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Aldose reductase (AKR1B1 in humans; Akr1b3 in mice), a key enzyme of the polyol pathway, mediates lipid accumulation in the murine heart and liver. The study objective was to explore potential roles for AKR1B1/Akr1b3 in the pathogenesis of obesity and its complications.The study employed mice treated with an inhibitor of aldose reductase or mice devoid of Akr1b3 were used to determine their response to a high-fat diet. The study used subcutaneous adipose tissue-derived adipocytes to investigate mechanisms by which AKR1B1/Akr1b3 promotes diet-induced obesity.Increased expression of aldose reductase and senescence in the adipose tissue of humans and mice with obesity were demonstrated. Genetic deletion of Akr1b3 or pharmacological blockade of AKRIB3 with zopolrestat reduced high-fat-diet-induced obesity, attenuated markers of adipose tissue senescence, and increased lipolysis.AKR1B1/Akr1b3 modulation of senescence in subcutaneous adipose tissue contributes to aberrant metabolic responses to high-fat feeding. These data unveil new opportunities to target these pathways to combat obesity. more...

Significance Forested ecosystems provide many ecological, economic, and societal benefits, but those benefits are threatened by climate change. Conservation strategies often assume that plants are currently growing in conditions well-suited to their growth, survival, and reproduction, regardless of whether this assumption is valid. We show that an ecosystem-foundational species in California, valley oak (Quercus lobata), is already mismatched to current temperature and will likely experience further declines in growth rates as temperatures rise over the next century. Given this mismatch, new approaches to climate change management are needed. By using genomic information and identifying genotypes with faster growth rates under warmer temperatures, we present an approach to mitigate negative consequences of rising temperatures for species that may already be experiencing maladaptation., Climate change over the next century is predicted to cause widespread maladaptation in natural systems. This prediction, as well as many sustainable management and conservation practices, assumes that species are adapted to their current climate. However, this assumption is rarely tested. Using a large-scale common garden experiment combined with genome-wide sequencing, we found that valley oak (Quercus lobata), a foundational tree species in California ecosystems, showed a signature of adaptational lag to temperature, with fastest growth rates occurring at cooler temperatures than populations are currently experiencing. Future warming under realistic emissions scenarios was predicted to lead to further maladaptation to temperature and reduction in growth rates for valley oak. We then identified genotypes predicted to grow relatively fast under warmer temperatures and demonstrated that selecting seed sources based on their genotype has the potential to mitigate predicted negative consequences of future climate warming on growth rates in valley oak. These results illustrate that the belief of local adaptation underlying many management and conservation practices, such as using local seed sources for restoration, may not hold for some species. If contemporary adaptational lag is commonplace, we will need new approaches to help alleviate predicted negative consequences of climate warming on natural systems. We present one such approach, “genome-informed assisted gene flow,” which optimally matches individuals to future climates based on genotype–phenotype–environment associations. more...

Climate refugia are locations where plants are able to survive periods of regionally adverse climate. Such refugia may affect evolutionary processes and the maintenance of biodiversity. Numerous refugia have been identified in the context of Quaternary climate oscillations. With climate warming, there is an increasing need to apply insights from the past to characterize potential future refugia. Mountainous regions, due to the provision of spatially heterogeneous habitats, may contain high biodiversity, particularly important during climate oscillations. Here, we highlight the importance of mountaintops as climate refugia, using the example of high-mountain oaks which are distributed on the ranges of the Himalaya–Hengduan Mountains, and at high elevations in tropical rainforests. The occurrences of cold-adapted high-mountain oaks on mountaintops amidst tropical rainforest indicate that such locations are and will be climate refugia as global warming continues. We examine factors that predict the occurrence of future climate refugia on mountaintops using recognized historical refugia. Future research is needed to elucidate the fine-scale processes and particular geographic locations that buffer species against the rapidly changing climate to guide biodiversity conservation efforts under global warming scenarios. more...

Amyotrophic lateral sclerosis (ALS) is an incurable disease characterized by proteinaceous aggregate accumulation and neuroinflammation culminating in rapidly progressive lower and upper motor neuron death. To interrogate cell-intrinsic and inter-cell type perturbations in ALS, single-nucleus RNA sequencing was performed on the lumbar spinal cord in the murine ALS model SOD1 more...

