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Most tree species underwent cycles of contraction and expansion during the Quaternary. These cycles led to an ancient and complex genetic structure that has since been affected by extensive gene flow and by strong local adaptation. The extent to which hybridization played a role in this multi-layered genetic structure is important to be investigated. To study the effect of hybridization on the joint population genetic structure of two dominant species of the Eurasian boreal forest, Picea abies and P. obovata, we used targeted resequencing and obtained around 480 K nuclear SNPs and 87 chloroplast SNPs in 542 individuals sampled across most of their distribution ranges. Despite extensive gene flow and a clear pattern of Isolation-by-Distance, distinct genetic clusters emerged, indicating the presence of barriers and corridors to migration. Two cryptic refugia located in the large hybrid zone between the two species played a critical role in shaping their current distributions. The two species repeatedly hybridized during the Pleistocene and the direction of introgression depended on latitude. Our study suggests that hybridization helped both species to overcome main shifts in their distribution ranges during glacial cycles and highlights the importance of considering whole species complex instead of separate entities to retrieve complex demographic histories.
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DNA methylation is environment-sensitive and can mediate stress responses. In long-lived trees, changing environments might cumulatively shape the methylome landscape over their lifetime. However, because high-resolution methylome studies usually focus on single environmental cues, it remains unclear to what extent the methylation responses are generic or stress-specific, and how this relates to their long-term stability. Here, we studied the methylome plasticity of a Populus nigra cv. 'Italica' clone that is widespread across Europe. Adult trees from a variety of geographic locations were clonally propagated in a common garden experiment, and the ramets were exposed to cold, heat, drought, herbivory, rust infection, and salicylic acid treatments. Through comprehensive whole-genome bisulfite sequencing, we analyzed stress-induced and naturally occurring DNA methylation variants. Stress-induced methylation changes predominantly targeted transposable elements. When occurring in CG/CHG contexts, the same regions were often affected by multiple stresses, suggesting a generic response of the methylome. Drought stress caused a distinct CHH hypermethylation response in transposable elements, affecting entire TE superfamilies near drought-responsive genes. Methylation differences in CG/CHG contexts that were induced by stress treatments showed striking overlap with methylation differences observed between trees from distinct geographical locations. Thus, we revealed genomic hotspots of methylation change that are not stress-specific and that contribute to natural DNA methylation variation, and we identified specific transposable element superfamilies that respond to a specific stress with possible functional consequences. Our results underscore the importance of studying the effects of multiple stressors in a single experiment for recognizing general versus stress-specific methylome responses.
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PREMISE: Vertical stratification is a key feature of tropical forests and plant-frugivore interactions. However, it is unclear whether equally strong patterns of vertical stratification exist for plant-nectarivore interactions and, if so, which factors drive these patterns. Further, nectar-inhabiting bacteria, acting as "hidden players" in plant-nectarivore interactions, might be vertically stratified, either in response to differences among strata in microenvironmental conditions or to the nectarivore community serving as vectors. METHODS: We observed visitations by a diverse nectarivore community to the liana Marcgravia longifolia in a Peruvian rainforest and characterized diversity and community composition of nectar-inhabiting bacteria. Unlike most other plants, M. longifolia produces inflorescences across forest strata, enabling us to study effects of vertical stratification on plant-nectarivore interactions without confounding effects of plant species and stratum. RESULTS: A significantly higher number of visits were by nectarivorous bats and hummingbirds in the midstory than in the understory and canopy, and the visits were strongly correlated to flower availability and nectar quantity and quality. Trochiline hummingbirds foraged across all strata, whereas hermits remained in the lower strata. The Shannon diversity index for nectar-inhabiting bacterial communities was highest in the midstory. CONCLUSIONS: Our findings suggest that vertical niche differentiation in plant-nectarivore interactions seems to be partly driven by resource abundance, but other factors such as species-specific preferences of hummingbirds, likely caused by competition, play an important role. We conclude that vertical stratification is an important driver of a species' interaction niche highlighting its role for promoting biodiversity and ecosystem functioning.
