Admixture, the mixing of historically isolated gene pools, can have immediate consequences for the genetic architecture of fitness traits. Admixture may be especially important for newly colonized populations, such as during range expansion and species invasions, by generating heterozygosity that can boost fitness through heterosis. Despite widespread evidence for admixture during species invasions, few studies have examined the demographic history leading to admixture, how admixture affects the heterozygosity and fitness of invasive genotypes, and whether such fitness effects are maintained through time. We address these questions using the invasive plant Silene vulgaris, which shows evidence of admixture in both its native Europe and in North America where it has invaded. Using multilocus genotype data in conjunction with approximate Bayesian computation analysis of demographic history, we showed that admixture during the invasion of North America was independent from and much younger than admixture in the native range of Europe. We tested for fitness consequences of admixture in each range and detected a significant positive heterozygosity-fitness correlation (HFC) in North America; in contrast, no HFC was present in Europe. The lack of HFC in Europe may reflect the longer time since admixture in the native range, dissipating associations between heterozygosity at markers and fitness loci. Our results support a key short-term role for admixture during the early stages of invasion by generating HFCs that carry populations past the threat of extinction from inbreeding and demographic stochasticity.
The enemy release hypothesis predicts that invasive species will receive less damage from enemies, compared to co-occurring native and noninvasive exotic species in their introduced range. However, release operating early in invasion could be lost over time and with increased range size as introduced species acquire new enemies. We used three years of data, from 61 plant species planted into common gardens, to determine whether (1) invasive, noninvasive exotic, and native species experience differential damage from insect herbivores. and mammalian browsers, and (2) enemy release is lost with increased residence time and geographic spread in the introduced range. We find no evidence suggesting enemy release is a general mechanism contributing to invasiveness in this region. Invasive species received the most insect herbivory, and damage increased with longer residence times and larger range sizes at three spatial scales. Our results show that invasive and exotic species fail to escape enemies, particularly over longer temporal and larger spatial scales.
Highlights d The R2R3-MYB transcription factor AN2 is a hotspot for evolutionary change d Resurrection of AN2 by a 2-bp deletion during reversal to bee pollination d Complex trait modified by two regulatory mutations of large effect d Trait reversal is possible in recent radiations
Members of the angiosperm genus Silene are widely used in studies of ecology and evolution, but available genomic and population genetic resources within Silene remain limited. Deep transcriptome (i.e. expressed sequence tag or EST) sequencing has proven to be a rapid and cost-effective means to characterize gene content and identify polymorphic markers in non-model organisms. In this study, we report the results of 454 GS-FLX Titanium sequencing of a polyA-selected and normalized cDNA library from Silene vulgaris. The library was generated from a single pool of transcripts, combining RNA from leaf, root and floral tissue from three genetically divergent European subpopulations of S. vulgaris. A single full-plate 454 run produced 959,520 reads totalling 363.6 Mb of sequence data with an average read length of 379.0 bp after quality trimming and removal of custom library adaptors. We assembled 832,251 (86.7%) of these reads into 40,964 contigs, which have a total length of 25.4 Mb and can be organized into 18,178 graph-based clusters or 'isogroups'. Assembled sequences were annotated based on homology to genes in multiple public databases. Analysis of sequence variants identified 13,432 putative single-nucleotide polymorphisms (SNPs) and 1320 simple sequence repeats (SSRs) that are candidates for microsatellite analysis. Estimates of nucleotide diversity from 1577 contigs were used to generate genome-wide distributions that revealed several outliers with high diversity. All of these resources are publicly available through NCBI and/or our website (http://silenegenomics.biology.virginia.edu) and should provide valuable genomic and population genetic tools for the Silene research community.
Red flower color has arisen multiple times and is generally associated with hummingbird pollination. The majority of evolutionary transitions to red color proceeded from purple lineages and tend to be genetically simple, almost always involving a few loss-of-function mutations of major phenotypic effect. Here we report on the complex evolution of a novel red floral color in the hummingbird-pollinated Petunia exserta (Solanaceae) from a colorless ancestor. The presence of a red color is remarkable because the genus cannot synthesize red anthocyanins and P. exserta retains a nonfunctional copy of the key MYB transcription factor AN2. We show that moderate up-regulation and a shift in tissue specificity of an AN2 paralog, DEEP PURPLE (DPL), restores anthocyanin biosynthesis in P. exserta. An essential shift in anthocyanin hydroxylation occurred through re-balancing the expression of three hydroxylating genes. Furthermore, the down-regulation of an acyltransferase promotes reddish hues in typically purple pigments by preventing acyl group decoration of anthocyanins. This study presents a rare case of a genetically complex evolutionary transition towards the gain of a novel red color.
The predictability of evolution, or whether lineages repeatedly follow the same evolutionary trajectories during phenotypic convergence remains an open question of evolutionary biology. In this study, we investigate evolutionary convergence at the biochemical pathway level and test the predictability of evolution using floral anthocyanin pigmentation, a trait with a well-understood genetic and regulatory basis. We reconstructed the evolution of floral anthocyanin content across 28 species of the Andean clade Iochrominae (Solanaceae) and investigated how shifts in pigmentation are related to changes in expression of 7 key anthocyanin pathway genes. We used phylogenetic multivariate analysis of gene expression to test for phenotypic and developmental convergence at a macroevolutionary scale. Our results show that the four independent losses of the ancestral pigment delphinidin involved convergent losses of expression of the three late pathway genes (F3'5'h, Dfr and Ans). Transitions between pigment types affecting floral hue (e.g. blue to red) involve changes to the expression of branching genes F3'h and F3'5'h, while the expression levels of early steps of the pathway are strongly conserved in all species. These patterns support the idea that the macroevolution of floral pigmentation follows predictable evolutionary trajectories to reach convergent phenotype space, repeatedly involving regulatory changes. This is likely driven by constraints at the pathway level, such as pleiotropy and regulatory structure.
Flavonoid production increases along elevational gradients in S. vulgaris, with clinal variation in calyx anthocyanins and increasing leaf non-anthocyanin flavonoid concentrations. Despite the photoprotective and antiherbivore properties of some flavonoids, flavonoid production in flowers and leaves was correlated with population microclimatic variables: temperature and precipitation. Taken together, the results suggest that different flavonoid groups are targeted by selection in different tissues and provide evidence for divergent patterns of selection for flavonoids between high and low elevations.
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