Stepwise evolution of floral pigmentation predicted by biochemical pathway structure

Ng, Julienne; Freitas, Loreta B.; Smith, Stacey D.

doi:10.1111/evo.13589

Cited by 18 publications

(13 citation statements)

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“…In addition to deoxyanthocyanidins, several hydroxyanthocyanidins (pelargonidin, cyanidins, delphinidin) were also found in various combinations across the Gesnerioideae (Figure 3 and Supplementary Figure S1). A previous study on Solanaceae reported that, even though the species of this family were able to produce all three main groups of anthocyanins, they often produce only one type of anthocyanin or a mix of two anthocyanins with consecutive hydroxylation levels (e.g., pelargonidin-cyanidin or cyanidinmalvidin), and none of the studied species produced all three pigment types (Ng et al, 2018). It has been proposed that the anthocyanin composition is constrained by the stepwise structure of the biosynthetic pathway that leads to the successive production of the red mono-hydroxylated pelargonidin, purple di-hydroxylated cyanidin, and the blue tri-hydroxylated delphinidin pigments (des Marais and Rausher, 2008;Ng et al, 2018).…”

Section: The Alternative Branches Of the Anthocyanin Pathway In The Gmentioning

confidence: 89%

“…On the other hand, bird-pollinated flowers frequently have a distinctive orange/red color, which is better detected by birds than by bees especially against a green vegetation background (Lunau et al, 2011;Shrestha et al, 2013;Burd et al, 2014;Bergamo et al, 2016). Despite the importance of color signaling in plantpollinator interactions, the biochemical basis of color shifts has been investigated in a limited number of studies (Hoballah et al, 2007;Sobel and Streisfeld, 2013;Ng and Smith, 2016), and our understanding of how pigment biosynthesis pathways shaped the evolution of floral color is still limited (Cronk and Ojeda, 2008;Rausher, 2008;Ng et al, 2018;Wheeler and Smith, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Chemical Basis of Floral Color Signals in Gesneriaceae: The Effect of Alternative Anthocyanin Pathways

et al. 2020

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Changes in floral pigmentation can have dramatic effects on angiosperm evolution by making flowers either attractive or inconspicuous to different pollinator groups. Flower color largely depends on the type and abundance of pigments produced in the petals, but it is still unclear whether similar color signals rely on same biosynthetic pathways and to which extent the activation of certain pathways influences the course of floral color evolution. To address these questions, we investigated the physical and chemical aspects of floral color in the Neotropical Gesnerioideae (ca. 1,200 spp.), in which two types of anthocyanins, hydroxyanthocyanins, and deoxyanthocyanins, have been recorded as floral pigments. Using spectrophotometry, we measured flower reflectance for over 150 species representing different clades and pollination syndromes. We analyzed these reflectance data to estimate how the Gesnerioideae flowers are perceived by bees and hummingbirds using the visual system models of these pollinators. Floral anthocyanins were further identified using high performance liquid chromatography coupled to mass spectrometry. We found that orange/red floral colors in Gesnerioideae are produced either by deoxyanthocyanins (e.g., apigenidin, luteolinidin) or hydroxyanthocyanins (e.g., pelargonidin). The presence of deoxyanthocyanins in several lineages suggests that the activation of the deoxyanthocyanin pathway has evolved multiple times in the Gesnerioideae. The hydroxyanthocyanin-producing flowers span a wide range of colors, which enables them to be discriminated by hummingbirds or bees. By contrast, color diversity among the deoxyanthocyanin-producing species is lower and mainly represented at longer wavelengths, which is in line with the hue discrimination optima for hummingbirds. These results indicate that Gesnerioideae have evolved two different biochemical mechanisms to generate orange/red flowers, which is associated with hummingbird pollination. Our findings also suggest that the activation of the deoxyanthocyanin pathway has restricted flower color diversification to orange/red hues, supporting the potential constraining role of this alternative biosynthetic pathway on the evolutionary outcome of phenotypical and ecological diversification.

