Unraveling the Olfactory Biases of Male Euglossine Bees: Species-Specific Antennal Responses and Their Evolutionary Significance for Perfume Flowers

Abstract

Male euglossine bees exhibit unique adaptations for the acquisition and accumulation of chemical compounds from “perfume flowers” and other sources. During courtship display, male bees expose perfume mixtures, presumably to convey species-specific recognition and/or mate choice signals to females. Because olfaction regulates both signal production (in males) and signal detection (in females) in this communication system, strong selective pressures are expected to act on the olfactory system, which could lead to sensory specialization in favor of an increased sensitivity to specific chemical compounds. The floral scents of euglossine-pollinated plants are hypothesized to have evolved in response to the preexisting sensory biases of their male euglossine bee pollinators. However, this has never been investigated at the peripheral olfactory circuitry of distinct pollinating genera. Here, we present a comparative analysis using electroantennography (EAG) of males across the phylogeny of 29 euglossine bee species, among them Euglossa and Eulaema species. First, we tested whether antennal responses differ among different euglossine genera, subgenera and species. Secondly, we conducted a comparative phylogenetic analysis to investigate the macroevolutionary patterns of antennal responses across the euglossine bee phylogeny. We found that antennal response profiles are very unique on the species level and differ on the subgenus and the genus level. The differences can be explained by chemical compounds typically found in the floral scent bouquets of perfume flowers and specific compounds of species either pollinated by Euglossa (e.g., ipsdienol) or Eulaema bees (e.g., (−)-(E)-carvone epoxide). Also, we detected a phylogenetic signal in mean antennal responses and found that especially at the species level of our simulation the overall antennal responses exhibit greater disparity relative to a null model of pure Brownian-motion across the phylogeny. Altogether, our results suggest that (1) euglossine bee species exhibit species-specific antennal responses that differ among euglossine genera and subgenera, (2) antennal responses diverge early after speciation events, and (3) scent composition of perfume flowers evolved in response to pollinator-mediated selection imposed by preexisting sensory biases in euglossine bees.

Floral Scent Chemistry and Pollinators of a Sexually Dimorphic Neotropical Orchid

“…Consequently, pollination systems of unisexual flowers could ensure pollen transfer for the host plant through the similarity of the floral scents, which should guarantee a floral constancy of the pollinators [ 15 , 28 ]. Thus, the occurrence of sexually mono- and dimorphic scent patterns within the genus Catasetum might reflect the distinct selective pressures as a consequence of olfactory/behavioural biases of specific euglossine pollinators [ 10 , 17 , 29 ].…”

The volatile chemistry of orchid pollination

“…52,53,[73][74][75]97 Linalool (37) has also been conrmed to be active in eld bioassays to the euglossine bee pollinators of several perfume rewarding orchids. 94,[98][99][100] Terpenoids 38 and 39 have also been conrmed as behaviourally active to the male Eulama euglossine bee pollinator of the orchid Sarcoglottis acaulis in eld studies. Interestingly, in this case the typical perfume collecting behaviour was not observed at either the orchid ower or the chemical baits, and instead pollinators appeared to forage for nectar, despite the specic attraction of males.…”

“…94 More recently, this isomer has also been shown to elicit strong antennal responses from many other species of perfume-collecting bees across several genera. 98 The related 1,2,4-trimethoxybenzene (59) has also been shown to elicit antennal responses in several perfume-collecting bee species. 98,113 Outside of perfume rewarding systems, Salzmann et al 141 found that the volatile prole of the bumblebee-pollinated Anacamptis coriophora was dominated by benzenoids, most notably 58 and 4-methoxybenzaldehyde.…”

“…98 The related 1,2,4-trimethoxybenzene (59) has also been shown to elicit antennal responses in several perfume-collecting bee species. 98,113 Outside of perfume rewarding systems, Salzmann et al 141 found that the volatile prole of the bumblebee-pollinated Anacamptis coriophora was dominated by benzenoids, most notably 58 and 4-methoxybenzaldehyde. These two compounds were the only compounds emitted by the orchid found to elicit a response from Bombus terrestris queen antennae.…”

“Complexity of the male perfume of Eulaema nigrita L. (Apidae: Euglossini) from forest and woody physiognomies of the Brazilian savanna: is there a relationship with body size and wing wear?”,

“…Although the exact role of orchid bee perfume is unknown, previous works showed evidence about its importance as a sexual signaling trait involved in the reproductive isolation of species on sensory Mitko et al 2016;Brandt et al 2021), behavioral (Eltz et al 2008), and macroevolutionary scale (Zimmermann et al 2009;Weber et al 2016). Terpenes, aromatics and other organic compounds make up the bouquets and have demonstrated its role as highly specialized signaling markers at the species level (Eltz et al 2006;Eltz et al 2008).…”