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

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 Chemical Ecology Department of Evolutionary Neuroethology Hans Knoell Strasse 8 D 07745 Jena Germany Czech University of Life Sciences Faculty of Forestry and Wood Sciences EXTEMIT K Kamýcká 129 165 00 Praha Suchdol Czech Republic

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