An animal's fitness strongly depends on successful feeding, avoidance of predators and reproduction. All of these behaviours commonly involve chemosensation. As a consequence, when species' ecological niches and life histories differ, their chemosensory abilities need to be adapted accordingly. The intertidal insect Clunio marinus (Diptera: Chironomidae) has tuned its olfactory system to two highly divergent niches. The long-lived larvae forage in a marine environment. During the few hours of terrestrial adult life, males have to find the female pupae floating on the water surface, free the cryptic females from their pupal skin, copulate and carry the females to the oviposition sites. In order to explore the possibility for divergent olfactory adaptations within the same species, we investigated the chemosensory system of C. marinus larvae, adult males and adult females at the morphological and molecular level. The larvae have a well-developed olfactory system, but olfactory gene expression only partially overlaps with that of adults, likely reflecting their marine vs. terrestrial lifestyles. The olfactory system of the short-lived adults is simple, displaying no glomeruli in the antennal lobes. There is strong sexual dimorphism, the female olfactory system being particularly reduced in terms of number of antennal annuli and sensilla, olfactory brain centre size and gene expression. We found hints for a pheromone detection system in males, including large trichoid sensilla and expression of specific olfactory receptors and odorant binding proteins. Taken together, this makes C. marinus an excellent model to study within-species evolution and adaptation of chemosensory systems.

Center for Integrative Bioinformatics Vienna Max F Perutz Laboratories University of Vienna Medical University Vienna Dr Bohr Gasse 9 A 1030 Wien Austria

Czech University of Life Sciences Faculty of Forestry and Wood Sciences EXTEMIT K Kamýcká 129 165 00 Praha Suchdol Czech Republic

Justus Liebig University Giessen Institute for Insect Biotechnology Heinrich Buff Ring 26 32 D 35392 Gießen Germany

Max Planck Institute for Chemical Ecology Department of Entomology Hans Knoell Strasse 8 D 07745 Jena Germany

Max Planck Institute for Chemical Ecology Department of Evolutionary Neuroethology Hans Knoell Strasse 8 D 07745 Jena Germany

Max Planck Institute for Evolutionary Biology Max Planck Research Group Biological Clocks August Thienemann Strasse 2 24306 Plön Germany

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Hansson BS, Anton S. Function and Morphology of the Antennal Lobe: New Developments. Annual Review of Entomology. 2000;45:203–231. doi: 10.1146/annurev.ento.45.1.203. PubMed DOI

Neumann D. Die lunare und tägliche Schlüpfperiodik der Mücke Clunio - Steuerung und Abstimmung auf die Gezeitenperiodik. Zeitschrift für Vergleichende. Physiologie. 1966;53:1–61.

Kaiser, T. S. In Annual, Lunar, and Tidal Clocks (eds Hideharu Numata & Barbara Helm) Ch. 7, 121–141 (Springer Japan, 2014).

Caspers H. Rhythmische Erscheinungen in der Fortpflanzung von Clunio marinus (Dipt. Chiron.) und das Problem der lunaren Periodizitaet bei Organismen. Archiv für Hydrobiologie. 1951;Supplement 18:415–594.

Neumann, D. In Annual, Lunar, and Tidal Clocks (eds Hideharu Numata & Barbara Helm) Ch. 1, 3–24 (Springer Japan, 2014).

Kaiser TS, et al. The genomic basis of circadian and circalunar timing adaptations in a midge. Nature. 2016;540:69–73. doi: 10.1038/nature20151. PubMed DOI PMC

Hashimoto H. Peculiar mode of emergence in the marine Chironomid Clunio (Diptera, Chironomidae) Science reports of the Tokyo Kyoiku Daigaku (B) 1957;8:217–226.

Dordel HJ. The Process of Copulation in Marine Chironomid Clunio marinus (Diptera) Canadian Entomologist. 1971;103:404–406. doi: 10.4039/Ent103404-3. DOI

Mciver SB. Sensilla of Mosquitos (Diptera, Culicidae) Journal of Medical Entomology. 1982;19:489–535. doi: 10.1093/jmedent/19.5.489. PubMed DOI

Venkatesh S, Singh RN. Sensilla on the 3rd Antennal Segment of Drosophila melanogaster Meigen (Diptera, Drosophilidae) Int. J. Insect. Morphol. 1984;13:51–63. doi: 10.1016/0020-7322(84)90032-1. DOI

Fernandes FF, Pimenta PFP, Linardi PM. Antennal sensilla of the new world screwworm fly, Cochliomyia hominivorax (Diptera: Calliphoridae) Journal of Medical Entomology. 2004;41:545–551. doi: 10.1603/0022-2585-41.4.545. PubMed DOI

Isaac C, Ravaiano SV, Pascini TV, Martins GF. The Antennal Sensilla of Species of the Palpalis Group (Diptera: Glossinidae) Journal of Medical Entomology. 2015;52:614–621. doi: 10.1093/jme/tjv050. PubMed DOI

Sengupta, S. & Smith, D. P. How Drosophila Detect Volatile Pheromones. (2014). PubMed

Saether OA. Glossary of chironomid morphology terminology (Diptera: Chironomidae) Entomol. Scand. 1980;14:1–51.

