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Stinchcombe, J. R.

Publications and source records attributed to Stinchcombe, J. R..

At least 19 recordsLinked to original sources

Historical genomes reveal scale-dependent predictability of climate adaptation

Predicting evolution remains a central challenge in biology. Contemporary spatial patterns are increasingly used as space-for-time proxies to forecast evolutionary responses to environmental change, yet the reliability of such predictions--and whether it varies among biological scales--remains unclear. Using historical and contemporary genomes of the invasive weed Ambrosia artemisiifolia--spanning the species' native range, invasions on two continents and nearly two centuries--we show that genomically predicted flowering-time clines remained stable in the native range while introduced populations re-evolved them. Haploblocks--likely structural variants--were likewise temporally stable in the native range, and two showed striking parallel evolution across all three ranges. Climate-associated SNPs with the strongest contemporary clines showed the greatest temporal change, with limited and variable parallelism among introduced ranges. Together, these results suggest adaptive evolution is partly predictable even when individual genomic trajectories remain flexible and contingent, with predictability emerging most clearly at the level of polygenic traits and large structural variants.

evolutionary biology↗

A rare deletion of BZ1 in the ivy-leaf morning glory eliminates anthocyanin-based pigmentation.

Anthocyanin biosynthesis is a highly branched network with upstream mutations leading to the loss of many other branches beyond just anthocyanins like flavonols, isoflavonoids, and proanthocyanidins. Consequently, disentangling the specific effects of anthocyanins on plant fitness from those of other branches is difficult unless a mutant impacting the terminal step of anthocyanin biosynthesis can be found. We discovered an Ipomoea hederacea plant (ivy-leaf morning glory) lacking anthocyanins due to a genetic deletion in the terminal step of the anthocyanin biosynthetic pathway. Anthocyanin loss follows a recessive, Mendelian inheritance pattern. Anthocyanin loss is perfectly correlated with a lack of expression of the anthocyanin biosynthesis gene IhUF3GT1 (anthocyanidin-3-O-glucosyltransferase). IhUF3GT1 is the gene most strongly and consistently differentially expressed between unpigmented and pigmented flowers in F2 siblings. A deletion of half of the IhUF3GT1 gene which includes the start codon is the genetic basis underlying a loss of IhUF3GT1 expression and, consequently, anthocyanins in unpigmented plants. The IhUF3GT1 deletion is rare and unique to the unpigmented line. Genome coverage analyses demonstrate that no other pigmented I. hederacea line (of 123 screened) has a loss-of-function mutation in IhUF3GT1. Furthermore, we confirm cosegregation of the IhUF3GT1 deletion with the unpigmented phenotype in F3 progeny from a cross where all unpigmented plants are homozygous for the IhUF3GT1 deletion. Taken together, we describe the genetic basis of a novel unpigmented mutant in I. hederacea, creating a potentially important model for studying the fitness effects of anthocyanin loss.

evolutionary biology↗

Newly arisen indel governs a leaf shape polymorphism in the Ivy Leaf Morning Glory (Ipomoea hederacea)

Leaf shape varies widely across plant taxa and has repeatedly been shown to affect ecophysiology, interspecific interactions, and fitness. We used population genomics, genome wide association studies (GWAS), and comparative genomics to determine the genetic basis and evolutionary history of an uncharacterized Mendelian leaf shape polymorphism in Ipomoea hederacea. To do so, we assembled a reference genome and generated whole genome sequencing for 123 individuals from 55 populations. We identified a 117 kb indel that perfectly co-segregates with leaf shape by conducting a GWAS and assessing differences in coverage. Syntenic orthologs for genes on the indel were present in five other Ipomoea species with various leaf shapes, indicating the indel is a newly arisen deletion in I. hederacea despite similar leaf shape phenotypes in the other species. More broadly, these results illustrate how a range of leaf shape phenotypes can be produced by distinct genetic mechanisms even in closely related species. Although none of the genes on the indel itself are known leaf shape candidates, there are multiple leaf shape candidate genes in close proximity that are involved in the auxin biosynthesis pathway. Additionally, the genes within the indel have gene functions that could affect other potentially ecologically relevant traits that have previously been shown to be associated with leaf shape in I. hederacea. Therefore, the pleiotropic effects of the indel polymorphism can have important implications for understanding the ecological mechanisms influencing a well-documented leaf shape latitudinal cline in I. hederacea. Significance StatementIpomoea hederacea has been used to investigate the ecological and evolutionary effects of leaf shape because of a well-documented latitudinal leaf shape cline governed by an uncharacterized Mendelian polymorphism in this species. We identified a 117 kb indel that perfectly co-segregates with leaf shape in I. hederacea. The indel appears to be a distinct genetic mechanism than those governing similar leaf shapes in other closely related Ipomoea species. Additionally, possible pleiotropic effects of the indel on other traits has important implications for understanding the ecology and evolution of leaf shape variation in I. hederacea. Therefore, the results and the new genomic resources that we developed will facilitate future work understanding the genetic, developmental, and ecological mechanisms governing leaf shape variation.