Fundamental modulation of energy metabolism in immune cells is increasingly being recognized for the ability to impart important changes in cellular properties. In homeostasis, cells of the innate immune system, such as monocytes, macrophages and dendritic cells (DCs), are enabled to respond rapidly to various forms of acute cellular and environmental stress, such as pathogens. In chronic stress milieus, these cells may undergo a re-programming, thereby triggering processes that may instigate tissue damage and failure of resolution. In settings of metabolic dysfunction, moieties such as excess sugars (glucose, fructose and sucrose) accumulate in the tissues and may form advanced glycation end products (AGEs), which are signaling ligands for the receptor for advanced glycation end products (RAGE). In addition, cellular accumulation of cholesterol species such as that occurring upon macrophage engulfment of dead/dying cells, presents these cells with a major challenge to metabolize/efflux excess cholesterol. RAGE contributes to reduced expression and activities of molecules mediating cholesterol efflux. This Review chronicles examples of the roles that sugars and cholesterol, via RAGE, play in immune cells in instigation of maladaptive cellular signaling and the mediation of chronic cellular stress. At this time, emerging roles for the ligand-RAGE axis in metabolism-mediated modulation of inflammatory signaling in immune cells are being unearthed and add to the growing body of factors underlying pathological immunometabolism. more...

The genus Quercus, which emerged ∼55 million years ago during globally warm temperatures, diversified into ∼450 extant species. We present a high-quality de novo genome assembly of a California endemic oak, Quercus lobata, revealing features consistent with oak evolutionary success. Effective population size remained large throughout history despite declining since early Miocene. Analysis of 39,373 mapped protein-coding genes outlined copious duplications consistent with genetic and phenotypic diversity, both by retention of genes created during the ancient γ whole genome hexaploid duplication event and by tandem duplication within families, including numerous resistance genes and a very large block of duplicated DUF247 genes, which have been found to be associated with self-incompatibility in grasses. An additional surprising finding is that subcontext-specific patterns of DNA methylation associated with transposable elements reveal broadly-distributed heterochromatin in intergenic regions, similar to grasses. Collectively, these features promote genetic and phenotypic variation that would facilitate adaptability to changing environments. more...

The genus Quercus, which emerged ~55 million years ago during globally warm temperatures, diversified into ~450 species. We present a high-quality de novo genome assembly of a California endemic oak, Quercus lobata, revealing features consistent with oak evolutionary success. Effective population size remained large throughout history despite declining since the early Miocene. Analysis of 39,373 mapped protein-coding genes outlined copious duplications consistent with genetic and phenotypic diversity, both by retention of genes created during the ancient γ whole genome hexaploid duplication event and by tandem duplication within families, including the numerous resistance genes and also unexpected candidate genes for an incompatibility system involving multiple non-self-recognition genes. An additional surprising finding is that subcontext-specific patterns of DNA methylation associated with transposable elements reveal broadly-distributed heterochromatin in intergenic regions, similar to grasses (another highly successful taxon). Collectively, these features promote genetic and phenotypic variation that would facilitate adaptability to changing environments. more...

Local adaptation is a critical evolutionary process that allows plants to grow better in their local compared to non-native habitat and results in species-wide geographic patterns of adaptive genetic variation. For forest tree species with a long generation time, this spatial genetic heterogeneity can shape the ability of trees to respond to rapid climate change. Here, we identify genomic variation that may confer local environmental adaptations and then predict the extent of adaptive mismatch under future climate as a tool for forest restoration or management of the widely distributed high-elevation oak species Quercus rugosa in Mexico. Using genotyping by sequencing, we identified 5,354 single nucleotide polymorphisms (SNPs) genotyped from 103 individuals across 17 sites in the Trans-Mexican Volcanic Belt, and, after controlling for neutral genetic structure, we detected 74 F ST outlier SNPs and 97 SNPs associated with climate variation. Then, we deployed a nonlinear multivariate model, Gradient Forests, to map turnover in allele frequencies along environmental gradients and predict areas most sensitive to climate change. We found that spatial patterns of genetic variation were most strongly associated with precipitation seasonality and geographic distance. We identified regions of contemporary genetic and climatic similarities and predicted regions where future populations of Q. rugosa might be at risk due to high expected rate of climate change. Our findings provide preliminary details for future management strategies of Q. rugosa in Mexico and also illustrate how a landscape genomic approach can provide a useful tool for conservation and resource management strategies. more...

Identifying and quantifying the importance of environmental variables in structuring population genetic variation can help inform management decisions for conservation, restoration, or reforestation purposes, in both current and future environmental conditions. Landscape genomics offers a powerful approach for understanding the environmental factors that currently associate with genetic variation, and given those associations, where populations may be most vulnerable under future environmental change. Here, we applied genotyping by sequencing to generate over 11,000 single nucleotide polymorphisms from 311 trees and then used nonlinear, multivariate environmental association methods to examine spatial genetic structure and its association with environmental variation in an ecologically and economically important tree species endemic to Hawaii, Acacia koa. Admixture and principal components analyses showed that trees from different islands are genetically distinct in general, with the exception of some genotypes that match other islands, likely as the result of recent translocations. Gradient forest and generalized dissimilarity models both revealed a strong association between genetic structure and mean annual rainfall. Utilizing a model for projected future climate on the island of Hawaii, we show that predicted changes in rainfall patterns may result in genetic offset, such that trees no longer may be genetically matched to their environment. These findings indicate that knowledge of current and future rainfall gradients can provide valuable information for the conservation of existing populations and also help refine seed transfer guidelines for reforestation or replanting of koa throughout the state. more...

