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Olfactory Specialization for Perfume Collection in Male Orchid Bees Lukasz Mitko1, Marjorie G

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Olfactory Specialization for Perfume Collection in Male Orchid Bees Lukasz Mitko1, Marjorie G © 2016. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2016) 219, 1467-1475 doi:10.1242/jeb.136754 RESEARCH ARTICLE Olfactory specialization for perfume collection in male orchid bees Lukasz Mitko1, Marjorie G. Weber2, Santiago R. Ramirez3, Erik Hedenström4, William T. Wcislo5 and Thomas Eltz1,* ABSTRACT Elgar, 2008). Signal specificity may be achieved by the use of a Insects rely on the olfactory system to detect a vast diversity of single complex molecule that is rare in nature and therefore difficult airborne molecules in their environment. Highly sensitive olfactory to duplicate by other organisms (Chow and Wang, 1981). tuning is expected to evolve when detection of a particular chemical Alternatively, and more commonly, signal specificity can be with great precision is required in the context of foraging and/or finding attained through a blend of relatively simple and common mates. Male neotropical orchid bees (Euglossini) collect odoriferous components (Bjostad et al., 1987). Insect pheromones are usually substances from multiple sources, store them in specialized tibial synthesized de novo or modified from dietary precursors (Roelofs, pouches and later expose them at display sites, presumably as 1995). In the case of orchid bees (Apidae, Euglossini; >200 mating signals to females. Previous analysis of tibial compounds species), however, blends of volatiles are harvested directly from the among sympatric species revealed substantial chemical disparity in environment. chemical composition among lineages with outstanding divergence Male orchid bees collect and store volatile chemicals from between closely related species. Here, we tested whether specific flowers of orchids and other plants, as well as non-floral sources perfume phenotypes coevolve with matching olfactory adaptations in such as rotting wood, bark exudates, leaves and feces (Dodson et al., male orchid bees to facilitate the location and harvest of species- 1969; Vogel, 1966). This behavior of scent collection evolved specific perfume compounds. We conducted electroantennographic approximately 38 million years ago (Engel, 1999; Ramírez et al., (EAG) measurements on males of 15 sympatric species in the genus 2011) and a great number of neotropical plant species, many of them Euglossa that were stimulated with 18 compounds present in variable orchids, have adapted to male orchid bees as pollinators by proportions in male hind tibiae. Antennal response profiles were producing floral scents (Dressler, 1982; Knudsen et al., 1999; species-specific across all 15 species, but there was no conspicuous Ramírez et al., 2002; Williams, 1982). These scents are highly differentiation between closely related species. Instead, we found that attractive to euglossine males over long distances (Ackerman, the observed variation in EAG activity follows a Brownian motion 1983b; Janzen, 1971, 1981), thus ensuring efficient pollination of model of trait evolution, where the probability of differentiation low-density plant taxa. The process of fragrance collection involves increases proportionally with lineage divergence time. However, we a range of morphological, biochemical and behavioral adaptations. identified strong antennal responses for some chemicals that are Specialized hind-tibial pouches enable males to store volatile present as major compounds in the perfume of the same species, substances over long periods of time, ultimately accumulating ‘ ’ thus suggesting that sensory specialization has occurred within complex blends of species-specific perfumes (Eltz et al., 2005a; multiple lineages. This sensory specialization was particularly Zimmermann et al., 2009). Finally, the perfumes are actively apparent for semi-volatile molecules (‘base note’ compounds), thus exposed by males at the sites where mating takes place (Eltz et al., supporting the idea that such compounds play an important role in 2005b) and probably serve as pheromonal analogues (Zimmermann chemical signaling of euglossine bees. Overall, our study found no et al., 2006). At present, more than 40 synthetic chemical close correspondence between antennal responses and behavioral compounds have been reported to attract euglossine bee males preferences/tibial contents, but confirms the utility of EAG profiling for and most of them are also known from natural sources (Ramírez discovering certain behaviorally active compounds. et al., 2002; Roubik and Hanson, 2004; Williams and Whitten, 1983). Species-specific preferences for collecting certain KEY WORDS: Euglossini, EAG, Olfaction, Olfactory specialization, compounds are evident (Ackerman, 1989), resulting in distinct Fragrance, Pheromone tibial blends (Eltz et al., 2005a). There is, however, broad overlap in the range of chemicals collected by different species (Ackerman, INTRODUCTION 1983a; Janzen et al., 1982; Pearson and Dressler, 1985) as well as Many insects use chemical signals to attract, locate and identify geographical and seasonal shifts of preferences (Ackerman, 1989; conspecific mates (Cardé and Baker, 1984; Roelofs, 1995; Wyatt, Pokorny et al., 2013). 