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1. Data from: A few essential genetic loci distinguish Penstemon species with flowers adapted to pollination by bees or hummingbirds

   https://doi.org/10.5061/dryad.xpnvx0kmp  

   Wessinger, Carolyn ( January 2023 , Dryad)

   In the formation of species, adaptation by natural selection generates distinct combinations of traits that function well together. The maintenance of adaptive trait combinations in the face of gene flow depends on the strength and nature of selection acting on the underlying genetic loci. Floral pollination syndromes exemplify the evolution of trait combinations adaptive for particular pollinators. The North American wildflower genus Penstemon displays remarkable floral syndrome convergence, with at least 20 separate lineages that have evolved from ancestral bee pollination syndrome (wide blue-purple flowers that present a landing platform for bees and small amounts of nectar) to hummingbird pollination syndrome (bright red narrowly tubular flowers offering copious nectar). Related taxa that differ in floral syndrome offer an attractive opportunity to examine the genomic basis of complex trait divergence. In this study, we characterized genomic divergence among 229 individuals from a Penstemon species complex that includes both bee and hummingbird floral syndromes. Field plants are easily classified into species based on phenotypic differences and hybrids displaying intermediate floral syndromes are rare. Despite unambiguous phenotypic differences, genomewide differentiation between species is minimal. Hummingbird-adapted populations are more genetically similar to nearby bee-adapted populations than to geographically distant hummingbird-adapted populations, in terms of genomewide dXY. However, a small number of genetic loci are strongly differentiated between species. These ~ 20 "species-diagnostic loci", which appear to have nearly fixed differences between pollination syndromes, are sprinkled throughout the genome in high recombination regions. Several map closely to previously established floral trait QTLs. The striking difference between the diagnostic loci and the genome as whole suggests strong selection to maintain distinct combinations of traits, but with sufficient gene flow to homogenize the genomic background. A surprisingly small number of alleles confer phenotypic differences that form the basis of species identity in this species complex. 

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2. Nectary size is a pollination syndrome trait in Penstemon

   https://doi.org/10.1111/nph.15769  

   Katzer, Amanda M. ; Wessinger, Carolyn A. ; Hileman, Lena C. ( March 2019 , New Phytologist)

   Evolution of complex phenotypes depends on the adaptive importance of individual traits, and the developmental changes required to modify traits. Floral syndromes are complex adaptations to pollinators that include color, nectar, and shape variation. Hummingbird‐adapted flowers have evolved a remarkable number of times from bee‐adapted ancestors inPenstemon, and previous work demonstrates that color over shape better distinguishes bee from hummingbird syndromes. Here, we examined the relative importance of nectar volume and nectary development in definingPenstemonpollination syndromes.

   We tested the evolutionary association of nectar volume and nectary area with pollination syndrome across 19Penstemonspecies. In selected species, we assessed cellular‐level processes shaping nectary size. Within a segregating population from an intersyndrome cross, we assessed trait correlations between nectar volume, nectary area, and the size of stamens on which nectaries develop.

   Nectar volume and nectary area displayed an evolutionary association with pollination syndrome. These traits were correlated within a genetic cross, suggesting a mechanistic link. Nectary area evolution involves parallel processes of cell expansion and proliferation.

   Our results demonstrate that changes to nectary patterning are an important contributor to pollination syndrome diversity and provide further evidence that repeated origins of hummingbird adaptation involve parallel developmental processes inPenstemon.

    

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3. Adaptation to hummingbird pollination is associated with reduced diversification in Penstemon

   https://doi.org/10.1002/evl3.130  

   Wessinger, Carolyn_A ; Rausher, Mark_D ; Hileman, Lena_C ( October 2019 , Evolution Letters)

   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.

    

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4. Convergence without divergence in North American red-flowering Silene

   https://doi.org/10.3389/fpls.2022.945806  

   Berardi, Andrea E. ; Betancourt Morejón, Ana C. ; Hopkins, Robin ( September 2022 , Frontiers in Plant Science)

   Combinations of correlated floral traits have arisen repeatedly across angiosperms through convergent evolution in response to pollinator selection to optimize reproduction. While some plant groups exhibit very distinct combinations of traits adapted to specific pollinators (so-called pollination syndromes), others do not. Determining how floral traits diverge across clades and whether floral traits show predictable correlations in diverse groups of flowering plants is key to determining the extent to which pollinator-mediated selection drives diversification. The North AmericanSilenesectionPhysolychnisis an ideal group to investigate patterns of floral evolution because it is characterized by the evolution of novel red floral color, extensive floral morphological variation, polyploidy, and exposure to a novel group of pollinators (hummingbirds). We test for correlated patterns of trait evolution that would be consistent with convergent responses to selection in the key floral traits of color and morphology. We also consider both the role of phylogenic distance and geographic overlap in explaining patterns of floral trait variation. Inconsistent with phenotypically divergent pollination syndromes, we find very little clustering of North AmericanSileneinto distinct floral morphospace. We also find little evidence that phylogenetic history or geographic overlap explains patterns of floral diversity in this group. White- and pink-flowering species show extensive phenotypic diversity but are entirely overlapping in morphological variation. However, red-flowering species have much less phenotypic disparity and cluster tightly in floral morphospace. We find that red-flowering species have evolved floral traits that align with a traditional hummingbird syndrome, but that these trait values overlap with several white and pink species as well. Our findings support the hypothesis that convergent evolution does not always proceed through comparative phenotypic divergence, but possibly through sorting of standing ancestral variation.

    

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5. Evolutionary convergence on hummingbird pollination in Neotropical Costus provide insight into the causes of pollinator shifts

   https://doi.org/10.7291/D1C39G  

   Kay, Kathleen ; Grossenbacher, Dena ( January 2022 , Dryad)

   1. The evolution of hummingbird pollination is common across angiosperm lineages throughout the Americas, presenting an opportunity to examine convergence in both traits and environments to better understand how complex phenotypes arise. We examine multiple independent shifts from bee to hummingbird pollination in the Neotropical spiral gingers (Costus) and use our data to address several common explanations for the prevalence of bee to bird pollination transitions. 2. We use floral traits of species with observed pollinators to predict pollinators of unobserved species and reconstruct ancestral pollination states on a well-resolved phylogeny. We examine whether independent transitions evolve towards the same phenotypic optimum and whether shifts to hummingbird pollination are associated with high elevation or climatic niche. 3. Traits predicting hummingbird pollination include small flower size, brightly-colored floral bracts, and the absence of nectar guides. We find many shifts to hummingbird pollination and no reversals, a single shared phenotypic optimum across hummingbird flowers, and no association between pollination and elevation or climatic niche. 4. Costus presents surprising findings compared to other plant clades. Hummingbird flowers are consistently smaller than bee flowers and primary flower colors are not predictive of pollinators. Moreover, hummingbird pollination shows no association with high elevation, as found in other tropical plants. 

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