Within the scope of this study, current distribution areas and habitat preferences of Kasnak oak (Quercus vulcanica [Boiss. et Heldr. ex] Kotschy) species, which is known as one of the most rarest oak species in the world, have been revealed and a new distribution area has been determined around Ankara-Nallıhan-Sarıcali Mountain for the distribution map. Within the new distributon area, extent of occurrence calculated to be 166.597.545 km2, an area of occupancy calculated to be 68.000 km2 so, the threat category was updated as Least Concern (LC) in this study. Latitude, longitude, altitude (m), geographic location, geographical exposure, slope (%), parent material type, vegetation type, vegetation height (m) and the data related to vegetation cover (%) and climate data were recorded and evaluated during 2018 and 2019 field work. In addition, 112 species and 11 endemic were identified in the same habitat of the Kasnak oak. Consequently, in order to protect the genetic resources of the Kasnak oak species which is endemic to the country, it is very important to update the current distribution areas of the species and to preserve the biological diversity of the country., Bu çalışma kapsamında, yeryüzünde en nadir yayılış gösteren meşe türlerinden biri olarak bilinen endemik Kasnak meşesi (Quercus vulcanica [Boiss. et Heldr. ex] Kotschy) türünün güncel yayılış alanları ve habitat tercihleri ortaya konulmuş, Ankara-Nallıhan-Sarıçalı Dağı çevresinde yeni bir yayılış alanı daha saptanmıştır. Saptanan bu yeni alanının da ilavesiyle türün IUCN kategorisi yeniden değerlendirilerek türün yayılış alanı 166.597.545 km2, yaşam alanı da 68.000 km2 olarak hesaplanmış ve Düşük Riskli (LC: Least Concern) tehlike kategorisi güncellenmiştir. 2018-2019 yıllarında yapılan arazi çalışmaları kapsamında türün mevcut yayılış alanlarına dair enlem, boylam, yükselti (m), coğrafi konum, bakı, eğim (%), anakaya tipi, vejetasyon tipi, vejetasyon yüksekliği (m) ve vejetasyon (%) ile ilişkili veriler kaydedilerek değerlendirilmiştir. Ayrıca, yeni tespit edilen yayılış alanında kasnak meşesi ile birlikte yayılış gösteren bitki toplulukları da belirlenmiş ve 11’i endemik toplam 112 tür tespit edilmiştir. Sonuç olarak, ülkemize endemik Kasnak meşesi türünün gen kaynaklarının korunması ve türün yayılış alanlarının güncellenmesi, ülkemiz biyolojik çeşitliliğinin korunması açısından son derece önem arz etmektedir. more...

Understanding how the environment shapes genetic variation provides critical insight about the evolution of local adaptation in natural populations. At multiple spatial scales and multiple geographic contexts within a single species, such information could address a number of fundamental questions about the scale of local adaptation and whether or not the same loci are involved at different spatial scales or geographic contexts. We used landscape genomic approaches from three local elevational transects and rangewide sampling to (a) identify genetic variation underlying local adaptation to environmental gradients in the California endemic oak, Quercus lobata; (b) examine whether putatively adaptive SNPs show signatures of selection at multiple spatial scales; and (c) map putatively adaptive variation to assess the scale and pattern of local adaptation. Of over 10 k single-nucleotide polymorphisms (SNPs) generated with genotyping-by-sequencing, we found signatures of natural selection by climate or local environment at over 600 SNPs (536 loci), some at multiple spatial scales across multiple analyses. Candidate SNPs identified with gene-environment tests (LFMM) at the rangewide scale also showed elevated associations with climate variables compared to the background at both rangewide and elevational transect scales with gradient forest analysis. Some loci overlap with those detected in other oak species, raising the question of whether the same loci might be involved in local climate adaptation in different congeneric species that inhabit different geographic contexts. Mapping landscape patterns of adaptive versus background genetic variation identified regions of marked local adaptation and suggests nonlinear association of candidate SNPs and environmental variables. Taken together, our results offer robust evidence for novel candidate genes for local climate adaptation at multiple spatial scales. more...