plant biology↗

Selection shapes the evolution of genome size in a globally invasive plant

O_LIBiological invasions provide powerful natural experiments for understanding how genome architecture responds to novel climatic environments. Transposable elements (TEs) can rapidly restructure genomes, yet their role in adaptive genome size evolution during invasion remains poorly understood. C_LIO_LIHere, we examined genome size and TE abundance in 439 individuals of globally invasive common ragweed (Ambrosia artemisiifolia L.) across native (North American) and invasive (European, Australian) ranges. By integrating whole-genome resequencing, flow cytometry, and trait versus genetic differentiation comparison (QST-FST), we tested whether genome size evolution is shaped by selection, climate, and life-history traits. C_LIO_LIGenome size was significantly larger in Australian genotypes, driven by increased TE and rRNA (ribosomal RNA) abundance. Crucially, trait versus genetic differentiation comparison provided evidence of divergent selection on genome size in North American and European populations, but not in Australia. Genome size was correlated with mean annual temperature (MAT) across all ranges, linking genomic traits to environmental variables. C_LIO_LIGenome size evolution during invasion can be rapid, adaptive, and range-specific, with TE-driven genome expansion emerging as a potential genomic response to the demographic and environmental pressures accompanying colonization of novel environments. C_LI

evolutionary biology↗

Simulated drought with Polyethylene-Glycol (PEG) decreases above-ground performance and increases nodulation in the legume Medicago lupulina

Under climate change, understanding how plants and crops respond to drought is essential for basic research in ecology and evolution, and improving agricultural resilience. One common method of simulating drought in experimental conditions is by applying polyethylene glycol (PEG) to plants. We investigated drought growth responses in Medicago lupulina (black medic) using PEG to simulate drought stress. We grew Medicago lupulina plants inoculated with Sinorhizobium meliloti in Magenta boxes under controlled conditions and randomly assigned them to one of three treatments: a control, PEG applied to the bottom (PEG added to the bottom-watering container of a magenta box), or PEG applied from the top (PEG poured over the growth media). After 60 days, we measured true leaf number, nodule count, and below- and above-ground dry biomass. PEG treatments significantly reduced above-ground growth, including total biomass and leaf number, but unexpectedly increased nodulation. Our results suggest that while PEG effectively simulates drought stress on above-ground growth parameters, it may not accurately simulate drought effects on rhizobial symbiosis. PEG treatments had no effect on below-ground biomass, suggesting that increased nodulation is not a result of increased plant investment in below-ground growth under simulated drought. We hypothesize that PEG, as a persistent liquid that plants do not absorb, created conditions favorable for nodulation. Overall, these results highlight the importance of interpreting PEG-simulated drought experiments with caution when assessing mutualistic interactions.

