A striking characteristic of the Western North American flora is the repeated evolution of hummingbird pollination from insect-pollinated ancestors. This pattern has received extensive attention as an opportunity to study repeated trait evolution as well as potential constraints on evolutionary reversibility, with little attention focused on the impact of these transitions on species diversification rates. Yet traits conferring adaptation to divergent pollinators potentially impact speciation and extinction rates, because pollinators facilitate plant reproduction and specify mating patterns between flowering plants. Here, we examine macroevolutionary processes affecting floral pollination syndrome diversity in the largest North American genus of flowering plants, Penstemon. Within Penstemon, transitions from ancestral bee-adapted flowers to hummingbird-adapted flowers have frequently occurred, although hummingbird-adapted species are rare overall within the genus. We inferred macroevolutionary transition and state-dependent diversification rates and found that transitions from ancestral bee-adapted flowers to hummingbird-adapted flowers are associated with reduced net diversification rate, a finding based on an estimated 17 origins of hummingbird pollination in our sample. Although this finding is congruent with hypotheses that hummingbird adaptation in North American Flora is associated with reduced species diversification rates, it contrasts with studies of neotropical plant families where hummingbird pollination has been associated with increased species diversification. We further used the estimated macroevolutionary rates to predict the expected pattern of floral diversity within Penstemon over time, assuming stable diversification and transition rates. Under these assumptions, we find that hummingbird-adapted species are expected to remain rare due to their reduced diversification rates. In fact, current floral diversity in the sampled Penstemon lineage, where less than one-fifth of species are hummingbird adapted, is consistent with predicted levels of diversity under stable macroevolutionary rates.
Pendulous flowers (due to a flexible pedicel) are a common, convergent trait of hummingbird-pollinated flowers. However, the role of flexible pedicels remains uncertain despite several functional hypotheses. Here we present and test the ‘lever action hypothesis’: flexible pedicels allow pendulous flowers to move upwards from all sides, pushing the stigma and anthers against the underside of the feeding hummingbird regardless of which nectary is being visited.
To test whether this lever action increased pollination success, we wired emasculated flowers of serpentine columbine, Aquilegia eximia, to prevent levering and compared pollination success of immobilized flowers with emasculated unwired and wire controls.
Seed set was significantly lower in wire-immobilized flowers than unwired control and wire control flowers. Video analysis of visits to wire-immobilized and unwired flowers demonstrated that birds contacted the stigmas and anthers of immobilized flowers less often than those of flowers with flexible pedicels.
We conclude that flexible pedicels permit the levering of reproductive structures onto a hovering bird. Hummingbirds, as uniquely large, hovering pollinators, differ from flies or bees which are too small to cause levering of flowers while hovering. Thus, flexible pedicels may be an adaptation to hummingbird pollination, in particular due to hummingbird size. We further speculate that this mechanism is effective only in radially symmetric flowers; in contrast, zygomorphic hummingbird-pollinated flowers are usually more or less horizontally oriented rather than having pendulous flowers and flexible pedicels.
- Award ID(s):
- 1831164
- NSF-PAR ID:
- 10130134
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Annals of Botany
- Volume:
- 125
- Issue:
- 1
- ISSN:
- 0305-7364
- Page Range / eLocation ID:
- p. 59-65
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract -
more » « less
Premise Variation in pollen‐ovule ratios is thought to reflect the degree of pollen transfer efficiency—the more efficient the process, the fewer pollen grains needed. Few studies have directly examined the relationship between pollen‐ovule ratio and pollen transfer efficiency. For active pollination in the pollination brood mutualisms of yuccas and yucca moths, figs and fig wasps, senita and senita moths, and leafflowers and leafflower moths, pollinators purposefully collect pollen and place it directly on the stigmatic surface of conspecific flowers. The tight coupling of insect reproductive interests with pollination of the flowers in which larvae develop ensures that pollination is highly efficient.
Methods We used the multiple evolutionary transitions between passive pollination and more efficient active pollination to test if increased pollen transfer efficiency leads to reduced pollen‐ovule ratios. We collected pollen and ovule data from a suite of plant species from each of the pollination brood mutualisms and used phylogenetically controlled tests and sister‐group comparisons to examine whether the shift to active pollination resulted in reduced pollen‐ovule ratios.