The eastern North American white oaks, a complex of approximately 16 potentially interbreeding species, have become a classic model for studying the genetic nature of species in a syngameon. Genetic work over the past two decades has demonstrated the reality of oak species, but gene flow between sympatric oaks raises the question of whether there are conserved regions of the genome that define oak species. Does gene flow homogenize the entire genome? Do the regions of the genome that distinguish a species in one part of its range differ from the regions that distinguish it in other parts of its range, where it grows in sympatry with different species? Or are there regions of the genome that are relatively conserved across species ranges? In this study, we revisit seven species of the eastern North American white oak syngameon using a set of 80 SNPs selected in a previous study because they show differences among, and consistency within, the species. We test the hypothesis that there exist segments of the genome that do not become homogenized by repeated introgression, but retain distinct alleles characteristic of each species. We undertake a rangewide sampling to investigate whether SNPs that appeared to be fixed based on a relatively small sample in our previous work are fixed or nearly fixed across the range of the species. Each of the seven species remains genetically distinct across its range, given our diagnostic set of markers, with relatively few individuals exhibiting admixture of multiple species. SNPs map back to all 12Quercuslinkage groups (chromosomes) and are separated from each other by an average of 7.47 million base pairs (± 8.74 million bp, s.d.), but are significantly clustered relative to a random null distribution, suggesting that our SNP toolkit reflects genome-wide patterns of divergence while potentially being concentrated in regions of the genome that reflect a higher-than-average history of among-species divergence. This application of a DNA toolkit designed for the simple problem of identifying species in the field has an important implication: the eastern North American white oak syngameon is composed of entities that most taxonomists would consider “good species,” and species in the syngameon retain their genetic cohesion because characteristic portions of the genome do not become homogenized despite a history of introgression. more...

Phylogeography documents the spatial distribution of genetic lineages that result from demographic processes, such as population expansion, population contraction, and gene movement, shaped by climate fluctuations and the physical landscape. Because most phylogeographic studies have used neutral markers, the role of selection may have been undervalued. In this paper, we contend that plants provide a useful evolutionary lesson about the impact of selection on spatial patterns of neutral genetic variation, when the environment affects which individuals can colonize new sites, and on adaptive genetic variation, when environmental heterogeneity creates divergence at specific loci underlying local adaptation. Specifically, we discuss five characteristics found in plants that intensify the impact of selection: sessile growth form, high reproductive output, leptokurtic dispersal, isolation by environment, and the potential to evolve longevity. Collectively, these traits exacerbate the impact of environment on movement between populations and local selection pressures—both of which influence phylogeographic structure. We illustrate how these unique traits shape these processes with case studies of the California endemic oak, Quercus lobata , and the western North American lichen, Ramalina menziesii . Obviously, the lessons we learn from plant traits are not unique to plants, but they highlight the need for future animal, plant, and microbe studies to incorporate its impact. Modern tools that generate genome-wide sequence data are now allowing us to decipher how evolutionary processes affect the spatial distribution of different kinds of genes and also to better model future spatial distribution of species in response to climate change. more...

Aim Ecological differentiation of closely related species has attracted wide attention to explore its evolutionary significance in speciation. In particular, the prevalence of ecological speciation of sister species driven by Quaternary climate changes is debated. Here, we used two parapatric sister species, Roscoea humeana and R. cautleoides, to test whether ecological speciation was associated with Quaternary climate changes in these taxa. Location Hengduan-Mountain Region (HMR), south-west of China. Methods Nuclear ribosomal (ITS) and chloroplast DNA (cpDNA: psbA–trnH and trnL–trnF) were sequenced from 200 individuals. Gene genealogies were reconstructed using network, Bayesian inference and maximum likelihood methods. Interspecific divergence times were estimated with an isolation with migration model. Suitable habitats for each species were estimated with ecological niche modelling using Maxent and BIOCLIM. Niche overlap and niche divergence were tested using Schoener's D and Warren's I. Principal components analysis (PCA), multivariate analysis of variance (MANOVA) and discriminant function analysis (DFA) were also used to test ecological differentiation. Results Gene genealogies indicated that the low-elevational species R. cautleoides was derived from the high-elevational species R. humeana. Divergence among species occurred during the middle to late Quaternary (0.01–1.48 Ma). The species distribution and phylogeographical pattern were inconsistent with a geographical barrier. Niche models and statistical analyses showed significant ecological differentiation. Main conclusions Divergence between R. humeana and R. cautleoides was recent and coincident with Quaternary climate cycles. Ecological niche differentiation within Quaternary refugia may have promoted speciation. more...

