Flower Diversification Across “Pollinator Climates”: Sensory Aspects of Corolla Color Evolution in the Florally Diverse South American Genus Jaborosa (Solanaceae)

Abstract

Flower phenotype may diverge within plant lineages when moving across “pollinator climates” (geographic differences in pollinator abundance or preference). Here we explored the potential importance of pollinators as drivers of floral color diversification in the nightshade genus Jaborosa, taking into account color perception capabilities of the actual pollinators (nocturnal hawkmoths vs. saprophilous flies) under a geographic perspective. We analyzed the association between transitions across environments and perceptual color axes using comparative methods. Our results revealed two major evolutionary themes in Jaborosa: (1) a “warm subtropical sphingophilous clade” composed of three hawkmoth-pollinated species found in humid lowland habitats, with large white flowers that clustered together in the visual space of a model hawkmoth (Manduca sexta) and a “cool-temperate brood-deceptive clade” composed of largely fly-pollinated species with small dark flowers found at high altitudes (Andes) or latitudes (Patagonian Steppe), that clustered together in the visual space of a model blowfly (Lucilia sp.) and a syrphid fly (Eristalis tenax). Our findings suggest that the ability of plants to colonize newly formed environments during Andean orogeny and the ecological changes that followed were concomitant with transitions in flower color as perceived by different pollinator functional groups. Our findings suggest that habitat and pollination mode are inextricably linked in the history of this South American plant lineage.

Floral Scent Evolution in the Genus Jaborosa (Solanaceae): Influence of Ecological and Environmental Factors

“…In the Subtropical Lowland clade, the scent blends of J. odonelliana and J. integrifolia , which replace each other ecologically from east to west in northern Argentina (see Figure 1 in ref. [ 56 ]), shared oxygenated sesquiterpenoids ((E)-nerolidol, isomers of farnesol and (E,E)-farnesal), whereas the floral scent of partially sympatric J. integrifolia and J. runcinata overlapped in a few aromatic compounds (benzyl alcohol, benzaldehyde, benzyl benzoate), with additional related compounds (methyl benzoate, methyl salicylate) unique to the more complex blend of J. integrifolia . Available evidence indicates that these three species are pollinated infrequently by large nocturnal moths [ 56 ].…”

“…We were motivated to study the evolution of floral scent in the genus Jaborosa because the two primary modes of pollination are so utterly different (i.e., brood site deception of saprophilous flies vs. honest nectar-rewarding pollination by hawkmoths), as are the geographic distributions associated with distinct pollinator climates [ 56 ]. To achieve our goal, we surmounted several challenges.…”

“…In particular, we considered that the nightshade genus Jaborosa Juss., with two clades showing different ecological histories and contrasting pollination environments (hawkmoths, saprophilous flies and generalized small insects [ 55 , 56 ]), presents an opportunity to explore the evolution of floral scent under novel pollinator climates. The aim of this study was to chemically characterize floral scent in the two clades of Jaborosa , that have different geographic affinities: the “Subtropical Lowland clade” includes species inhabiting lowland areas, and the “Andean clade” includes species mainly distributed across the Andes mountain range and Patagonian steppe of temperate South America.…”

“…The aim of this study was to chemically characterize floral scent in the two clades of Jaborosa , that have different geographic affinities: the “Subtropical Lowland clade” includes species inhabiting lowland areas, and the “Andean clade” includes species mainly distributed across the Andes mountain range and Patagonian steppe of temperate South America. A previous study suggested that the ability of Jaborosa species to colonize newly formed environments during Andean orogeny and its subsequent ecological changes were concomitant with transitions in flower color, as perceived by different pollinator functional groups [ 56 ]. Here, we asked whether Jaborosa species with different pollination modes differ predictably in floral scent profiles, taking into account the evolutionary and geoclimatic context of diversification across the genus.…”

“…Here, we asked whether Jaborosa species with different pollination modes differ predictably in floral scent profiles, taking into account the evolutionary and geoclimatic context of diversification across the genus. Our previous studies of Jaborosa have addressed functional aspects of floral scent in focal case studies [ 57 , 58 ], phylogenetic reconstruction [ 55 ] and broader genus-wide trends in flower color as perceived by pollinators [ 56 ]. Here, we have used an ecological niche modelling (ENM) approach to analyze which environmental variable(s) (e.g., latitude, elevation, temperature, and precipitation) have exerted the strongest influence on floral scent profiles across a broader sample (eight spp.)…”