A major locus controls a biologically active pheromone component in Heliconius melpomene

Pheromones are important for courtship and mate choice in many insects, but we know relatively little of their role in butterflies. The butterfly Heliconius melpomene uses a complex blend of wing androconial compounds during courtship. Electroantennography in H. melpomene and its close relative H. cydno showed that responses to androconial extracts were not species-specific. Females of both species responded more strongly to the H. cydno extract, suggesting conservation of peripheral nervous system elements across the two species. Individual blend components provoked little to no response, with the exception of octadecanal, a major component of the H. melpomene blend. Supplementing octadecanal on the wings of octadecanal-rich H. melpomene males led to an increase in the time until mating, demonstrating the bioactivity of octadecanal in Heliconius. Using quantitative trait locus (QTL) mapping, we identified a single locus on chromosome 20 responsible for 41% of the parental species’ difference in octadecanal production. This QTL does not overlap with any of the major wing color or mate choice loci, nor does it overlap with known regions of elevated or reduced FST. A set of 16 candidate fatty acid biosynthesis genes lies underneath the QTL.

[1]  K. Haynes 6. Genetic Control of Moth Sex Pheromone Signal and Response , 2019 .

[2]  W. Conner,et al.  12. Male Pheromones in Moths: Reproductive Isolation, Sexy Sons, and Good Genes , 2019 .

[3]  K. M. Kozak,et al.  Species specificity and intraspecific variation in the chemical profiles of Heliconius butterflies across a large geographic range , 2019, bioRxiv.

[4]  B. Yandell,et al.  R/qtl2: Software for Mapping Quantitative Trait Loci with High-Dimensional Data and Multiparent Populations , 2018, Genetics.

[5]  Yongjun Du,et al.  Minor Components Play an Important Role in Interspecific Recognition of Insects: A Basis to Pheromone Based Electronic Monitoring Tools for Rice Pests , 2018, Insects.

[6]  Pjotr Prins,et al.  R/qtl2: Software for Mapping Quantitative Trait Loci with High-Dimensional Data and Multiparent Populations , 2018, Genetics.

[7]  V. Ruta,et al.  Evolution of a central neural circuit underlies Drosophila mate preferences , 2018, Nature.

[8]  C. Jiggins,et al.  Male pheromone composition depends on larval but not adult diet in Heliconius melpomene , 2018, bioRxiv.

[9]  Simon H. Martin,et al.  Genetic dissection of assortative mating behavior , 2018, bioRxiv.

[10]  Thomas L. Turner,et al.  Male mate choice via cuticular hydrocarbon pheromones drives reproductive isolation between Drosophila species , 2018, Evolution; international journal of organic evolution.

[11]  Pessoa Pinharanda,et al.  The genomic basis of species barriers in Heliconius butterflies , 2017 .

[12]  Pasi Rastas,et al.  Lep-MAP3: robust linkage mapping even for low-coverage whole genome sequencing data , 2017, Bioinform..

[13]  K. Dasmahapatra,et al.  The Scent Chemistry of Heliconius Wing Androconia , 2017, Journal of Chemical Ecology.

[14]  Richard Durbin,et al.  No evidence for maintenance of a sympatric Heliconius species barrier by chromosomal inversions , 2017, Evolution letters.

[15]  C. Jiggins,et al.  Male sex pheromone components in Heliconius butterflies released by the androconia affect female choice , 2017, bioRxiv.

[16]  R. Merrill,et al.  Divergence in brain composition during the early stages of ecological specialization in Heliconius butterflies , 2017, Journal of evolutionary biology.

[17]  G. Lamas,et al.  The Ecology and Evolution of Heliconius Butterflies , 2017 .

[18]  Simon H. Martin,et al.  Complex modular architecture around a simple toolkit of wing pattern genes. , 2017, Nature ecology & evolution.

[19]  J. Feder,et al.  Sensory specificity and speciation: a potential neuronal pathway for host fruit odour discrimination in Rhagoletis pomonella , 2016, Proceedings of the Royal Society B: Biological Sciences.

