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

   https://doi.org/10.1371/journal.pbio.3002294  

   Wessinger, Carolyn A.; Katzer, Amanda M.; Hime, Paul M.; Rausher, Mark D.; Kelly, John K.; Hileman, Lena C. (September 2023, PLOS Biology)

   Barton, Nick H. (Ed.)

   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 genusPenstemondisplays 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 aPenstemonspecies 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, genome-wide 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 genome-wided_XY. However, a small number of genetic loci are strongly differentiated between species. These approximately 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 quantitative trait loci (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. 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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3. 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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4. Evolutionary convergence on hummingbird pollination in Neotropical Costus provides insight into the causes of pollinator shifts

   https://doi.org/10.1111/nph.18464  

   Kay, Kathleen M.; Grossenbacher, Dena L. (September 2022, New Phytologist)

   Summary The evolution of hummingbird pollination is common across angiosperms throughout the Americas, presenting an opportunity to examine convergence in both traits and environments to better understand how complex phenotypes arise. Here we examine independent shifts from bee to hummingbird pollination in the Neotropical spiral gingers (Costus) and address common explanations for the prevalence of transitions from bee to hummingbird pollination.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 correlate with elevation or climate.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 climate.Evolutionary shifts to hummingbird pollination inCostusare highly convergent and directional, involve a surprising set of traits when compared with other plants with analogous transitions and refute the generality of several common explanations for the prevalence of transitions from bee to hummingbird pollination. 

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5. The genetic architecture of floral trait divergence between hummingbird‐ and self‐pollinated monkeyflower ( Mimulus ) species

   https://doi.org/10.1111/nph.20348  

   Chen, Hongfei; Berg, Colette_S; Samuli, Matthew; Sotola, V_Alex; Sweigart, Andrea_L; Yuan, Yao‐Wu; Fishman, Lila (December 2024, New Phytologist)

   Summary Pollination syndromes are a key component of flowering plant diversification, prompting questions about the architecture of single traits and genetic coordination among traits. Here, we investigate the genetics of extreme floral divergence between naturally hybridizing monkeyflowers,Mimulus parishii(self‐pollinated) andM. cardinalis(hummingbird‐pollinated).We mapped quantitative trait loci (QTLs) for 18 pigment, pollinator reward/handling, and dimensional traits in parallel sets of F₂hybrids plus recombinant inbred lines and generated nearly isogenic lines (NILs) for two dimensional traits, pistil length and corolla size.Our multi‐population approach revealed a highly polygenic basis (n = 190 QTLs total) for pollination syndrome divergence, capturing minor QTLs even for pigment traits with leading major loci. There was significant QTL overlap within pigment and dimensional categories. Nectar volume QTLs clustered with those for floral dimensions, suggesting a partially shared module. The NILs refined two pistil length QTLs, only one of which has tightly correlated effects on other dimensional traits.An overall polygenic architecture of floral divergence is partially coordinated by genetic modules formed by linkage (pigments) and likely pleiotropy (dimensions plus nectar). This work illuminates pollinator syndrome diversification in a model radiation and generates a robust framework for molecular and ecological genomics. 

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