plant biology↗

The ecological dynamics and consequences of phytoplasma in a spring ephemeral

Ecologists have long sought to link within-population dynamics to patterns of species occurrence and persistence across the range. Theoretical models suggest pathogens have important implications for plant populations and perhaps even limit plant distributions, though more empirical evidence is needed, especially in wild plant populations. In the field, we characterized the infection dynamics of phytoplasma, a vectored and sterilizing bacterial pathogen, in wild populations of white trillium. We identified the highest molecular matches for the local bacterial strain and putative vectors. We then leveraged iNaturalist data to reveal patterns and potential drivers of phytoplasma occurrence across the range of white trillium. Within populations, we found that phytoplasma symptoms were more likely in low host density plots, where insects occupied a higher proportion of trillium, indicative of an encounter-dilution effect. Leafhoppers in the genus Empoasca were positive for phytoplasma, suggesting they are a candidate vector of disease between trilliums at our field site. The closest match to our local phytoplasma was related to Candidatus Phytoplasma pruni, ribosomal group 16SrIII-F. Phytoplasma symptoms were widely distributed across trilliums range, even at range edges, and probability of symptoms was significantly increased by proximity to cropland. We studied the impacts of a sterilizing, vector-transmitted pathogen on host plant populations and patterns of infection across host range. Our results suggest sap-feeding insects do not occupy all hosts at high host densities, thereby reducing transmission and leading to higher likelihood of finding infection at low host densities, and a higher proportion of host plants infected at low host densities. At a range-wide scale, we found evidence that the pathogen was able to persist across both the core and edge of host ranges. Thus, negative-density dependent sterilizing pathogens may challenge host populations across the range.

ecology↗

High-throughput developmental assay of cold tolerance in Caenorhabditis elegans

Temperature can impose strong selection causing thermal tolerance variation between individuals, populations, and species. We developed a high-throughput larval development assay for cold tolerance in the model organism Caenorhabditis elegans. We exposed animals to 4{degrees}C cold treatments for either 12 or 24 hours. Animals exposed to the 24-hour cold treatment exhibited greater variation and heritability in cold tolerance during the L1 larval stage. The high-throughput approach that we developed is easily scalable to simultaneously measure a large number of strains, which makes it ideal for studying the genetics and evolution of cold tolerance in Caenorhabditis nematodes.

evolutionary biology↗

Cis-regulation of gene expression between sexes and life stages in Rumex hastatulus

The potential for conflict between sexes and life stages while sharing predominantly the same genome has important evolutionary consequences. In dioecious angiosperms, genes beneficial for the haploid pollen stage may reduce the fitness of diploid offspring of both males and females. However, we still lack an understanding of the extent of shared genetic architecture for gene expression between the sexes or life stages in plants, a key component for predicting the potential for conflict. We performed expression quantitative trait loci (eQTL) mapping to test if standing variation affects sexes and life stages differently using a population sample of the dioecious outcrossing plant Rumex hastatulus. We compared effect sizes and allele frequencies of cis-eQTLs in male and female leaf tissues and pollen and tested for genotype-by-sex interactions for gene expression. We found stronger shared genetic architecture between sexes than between life stages, suggesting greater potential for ongoing sexual conflict in leaves, which have been shown to be sexually dimorphic in earlier studies. In contrast, conflict over optimal gene expression between pollen and leaves may be easily resolved due to their distinct genetic architectures. Additionally, our burden of rare allele test suggested a signature of stabilizing selection against extreme gene expression in leaves. Our study highlights the use of eQTLs to investigate selection on gene expression and the evolution of conflict between sexes and life stages in dioecious species.

evolutionary biology↗

A resurrection experiment reveals reduced adaptive potential in a common agricultural weed

Teaser TextAdaptive evolution is essential for populations facing rapid anthropogenic change, yet realized evolutionary responses often fall short of expectations. Using a resurrection experiment with Ipomoea purpurea, we reveal that the genetic covariance structure underlying pollination and mating-system traits has become more constraining over time. Traits involved in pollinator attraction evolved within a decade, but flowering phenology--critical for coping with climate-driven shifts--was hindered by increasingly restrictive genetic covariances. Our findings suggest that temporal changes in genetic constraints can substantially dampen adaptive potential, even when selection pressures are strong. Adaptive evolution is critical to population responses under accelerating anthropogenic global change. Although theory and some empirical work suggest that contemporary rates of environmental change can be met by equally rapid evolutionary shifts, mismatches between expected and realized evolution remain common in natural systems. Using a resurrection approach, we demonstrate that the structure of genetic covariances among pollination and mating-system traits in the common morning glory (Ipomoea purpurea) is increasingly constraining evolutionary trajectories. Pollinator-attracting traits evolved or became more favored on a rapid time scale of less than ten years, but genetic covariances between traits limited the adaptive rate and evolutionary trajectory of flowering phenology, a trait with widely recognized importance in adapting to climatic shifts. Our results show that changing patterns of genetic constraint can substantially reduce adaptive potential even when selection favors rapid trait evolution.