[20]  Manuel Koller,et al.  robustlmm : An R Package for Robust Estimation of Linear Mixed-Effects Models , 2016 .

[21]  P. Andolfatto,et al.  Population differences in olfaction accompany host shift in Drosophila mojavensis , 2016, Proceedings of the Royal Society B: Biological Sciences.

[22]  M. Blaxter,et al.  Lepbase: the Lepidopteran genome database , 2016, bioRxiv.

[23]  D. Heckel,et al.  The Genetic Basis of Pheromone Evolution in Moths. , 2016, Annual review of entomology.

[24]  A. Borg-Karlson,et al.  It's All in the Mix: Blend-Specific Behavioral Response to a Sexual Pheromone in a Butterfly , 2016, Front. Physiol..

[25]  L. Vaníčková,et al.  Identification and field and laboratory tests of the sex pheromone of Cerconota anonella Sepp. (Lepidoptera: Oecophoridae) , 2016 .

[26]  C. Löfstedt,et al.  4. Evolutionary Patterns of Pheromone Diversity in Lepidoptera , 2016 .

[27]  M. Joron,et al.  Beyond magic traits: Multimodal mating cues in Heliconius butterflies , 2015, Evolution; international journal of organic evolution.

[28]  J. Yew,et al.  Insect pheromones: An overview of function, form, and discovery. , 2015, Progress in lipid research.

[29]  Åsa K. Björklund,et al.  Tn5 transposase and tagmentation procedures for massively scaled sequencing projects , 2014, Genome research.

[30]  B. Hansson,et al.  Shifts in sensory neuron identity parallel differences in pheromone preference in the European corn borer , 2014, Front. Ecol. Evol..

[31]  J. Gershenzon,et al.  Little peaks with big effects: establishing the role of minor plant volatiles in plant-insect interactions. , 2014, Plant, cell & environment.

[32]  E. Bermingham,et al.  Phylogeography of Heliconius cydno and its closest relatives: disentangling their origin and diversification , 2014, Molecular ecology.

[33]  Jean-Marc Lassance,et al.  Sex pheromone biosynthetic pathways are conserved between moths and the butterfly Bicyclus anynana , 2014, Nature Communications.

[34]  James Mallet,et al.  Multilocus Species Trees Show the Recent Adaptive Radiation of the Mimetic Heliconius Butterflies , 2014, bioRxiv.

[35]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[36]  Simon H. Martin,et al.  Genome-wide evidence for speciation with gene flow in Heliconius butterflies , 2013, Genome research.

[37]  S. Rollmann,et al.  Divergence in Olfactory Host Plant Preference in D. mojavensis in Response to Cactus Host Use , 2013, PloS one.

[38]  Heng Li Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM , 2013, 1303.3997.

[39]  S. Via Divergence hitchhiking and the spread of genomic isolation during ecological speciation-with-gene-flow , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  R. Butlin,et al.  A framework for comparing processes of speciation in the presence of gene flow , 2011, Molecular ecology.

[41]  R. Durbin,et al.  Inference of human population history from individual whole-genome sequences. , 2011, Nature.

[42]  T. Ando,et al.  Analyses of lepidopteran sex pheromones by mass spectrometry , 2011 .

[43]  D. Suckling,et al.  New Sex Pheromone Blend for the Lightbrown Apple Moth, Epiphyas postvittana , 2011, Journal of Chemical Ecology.

[44]  John Fox,et al.  Robust Regression in R An Appendix to An R Companion to Applied Regression, Second Edition , 2011 .

[45]  William N. Venables,et al.  Modern Applied Statistics with S , 2010 .

[46]  Sanford Weisberg,et al.  An R Companion to Applied Regression , 2010 .

[47]  M. Ryan,et al.  Sexually dimorphic sensory gating drives behavioral differences in túngara frogs , 2010, Journal of Experimental Biology.

