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Gene loss and parallel evolution contribute to species difference in flower color.

ABSTRACT: Although the importance of regulatory and functional sequence evolution in generating species differences has been studied to some extent, much less is known about the role of other types of genomic changes, such as fluctuation in gene copy number. Here, we apply analyses of gene function and expression of anthocyanin pigment pathway genes, as well as cosegregation analyses in backcross populations, to examine the genetic changes involved in the shift from blue to red flowers in Andean Iochroma (Solanaceae). We demonstrate that deletion of a gene coding for an anthocyanin pathway enzyme was necessary for the transition to red floral pigmentation. The downregulation of a second pathway gene was also necessary for the novel flower color, and this regulatory pattern parallels the genetic change in the two other red-flowered species in the sister family Convolvulaceae in which flower color change has been examined genetically. Finally, we document a shift in enzymatic function at a third locus, but the importance of this change in the transition to red flowers depends on the exact order with which the three changes occurred. This study shows that gene inactivation or loss can be involved in the origin of phenotypic differences between species, thereby restricting the possibility of reversion to the ancestral state. It also demonstrates that parallel evolution of red flowers in three different species occurs via a common developmental/regulatory change but by mutations in different genes.

SUBMITTER: Smith SD

PROVIDER: S-EPMC3203625 | biostudies-literature | 2011 Oct

REPOSITORIES: biostudies-literature

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Gene loss and parallel evolution contribute to species difference in flower color.

Smith Stacey D SD Rausher Mark D MD

Molecular biology and evolution 20110506 10

Although the importance of regulatory and functional sequence evolution in generating species differences has been studied to some extent, much less is known about the role of other types of genomic changes, such as fluctuation in gene copy number. Here, we apply analyses of gene function and expression of anthocyanin pigment pathway genes, as well as cosegregation analyses in backcross populations, to examine the genetic changes involved in the shift from blue to red flowers in Andean Iochroma ...[more]

PMID: 21551271

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Project description: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.

Project description:Plants exhibit a wide array of floral forms and pollinators can act as agent of selection on floral traits. Two trends have emerged from recent reviews of pollinator-mediated selection in plants. First, pollinator-mediated selection on plant-level attractants such as floral display size is stronger than on flower-level attractant such as flower color. Second, when comparing plant species, distinct pollinators can exert different selection patterns on floral traits. In addition, many plant species are visited by a diverse array of pollinators but very few studies have examined selection by distinct pollinators. In the current study, we examined phenotypic selection on flower color and floral display size by three distinct bee species, the European honey bee, Apis mellifera, the common eastern bumble bee, Bombus impatiens, and the alfalfa leafcutting bee, Megachile rotundata, foraging on Medicago sativa. To estimate phenotypic selection by each bee species and for all bees combined simultaneously and on the same group of plants, we introduce a new method that combines pollinator visitation data to seed set and floral trait measurements data typical of phenotypic selection study. When comparing floral traits, all bee species selected on the number of racemes per stem and the number of stems per plant, two components of floral display size. However, only leafcutting bees selected on hue or flower color and only bumble bees selected on chroma or darkness of flowers. Selection on chroma occurred via correlational selection between chroma and number of open flowers per raceme and we examine how correlational selection may facilitate the evolution of flower color in plant populations. When comparing bee species, the three bee species exerted similar selection pattern on some floral traits but different patterns on other floral traits and differences in selection patterns were observed between flower-level and plant-level attractants. The trends detected were consistent with previous studies and we advocate the approach introduced here for future studies examining the impact of distinct pollinators on floral trait evolution.

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Gene loss and parallel evolution contribute to species difference in flower color.

Publications

Gene loss and parallel evolution contribute to species difference in flower color.

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