An Olfactory Shift Is Associated with Male Perfume Differentiation and Species Divergence in Orchid Bees

Abstract

Saltational changes may underlie the diversification of pheromone communication systems in insects, which are normally under stabilizing selection favoring high specificity in signals and signal perception. In orchid bees (Euglossini), the production of male signals depends on the sense of smell: males collect complex blends of volatiles (perfumes) from their environment, which are later emitted as pheromone analogs at mating sites. We analyzed the behavioral and antennal response to perfume components in two male morphotypes of Euglossa cf. viridissima from Mexico, which differ in the number of mandibular teeth. Tridentate males collected 2-hydroxy-6-nona-1,3-dienyl-benzaldehyde (HNDB) as the dominant component of their perfume. In bidentate males, blends were broadly similar but lacked HNDB. Population genetic analysis revealed that tri- and bidentate males belong to two reproductively isolated lineages. Electroantennogram tests (EAG and GC-EAD) showed substantially lower antennal responses to HNDB in bidentate versus tridentate males, revealing for the first time a mechanism by which closely related species acquire different chemical compounds from their habitat. The component-specific differences in perfume perception and collection in males of two sibling species are in agreement with a saltational, olfaction-driven mode of signal perfume evolution. However, the response of females to the diverged signals remains unknown.

Olfactory specialization for perfume collection in male orchid bees

“…This compound elicited a strong response exclusively in Euglossa mixta, which is the only species investigated here that contains HNDB in its hind legs. Antennal responses to HNDB were previously found to be high in Mexican Euglossa dilemma, which also collects and contains HNDB, but not in its sympatric sibling species, Euglossa viridissima, which does not (Eltz et al, 2008). Thus, E. dilemma, which is distributed from central Mexico to western Costa Rica, and E. mixta, distributed from southern Mexico to Brazil, uniquely share both behavioral preferences and high antennal sensitivity for HNDB.…”

“…In the case of male orchid bees, olfactory specialization is expected because detecting and finding scattered perfume sources may entail traveling long distances (Pokorny et al, 2015). Species-specific perfume preferences were previously shown to have led to species-and compound-specific antennal specialization (Eltz et al, , 2008Schiestl and Roubik, 2003). The present study is the first, however, to compare antennal response profiles across a larger number of species in a phylogenetic framework.…”

“…In order to reveal potential sensory adaptations, we used electroantennography (EAG) to screen overall antennal sensitivity for a large range of substances. This method is generally suitable to detect sensory specialization in the antennae (Roelofs, 1984) and has been used to investigate odor detection in diverse insects (Schiestl and Marion-Poll, 2002), including orchid bees (Eltz et al, , 2008Eltz and Lunau, 2005;Milet-Pinheiro et al, 2015;Schiestl and Roubik, 2003). We used two different approaches.…”

Identification of cryptic species and morphotypes in male Euglossa: morphometric analysis of forewings (Hymenoptera: Euglossini)

“…Due to their particular mode of sexual attraction, seemly based on non-visual mating signals (chemical display by males; Eltz et al 2005), species of euglossines could have diverged without substantial changes in morphology and meristic characters (Eltz et al 2008), thus remaining cryptic under traditional alpha taxonomy (Bickford et al 2007). In this respect, geometric morphometrics data can be of much help in the taxonomic revision of euglossines.…”

Two common species dominate the species-rich Euglossine bee fauna of an Atlantic Rainforest remnant in Pernambuco, Brazil

“…amazonica on a total of six. To better understand the relationships of male euglossine bees to floral perfumes and their sensory ability to smell specific scent compounds, it is necessary to apply chemo-ecological tools, for example to test for electrophysiological antennal responses of the different species (see for example Eltz et al, 2008).…”