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Stone, B. W.

Publications and source records attributed to Stone, B. W..

5 recordsLinked to original sources

Rapid floral syndrome convergence in Penstemon through independent genetic variation

The repeated evolution of certain complex traits within a given lineage is compelling and presents an opportunity for understanding selective and genetic features that promote rapid multi-trait adaptation. The North American plant genus Penstemon is one such example, with numerous evolutionary shifts from ancestral bee syndrome to hummingbird syndrome flowers. Here, we traced the evolution of multi-trait floral phenotypes within a focal clade of Penstemon using a new whole genome phylogenomic estimate and found four independent origins of the hummingbird syndrome. We found strong evolutionary convergence in floral traits across these four origins and observed that the hummingbird syndrome assembled rapidly, without leaving a signal of stepwise modification of traits. Patterns of evolutionary correlations among floral traits in bee syndrome Penstemon species likely enable rapid shifts to hummingbird syndrome. Using phylogenomic tests for introgression, we found no evidence that adaptive introgression has fueled the four repeated origins of hummingbird syndrome flowers. Patterns of allele sharing were instead consistent with substantial levels of incomplete lineage sorting, suggesting repeated complex adaptation involves de novo mutation or adaptation from ancestral variation.

evolutionary biology↗

Genomic signatures of reproductive isolation are decoupled from floral divergence in a long-standing hybrid zone

A central goal in evolutionary biology is to understand how species boundaries are maintained despite gene flow. Two North American wildflower species with divergent floral syndromes, Penstemon davidsonii (bee syndrome) and P. newberryi (bird syndrome), have formed hybrid zones in the eastern Sierra Nevada for at least 85 years. We combined multiple approaches to test whether divergent floral syndromes enforce reproductive isolation as predicted by classic models of pollinator-driven ecological speciation. The two parent species exhibited strong divergence across multivariate trait space and have maintained genomic differentiation despite persistent hybridization. Floral hue, a key component of pollination syndrome, mapped to a single genomic region containing two candidate genes with large effects on anthocyanin pigment composition. Pollinator visual models indicated that genetic variation at this region affects detectability to hummingbirds, but not bees. Genomic cline analyses identified many significantly steep clines, suggesting a polygenic basis to reproductive isolation. Surprisingly, these barriers appear unrelated to floral isolation; the major floral hue locus exhibits a strikingly shallow genomic cline and elevated heterozygosity, suggesting pervasive gene flow. Our results reveal that conspicuous trait divergence can be decoupled from reproductive barriers, challenging assumptions about how reproductive isolation is maintained in hybridizing populations.

evolutionary biology↗

Ecological diversification in an adaptive radiation of plants: the role of de novo mutation and introgression

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 vs. pre-existing 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 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.

evolutionary biology↗

Asynchronous rates of lineage, phenotype, and niche diversification in a continental-scale adaptive radiation

Rapidly diversifying clades are central to the study of diversification dynamics. This central importance is perhaps most apparent when rapid evolution occurs across several axes of diversification (e.g., lineage, phenotype, and niche); such clades facilitate investigations into the interplay between adaptive and non-adaptive diversification mechanisms. Yet, empirical evidence from rapidly evolving clades remains unclear about the relationships, if any, across diversification axes. This is especially apparent regarding the timing of diversification rate shifts. We address this knowledge gap through comparisons of the rate and timing of lineage, phenotypic, and niche diversification in Penstemon, a rapidly-evolving angiosperm genus. We find that diversification rate shifts in Penstemon are asynchronous; while we identify a burst and subsequent slowdown in lineage diversification rate [~]2.0-2.5 MYA, shifts in phenotypic and niche diversification rates either lagged behind temporally or did not occur at all. We posit that this asynchronicity in diversification rate shifts is the result of initial niche-neutral diversification followed by adaptive, density-dependent processes. Our findings contribute to a growing body of evidence that asynchronous shifts in diversification rates may be common and question the applicability of expectations for diversification dynamics across disparate empirical systems.

evolutionary biology↗

Phylogeographic analysis of shrubby beardtongues reveals range expansions during the Last Glacial Maximum and implicates the Klamath Mountains as a hotspot for hybridization

Quaternary glacial cycles often altered species geographic distributions, which in turn altered the geographic structure of a species genetic diversity. In many cases, glacial expansion forced species in temperate climates to contract their ranges and reside in small pockets of suitable habitat (refugia), where they were likely to interact closely with other species, setting the stage for potential gene exchange. These introgression events, in turn, would have degraded species boundaries, making the inference of phylogenetic relationships challenging. Using high-throughput sequence data, we employ a combination of species distribution models, models of demographic history, and hybridization tests to assess the effect of glaciation on the geographic distributions, phylogenetic relationships, and patterns of gene flow of five species of Penstemon subgenus Dasanthera, long-lived shrubby angiosperms distributed throughout the Pacific Northwest of North America. Surprisingly, we find that rather than reducing their ranges to small refugia, most Penstemon subgenus Dasanthera species experienced increases in suitable habitat during the Last Glacial Maximum. We also find substantial evidence for gene exchange between species, with the bulk of introgression events occurring in or near the Klamath Mountains of southwestern Oregon and northwestern California. Subsequently, our phylogenetic inference reveals blurred taxonomic boundaries in the Klamath Mountains, where introgression is most prevalent. Our results question the classical paradigm of temperate species responses to glaciation, and highlight the importance of contextualizing phylogenetic inference with the demographic histories of the species of interest.

evolutionary biology↗