evolutionary biology↗

Differences in stomatal conductance between leaf shape genotypes of Ipomoea hederacea suggest divergent ecophysiological strategies

Intraspecific variation in leaf shape affects many physiological processes but its impact on plant distribution is underexplored. Using a common garden, we studied daytime thermoregulation of lobed and entire leaf genotypes of Ipomoea hederacea, which displays a latitudinal leaf shape cline. Both leaf shapes maintained similar temperatures but entire leaf genotypes had significantly increased stomatal conductance in warmer/sunnier weather. With less potential water loss, lobed genotypes may have advantages in drier conditions. Lobed genotypes are more common in the north of the species range, which receives less summer precipitation, suggesting water availability as a potential clinally varying selective agent.

plant biology↗

Do rhizobia buffer legumes against climate-mediated microbiome effects?

Climate change is altering both soil microbial communities and the ecological context of plant-microbe interactions. Heat, drought, and their legacies can alter soil microbiomes and potential plant symbionts, but the direct consequences of these microbial changes on plant performance and plant investment in symbiosis remain underexplored. Predicting how soil microbes modulate plant resilience to heat and drought is critical to mitigating the negative effects of climate change on ecosystems and agriculture. In this study, we conducted growth chamber experiments to isolate the microbially-mediated indirect effects of heat and drought on plant performance and symbiosis. In the first experiment, focused on drought, we found that drought and drought-treated microbes, along with their interaction, significantly decreased the biomass of Medicago lupulina plants compared to well-watered microbiomes and conditions. In a second experiment, we then tested how the addition of a well-known microbial mutualist, Sinorhizobium meliloti, affected heat- and drought-treated microbiomes impact on M. lupulina. We found that drought-adapted microbiomes negatively impacted legume performance by increasing mortality and reducing branch number, but that adding rhizobia erased differences in plant response to climate treated soils. In contrast, heat-adapted microbiomes did not differ significantly from control microbiomes in their effects on a legume. Our results suggest microbial legacy effects, mutualist partners, and their interactions are important in mediating plant responses to drought, with some mutualists equalizing plant responses across microbial legacies.

ecology↗

Testing for the genomic footprint of conflict between life stages in an angiosperm and a moss species

The maintenance of genetic variation by balancing selection is of considerable interest to evolutionary biologists. An important but understudied potential driver of balancing selection is antagonistic pleiotropy between diploid and haploid stages of the plant life cycle. Despite sharing a common genome, sporophytes (2n) and gametophytes (n) may undergo differential or even opposing selection. Theoretical work suggests the antagonistic pleiotropy between life stages can generate balancing selection and maintain genetic variation. Despite the potential for far-reaching consequences of gametophytic selection, empirical tests of its pleiotropic effects (neutral, synergistic, or antagonistic) on sporophytes are generally lacking. Here, we examined the population genomic signals of selection across life stages in the angiosperm Rumex hastatulus and the moss Ceratodon purpureus. We compared gene expression among life stages and between sexes, combined with neutral diversity statistics and the analysis of the distribution of fitness effects. In contrast to what would be predicted under balancing selection due to antagonistic pleiotropy, we found that unbiased genes between life stages were under stronger purifying selection, likely explained by a predominance of synergistic pleiotropy between life stages and strong purifying selection on broadly expressed genes. In addition, we found that 30% of candidate genes under balancing selection in R. hastatulus were located within inversion polymorphisms. Our findings provide novel insights into the genome-wide characteristics and consequences of plant gametophytic selection. SignificanceThe genome-wide importance of balancing selection has been a key question in evolutionary biology. Despite theoretical support for the potential of balancing selection generated by antagonistic pleiotropy between plant life stages, to our knowledge no empirical studies have systematically investigated this on a genome-wide scale. Our results revealed genome-wide patterns more consistent with synergistic pleiotropy, with gametophyte-biased genes more likely to be under relaxed purifying selection in both the angiosperm and moss species we investigated. In addition, our study suggests gene expression level and breadth has a greater effect on selection efficacy than differences between ploidy levels in different life stages.