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Ecosistema , Néctar de las Plantas , Animales , Bosques , Biodiversidad , Flores , Aves/fisiologíaRESUMEN
Climate change is increasing the frequency and intensity of drought events in many boreal forests. Trees are sessile organisms with a long generation time, which makes them vulnerable to fast climate change and hinders fast adaptations. Therefore, it is important to know how forests cope with drought stress and to explore the genetic basis of these reactions. We investigated three natural populations of white spruce (Picea glauca) in Alaska, located at one drought-limited and two cold-limited treelines with a paired plot design of one forest and one treeline plot. We obtained individual increment cores from 458 trees and climate data to assess dendrophenotypes, in particular the growth reaction to drought stress. To explore the genetic basis of these dendrophenotypes, we genotyped the individual trees at 3000 single nucleotide polymorphisms in candidate genes and performed genotype-phenotype association analysis using linear mixed models and Bayesian sparse linear mixed models. Growth reaction to drought stress differed in contrasting treeline populations. Therefore, the populations are likely to be unevenly affected by climate change. We identified 40 genes associated with dendrophenotypic traits that differed among the treeline populations. Most genes were identified in the drought-limited site, indicating comparatively strong selection pressure of drought-tolerant phenotypes. Contrasting patterns of drought-associated genes among sampled sites and in comparison to Canadian populations in a previous study suggest that drought adaptation acts on a local scale. Our results highlight genes that are associated with wood traits which in turn are critical for the establishment and persistence of future forests under climate change.
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Picea , Tracheophyta , Teorema de Bayes , Canadá , Cambio Climático , Sequías , BosquesRESUMEN
Early-stage fitness variation has been seldom evaluated at broad scales in forest tree species, despite the long tradition of studying climate-driven intraspecific genetic variation. In this study, we evaluated the role of climate in driving patterns of population differentiation at early-life stages in Pinus sylvestris and explored the fitness and growth consequences of seed transfer within the species range. We monitored seedling emergence, survival and growth over a 2-yr period in a multi-site common garden experiment which included 18 European populations and spanned 25° in latitude and 1700 m in elevation. Climate-fitness functions showed that populations exhibited higher seedling survival and growth at temperatures similar to their home environment, which is consistent with local adaptation. Northern populations experienced lower survival and growth at warmer sites, contrary to previous studies on later life stages. Seed mass was higher in populations from warmer areas and was positively associated with survival and growth at more southern sites. Finally, we did not detect a survival-growth trade-off; on the contrary, bigger seedlings exhibited higher survival probabilities under most climatic conditions. In conclusion, our results reveal that contrasting temperature regimes have played an important role in driving the divergent evolution of P. sylvestris populations at early-life stages.
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Pinus sylvestris , Pinus , Aclimatación , Cambio Climático , Plantones , TemperaturaRESUMEN
Understanding the dynamics of selection is key to predicting the response of tree species to new environmental conditions in the current context of climate change. However, selection patterns acting on early recruitment stages and their climatic drivers remain largely unknown in most tree species, despite being a critical period of their life cycle. We measured phenotypic selection on Pinus sylvestris seed mass, emergence time and early growth rate over 2 yr in four common garden experiments established along the latitudinal gradient of the species in Europe. Significant phenotypic plasticity and among-population genetic variation were found for all measured phenotypic traits. Heat and drought negatively affected fitness in the southern sites, but heavy rainfalls also decreased early survival in middle latitudes. Climate-driven directional selection was found for higher seed mass and earlier emergence time, while the form of selection on seedling growth rates differed among sites and populations. Evidence of adaptive and maladaptive phenotypic plasticity was found for emergence time and early growth rate, respectively. Seed mass, emergence time and early growth rate have an adaptive role in the early stages of P. sylvestris and climate strongly influences the patterns of selection on these fitness-related traits.
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Pinus sylvestris , Pinus , Cambio Climático , Europa (Continente) , Fenotipo , Pinus sylvestris/genética , TemperaturaRESUMEN
Variation in genetic diversity across species ranges has long been recognized as highly informative for assessing populations' resilience and adaptive potential. The spatial distribution of genetic diversity within populations, referred to as fine-scale spatial genetic structure (FSGS), also carries information about recent demographic changes, yet it has rarely been connected to range scale processes. We studied eight silver fir (Abies alba Mill.) population pairs (sites), growing at high and low elevations, representative of the main genetic lineages of the species. A total of 1,368 adult trees and 540 seedlings were genotyped using 137 and 116 single nucleotide polymorphisms (SNPs), respectively. Sites revealed a clear east-west isolation-by-distance pattern consistent with the post-glacial colonization history of the species. Genetic differentiation among sites (FCT = 0.148) was an order of magnitude greater than between elevations within sites (FSC = 0.031), nevertheless high elevation populations consistently exhibited a stronger FSGS. Structural equation modelling revealed that elevation and, to a lesser extent, post-glacial colonization history, but not climatic and habitat variables, were the best predictors of FSGS across populations. These results suggest that high elevation habitats have been colonized more recently across the species range. Additionally, paternity analysis revealed a high reproductive skew among adults and a stronger FSGS in seedlings than in adults, suggesting that FSGS may conserve the signature of demographic changes for several generations. Our results emphasize that spatial patterns of genetic diversity within populations provide information about demographic history complementary to non-spatial statistics, and could be used for genetic diversity monitoring, especially in forest trees.