International audience; Quercus magnoliifolia and Q. resinosa are two Mexican white oak species that have been taxonomically reported to exhibit morphological similarities and possible hybridization. The objective of this study was to compare the variation in Q. magnoliifolia and Q. resinosa throughout their distribution range to identify the degree of species differentiation using morphological, ecological and genetic tools. Morphological analysis showed differentiation in leaf shape between the species corresponding to the taxonomical identification of Q. magnoliifolia and Q. resinosa in almost all cases, but intermediate individuals were identified in the middle of the species ranges. Comparison of ecological niche models for Q. magnoliifolia and Q. resinosa showed non-equivalent ecological niches, high climatic niche differences and low to moderate spatial and environmental niche overlap, mainly along the Trans-Mexican Volcanic Belt where morphologically intermediate individuals between species were more frequently located, suggesting recent hybridization by secondary contact. In contrast, we found low but significant genetic differentiation between Q. magnoliifolia and Q. resinosa and lower interspecific than intraspecific genetic differentiation, and Bayesian clustering analysis (K = 2) failed to assign each species to a unique genotype, suggesting shared ancestral variation as the cause of genetic similarity between species due to recent divergence. In conclusion, although neutral molecular markers do not distinguish the species Q. magnoliifolia and Q. resinosa, we found morphological and ecological differentiation between these oaks that provide preliminary evidence for divergent selection. more...

International audience; The eastern North American white oaks, a complex of approximately 16 potentially interbreeding species, have become a classic model for studying the genetic nature of species in a syngameon. Genetic work over the past two decades has demonstrated the reality of oak species, but gene flow between sympatric oaks raises the question of whether there are conserved regions of the genome that define oak species. Does gene flow homogenize the entire genome? Do the regions of the genome that distinguish a species in one part of its range differ from the regions that distinguish it in other parts of its range, where it grows in sympatry with different species? Or are there regions of the genome that are relatively conserved across species ranges? In this study, we revisit seven species of the eastern North American white oak syngameon using a set of 80 single-nucleotide polymorphisms (SNPs) selected in a previous study because they show differences among, and consistency within, the species. We test the hypothesis that there exist segments of the genome that do not become homogenized by repeated introgression, but retain distinct alleles characteristic of each species. We undertake a range-wide sampling to investigate whether SNPs that appeared to be fixed based on a relatively small sample in our previous work are fixed or nearly fixed across the range of the species. Each of the seven species remains genetically distinct across its range, given our diagnostic set of markers, with relatively few individuals exhibiting admixture of multiple species. SNPs map back to all 12 Quercus linkage groups (chromosomes) and are separated from each other by an average of 7.47 million bp ((+) 8.74 million bp, SD), but are significantly clustered relative to a random null distribution, suggesting that our SNP toolkit reflects genome-wide patterns of divergence while potentially being concentrated in regions of the genome that reflect a higher-than-average history of among-species divergence. This application of a DNA toolkit designed for the simple problem of identifying species in the field has two important implications. First, the eastern North American white oak syngameon is composed of entities that most taxonomists would consider "good species." Second, and more fundamentally, species in the syngameon are genetically coherent because characteristic portions of the genome remain divergent despite a history of introgression. Understanding the conditions under which some loci diverge while others introgress is key to understanding the origins and maintenance of global tree diversity. more...

DNA methylation in plants affects transposon silencing, transcriptional regulation and thus phenotypic variation. One unanswered question is whether DNA methylation could be involved in local adaptation of plant populations to their environments. If methylation alters phenotypes to improve plant response to the environment, then methylation sites or the genes that affect them could be a target of natural selection. Using reduced-representation bisulphite sequencing (RRBS) data, we assessed whether climate is associated with variation in DNA methylation levels among 58 naturally occurring, and species-wide samples of valley oak (Quercus lobata) collected across climate gradients. We identified the genomic context of these variants referencing a new draft valley oak genome sequence. Methylation data were obtained for 341 107 cytosines, of which we deemed 57 488 as single-methylation variants (SMVs), found in the CG, CHG and CHH sequence contexts. Environmental association analyses revealed 43 specific SMVs that are significantly associated with any of four climate variables, the majority of which are associated with mean maximum temperature. The 43 climate-associated SMVs tend to occur in or near genes, several of which have known involvement in plant response to environment. Multivariate analyses show that climate and spatial variables explain more overall variance in CG-SMVs among individuals than in SNPs, CHG-SMVs or CHH-SMVs. Together, these results from natural oak populations provide initial evidence for a role of CG methylation in locally adaptive evolution or plasticity in plant response. more...

Here we study hybridization, introgression and lineage diversification in the widely distributed canyon live oak (Quercus chrysolepis) and the relict island oak (Q. tomentella), two Californian golden cup oaks with an intriguing biogeographical history. We employed restriction-site-associated DNA sequencing and integrated phylogenomic and population genomic analyses to study hybridization and reconstruct the evolutionary past of these taxa. Our analyses revealed the presence of two cryptic lineages within Q. chrysolepis. One of these lineages shares its most recent common ancestor with Q. tomentella, supporting the paraphyly of Q. chrysolepis. The split of these lineages was estimated to take place during the late Pliocene or the early Pleistocene, a time corresponding well with the common presence of Q. tomentella in the fossil records of continental California. Analyses also revealed historical hybridization among lineages, high introgression from Q. tomentella into Q. chrysolepis in their current area of sympatry, and widespread admixture between the two lineages of Q. chrysolepis in contact zones. Our results support that the two lineages of Q. chrysolepis behave as a single functional species phenotypically and ecologically well differentiated from Q. tomentella, a situation that can be only accommodated considering hybridization and speciation as a continuum with diffuse limits. more...