evolutionary biology↗

Rapid parallel adaptation in distinct invasions of Ambrosia artemisiifolia is driven by large-effect structural variants

When introduced to multiple distinct ranges, invasive species provide a compelling natural experiment for understanding the repeatability of adaptation. Ambrosia artemisiifolia is an invasive, noxious weed and chief cause of hay fever. Leveraging over 400 whole-genome sequences spanning the native range in North America and two invasions in Europe and Australia, we inferred demographically distinct invasion histories on each continent. Despite substantial differences in genetic source and effective population size changes during introduction, scans of both local climate adaptation and divergence from the native range revealed genomic signatures of parallel adaptation between invasions. Disproportionately represented among these parallel signatures are 37 large haploblocks - indicators of structural variation - that cover almost 20% of the genome and exist as standing genetic variation in the native range. Many of these haploblocks are associated with traits important for adaptation to local climate, like size and the timing of flowering, and have rapidly reformed native range clines in invasive ranges. Others show extreme frequency divergence between ranges, consistent with a response to divergent selection on different continents. Our results demonstrate the key role of large-effect standing variants in rapid adaptation during range expansion, a pattern that is robust to diverse invasion histories.

genomics↗

Variation in a microbial mutualist has cascading consequences for host-parasite interactions

Strains of microbial symbionts often vary in their effect on their host. However, little is known about how the genetic variation in microbial symbiont populations impacts host interactions with other co-colonizing microbes. We investigated how different strains of nitrogen-fixing rhizobial bacteria affect their host plants response to parasitic root-knot nematodes in the legume Medicago truncatula. Using dual RNAseq of the root organs harboring rhizobia or nematodes, we identified genes from plant host, rhizobia, and nematode whose expression differed between parasite-infected and-uninfected plants, and between plants inoculated with different rhizobial strains. At the site of host-parasite interactions (in nematode galls), hundreds of host genes and few nematode genes differed in expression between host plants inoculated with different rhizobia strains. At the site of host-mutualist interactions (in rhizobia nodules), hundreds of host genes and few rhizobial genes responded to parasite infection. The vast majority of parasite-induced changes in host gene expression depended on the resident rhizobia strain. We additionally observed differences in parasite load and in some root architecture traits between plants inoculated with different rhizobia strains, showing that genetic variation in a mutualistic symbiont impacted parasite colonization. The transcriptomic and phenotypic differences we observed suggest that microbial indirect genetic effects play an underappreciated role in their hosts interactions with other co-colonizing microorganisms.

ecology↗

Elevated rates of molecular evolution genome-wide in mutualist legumes and rhizobia

Rates of molecular evolution vary greatly among even closely related species. Although theory predicts that antagonistic interactions between species increase rates of molecular evolution, predictions for how mutualism affects evolutionary rates are mixed. Here, we compared rates of molecular evolution between 1) mutualistic and non-mutualistic legumes, 2) an independent set of symbiotic rhizobia and their non-symbiotic close relatives, and 3) symbiotic and non-symbiotic clades within Ensifer, a diverse genus of bacteria with various lifestyles. We assembled transcriptomes de novo for 12 legume species and then calculated dN/dS ratios at orthologous genes in all species to determine if genes in mutualistic plants evolve faster or slower than in their non-mutualistic relatives. We also calculated dN/dS ratios in symbiosis genes known to be important for nodulation with rhizobia. We found that mutualists have higher rates of molecular evolution genome-wide compared to non-mutualist legumes. We next calculated dN/dS ratios in 14 bacteria species across the proteobacteria phylogeny that differ in whether they associate mutualistically with plants, using previously published data. We found that in most pairs, symbiotic rhizobia show higher dN/dS values compared to their non-symbiotic relatives. Finally, within a bacterial genus with many well-characterized mutualist species (Ensifer), we calculated dN/dS ratios in symbiotic and non-symbiotic clades and found that symbiotic lineages have higher rates of molecular evolution genome-wide, but not at genes on the symbiotic plasmid pSymB. Our results suggest that although mutualism between legumes and rhizobia is associated with elevated rates of molecular evolution genome-wide, symbiosis genes may be evolutionarily stagnant.

