Abstract
Insect genes encoding odorant receptors (ORs) and odorant-binding proteins (OBPs) comprise Lepidoptera (moths and butterflies)-specific subfamilies named pheromone receptors (PRs) and pheromone-binding proteins (PBPs), respectively. Both subfamilies are monophyletic, and some of the genes in these groups are responsible for sex pheromone recognition. Recent progress in sequencing by next-generation sequencers has facilitated the detection of gains, losses, and translocations of these genes, which have occurred in a wide variety of lepidopteran lineages. The evolutionary history of these genes provides valuable insights into how the sex pheromone recognition system has evolved in Lepidoptera.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Bengtsson JM, Trona F, Montagne N et al (2012) Putative chemosensory receptors of the codling moth, Cydia pomonella, identified by antennal transcriptome analysis. PLoS One 7:e31620
Benton R, Vannice KS, Gomez-Diaz C et al (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136:149–162
Brand P, Robertson HM, Lin W et al (2018) The origin of the odorant receptor gene family in insects. elife 7:e38340
Briscoe AD, Macias-Munoz A, Kozak KM et al (2013) Female behaviour drives expression and evolution of gustatory receptors in butterflies. PLoS Genet 9:E1003620
Challis RJ, Kumar S, Dasmahapatra KK et al (2016) Lepbase: the Lepidopteran genome database. bioRxiv preprint. https://doi.org/10.1101/056994
Chipman AD, Ferrier DEK, Brena C et al (2014) The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima. PLoS Biol 12:e1002005
Croset V, Rytz R, Cummins SF et al (2010) Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet 6:e1001064
Dopman EB, Bogdanowicz SM, Harrison RG (2004) Genetic mapping of sexual isolation between E and Z pheromone strains of the European corn borer (Ostrinia nubilalis). Genetics 167:301–309
Engsontia P, Sangket U, Chotigeat W (2014) Molecular evolution of the odorant and gustatory receptor genes in lepidopteran insects: implications for their adaptation and speciation. J Mol Evol 79:21–39
Eyun SI, Soh HY, Posavi M et al (2017) Evolutionary history of chemosensory-related gene families across the arthropoda. Mol Biol Evol 34:1838–1862
Gohl T, Krieger J (2006) Immunolocalization of a candidate pheromone receptor in the antenna of the male moth, Heliothis virescens. Invertebr Neurosci 6:13–21
Gong D, Zhang H, Zhao P et al (2009) The odorant binding protein gene family from the genome of silkworm, Bombyx mori. BMC Genomics 10:332
Gould F, Estocka M, Hillierb NK et al (2010) Sexual isolation of male moths explained by a single pheromone response QTL containing four receptor genes. Proc Natl Acad Sci U S A 107:8660–8665
Grosse-Wilde E, Kuebler LS, Bucks S, Vogel H, Wicher D, Hansson BS et al (2011) Antennal transcriptome of Manduca sexta. Proc Natl Acad Sci 108:7449–7454. https://doi.org/10.1073/pnas.1017963108. PMID:21498690
Gulia-Nuss M, Nuss AB, Meyer JM et al (2016) Genomic insights into the Ixodes scapularis tick vector of Lyme disease. Nat Commun 7:10507
Leal WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58:373–391
Liénard MA, Wang HL, Lassance JM et al (2014) Sex pheromone biosynthetic pathways are conserved between moths and the butterfly Bicyclus anynana. Nat Commun 5:3957
Liu Y, Gu S, Zhang Y et al (2012) Candidate olfaction genes identified within the Helicoverpa armigera antennal transcriptome. PLoS One 7:e48260
Missbach C, Dweck HK, Vogel H et al (2014) Evolution of insect olfactory receptors. elife 3:e02115
Miura N, Nakagawa T, Tatsuki S et al (2009) A male-specific odorant receptor conserved through the evolution of sex pheromones in Ostrinia moth species. Int J Biol Sci 5:319–330
Nei M, Niimura Y, Nozawa M (2008) The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat Rev Genet 9:951–963
Nieberding CM, de Vos H, Schneider MV et al (2008) The male sex pheromone of the butterfly Bicyclus anynana: towards an evolutionary analysis. PLoS One 3(7):e2751
Regier JC, Mitter C, Zwick A et al (2013) A large-scale, higher-level, molecular phylogenetic study of the insect order Lepidoptera (moths and butterflies). PLoS One 8:e58568
Robertson HM (2015) The insect chemoreceptor superfamily is ancient in animals. Chem Senses 40:609–614
Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor superfamily in Drosophila melanogaster. Proc Natl Acad Sci U S A 100:173–180