[48]  R. Peakall,et al.  Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptive Chiloglottis orchids: implications for pollinator-driven speciation. , 2010, The New phytologist.

[49]  M. Stengl Pheromone Transduction in Moths , 2010, Front. Cell. Neurosci..

[50]  C. Jiggins,et al.  Pervasive genetic associations between traits causing reproductive isolation in Heliconius butterflies , 2010, Proceedings of the Royal Society B: Biological Sciences.

[51]  Erik Hedenström,et al.  Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones , 2010, Nature.

[52]  A. M. Araújo,et al.  Courtship behavior of Heliconius erato phyllis (Lepidoptera, Nymphalidae) towards virgin and mated females: conflict between attraction and repulsion signals? , 2010, Journal of Ethology.

[53]  E. Dopman,et al.  COMPONENTS OF REPRODUCTIVE ISOLATION BETWEEN NORTH AMERICAN PHEROMONE STRAINS OF THE EUROPEAN CORN BORER , 2009, Evolution; international journal of organic evolution.

[54]  J. V. van Loon,et al.  Aphrodisiac Pheromones from the Wings of the Small Cabbage White and Large Cabbage White Butterflies, Pieris rapae and Pieris brassicae , 2009, Chembiochem : a European journal of chemical biology.

[55]  R. Butlin,et al.  On the scent of speciation: the chemosensory system and its role in premating isolation , 2009, Heredity.

[56]  Jean-Marc Lassance,et al.  Concerted evolution of male and female display traits in the European corn borer, Ostrinia nubilalis , 2009, BMC Biology.

[57]  M. Ryan,et al.  Candidate neural locus for sex differences in reproductive decisions , 2008, Biology Letters.

[58]  B. Hansson,et al.  Reversed functional topology in the antennal lobe of the male European corn borer , 2008, Journal of Experimental Biology.

[59]  P. Brakefield,et al.  The Male Sex Pheromone of the Butterfly Bicyclus anynana: Towards an Evolutionary Analysis , 2008, PloS one.

[60]  M. Elgar,et al.  The evolution of pheromone diversity. , 2008, Trends in ecology & evolution.

[61]  E. Dopman,et al.  Molecular Differentiation at Nuclear Loci in French Host Races of the European Corn Borer (Ostrinia nubilalis) , 2007, Genetics.

[62]  Ziheng Yang PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[63]  Anna-Karin Borg-Karlson,et al.  Male sex pheromone release and female mate choice in a butterfly , 2007, Journal of Experimental Biology.

[64]  H. Fadamiro,et al.  Behavioral and Electroantennogram Responses of Phorid fly Pseudacteon tricuspis (Diptera: Phoridae) to Red Imported Fire Ant Solenopsis invicta Odor and Trail Pheromone , 2007, Journal of Insect Behavior.

[65]  D. Kemp,et al.  Multimodal signalling: structural ultraviolet reflectance predicts male mating success better than pheromones in the butterfly Colias eurytheme L. (Pieridae) , 2007, Animal Behaviour.

[66]  G. Turner,et al.  Female preference for conspecific males based on olfactory cues in a Lake Malawi cichlid fish , 2005, Biology Letters.

[67]  C. Kim,et al.  Male sex pheromone of a giant danaine butterfly,Idea leuconoe , 1996, Journal of Chemical Ecology.

[68]  Y. Chow,et al.  Isolation, identification, and synthesis of sex pheromone components of female tea cluster caterpillar,Andraca bipunctata walker (Lepidoptera: Bombycidae) in Taiwan , 1996, Journal of Chemical Ecology.

[69]  D. J. Chamberlain,et al.  Components of female sex pheromone of spotted bollworm,Earias vittella F. (Lepidoptera: Noctuidae): Identification and field evaluation in Pakistan , 1988, Journal of Chemical Ecology.

[70]  C. Wysocki,et al.  Facts, fallacies, fears, and frustrations with human pheromones. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[71]  A. Borg-Karlson,et al.  Antiaphrodisiacs in Pierid Butterflies: A Theme with Variation! , 2003, Journal of Chemical Ecology.

