e1000168 (2009).
Rosenfield, C.-L., You, K. M., Herrick-Marsella, P., Roelofs, W. L. & Knipple, D. C. Structural and functional conservation and divergence among acyl-CoA desaturases of two noctuid species, the corn earworm, Helicoverpa zea, and the cabbage looper, Trichoplusia ni. Insect Biochem. Mol. Biol. 31, 949-964 (2001). (Pubitemid 32785896)
Liénard, M. et al. Elucidation of the sex-pheromone biosynthesis producing 5,7-dodecadienes in Dendrolimus punctatus (Lepidoptera: Lasiocampidae) reveals D11- and D9-desaturases with unusual catalytic properties. Insect Biochem. Mol. Biol. 40, 440-452 (2010).
Papanicolaou, A., Gebauer-Jung, S., Blaxter, M., McMillan, O. & Jiggins, C. ButterflyBase: a platform for lepidopteran genomics. Nucleic Acids Res. 36, D582-D587 (2008). (Pubitemid 351149789)
Knipple, D. C. et al. Cloning and functional expression of a cDNA encoding a pheromone gland-specific acyl-CoA D11-desaturase of the cabbage looper moth, Trichoplusia ni. Proc. Natl Acad. Sci. USA 95, 15287-15292 (1998). (Pubitemid 29018691)
Bjostad, L. B., Wolf, W. & Roelofs, W. L. in Pheromone Biochemistry. (eds Blomquist, G. J. & Prestwich, G. D.) 77-120 (Academic Press, 1987).
Schulz, S., Estrada, C., Yildizhan, S., Boppre, M. & Gilbert, L. An antiaphrodisiac in Heliconius melpomene Butterflies. J. Chem. Ecol. 34, 82-93 (2008).
Symonds, M. R. E. & Elgar, M. A. The evolution of pheromone diversity. Trends Ecol. Evol. 23, 220-228 (2008).
Zhang, J. Evolution by gene duplication: an update. Trends Ecol. Evol. 18, 292-298 (2003). (Pubitemid 36631749)
Hughes, A. L. The evolution of functionally novel proteins after gene duplication. Proc. Biol. Sci. 256, 119-124 (1994). (Pubitemid 24168165)
Lassance, J.-M. & Lo & die;fstedt, C. Concerted evolution of male and female display traits in the European corn borer, Osrinia nubilalis.. BMC Biol. 10, 7 (2009).
Symonds, M. R. E. & Elgar, M. A. The mode of pheromone evolution: evidence from bark beetles. Proc. Biol. Sci. 271, 839-846 (2004). (Pubitemid 38491271)
Bjostad, L. & Roelofs, W. Sex pheromone biosynthetic precursors in Bombyx mori. Insect Biochem. 14, 275-278 (1984).
Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (1997). (Pubitemid 27359211)
Kearse, M. et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647-1649 (2012).
Katoh, S. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780 (2013).
Guindon, S. & Pascual, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704 (2003). (Pubitemid 37365050)
Milne, I. et al. TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 25, 126-127 (2009).
Zhang, H., Gao, S., Lercher, M., Hu, S. & Chen, W.-H. EvolView, an online tool for visualizing, annotating and managing phylogenetic trees. Nucleic Acids Res. 40, W569-W572 (2012).