Abstract
Differential visitation of pollinators due to divergent floral traits can lead to reproductive isolation via assortative pollen flow, which may ultimately be a driving force in plant speciation, particularly in areas of overlap. We evaluate the effects of pollinator behavioral responses to variation of intraspecific floral color and nectar rewards, on reproductive isolation between two hybrid flower color morphs (fuchsia and blue) and their parental species Penstemon roseus and P. gentianoides with a mixed-pollination system. We show that pollinators (bumblebees and hummingbirds) exhibit different behavioral responses to fuchsia and blue morphs, which could result from differential attraction or deterrence. In addition to differences in color (spectral reflectance), we found that plants with fuchsia flowers produced more and larger flowers, produced more nectar and were more visited by pollinators than those with blue flowers. These differences influenced the foraging behavior and effectiveness as pollinators of both bumblebees and hummingbirds, which contributed to reproductive isolation between the two hybrid flower color morphs and parental species. This study demonstrates how differentiation of pollination traits promotes the formation of hybrid zones leading to pollinator shifts and reproductive isolation. While phenotypic traits of fuchsia and red flowers might encourage more efficient hummingbird pollination in a mixed-pollination system, the costs of bumblebee pollination on plant reproduction could be the drivers for the repeated shifts from bumblebee- to hummingbird-mediated pollination.
Highlights
Transitions from one to another pollinator type have played a fundamental role in divergence of flower phenotypes, development of reproductive isolation among incipient species and, in the origin and diversification of Angiosperms[1,2,3]
We addressed the following questions: (1) Are the parental species, P. gentianoides and P. roseus, and their hybrids distinguishable by bumblebees and hummingbirds? (2) Do parental species and hybrid flower color morphs differ in their detectability when considering the visual color abilities of bumblebees and hummingbirds? (3) Is the natural variation in floral and nectar traits associated with differences in foraging behavior and pollinator effectiveness of floral visitors? (4) Do female reproductive success and reproductive isolation (RI) differ between the flower color morphs and parental species?
Our results indicate that P. roseus and fuchsia flowers conform with recent evidence for repeated transitions toward increased nectar production in hummingbird-syndrome Penstemon[18,46], and that evolutionary transitions from one syndrome to another require changes in multiple floral traits required for pollination syndrome evolution[16,18,53]
Summary
Transitions from one to another pollinator type have played a fundamental role in divergence of flower phenotypes, development of reproductive isolation among incipient species and, in the origin and diversification of Angiosperms[1,2,3]. Transitions to hummingbird pollination in Penstemon are usually associated with the evolution of bright red to magenta, long and narrow flowers that have exserted reproductive organs and produce large amounts of dilute nectar[2,17,18,35,39,40]. Despite this and other changes in floral dimension and flower orientation, the majority of the pollination-syndrome transitions in Penstemon seem to be more predicted by transitions from blue-purple to red flowers[17]. These transitions involve the loss of the enzyme that is responsible for converting precursors of red pigments into those of blue pigments[41], which strongly hinder evolutionary reversals in Penstemon[42]
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