[72]  J. E. Oliver,et al.  Pheromone hydrolysis by cuticular and interior esterases of the antennae, legs, and wings of the cabbage looper moth,Trichoplusia ni (Hübner) , 1982, Journal of Chemical Ecology.

[73]  J. Kochansky,et al.  Sex pheromone of the european corn borer,Ostrinia nubilalis (Lepidoptera: Pyralidae), in New York , 1975, Journal of Chemical Ecology.

[74]  J. Mcchesney,et al.  Aphrodisiac pheromones of the sulfur butterfliesColias eurytheme andC. Philodice (Lepidoptera, Pieridae) , 2004, Journal of Chemical Ecology.

[75]  Bonnie L Bassler,et al.  Chemical communication among bacteria , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[76]  J. Mallet,et al.  Mimicry: developmental genes that contribute to speciation , 2003, Evolution & development.

[77]  N. Finney,et al.  A Simple and Advantageous Protocol for the Oxidation of Alcohols with o‐Iodoxybenzoic Acid (IBX). , 2002 .

[78]  N. Finney,et al.  A simple and advantageous protocol for the oxidation of alcohols with O-iodoxybenzoic acid (IBX). , 2002, Organic letters.

[79]  Carole Ober,et al.  Paternally inherited HLA alleles are associated with women's choice of male odor , 2002, Nature Genetics.

[80]  Brian D. Ripley,et al.  Modern Applied Statistics with S Fourth edition , 2002 .

[81]  James Mallet,et al.  Reproductive isolation caused by colour pattern mimicry , 2001, Nature.

[82]  C. D. Jones Extension of the Castle-Wright effective factor estimator to sex linkage and haplodiploidy. , 2001, The Journal of heredity.

[83]  D. Ross,et al.  SEX PHEROMONE BLEND OF THE PANDORA MOTH (LEPIDOPTERA: SATURNIIDAE), AN OUTBREAK PEST IN PINE FORESTS (PINACEAE) , 2000, Canadian Entomologist.

[84]  F. Zufall,et al.  The cellular and molecular basis of odor adaptation. , 2000, Chemical senses.

[85]  Ziheng Yang,et al.  PAML: a program package for phylogenetic analysis by maximum likelihood , 1997, Comput. Appl. Biosci..

[86]  S. Schulz,et al.  The pheromone system of the male danaine butterfly, Idea leuconoe. , 1996, Bioorganic & medicinal chemistry.

[87]  H. Brown,et al.  Reaction of sodium aluminum hydride with selected organic compounds containing representative functional groups. Comparison of the reducing characteristics of lithium and sodium aluminum hydrides , 1993 .

[88]  R. Vane‐Wright,et al.  Visual and Chemical Signalling in Butterflies: Functional and Phylogenetic Perspectives , 1993 .

[89]  G. Bush,et al.  Rhagoletis sibling species and host races differ in host odor recognition , 1990 .

[90]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[91]  J. Tumlinson,et al.  Identification of a pheromone blend attractive to Manduca sexta (L.) males in a wind tunnel , 1989 .

[92]  K. Usui,et al.  Sex Pheromone of the Rice Stem Borer, Chilo suppressalis (WALKER) (Lepidoptera : Pyralidae) : the Third Component, Z-9-Hexadecenal , 1983 .

[93]  J. Felsenstein SKEPTICISM TOWARDS SANTA ROSALIA, OR WHY ARE THERE SO FEW KINDS OF ANIMALS? , 1981, Evolution; international journal of organic evolution.

[94]  T. Eisner,et al.  Sex Pheromone of the Queen Butterfly: Biology , 1969, Science.

[95]  Y. Meinwald,et al.  Sex Pheromone of the Queen Butterfly: Chemistry , 1969, Science.

[96]  T. E. Pliske Sex pheromone of the Queen butterfly , 1969 .