Rytz R, Croset V, Benton R (2013) Ionotropic Receptors (IRs): chemosensory ionotropic glutamate receptors in Drosophila and beyond. Insect Biochem Mol Biol 43:888–897
Saina M, Busengdal H, Sinigaglia C et al (2015) A cnidarian homologue of an insect gustatory receptor functions in developmental body patterning. Nat Commun 6:6243
Sakurai T, Nakagawa T, Mitsuno H et al (2004) The sex pheromone receptor in the silkworm moth Bombyx mori. Proc Natl Acad Sci U S A 101:16653–16658
Sánchez-Gracia A, Vieira FG, Rozas J (2009) Molecular evolution of the major chemosensory gene families in insects. Heredity 103:208–216
SilkBase (2006) Univ. of Tokyo, Tokyo. http://silkbase.ab.a.u-tokyo.ac.jp/cgi-bin/index.cgi. Accessed Sept–Nov 2018
Sun M, Liu Y, Walker WB et al (2013) Identification and characterization of pheromone receptors and interplay between receptors and pheromone binding proteins in the diamondback moth, P. xyllostella. PLoS One 8:e62098
Tanaka K, Uda Y, Ono Y et al (2009) Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile. Curr Biol 19:881–890
Tian Z, Sun L, Li Y et al (2018) Antennal transcriptome analysis of the chemosensory gene families in Carposina sasakii (Lepidoptera: Carposinidae). BMC Genomics 19:544
Vieira FG, Rozas J (2011) Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system. Genome Biol Evol 3:476–490
Vogt RG, Grosse-Wilde E, Zhou JJ (2015) The Lepidoptera odorant binding protein gene family: gene gain and loss within the GOBP/PBP complex of moths and butterflies. Insect Biochem Mol Biol 62:142–153
Vosshall LB, Hansson BS (2011) A unified nomenclature system for the insect olfactory coreceptor. Chem Senses 36:497–498
Wanner KW, Nichols AS, Allen JE et al (2010) Sex pheromone receptor specificity in the European corn borer moth, Ostrinia nubilalis. PLoS One 5:e8685
Xu P, Garczynski SF, Atungulu E et al (2012) Moth sex pheromone receptors and deceitful parapheromones. PLoS One 7:e41653
Yang B, Ozaki K, Ishikawa Y et al (2015) Identification of candidate odorant receptors in Asian corn borer Ostrinia furnacalis. PLoS One 10:e0121261
Yang S, Cao D, Wang G et al (2017) Identification of genes involved in chemoreception in Plutella xyllostella by antennal transcriptome analysis. Sci Rep 7:11941
Yasukochi Y, Miura N, Nakano R et al (2011) A sex-linked pheromone receptor genes of the European corn borer, Ostrinia nubilalis, are in tandem arrays. PLOS ONE 6:e18843
Yasukochi Y, Ohno M, Shibata R et al (2016) A FISH-based chromosome map for the European corn borer yields insights into ancient chromosomal fusions in the silkworm. Heredity 116:75–83
Yasukochi Y, Yang B, Fujimoto T et al (2018) Conservation and lineage-specific rearrangements in the GOBP/PBP gene complex of distantly related ditrysian Lepidoptera. PLoS One 13:e0192762
Yuvaraj JK, Corcoran JA, Andersson MN et al (2017) Characterization of odorant receptors from a nonditrysian moth, Eriocrania semipurpurella sheds light on the origin of sex pheromone receptors in Lepidoptera. Mol Biol Evol 34:2733–2746
Yuvaraj JK, Andersson MN, Corcoran JA et al (2018a) Functional characterization of odorant receptors from Lampronia capitella suggests a non-ditrysian origin of the lepidopteran pheromone receptor clade. Insect Biochem Mol Biol 100:39–47
Yuvaraj JK, Andersson MN, Zhang D et al (2018b) Antennal transcriptome analysis of the chemosensory gene families from Trichoptera and basal Lepidoptera. Front Physiol 9:1365
Zhang S, Zhang Z, Wang H et al (2014) Antennal transcriptome analysis and comparison of olfactory genes in two sympatric defoliators, Dendrolimus houi and Dendrolimus kikuchii (Lepidoptera: Lasiocampidae). Insect Biochem Mol Biol 52:69–81
Acknowledgments
I greatly appreciate Yukio Ishikawa for providing me the opportunity to publish this chapter and important contributions to our articles referred to in this chapter. I also thank Ken Sahara, Nami Miura, Bin Yang, Ryo Nakano, and Takashi Matsuo for their helpful assistance.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Yasukochi, Y. (2020). Evolutionary History of Lepidopteran Genes Associated with Sex Pheromone Recognition. In: Ishikawa, Y. (eds) Insect Sex Pheromone Research and Beyond. Entomology Monographs. Springer, Singapore. https://doi.org/10.1007/978-981-15-3082-1_10
Download citation
DOI: https://doi.org/10.1007/978-981-15-3082-1_10
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-15-3081-4
Online ISBN: 978-981-15-3082-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)