Many plant species exhibit heterophylly, displaying different leaves upon a single plant. The molecular mechanisms regulating this phenomenon, however, have remained elusive. In this study, the transcriptomes of submerged and floating leaves of an aquatic heterophyllous plant, Potamogeton octandrus Poir, were sequenced using a high-throughput sequencing technique (RNA-Seq), which aims to assist with the gene discovery and functional studies of genes involved in heterophyllous leaf development. A total of 81,103 unigenes were identified from the submerged and floating leaves, and a total of 6,822 differentially expressed genes (DEGs) were identified by comparing the samples from each developmental stage. KEGG pathway enrichment analysis categorized these unigenes into 128 pathways (p-value < 10-5). A total of 24,025 differentially expressed genes were involved in the carbon metabolic pathway, biosynthesis of amino acids, ribosomes, and plant-pathogen interaction. KEGG pathway enrichment analysis categorized a total of 70 DEGs into plant hormone signal transduction pathways. This study describes the initial results of the high-throughput transcriptome sequencing of heterophylly. Understanding the transcriptomes of floating and submerged leaves of the aquatic plant P. octandrus will assist with gene cloning and functional studies of genes involved in leaf development. This is especially the case with those involved in heterophyllous leaf development. more...

A long-term debate in evolutionary biology is the extent to which reproductive isolation is a necessary element of speciation. Hybridizing plants in general are cited as evidence against this notion, and oaks specifically have been used as the classic example of species maintenance without reproductive isolation. Here, we use thousands of SNPs generated by RAD sequencing to describe the phylogeny of a set of sympatric white oak species in California and then test whether these species exhibit pervasive interspecific gene exchange. Using RAD sequencing, we first constructed a phylogeny of ten oak species found in California. Our phylogeny revealed that seven scrub oak taxa occur within one clade that diverged from a common ancestor with Q. lobata, that they comprise two subclades, and they are not monophyletic but include the widespread tree oak Q. douglasii. Next, we searched for genomic patterns of allele sharing consistent with gene flow between long-divergent tree oaks with scrub oaks. Specifically, we utilized the D-statistic as well as model-based inference to compare the signature of shared alleles between two focal tree species (Q. lobata and Q. engelmannii) with multiple scrub species within the two subclades. We found that introgression is not equally pervasive between sympatric tree and scrub oak species. Instead, gene flow commonly occurs from scrub oaks to recently sympatric Q. engelmannii, but less so from scrub oaks to long-sympatric Q. lobata. This case study illustrates the influence of ancient introgression and impact of reproductive isolating mechanisms in preventing indiscriminate interspecific gene exchange. more...

Identifying and quantifying the importance of environmental variables in structuring population genetic variation can help inform management decisions for conservation, restoration, or reforestation purposes, in both current and future environmental conditions. Landscape genomics offers a powerful approach for understanding the environmental factors that currently associate with genetic variation, and given those associations, where populations may be most vulnerable under future environmental change. Here, we applied genotyping by sequencing to generate over 11,000 single nucleotide polymorphisms from 311 trees and then used nonlinear, multivariate environmental association methods to examine spatial genetic structure and its association with environmental variation in an ecologically and economically important tree species endemic to Hawaii, Acacia koa. Admixture and principal components analyses showed that trees from different islands are genetically distinct in general, with the exception of some genotypes that match other islands, likely as the result of recent translocations. Gradient forest and generalized dissimilarity models both revealed a strong association between genetic structure and mean annual rainfall. Utilizing a model for projected future climate on the island of Hawaii, we show that predicted changes in rainfall patterns may result in genetic offset, such that trees no longer may be genetically matched to their environment. These findings indicate that knowledge of current and future rainfall gradients can provide valuable information for the conservation of existing populations and also help refine seed transfer guidelines for reforestation or replanting of koa throughout the state. more...

