Abstract

•Background and Aims Animal-pollinated angiosperms have evolved a variety of signalling mechanisms to attract pollinators. Floral scent is a key component of pollinator attraction, and its chemistry modulates both pollinator behaviour and the formation of plant–pollinator networks. The neotropical orchid genus Gongora exhibits specialized pollinator associations with male orchid bees (Euglossini). Male bees visit orchid flowers to collect volatile chemical compounds that they store in hind-leg pouches to use subsequently during courtship display. Hence, Gongora floral scent compounds simultaneously serve as signalling molecules and pollinator rewards. Furthermore, because floral scent acts as the predominant reproductive isolating barrier among lineages, it has been hypothesized that chemical traits are highly species specific. A comparative analysis of intra- and inter-specific variation of floral scent chemistry was conducted to investigate the evolutionary patterns across the genus.•Methods Gas chromatography–mass spectrometry (GC-MS) was used to analyse the floral scent of 78 individuals belonging to 28 different species of Gongora from two of the three major lineages sampled across the neotropical region. Multidimensional scaling and indicator value analyses were implemented to investigate the patterns of chemical diversity within and among taxonomic groups at various geographic scales. Additionally, pollinator observations were conducted on a sympatric community of Gongora orchids exhibiting distinct floral scent phenotypes.•Key Results A total of 83 floral volatiles, mainly terpenes and aromatic compounds, were detected. Many of the identified compounds are common across diverse angiosperm families (e.g. cineole, eugenol, β-ocimene, β-pinene and terpinen-4-ol), while others are relatively rare outside euglossine bee-pollinated orchid lineages. Additionally, 29 volatiles were identified that are known to attract and elicit collection behaviour in male bees. Floral scent traits were less variable within species than between species, and the analysis revealed exceptional levels of cryptic diversity. Gongora species were divided into 15 fragrance groups based on shared compounds. Fragrance groups indicate that floral scent variation is not predicted by taxonomic rank or biogeographic region.•Conclusions Gongora orchids emit a diverse array of scent molecules that are largely species specific, and closely related taxa exhibit qualitatively and quantitatively divergent chemical profiles. It is shown that within a community, Gongora scent chemotypes are correlated with near non-overlapping bee pollinator assemblies. The results lend support to the hypothesis that floral scent traits regulate the architecture of bee pollinator associations. Thus, Gongora provides unique opportunities to examine the interplay between floral traits and pollinator specialization in plant–pollinator mutualisms.

Highlights

  • Mutualisms between flowering plants and their insect pollinators have shaped the evolution of floral traits and are thought to contribute significantly to angiosperm diversification (Darwin, 1862; Crepet, 1984; Johnson, 1996; Dodd, et al, 1999; Kay, 2006; Kay and Sargent, 2009; Schiestl and Schluter, 2009; van der Niet et al, 2014; Breitkopf et al, 2015)

  • Angiosperms emit an exceptionally diverse array of floral scent molecules (Knudsen et al, 1993; Knudsen and Gershenzon, 2006), and many classes of volatile compounds are recurrently associated with specific pollinators, suggesting that olfactory sensory mechanisms and behavioural preferences of pollinators have shaped the evolution of floral scent chemistry (Schiestl et al, 2010; Ramırez et al, 2011; Steiger et al, 2011; Schiestl and Dotterl, 2012; Jurgens et al, 2013)

  • We examined the distribution of floral scent in the genus Gongora across geography

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Summary

Introduction

Mutualisms between flowering plants and their insect pollinators have shaped the evolution of floral traits and are thought to contribute significantly to angiosperm diversification (Darwin, 1862; Crepet, 1984; Johnson, 1996; Dodd, et al, 1999; Kay, 2006; Kay and Sargent, 2009; Schiestl and Schluter, 2009; van der Niet et al, 2014; Breitkopf et al, 2015). Floral scent is thought to play a central role in mediating pollinator attraction and specificity, especially among highly specialized plant–pollinator interactions (Raguso, 2001; Schiestl and Ayasse, 2002; Mant et al, 2005; Peakall et al, 2010; Willmer, 2011; Xu et al, 2011; Jurgens et al, 2013; Peakall and Whitehead, 2014; van der Niet et al, 2014). The neotropical orchid genus Gongora (Orchidaceae: Cymbidieae) exhibits specialized mutualistic associations with scent-collecting male euglossine bees (Fig. 1), in which floral scent volatiles act simultaneously as attractant molecules and insect pollinator rewards (Dodson et al, 1969). Pollinator observations were conducted on a sympatric community of Gongora orchids exhibiting distinct floral scent phenotypes

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