Plasticity, pleiotropy and fitness trade-offs in Arabidopsis genotypes with different telomere lengths.

Telomere length has been implicated in the organismal response to stress, but the underlying mechanisms are unknown. Here we examine the impact of telomere length changes on the responses to three contrasting abiotic environments in Arabidopsis, and measure 32 fitness, developmental, physiological and leaf-level anatomical traits. We report that telomere length in wild-type and short-telomere mutants is resistant to abiotic stress, while the elongated telomeres in ku70 mutants are more plastic. We detected significant pleiotropic effects of telomere length on flowering time and key leaf physiological and anatomical traits. Furthermore, our data reveal a significant genotype by environment (G × E) interaction for reproductive fitness, with the benefits and costs to performance depending on the growth conditions. These results imply that life-history trade-offs between flowering time and reproductive fitness are impacted by telomere length variation. We postulate that telomere length in plants is subject to natural selection imposed by different environments.

Genetic Mapping Reveals an Anthocyanin Biosynthesis Pathway Gene Potentially Influencing Evolutionary Divergence between Two Subspecies of Scarlet Gilia (Ipomopsis aggregata).

Immense floral trait variation has likely arisen as an adaptation to attract pollinators. Different pollinator syndromes-suites of floral traits that attract specific pollinator functional groups-are repeatedly observed across closely related taxa or divergent populations. The observation of these trait syndromes suggests that pollinators use floral cues to signal the underlying nectar reward, and that complex trait combinations may persist and evolve through genetic correlations. Here, we explore pollinator preferences and the genetic architecture of floral divergence using an extensive genetic mapping study in the hybrid zone of two Ipomopsis aggregata subspecies that exhibit a hummingbird and a hawkmoth pollinator syndrome. We found that natural selection acts on several floral traits, and that hummingbirds and hawkmoths exhibited flower color preferences as predicted by their respective pollinator syndromes. Our quantitative trait loci (QTL) analyses revealed 46 loci affecting floral features, many of which colocalize across the genome. Two of these QTL have large effects explaining >15% of the phenotypic variance. The strongest QTL was associated with flower color and localized to a SNP in the anthocyanin biosynthesis pathway gene, dihydroflavonol-4-reductase (DFR). Further analysis revealed strong associations between DFR SNP variants, gene expression, and flower color across populations from the hybrid zone. Hence, DFR may be a target of pollinator-mediated selection in the hybrid zone of these two subspecies. Together, our findings suggest that hummingbirds and hawkmoths exhibit contrasting flower color preferences, which may drive the divergence of several floral traits through correlated trait evolution.

Ecological interactions and the fitness effect of water-use efficiency: Competition and drought alter the impact of natural MPK12 alleles in Arabidopsis.

The presence of substantial genetic variation for water-use efficiency (WUE) suggests that natural selection plays a role in maintaining alleles that affect WUE. Soil water deficit can reduce plant survival, and is likely to impose selection to increase WUE, whereas competition for resources may select for decreased WUE to ensure water acquisition. We tested the fitness consequences of natural allelic variation in a single gene (MPK12) that influences WUE in Arabidopsis, using transgenic lines contrasting in MPK12 alleles, under four treatments; drought/competition, drought/no competition, well-watered/competition, well-watered/no competition. Results revealed an allele × environment interaction: Low WUE plants performed better in competition, resulting from increased resource consumption. Contrastingly, high WUE individuals performed better in no competition, irrespective of water availability, presumably from enhanced water conservation and nitrogen acquisition. Our findings suggest that selection can influence MPK12 evolution, and represents the first assessment of plant fitness resulting from natural allelic variation at a single locus affecting WUE.

Natural selection maintains a single-locus leaf shape cline in Ivyleaf morning glory, Ipomoea hederacea.

Clines in phenotypic traits with an underlying genetic basis potentially implicate natural selection. However, neutral evolutionary processes such as random colonization, spatially restricted gene flow, and genetic drift could also result in similar spatial patterns, especially for single-locus traits because of their susceptibility to stochastic events. One way to distinguish between adaptive and neutral mechanisms is to compare the focal trait to neutral genetic loci to determine whether neutral loci demonstrate clinal variation (consistent with a neutral cline), or not. Ivyleaf morning glory, Ipomoea hederacea, exhibits a latitudinal cline for a Mendelian leaf shape polymorphism in eastern North America, such that lobed genotypes dominate northern populations and heart-shaped genotypes are restricted to southern populations. Here, we evaluate potential evolutionary mechanisms for this cline by first determining the allele frequencies at the leaf shape locus for 77 populations distributed throughout I. hederacea's range and then comparing the geographical pattern at this locus to neutral amplified fragment length polymorphism (AFLP) loci. We detected both significant clinal variation and high genetic differentiation at the leaf shape locus across all populations. In contrast, 99% of the putatively neutral loci do not display clinal variation, and I. hederacea populations show very little overall genetic differentiation, suggesting that there is a moderate level of gene flow. In addition, the leaf shape locus was identified as a major F(ST) outlier experiencing divergent selection, relative to all the AFLP loci. Together, these data strongly suggest that the cline in leaf shape is being maintained by spatially varying natural selection.