Landscape genomic studies analyze spatial patterns of genetic variation to test hypotheses about how demographic history, gene flow, and natural selection have shaped populations. For decades, angiosperm trees have served as outstanding model systems for landscape-scale genetic studies due to their extensive geographic ranges, large effective population sizes, abundant genetic diversity, and high gene flow. These characteristics were recognized early in the landscape genetics literature, and studies on angiosperm trees, particularly Populus and Quercus, tested hypotheses about how landscape features shaped neutral patterns of gene flow and population divergence. More recently, advances in sequencing and analysis methodologies have allowed for greater opportunities to directly test how natural selection acting locally across the landscape has shaped the genome-wide diversity of populations, often in the context of broad climatic gradients in growing season length. Despite, the methodological gains and successes of the last decade, landscape genomics studies face new challenges of study design, hypothesis testing, and validation. Here, we explore the development of landscape genetics and genomics in angiosperm trees and what we have learned from investigating the evolutionary consequences of life as a tree in heterogeneous landscapes. We outline the past, present, and potential future of landscape genomic studies in angiosperm trees, highlighting successes of the field, challenges to overcome, and ideas that scientists from all backgrounds engaged in landscape genomics should consider. more...

Reduced water availability during drought can create major stress for many plant species. Within a species, populations with a history of seasonal drought may have evolved the ability to tolerate drought more than those in areas of high precipitation and low seasonality. In this study, we assessed response to water stress in a California oak species, Quercus lobata Née, by measuring changes in gene expression profiles before and after a simulated drought stress treatment through water deprivation of seedlings in a greenhouse setting. Using whole-transcriptome sequencing from nine samples from three collection localities, we identified which genes are involved in response to drought stress and tested the hypothesis that seedlings sampled from climatically different regions of the species range respond to water stress differently. We observed a surprisingly massive transcriptional response to drought: 35,347 of 68,434 contigs (52%) were differentially expressed before versus after drought treatment, of which 18,111 were down-regulated and 17,236 were up-regulated. Genes functionally associated with abiotic stresses and death were enriched among the up-regulated genes, whereas metabolic and cell part-related genes were enriched among the down-regulated. We found 56 contigs that exhibited significantly different expression responses to the drought treatment among the three populations (treatment × population interaction), suggesting that those genes may be involved in local adaptation to drought stress. These genes have stress response (e.g., WRKY DNA-binding protein 51 and HSP20-like chaperones superfamily protein), metabolic (e.g., phosphoglycerate kinase and protein kinase superfamily protein), transport/transfer (e.g., cationic amino acid transporter 7 and K+ transporter) and regulatory functions (e.g., WRKY51 and Homeodomain-like transcriptional regulator). Baseline expression levels of 1310 unique contigs also differed among pairs of populations, and they were enriched for metabolic and cell part-related genes. Out of the large fraction of the transcriptome that was differentially expressed in response to our drought treatment, we identified several novel genes that are candidates for involvement in local adaptation to drought. more...

Natural hybridization, which can be involved in local adaptation and in speciation processes, has been linked to different sources of anthropogenic disturbance. Here, we use genotypic data to study range-wide patterns of genetic admixture between the serpentine-soil specialist leather oak (Quercus durata) and the widespread Californian scrub oak (Quercus berberidifolia). First, we estimated hybridization rates and the direction of gene flow. Second, we tested the hypothesis that genetic admixture increases with different sources of environmental disturbance, namely anthropogenic destruction of natural habitats and wildfire frequency estimated from long-term records of fire occurrence. Our analyses indicate considerable rates of hybridization (> 25%), asymmetric gene flow from Q. durata into Q. berberidifolia, and a higher occurrence of hybrids in areas where both species live in close parapatry. In accordance with the environmental disturbance hypothesis, we found that genetic admixture increases with wildfire frequency, but we did not find a significant effect of other sources of human-induced habitat alteration (urbanization, land clearing for agriculture) or a suite of ecological factors (climate, elevation, soil type). Our findings highlight that wildfires constitute an important source of environmental disturbance, promoting hybridization between two ecologically well-differentiated native species. more...

A fundamental goal of evolutionary biology is to understand how environment shapes genetic variation through its effect on demographic processes and through natural selection. In non-model species, transcriptome sequencing generates large single nucleotide polymorphism (SNP) panels to disentangle these influences. Quercus lobata (valley oak) offers an excellent system for such analyses because it has stably occupied a climatically heterogeneous landscape throughout California. We used 220,427 diallelic SNPs from 22 individuals identified against a recently assembled reference transcriptome to (1) quantify transcriptome-wide associations of SNPs with climate indicative of demographic responses to climate, (2) identify SNPs especially associated with climate and thus potential targets of natural selection, and (3) test the hypothesis that genetic diversity is high in climate-adaptive candidate genes. Constrained ordinations (redundancy analysis) and variance partitioning showed that genetic structure in Q. lobata was explained by spatial location (49 %) and climate (24 %), especially minimum temperature and summer/spring precipitation balance, suggesting that climate influences neutral demographic processes and gene flow. After accounting for underlying structure, individual-based environmental association analyses identified 79 SNPs from 49 transcripts as candidates under natural selection by climate. These candidate genes had significantly higher SNP rates per base pair per locus (θ W), nucleotide diversity (π), and gene diversity (G) than non-candidate genes. These results provide preliminary support for the hypothesis that balancing selection maintains diversity in climate-adaptive genes. Climate has likely shaped both population demography and local adaptation in valley oak. more...