Nolte Andreas, Gawalek Petra, Koerte Sarah, Wei HongYing, Schumann Robin, Werckenthin Achim, Krieger Jürgen, Stengl Monika. No Evidence for Ionotropic Pheromone Transduction in the Hawkmoth Manduca sexta. PLOS ONE. 2016;11(11):e0166060. doi: 10.1371/journal.pone.0166060. PubMed DOI PMC

Wicher D, et al. Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature. 2008;452:1007–U1010. doi: 10.1038/nature06861. PubMed DOI

Sato K, et al. Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature. 2008;452:1002–U1009. doi: 10.1038/nature06850. PubMed DOI

Krieger J, Klink O, Mohl C, Raming K, Breer H. A candidate olfactory receptor subtype highly conserved across different insect orders. Journal of Comparative Physiology A. 2003;189:519–526. doi: 10.1007/s00359-003-0427-x. PubMed DOI

Couto A, Alenius M, Dickson BJ. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Current Biology. 2005;15:1535–1547. doi: 10.1016/j.cub.2005.07.034. PubMed DOI

Hansson BS, Stensmyr MC. Evolution of Insect Olfaction. Neuron. 2011;72:698–711. doi: 10.1016/j.neuron.2011.11.003. PubMed DOI

Klagges BR, et al. Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. Journal of Neuroscience. 1996;16:3154–3165. doi: 10.1523/JNEUROSCI.16-10-03154.1996. PubMed DOI PMC

Benton R, Sachse S, Michnick SW, Vosshall LB. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. Plos Biology. 2006;4:240–257. doi: 10.1371/journal.pbio.0040020. PubMed DOI PMC

Butterwick Joel A., del Mármol Josefina, Kim Kelly H., Kahlson Martha A., Rogow Jackson A., Walz Thomas, Ruta Vanessa. Cryo-EM structure of the insect olfactory receptor Orco. Nature. 2018;560(7719):447–452. doi: 10.1038/s41586-018-0420-8. PubMed DOI PMC

Vosshall LB, Hansson BS. A Unified Nomenclature System for the Insect Olfactory Coreceptor. Chemical Senses. 2011;36:497–498. doi: 10.1093/chemse/bjr022. PubMed DOI

Stensmyr MC, et al. A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell. 2012;151:1345–1357. doi: 10.1016/j.cell.2012.09.046. PubMed DOI

Jones WD, Cayirlioglu P, Kadow IG, Vosshall LB. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature. 2007;445:86–90. doi: 10.1038/nature05466. PubMed DOI

Kwon JY, Dahanukar A, Weiss LA, Carlson JR. The molecular basis of CO2 reception in Drosophila. Proceedings of the National Academy of Sciences of the United States of America. 2007;104:3574–3578. doi: 10.1073/pnas.0700079104. PubMed DOI PMC

Weiss LA, Dahanukar A, Kwon JY, Banerjee D, Carlson JR. The Molecular and Cellular Basis of Bitter Taste in Drosophila. Neuron. 2011;69:258–272. doi: 10.1016/j.neuron.2011.01.001. PubMed DOI PMC

Freeman EG, Wisotsky Z, Dahanukar A. Detection of sweet tastants by a conserved group of insect gustatory receptors. Proceedings of the National Academy of Sciences of the United States of America. 2014;111:1598–1603. doi: 10.1073/pnas.1311724111. PubMed DOI PMC

Eirín-López, J., Rebordinos, L., Rooney, A. & Rozas, J. In Repetitive DNA Vol. 7, 170–196 (Karger Publishers, 2012).

Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell. 2009;136:149–162. doi: 10.1016/j.cell.2008.12.001. PubMed DOI PMC

Koh T-W, et al. The Drosophila IR20a clade of ionotropic receptors are candidate taste and pheromone receptors. Neuron. 2014;83:850–865. doi: 10.1016/j.neuron.2014.07.012. PubMed DOI PMC

Croset V, et al. Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genetics. 2010;6:e1001064. doi: 10.1371/journal.pgen.1001064. PubMed DOI PMC

Stewart, S., Koh, T.-W., Ghosh, A. C. & Carlson, J. R. Candidate ionotropic taste receptors in the Drosophila larva. Proceedings of the National Academy of Sciences, 201503292 (2015). PubMed PMC

Zhang YV, Ni J, Montell C. The molecular basis for attractive salt-taste coding in Drosophila. Science. 2013;340:1334–1338. doi: 10.1126/science.1234133. PubMed DOI PMC

Ni L, et al. The ionotropic receptors IR21a and IR25a mediate cool sensing in Drosophila. Elife. 2016;5:e13254. doi: 10.7554/eLife.13254. PubMed DOI PMC

Knecht ZA, et al. Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila. eLIFE. 2016;5:e17879. doi: 10.7554/eLife.17879. PubMed DOI PMC

Silbering AF, et al. Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. Journal of Neuroscience. 2011;31:13357–13375. doi: 10.1523/JNEUROSCI.2360-11.2011. PubMed DOI PMC

Hansell, D. A. & Carlson, C. A. Biogeochemistry of marine dissolved organic matter. (Academic Press, 2014).

Rytz R, Croset V, Benton R. Ionotropic receptors (IRs): chemosensory ionotropic glutamate receptors in Drosophila and beyond. Insect Biochemistry and Molecular Biology. 2013;43:888–897. doi: 10.1016/j.ibmb.2013.02.007. PubMed DOI

Abuin L, et al. Functional architecture of olfactory ionotropic glutamate receptors. Neuron. 2011;69:44–60. doi: 10.1016/j.neuron.2010.11.042. PubMed DOI PMC

Pelosi P, Calvello M, Ban LP. Diversity of odorant-binding proteins and chemosensory proteins in insects. Chemical Senses. 2005;30:I291–i292. doi: 10.1093/chemse/bjh229. PubMed DOI

Angeli S, et al. Purification, structural characterization, cloning and immunocytochemical localization of chemoreception proteins from Schistocerca gregaria. European Journal of Biochemistry. 1999;262:745–754. doi: 10.1046/j.1432-1327.1999.00438.x. PubMed DOI

Galindo K, Smith DP. A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla. Genetics. 2001;159:1059–1072. PubMed PMC

Celorio-Mancera MD, et al. Chemosensory proteins, major salivary factors in caterpillar mandibular glands. Insect Biochemistry and Molecular Biology. 2012;42:796–805. doi: 10.1016/j.ibmb.2012.07.008. PubMed DOI

Furusawa T, et al. Systematic investigation of the hemolymph proteome of Manduca sexta at the fifth instar larvae stage using one- and two-dimensional proteomics platforms. J Proteome Res. 2008;7:938–959. doi: 10.1021/pr070405j. PubMed DOI

Iovinella I, et al. Differential Expression of Odorant-Binding Proteins in the Mandibular Glands of the Honey Bee According to Caste and Age. J Proteome Res. 2011;10:3439–3449. doi: 10.1021/pr2000754. PubMed DOI

Pelosi P, Zhou JJ, Ban LP, Calvello M. Soluble proteins in insect chemical communication. Cellular and Molecular Life Sciences. 2006;63:1658–1676. doi: 10.1007/s00018-005-5607-0. PubMed DOI PMC

Vieira FG, Rozas J. Comparative Genomics of the Odorant-Binding and Chemosensory Protein Gene Families across the Arthropoda: Origin and Evolutionary History of the Chemosensory System. Genome Biology and Evolution. 2011;3:476–490. doi: 10.1093/Gbe/Evr033. PubMed DOI PMC

McKenzie Sean K, Oxley Peter R, Kronauer Daniel JC. Comparative genomics and transcriptomics in ants provide new insights into the evolution and function of odorant binding and chemosensory proteins. BMC Genomics. 2014;15(1):718. doi: 10.1186/1471-2164-15-718. PubMed DOI PMC

Zhou JJ, et al. Genome annotation and comparative analyses of the odorant-binding proteins and chemosensory proteins in the pea aphid Acyrthosiphon pisum. Insect Molecular Biology. 2010;19:113–122. doi: 10.1111/j.1365-2583.2009.00919.x. PubMed DOI

Smith DP. Volatile pheromone signalling in Drosophila. Physiological Entomology. 2012;37:19–24. doi: 10.1111/j.1365-3032.2011.00813.x. PubMed DOI PMC

Pelletier J, Leal WS. Characterization of olfactory genes in the antennae of the Southern house mosquito, Culex quinquefasciatus. Journal of Insect Physiology. 2011;57:915–929. doi: 10.1016/j.jinsphys.2011.04.003. PubMed DOI

Liu R, et al. Expression of chemosensory proteins in the tsetse fly Glossina morsitans morsitans is related to female host-seeking behaviour. Insect Molecular Biology. 2012;21:41–48. doi: 10.1111/j.1365-2583.2011.01114.x. PubMed DOI PMC

