Abstract
Most flowering plants depend on animal pollination for successful sexual reproduction. Floral signals such as color, shape, and odor are crucial in establishing this (often mutualistic) interaction. Plant and pollinator phenotypes can vary temporally but also spatially, thus creating mosaic-like patterns of local adaptations. Here, we investigated natural variation in floral morphology, flower volatile emission, and phenology in four accessions of a self-compatible wild tobacco, Nicotiana attenuata, to assess how these traits match the sensory perception of a known pollinator, the hawkmoth Manduca sexta. These accessions differ in floral traits and also in their habitat altitudes. Based on habitat temperatures, the accession occurring at the highest altitude (California) is less likely to be visited by M. sexta, while the others (Arizona, Utah 1, and Utah 2) are known to receive M. sexta pollinations. The accessions varied significantly in flower morphologies, volatile emissions, flower opening, and phenology, traits likely important for M. sexta perception and floral handling. In wind tunnel assays, we assessed the seed set of emasculated flowers after M. sexta visitation and of natural selfed and hand-pollinated selfed flowers. After moth visitations, plants of two accessions (Arizona and Utah 2) produced more capsules than the other two, consistent with predictions that accessions co-occurring with M. sexta would benefit more from the pollination services of this moth. We quantified flower and capsule production in four accessions in a glasshouse assay without pollinators to assess the potential for self-pollination. The two Utah accessions set significantly more seeds after pollen supplementation compared with those of autonomous selfing flowers, suggesting a greater opportunistic benefit from efficient pollinators than the other two. Moreover, emasculated flowers of the accession with the most exposed stigma (Utah 2) produced the greatest seed set after M. sexta visitation. This study reveals intraspecific variation in pollination syndromes that illuminate the potential of a plant species to adapt to local pollinator communities, changing environments, and altered pollination networks.
Highlights
Flowers exploit the sensory bias of insect pollinators to improve their chance of receiving outcrossed (Balamurali et al, 2015) or at least geitonogamous pollinations (Vaughton and Ramsey, 2010; Sukumaran et al, 2020), the opportunities for which differ considerably depending on plant densities, interpopulation distances, and phenologies (Carvalheiro et al, 2014; Kantsa et al, 2018)
Previous studies examining the interaction between M. sexta and N. attenuata have shown the importance of one particular floral volatile compound, benzyl acetone (BA; Kessler et al, 2015; Haverkamp et al, 2016b)
The presence of this compound increases the foraging success of the moth, as well as the reproductive output of the plant (Haverkamp et al, 2016b). The larvae of this hawkmoth is a voracious herbivore on N. attenuata, and its attraction as pollinator brings a risk of damage (Kessler et al, 2010, 2015; Reisenman et al, 2010; Kessler, 2012). This might select against exploiting M. sexta sensory bias and pollination service in some natural populations under less beneficial growth conditions (Gómez et al, 2009b)
Summary
Flowers exploit the sensory bias of insect pollinators to improve their chance of receiving outcrossed (Balamurali et al, 2015) or at least geitonogamous pollinations (Vaughton and Ramsey, 2010; Sukumaran et al, 2020), the opportunities for which differ considerably depending on plant densities, interpopulation distances, and phenologies (Carvalheiro et al, 2014; Kantsa et al, 2018). Previous studies examining the interaction between M. sexta and N. attenuata have shown the importance of one particular floral volatile compound, benzyl acetone (BA; Kessler et al, 2015; Haverkamp et al, 2016b) The presence of this compound increases the foraging success of the moth, as well as the reproductive output of the plant (Haverkamp et al, 2016b). The larvae of this hawkmoth is a voracious herbivore on N. attenuata, and its attraction as pollinator brings a risk of damage (Kessler et al, 2010, 2015; Reisenman et al, 2010; Kessler, 2012) This might select against exploiting M. sexta sensory bias and pollination service in some natural populations under less beneficial growth conditions (Gómez et al, 2009b). We propose that some accessions are more specialized on M. sexta pollination than others, following the idea of local specialization
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