Results Across all transitions between passive and active pollination in plants, actively pollinated plants had significantly lower pollen‐ovule ratios than closely related passively pollinated taxa. Phylogenetically corrected comparisons demonstrated that actively pollinated plant species had an average 76% reduction in the pollen‐ovule ratio.
Conclusions The results for active pollination systems support the general utility of pollen‐ovule ratios as indicators of pollination efficiency and the central importance of pollen transfer efficiency in the evolution of pollen‐ovule ratio.
-
more » « less
Abstract Premise A switch in pollinator can occur when a plant lineage enters a new habitat where the ancestral pollinator is less common, and a novel pollinator is more common. Because pollinator communities vary according to environmental tolerances and availability of resources, there may be consistent associations between pollination mode and specific regions and habitats. Such associations can be studied in lineages that have experienced multiple pollinator transitions, representing evolutionary replicates.
Methods Our study focused on a large clade of
Penstemon wildflower species in western North America, which has repeatedly evolved hummingbird‐adapted flowers from ancestral bee‐adapted flowers. For each species, we estimated geographic ranges from occurrence data and inferred environmental niches from climate, topographical, and soil data. Using a phylogenetic comparative approach, we investigated whether hummingbird‐adapted species occupy distinct geographic regions or habitats relative to bee‐adapted species.Results Hummingbird‐adapted species occur at lower latitudes and lower elevations than bee‐adapted species, resulting in a difference in their environmental niche. Bee‐adapted species sister to hummingbird‐adapted species are also found in relatively low elevations and latitudes, similar to their hummingbird‐adapted sister species, suggesting ecogeographic shifts precede pollinator divergence. Sister species pairs—regardless of whether they differ in pollinator—show relatively little geographic range overlap.
Conclusions Adaptation to a novel pollinator may often occur in geographic and ecological isolation from ancestral populations. The ability of a given lineage to adapt to novel pollinators may critically depend on its ability to colonize regions and habitats associated with novel pollinator communities.
-
more » « less
Premise Closely related plant species with overlapping ranges often experience competition for pollination services. Such competition can select for divergence in floral traits that attract pollinators or determine pollen placement. While most species in
Centropogon (Campanulaceae: Lobelioideae) have flowers that suggest adaptation to bat or hummingbird pollination, actual pollinators are rarely documented, and a few species have a mix of traits from both pollination syndromes. We studied the pollination biology of a “mixed‐syndrome” species and its co‐occurring congeners to examine the relationship between floral traits and visitation patterns forCentropogon .Methods Fieldwork at two sites in Bolivian cloud forests involved filming floral visitors, quantifying pollen transfer, and measuring floral traits. Stamen exsertion, which determines pollen placement, was measured from herbarium specimens across the geographic range of these species to test for character displacement.
Results Results show a generalization gradient, from primarily bat pollination in white‐flowered
Centropogon incanus , to bat pollination with secondary hummingbird pollination in the cream‐floweredC. brittonianus , to equal reliance on both pollinators in the red‐flowered, mixed‐syndromeC. mandonis . Pollen transfer between these species is further reduced by differences in stamen exsertion that are accentuated in zones of sympatry, a pattern consistent with character displacement.Conclusions Our results demonstrate that key differences in floral color and shape mediate a gradient of specialization in Bolivian
Centropogon . Interspecific pollen transfer is further reduced by potential character displacement of a key trait. Broadly, our results have implications for understanding the hyper‐diversity of Andean cloud forests, in which multiple species of the same genus frequently co‐occur. -
more » « less
Abstract Angiosperm flowers have diversified in adaptation to pollinators, but are also shaped by developmental and genetic histories. The relative importance of these factors in structuring floral diversity remains unknown. We assess the effects of development, function and evolutionary history by testing competing hypotheses on floral modularity and shape evolution in Merianieae (Melastomataceae). Merianieae are characterized by different pollinator selection regimes and a developmental constraint: tubular anthers adapted to specialized buzz-pollination. Our analyses of tomography-based 3-dimensional flower models show that pollinators selected for functional modules across developmental units and that patterns of floral modularity changed during pollinator shifts. Further, we show that modularity was crucial for Merianieae to overcome the constraint of their tubular anthers through increased rates of evolution in other flower parts. We conclude that modularity may be key to the adaptive success of functionally specialized pollination systems by making flowers flexible (evolvable) for adaptation to changing selection regimes.