PREMISE OF THE STUDY: Geography and climate shape the distribution of organisms, their genotypes, and their phenotypes. To understand historical and future evolutionary and ecological responses to climate, we compared the association of geography and climate of three oak species (Quercus engelmannii, Quercus berberidifolia, and Quercus cornelius-mulleri) in an environmentally heterogeneous region of southern California at three organizational levels: regional species distributions, genetic variation, and phenotypic variation. METHODS: We identified climatic variables influencing regional distribution patterns using species distribution models (SDMs), and then tested whether those individual variables are important in shaping genetic (microsatellite) and phenotypic (leaf morphology) variation. We estimated the relative contributions of geography and climate using multivariate redundancy analyses (RDA) with variance partitioning. KEY RESULTS: The modeled distribution of each species was influenced by climate differently. Our analysis of genetic variation using RDA identified small but significant associations between genetic variation with climate and geography in Q. engelmannii and Q. cornelius-mulleri, but not in Q. berberidifolia, and climate explained more of the variation. Our analysis of phenotypic variation in Q. engelmannii indicated that climate had more impact than geography, but not in Q. berberidifolia. Throughout our analyses, we did not find a consistent pattern in effects of individual climatic variables. CONCLUSIONS: Our comparative analysis illustrates that climate influences tree response at all organizational levels, but the important climate factors vary depending on the level and on the species. Because of these species-specific and level-specific responses, today’s sympatric species are unlikely to have similar distributions in the future more...

Understanding the factors promoting species formation is a major task in evolutionary research. Here, we employ an integrative approach to study the evolutionary history of the Californian scrub white oak species complex (genus Quercus). To infer the relative importance of geographical isolation and ecological divergence in driving the speciation process, we (i) analysed inter- and intraspecific patterns of genetic differentiation and employed an approximate Bayesian computation (ABC) framework to evaluate different plausible scenarios of species divergence. In a second step, we (ii) linked the inferred divergence pathways with current and past species distribution models (SDMs) and (iii) tested for niche differentiation and phylogenetic niche conservatism across taxa. ABC analyses showed that the most plausible scenario is the one considering the divergence of two main lineages followed by a more recent pulse of speciation. Genotypic data in conjunction with SDMs and niche differentiation analyses support that different factors (geography vs. environment) and modes of speciation (parapatry, allopatry and maybe sympatry) have played a role in the divergence process within this complex. We found no significant relationship between genetic differentiation and niche overlap, which probably reflects niche lability and/or that multiple factors, have contributed to speciation. Our study shows that different mechanisms can drive divergence even among closely related taxa representing early stages of species formation and exemplifies the importance of adopting integrative approaches to get a better understanding of the speciation process., JO was supported by a Ramón y Cajal Fellowship (RYC-2013-12501) and a research contract funded by Severo Ochoa Program (SEV-2012-0262). VN was supported by a FPI predoctoral fellowship from Ministerio de Economía y Competitividad. This work was supported by an internal EBD ‘Microproyectos’ grant to JO, financed by the Spanish Ministry of Economy and Competitiveness through the Severo Ochoa Program for Centres of Excellence in R + D + I (SEV-2012-0262). more...

PREMISE OF THE STUDY The ability of California tree populations to survive anthropogenic climate change will be shaped by the geographic structure of adaptive genetic variation. Our goal is to test whether climate-associated candidate genes show evidence of spatially divergent selection in natural populations of valley oak, Quercus lobata, as preliminary indication of local adaptation. METHODS Using DNA from 45 individuals from 13 localities across the species' range, we sequenced portions of 40 candidate genes related to budburst/flowering, growth, osmotic stress, and temperature stress. Using 195 single nucleotide polymorphisms (SNPs), we estimated genetic differentiation across populations and correlated allele frequencies with climate gradients using single-locus and multivariate models. RESULTS The top 5% of FST estimates ranged from 0.25 to 0.68, yielding loci potentially under spatially divergent selection. Environmental analyses of SNP frequencies with climate gradients revealed three significantly correlated SNPs within budburst/flowering genes and two SNPs within temperature stress genes with mean annual precipitation, after controlling for multiple testing. A redundancy model showed a significant association between SNPs and climate variables and revealed a similar set of SNPs with high loadings on the first axis. In the RDA, climate accounted for 67% of the explained variation, when holding climate constant, in contrast to a putatively neutral SSR data set where climate accounted for only 33%. CONCLUSIONS Population differentiation and geographic gradients of allele frequencies in climate-associated functional genes in Q. lobata provide initial evidence of adaptive genetic variation and background for predicting population response to climate change. more...