evolutionary biology↗

Predicting fitness related traits using gene expression and machine learning

Evolution by natural selection occurs at its most basic through the change in frequencies of alleles; connecting those genomic targets to phenotypic selection is an important goal for evolutionary biology in the genomics era. The relative abundance of gene products expressed in a tissue can be considered a phenotype intermediate to the genes and genomic regulatory elements themselves, and more traditionally measured macroscopic phenotypic traits such as flowering time, size, or growth. The high-dimensionality, low sample size nature of transcriptomic sequence data is a double-edged sword, however, as it provides abundant information but makes traditional statistics difficult. Machine learning has many features which handle high-dimensional data well and is thus useful in genetic sequence applications. Here we examined the association of fitness-components with gene expression data in Ipomoea hederacea (Ivyleaf Morning Glory) grown under field conditions. We combine the results of two different machine learning approaches and find evidence that expression of photosynthesis-related genes is likely under selection. We also find that genes related to stress and light response were overall important in predicting fitness. With this study we demonstrate the utility of machine learning models for smaller samples, and their potential application for understanding natural selection.

evolutionary biology↗

Genetic architecture of heritable leaf microbes

AbstractHost-associated microbiomes are shaped by both their environment and host genetics, and often impact host performance. The scale of host genetic variation important to microbes is largely unknown, yet fundamental to the community assembly of host-associated microbiomes, and with implications for the eco-evolutionary dynamics of microbes and hosts. Using Ipomoea hederacea, Ivy-leaved morning glory, we generated matrilines differing in quantitative genetic variation and leaf shape, which is controlled by a single Mendelian locus. We then investigated the relative roles of Mendelian and quantitative genetic variation in structuring the leaf microbiome, and how these two sources of genetic variation contributed to microbe heritability. We found that despite large effects of the environment, both Mendelian and quantitative genetic host variation contribute to microbe heritability, and that the cumulative small effect genomic differences due to matriline explained as much or more microbial variation than a single large effect locus. Furthermore, our results are the first to suggest that leaf shape itself contributes to variation in the abundances of some phyllosphere microbes. ImportanceWe investigated how host genetic variation affected the assembly of Ipomoea hederaceas natural microbiome. We found that the genetic architecture of leaf-associated microbiomes involves both quantitative genetic variation and Mendelian traits, with similar contributions to microbe heritability. The existence of Mendelian and quantitative genetic variation for host-associated microbes means that plant evolution at the leaf shape locus or other quantitative genetic loci has the potential to shape microbial abundance, and community composition.

ecology↗

Resistance and resiliency of soil microbiomes under climate change

Soil microbiomes play key roles in plant productivity and nutrient cycling, and we need to understand whether and how they will withstand the effects of global climate change. We exposed in situ soil microbial communities to multiple rounds of heat, drought, or both treatments, and profiled microbial communities with 16S rRNA and ITS amplicon sequencing during and after these climatic changes, and then tested how domain and symbiotic lifestyle affected responses. Fungal community composition strongly shifted due to drought and its legacy. In contrast, bacterial community composition resisted change during the experiment, but still was affected by the legacy of drought. We identified fungal and bacterial taxa with differential abundance due to heat and drought and found that taxa affected during climate events are not necessarily the taxa affected in recovery periods, showing the complexity and importance of legacy effects. Additionally, we found evidence that symbiotic groups of microbes important to plant performance respond in diverse ways to climate treatments and their legacy, suggesting plants may be impacted by past climatic events like drought and warming even if they do not experience the event themselves.

ecology↗