Structure and contingency determine mutational hotspots for flower color evolution

Abstract

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.

Floral pigments and their perception by avian pollinators in three Chilean Puya species

“…Variation in the ower color is often associated with the avonoid composition regulated through the biosynthesis pathway, which has been discussed in the ecological and evolutional contexts (Wheeler and Smith 2019; Wheeler et al, 2021). Our aglycone analysis unveiled that the three species share the same aglycones, likely synthesized via a avonoid biosynthesis pathway proposed in Fig.…”

Multiple mechanisms explain loss of anthocyanins from betalain‐pigmented Caryophyllales, including repeated wholesale loss of a key anthocyanidin synthesis enzyme

“…With this as context, anthocyanin pigmentation has been developed into a powerful model in which to explore the interaction between genetic architecture and trait transitions. Anthocyanin‐based floral coloration shows frequent transitions between different hues through changes in concentrations of red pelargonidins, purple cyanidins, and blue delphinidins (Wessinger & Rausher, 2012 ; Wheeler et al ., 2021 ). These transitions can be caused by repeated regulatory changes to the same or similar anthocyanin pathway genes (Larter et al ., 2018 ; Wheeler et al ., 2023 ).…”

“…These transitions can be caused by repeated regulatory changes to the same or similar anthocyanin pathway genes (Larter et al ., 2018 ; Wheeler et al ., 2023 ). The targets of these changes appear to be constrained by pleiotropy and the structure of the anthocyanin biosynthesis pathway (Streisfeld & Rausher, 2011 ; Larter et al ., 2018 ; Wheeler et al ., 2021 ). Some lineages have also repeatedly evolved white flowers by loss of anthocyanins (Ho & Smith, 2016 ; Wheeler et al ., 2023 ), by diverse mechanisms (Gates et al ., 2018 ; Duncan & Rausher, 2020 ), but with predictable molecular evolutionary consequences for genes in the pathway (Ho & Smith, 2016 ).…”