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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. 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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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. Out of Sight, Out of Mind: Widespread Nuclear and Plastid-Nuclear Discordance in the Flowering Plant Genus Polemonium (Polemoniaceae) Suggests Widespread Historical Gene Flow Despite Limited Nuclear Signal

   https://doi.org/10.1093/sysbio/syaa049  

   Rose, Jeffrey P ; Toledo, Cassio A ; Lemmon, Emily Moriarty ; Lemmon, Alan R ; Sytsma, Kenneth J ; Carstens, Bryan ( July 2020 , Systematic Biology)

   Abstract Phylogenomic data from a rapidly increasing number of studies provide new evidence for resolving relationships in recently radiated clades, but they also pose new challenges for inferring evolutionary histories. Most existing methods for reconstructing phylogenetic hypotheses rely solely on algorithms that only consider incomplete lineage sorting (ILS) as a cause of intra- or intergenomic discordance. Here, we utilize a variety of methods, including those to infer phylogenetic networks, to account for both ILS and introgression as a cause for nuclear and cytoplasmic-nuclear discordance using phylogenomic data from the recently radiated flowering plant genus Polemonium (Polemoniaceae), an ecologically diverse genus in Western North America with known and suspected gene flow between species. We find evidence for widespread discordance among nuclear loci that can be explained by both ILS and reticulate evolution in the evolutionary history of Polemonium. Furthermore, the histories of organellar genomes show strong discordance with the inferred species tree from the nuclear genome. Discordance between the nuclear and plastid genome is not completely explained by ILS, and only one case of discordance is explained by detected introgression events. Our results suggest that multiple processes have been involved in the evolutionary history of Polemonium and that the plastid genome does not accurately reflect species relationships. We discuss several potential causes for this cytoplasmic-nuclear discordance, which emerging evidence suggests is more widespread across the Tree of Life than previously thought. [Cyto-nuclear discordance, genomic discordance, phylogenetic networks, plastid capture, Polemoniaceae, Polemonium, reticulations.] 

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5. Ecological Diversification in an Adaptive Radiation of Plants: The Role of De Novo Mutation and Introgression

   https://doi.org/10.1093/molbev/msae007  

   Stone, Benjamin W ; Wessinger, Carolyn A ( January 2024 , Molecular Biology and Evolution)

   Josephs, Emily (Ed.)

   Adaptive radiations are characterized by rapid ecological diversification and speciation events, leading to fuzzy species boundaries between ecologically differentiated species. Adaptive radiations are therefore key systems for understanding how species are formed and maintained, including the role of de novo mutations versus preexisting variation in ecological adaptation and the genome-wide consequences of hybridization events. For example, adaptive introgression, where beneficial alleles are transferred between lineages through hybridization, may fuel diversification in adaptive radiations and facilitate adaptation to new environments. In this study, we employed whole-genome resequencing data to investigate the evolutionary origin of hummingbird-pollinated flowers and to characterize genome-wide patterns of phylogenetic discordance and introgression in Penstemon subgenus Dasanthera, a small and diverse adaptive radiation of plants. We found that magenta hummingbird-adapted flowers have apparently evolved twice from ancestral blue-violet bee-pollinated flowers within this radiation. These shifts in flower color are accompanied by a variety of inactivating mutations to a key anthocyanin pathway enzyme, suggesting that independent de novo loss-of-function mutations underlie the parallel evolution of this trait. Although patterns of introgression and phylogenetic discordance were heterogenous across the genome, a strong effect of gene density suggests that, in general, natural selection opposes introgression and maintains genetic differentiation in gene-rich genomic regions. Our results highlight the importance of both de novo mutation and introgression as sources of evolutionary change and indicate a role for de novo mutation in driving parallel evolution in adaptive radiations.

    

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