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Section: The Alternative Branches Of the Anthocyanin Pathway In The Gmentioning

confidence: 89%

Section: Introductionmentioning

confidence: 99%

Chemical Basis of Floral Color Signals in Gesneriaceae: The Effect of Alternative Anthocyanin Pathways

et al. 2020

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“…Organizing the simulations around this stepwise sequence of transitions allowed us to circumvent issues that arise from epistasis in the pathway model, wherein different starting states can result in differences between trajectories that are difficult to interpret (Ng et al. 2018).…”

Section: Methodsmentioning

confidence: 99%

“…Considering the structure of the flavonoid pathway, these represent stepwise shifts from three to two to one hydroxyl groups on the flavonoid backbone, and phylogenetic modeling shows that these stepwise transitions are the primary mode of evolutionary change (Ng et al. 2018). Transitions from blue to purple and purple to red have occurred in parallel in many clades and have been studied at the genetic level in several species pairs (Wessinger and Rausher 2012).…”

Section: Figurementioning

confidence: 99%

Structure and contingency determine mutational hotspots for flower color evolution

2021

Self Cite

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Evolutionary genetic studies have uncovered abundant evidence for genomic hotspots of phenotypic evolution, as well as biased patterns of mutations at those loci. However, the theoretical basis for this concentration of particular types of mutations at particular loci remains largely unexplored. In addition, historical contingency is known to play a major role in evolutionary trajectories, but has not been reconciled with the existence of such hotspots. For example, do the appearance of hotspots and the fixation of different types of mutations at those loci depend on the starting state and/or on the nature and direction of selection? Here, we use a computational approach to examine these questions, focusing the anthocyanin pigmentation pathway, which has been extensively studied in the context of flower color transitions. We investigate two transitions that are common in nature, the transition from blue to purple pigmentation and from purple to red pigmentation. Both sets of simulated transitions occur with a small number of mutations at just four loci and show strikingly similar peaked shapes of evolutionary trajectories, with the mutations of the largest effect occurring early but not first. Nevertheless, the types of mutations (biochemical vs. regulatory) as well as their direction and magnitude are contingent on the particular transition. These simulated color transitions largely mirror findings from natural flower color transitions, which are known to occur via repeated changes at a few hotspot loci. Still, some types of mutations observed in our simulated color evolution are rarely observed in nature, suggesting that pleiotropic effects further limit the trajectories between color phenotypes. Overall, our results indicate that the branching structure of the pathway leads to a predictable concentration of evolutionary change at the hotspot loci, but the types of mutations at these loci and their order is contingent on the evolutionary context.

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“…We evolved this mean 90% delphinidin state (hereafter referred to as simply the delphinidin state) to a 90% cyanidin state (corresponding to purple; hereafter referred to as simply the cyanidin state) and nally repeated the procedure to simulate the transition from cyanidin to 90% pelargonidin (corresponding to red; hereafter referred to as the pelargonidin state). Organizing the simulations around this stepwise sequence of transitions allowed us to circumvent issues that arise from epistasis in the pathway model, wherein dierent starting states can result in dierences between trajectories that are dicult to interpret (Ng et al 2018).…”

Section: Design Scheme For the Evolutionary Simulationsmentioning

confidence: 99%

Structure and contingency determine mutational hotspots for flower color evolution

Wheeler¹,

Wing²,

Smith³

2020

Preprint

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Evolutionary genetic studies have uncovered abundant evidence for genomic hotspots of phenotypic evolution, as well as biased patterns of mutations at those loci. However, the theoretical basis for this concentration of particular types of mutations at particular loci remains largely unexplored. In addition, historical contingency is known to play a major role in evolutionary trajectories, but has not been reconciled with the existence of such hotspots. For example, do the appearance of hotspots and the fixation of different types of mutations at those loci depend on the starting state and/or on the nature and direction of selection? Here we use a computational approach to examine these questions, focusing the anthocyanin pigmentation pathway, which has been extensively studied in the context of flower color transitions. We investigate two transitions that are common in nature, the transition from blue to purple pigmentation and from purple to red pigmentation. Both sets of simulated transitions occur with a small number of mutations at just four loci and show strikingly similar peaked shapes of evolutionary trajectories, with the mutations of largest effect occurring early but not first. Nevertheless, the types of mutations (biochemical vs. regulatory) as well as their direction and magnitude are contingent on the particular transition. These simulated color transitions largely mirror findings from natural flower color transitions, which are known to occur via repeated changes at a few hotspot loci. Still, some types of mutations observed in our simulated color evolution are rarely observed in nature, suggesting that pleiotropic effects further limit the trajectories between color phenotypes. Overall, our results indicate that the branching structure of the pathway leads to a predictable concentration of evolutionary change at hotspot loci, but the types of mutations at these loci and their order is contingent on the evolutionary context.

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Stepwise evolution of floral pigmentation predicted by biochemical pathway structure

Cited by 18 publications

References 97 publications

Chemical Basis of Floral Color Signals in Gesneriaceae: The Effect of Alternative Anthocyanin Pathways

Chemical Basis of Floral Color Signals in Gesneriaceae: The Effect of Alternative Anthocyanin Pathways

Structure and contingency determine mutational hotspots for flower color evolution

Structure and contingency determine mutational hotspots for flower color evolution

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