2008). The chemical composition of mating pheromones ranges The unique composition of mating pheromones can lead to from single molecules to diverse, complex blends (Symonds and prezygotic reproductive isolation among closely related lineages (Roelofs et al., 2002) and, because of communication interference 1Department of Animal Ecology, Evolution and Biodiversity, Ruhr-Universität among sympatric species with similar chemical signals, sexual Bochum, Bochum 44780, Germany. 2The Center for Population Biology, University chemical signals may be subject to diversifying selection (Coyne 3 of California, Davis, Davis, CA 95616, USA. Department of Evolution and Ecology, and Orr, 2004; Groot et al., 2006; Higgie et al., 2000). In fact, a University of California, Davis, CA 95616, USA. 4Chemistry, Department of Natural Sciences, Engineering and Mathematics, Mid Sweden University, Sundsvall SE- pattern consistent with diversifying selection in sympatry was found 851 70, Sweden. 5Smithsonian Tropical Research Institute, Apartado 0843-03092, for male orchid bee perfumes (Zimmermann et al., 2009). The Balboa, Ancon, Republic of Panama. chemical composition of blends collected by 15 sympatric species *Author for correspondence ([email protected]) of Euglossa from central Panama were more different from each other than expected under a model of neutral phenotypic evolution, Received 21 December 2015; Accepted 23 February 2016 and perfume disparity between species was particularly pronounced Journal of Experimental Biology 1467 RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 1467-1475 doi:10.1242/jeb.136754 between closely related lineages (Zimmermann et al., 2009). Based selected a set of 18 single compounds for the community-level on these findings, we hypothesized that the outstanding divergence analysis of sensory specialization, which we either purchased from of fragrances observed among closely related species is mediated by commercial suppliers or isolated from tibial bee extracts using an underlying species-specific sensory adaptation that evolved in preparative gas chromatography (see below and Table S1). These response to reproductive character displacement at the sensory compounds included both common compounds that were present level. In order to reveal potential sensory adaptations, we used and abundant in a range of species as well as compounds that were electroantennography (EAG) to screen overall antennal sensitivity present in only one or few species. To characterize the 18 for a large range of substances. This method is generally suitable compounds as ‘minor’ or ‘major’ (<5% or >5% of total fragrance to detect sensory specialization in the antennae (Roelofs, 1984) peak area) components in a given species, we used quantitative and has been used to investigate odor detection in diverse insects information compiled in a yet unpublished database on tibial (Schiestl and Marion-Poll, 2002), including orchid bees (Eltz contents of males of 66 species of Euglossa (M.G.W., L.M., T.E. et al., 2006, 2008; Eltz and Lunau, 2005; Milet-Pinheiro et al., 2015; and S.R.R., unpublished results). In addition to these 18 compounds Schiestl and Roubik, 2003). We used two different approaches. we also stimulated antennae with solvent (hexane) and unspecific In the first approach, we conducted a phylogenetically broad odor (geraniol and 2-undecanone) controls. Both geraniol and community-level comparison of 15 sympatric Panamanian species 2-undecanone elicit significant EAG responses but are neither in the genus Euglossa, testing for species-specific sensory tuning attractive to, nor known to occur in the tibial blends of males of the for compounds that were present and abundant in a range of species, studied species. as well as compounds that were typical only for certain species. For the sibling-species comparison, we used each of the eight Next, we compared the antennal response of the sibling species major compounds present in the tibial perfume of E. purpurea (see Euglossa purpurea Friese 1899 and Euglossa hansoni Moure 1989 below). We isolated these compounds using the preparative gas when presented with all the major compounds contained in the chromatography technique, which resulted in eight 2 ml test perfume mixture of E. purpurea in order to identify whether a solutions with a concentration of 500 µg ml−1 dissolved in sensory shift occurred between these
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