The effect of leaf shape on the thermoregulation and frost tolerance of an annual vine, Ipomoea hederacea (Convolvulaceae).

PREMISE OF STUDY: Leaf shape is predicted to have important ecophysiological consequences; for example, theory predicts that lobed leaves should track air temperature more closely than their entire-margined counterparts. Hence, leaf-lobing may be advantageous during cold nights (∼0°C) when there is the risk of damage by radiation frost (a phenomenon whereby leaves fall below air temperature because of an imbalance between radiational heat loss and convective heat gain). METHODS: Here, we test whether radiation frost can lead to differential damage between leaf shapes by examining a leaf-shape polymorphism in Ipomoea hederacea, where leaves are either lobed or heart-shaped depending on a single Mendelian locus. We logged leaf temperature during midautumn, and measured chlorophyll fluorescence and survival as proxies of performance. Furthermore, we tested if the leaf-shape locus confers freezing tolerance using freezing assays on leaf tissue from different leaf shapes. KEY RESULTS: We found that lobed leaves consistently remain warmer than heart-shaped leaves during the night, but that no pattern emerged during the day, and that temperature differences between leaf shapes were typically small. Furthermore, we found that leaf types did not differ in frost tolerance, but that a 1°C decrease leads to a transition from moderate to complete damage. CONCLUSIONS: Our results demonstrate that Ipomoea hederacea leaf shapes do experience different nighttime temperatures, and that only minor temperature differences can lead to disparate levels of freezing damage, suggesting that the differential thermoregulation could result in different levels of frost damage.

The genomic landscape of molecular responses to natural drought stress in Panicum hallii.

Environmental stress is a major driver of ecological community dynamics and agricultural productivity. This is especially true for soil water availability, because drought is the greatest abiotic inhibitor of worldwide crop yields. Here, we test the genetic basis of drought responses in the genetic model for C4 perennial grasses, Panicum hallii, through population genomics, field-scale gene-expression (eQTL) analysis, and comparison of two complete genomes. While gene expression networks are dominated by local cis-regulatory elements, we observe three genomic hotspots of unlinked trans-regulatory loci. These regulatory hubs are four times more drought responsive than the genome-wide average. Additionally, cis- and trans-regulatory networks are more likely to have opposing effects than expected under neutral evolution, supporting a strong influence of compensatory evolution and stabilizing selection. These results implicate trans-regulatory evolution as a driver of drought responses and demonstrate the potential for crop improvement in drought-prone regions through modification of gene regulatory networks.

Population dynamics and evolutionary history of the weedy vine Ipomoea hederacea in North America.

Disentangling the historical evolutionary processes that contribute to patterns of phenotypic and genetic variation is important for understanding contemporary patterns of both traits of interest and genetic diversity of a species. Ipomoea hederacea is a self-compatible species whose geographic origin is contested, and previous work suggests that although there are signals of adaptation (significant leaf shape and flowering time clines), no population structure or neutral genetic differentiation of I. hederacea populations was detected. Here, we use DNA sequence data to characterize patterns of genetic variation to establish a more detailed understanding of the current and historical processes that may have generated the patterns of genetic variation in this species. We resequenced ca. 5000 bp across 7 genes for 192 individuals taken from 24 populations in North America. Our results indicate that North American I. hederacea populations are ubiquitously genetically depauperate, and patterns of nucleotide diversity are consistent with population expansion. Contrary to previous findings, we discovered significant population subdivision and isolation-by-distance, but genetic structure was spatially discontinuous, potentially implicating long-distance dispersal. We further found significant genetic differentiation at sequenced loci but nearly fourfold stronger differentiation at the leaf shape locus, strengthening evidence that the leaf shape locus is under divergent selection. We propose that North American I. hederacea has experienced a recent founder event, and/or population dynamics are best described by a metapopulation model (high turnover and dispersal), leading to low genetic diversity and a patchy genetic distribution.

Quantitative genetic variance and multivariate clines in the Ivyleaf morning glory, Ipomoea hederacea.

Clinal variation is commonly interpreted as evidence of adaptive differentiation, although clines can also be produced by stochastic forces. Understanding whether clines are adaptive therefore requires comparing clinal variation to background patterns of genetic differentiation at presumably neutral markers. Although this approach has frequently been applied to single traits at a time, we have comparatively fewer examples of how multiple correlated traits vary clinally. Here, we characterize multivariate clines in the Ivyleaf morning glory, examining how suites of traits vary with latitude, with the goal of testing for divergence in trait means that would indicate past evolutionary responses. We couple this with analysis of genetic variance in clinally varying traits in 20 populations to test whether past evolutionary responses have depleted genetic variance, or whether genetic variance declines approaching the range margin. We find evidence of clinal differentiation in five quantitative traits, with little evidence of isolation by distance at neutral loci that would suggest non-adaptive or stochastic mechanisms. Within and across populations, the traits that contribute most to population differentiation and clinal trends in the multivariate phenotype are genetically variable as well, suggesting that a lack of genetic variance will not cause absolute evolutionary constraints. Our data are broadly consistent theoretical predictions of polygenic clines in response to shallow environmental gradients. Ecologically, our results are consistent with past findings of natural selection on flowering phenology, presumably due to season-length variation across the range.