Sclafani A, Ackroff K, Abumrad NA. CD36 gene deletion reduces fat preference and intake but not post-oral fat conditioning in mice. Am J Physiol-Reg I. 2007;293:R1823–R1832. doi: 10.1152/ajpregu.00211.2007. PubMed DOI

Silverstein, R. L. & Febbraio, M. CD36, a Scavenger Receptor Involved in Immunity, Metabolism, Angiogenesis, and Behavior. Science Signaling2, doi:ARTN re3 10.1126/scisignal.272re3 (2009). PubMed PMC

Benton R, Vannice KS, Vosshall LB. An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature. 2007;450:289–U213. doi: 10.1038/nature06328. PubMed DOI

Jin X, Ha TS, Smith DP. SNMP is a signaling component required for pheromone sensitivity in Drosophila. Proceedings of the National Academy of Sciences of the United States of America. 2008;105:10996–11001. doi: 10.1073/pnas.0803309105. PubMed DOI PMC

Vogt, R. G. In Insect Pheromone Biochemistry and Molecular Biology 391–445 (Elsevier, 2003).

Hashimoto, H. In Marine Insects (ed L. Cheng) 377–414 (North-Holland, 1976).

Sparks JT, Bohbot JD, Dickens JC. The genetics of chemoreception in the labella and tarsi of Aedes aegypti. Insect Biochemistry and Molecular Biology. 2014;48:8–16. doi: 10.1016/j.ibmb.2014.02.004. PubMed DOI

Xia Y, et al. The molecular and cellular basis of olfactory-driven behavior in Anopheles gambiae larvae. Proceedings of the National Academy of Sciences. 2008;105:6433–6438. doi: 10.1073/pnas.0801007105. PubMed DOI PMC

Singh, Y. N. & Singh, M. Metamorphic Changes in the Brain of Chironomus dolichotomus (Diptera, Chironomidae). J Hirnforsch21, 561–568 (1980). PubMed

Mysore K, Flannery EM, Tomchaney M, Severson DW, Duman-Scheel M. Disruption of Aedes aegypti olfactory system development through chitosan/siRNA nanoparticle targeting of semaphorin-1a. Plos Neglect Trop D. 2013;7:e2215. doi: 10.1371/journal.pntd.0002215. PubMed DOI PMC

Corkum LD, Belanger RM. Use of chemical communication in the management of freshwater aquatic species that are vectors of human diseases or are invasive. General and Comparative Endocrinology. 2007;153:401–417. doi: 10.1016/j.ygcen.2007.01.037. PubMed DOI

Schachtner J, Schmidt M, Homberg U. Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Arthropod Structure &. Development. 2005;34:257–299.

Strausfeld NJ, Sinakevitch I, Brown SM, Farris SM. Ground Plan of the Insect Mushroom Body: Functional and Evolutionary Implications. Journal of Comparative Neurology. 2009;513:265–291. doi: 10.1002/cne.21948. PubMed DOI PMC

Klinner, C. F. et al. Functional Olfactory Sensory Neurons Housed in Olfactory Sensilla on the Ovipositor of the Hawkmoth Manduca sexta. Front Ecol Evol4, doi:ARTN 13010.3389/fevo.2016.00130 (2016).

Katoh K, Kuma K, Toh H, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research. 2005;33:511–518. doi: 10.1093/nar/gki198. PubMed DOI PMC

Katoh K, Standley DM. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Molecular Biology and Evolution. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC

Price MN, Dehal PS, Arkin AP. FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix. Molecular Biology and Evolution. 2009;26:1641–1650. doi: 10.1093/molbev/msp077. PubMed DOI PMC

Liu Kevin, Linder C. Randal, Warnow Tandy. RAxML and FastTree: Comparing Two Methods for Large-Scale Maximum Likelihood Phylogeny Estimation. PLoS ONE. 2011;6(11):e27731. doi: 10.1371/journal.pone.0027731. PubMed DOI PMC

Vogel H, Badapanda C, Knorr E, Vilcinskas A. RNA-sequencing analysis reveals abundant developmental stage-specific and immunity-related genes in the pollen beetle Meligethes aeneus. Insect Molecular Biology. 2014;23:98–112. doi: 10.1111/imb.12067. PubMed DOI

Gotz S, et al. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Research. 2008;36:3420–3435. doi: 10.1093/nar/gkn176. PubMed DOI PMC

Jacobs, C. G. C. et al. Sex, offspring and carcass determine antimicrobial peptide expression in the burying beetle. Scientific Reports6, 25409, 10.1038/srep25409, https://www.nature.com/articles/srep25409#supplementary-information (2016). PubMed PMC