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Abies , Abies/genética , Ecosistema , Bosques , Estructuras Genéticas , Variación Genética , Árboles/genéticaRESUMEN
Trees are constantly exposed to climate fluctuations, which vary with both time and geographic location. Environmental changes that are outside of the physiological favorable range usually negatively affect plant performance and trigger responses to abiotic stress. Long-living trees in particular have evolved a wide spectrum of molecular mechanisms to coordinate growth and development under stressful conditions, thus minimizing fitness costs. The ongoing development of techniques directed at quantifying abiotic stress has significantly increased our knowledge of physiological responses in woody plants. However, it is only within recent years that advances in next-generation sequencing and biochemical approaches have enabled us to begin to understand the complexity of the molecular systems that underlie these responses. Here, we review recent progress in our understanding of the molecular bases of drought and temperature stresses in trees, with a focus on functional, transcriptomic, epigenetic, and population genomic studies. In addition, we highlight topics that will contribute to progress in our understanding of the plastic and adaptive responses of woody plants to drought and temperature in a context of global climate change.
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Estrés Fisiológico , Árboles , Sequías , Genómica , Plantas , Árboles/genéticaRESUMEN
Quantifying the individual reproductive success and understanding its determinants is a central issue in evolutionary research for the major consequences that the transmission of genetic variation from parents to offspring has on the adaptive potential of populations. Here, we propose to distil the myriad of information embedded in tree-ring time series into a set of tree-ring-based phenotypic traits to be investigated as potential drivers of reproductive success in forest trees. By using a cross-disciplinary approach that combines parentage analysis and a thorough dendrophenotypic characterisation of putative parents, we assessed sex-specific relationships between such dendrophenotypic traits (i.e., age, growth rate and parameters describing sensitivity to climate and to extreme climatic events) and reproductive success in Norway spruce. We applied a full probability method for reconstructing parent-offspring relationships between 604 seedlings and 518 adult trees sampled within five populations from southern and central Europe. We found that individual female and male reproductive success was positively associated with tree growth rate and age. Female reproductive success was also positively influenced by the correlation between growth and the mean temperature of the previous vegetative season. Overall, our results showed that Norway spruce individuals with the highest fitness are those who are able to keep high-growth rates despite potential growth limitations caused by reproductive costs and climatic limiting conditions. Identifying such functional links between the individual ecophysiological behaviour and its evolutionary gain would increase our understanding on how natural selection shapes the genetic composition of forest tree populations over time.
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Picea , Temperatura , Europa (Continente) , Bosques , Picea/genética , Picea/crecimiento & desarrollo , ReproducciónRESUMEN
Growing evidence shows that epigenetic mechanisms contribute to complex traits, with implications across many fields of biology. In plant ecology, recent studies have attempted to merge ecological experiments with epigenetic analyses to elucidate the contribution of epigenetics to plant phenotypes, stress responses, adaptation to habitat, and range distributions. While there has been some progress in revealing the role of epigenetics in ecological processes, studies with non-model species have so far been limited to describing broad patterns based on anonymous markers of DNA methylation. In contrast, studies with model species have benefited from powerful genomic resources, which contribute to a more mechanistic understanding but have limited ecological realism. Understanding the significance of epigenetics for plant ecology requires increased transfer of knowledge and methods from model species research to genomes of evolutionarily divergent species, and examination of responses to complex natural environments at a more mechanistic level. This requires transforming genomics tools specifically for studying non-model species, which is challenging given the large and often polyploid genomes of plants. Collaboration among molecular geneticists, ecologists and bioinformaticians promises to enhance our understanding of the mutual links between genome function and ecological processes.
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Ecología , Epigénesis Genética , Plantas , Metilación de ADN , EcosistemaRESUMEN
Spatial genetic structure (SGS) of plants results from the nonrandom distribution of related individuals. SGS provides information on gene flow and spatial patterns of genetic diversity within populations. Seed dispersal creates the spatial template for plant distribution. Thus, in zoochorous plants, dispersal mode and disperser behaviour might have a strong impact on SGS. However, many studies only report the taxonomic group of seed dispersers, without further details. The recent increase in studies on SGS provides the opportunity to review findings and test for the influence of dispersal mode, taxonomic affiliation of dispersers and their behaviour. We compared the proportions of studies with SGS among groups and tested for differences in strength of SGS using Sp statistics. The presence of SGS differed among taxonomic groups, with reduced presence in plants dispersed by birds. Strength of SGS was instead significantly influenced by the behaviour of seed dispersal vectors, with higher SGS in plant species dispersed by animals with behavioural traits that result in short seed dispersal distances. We observed high variance in the strength of SGS in plants dispersed by animals that actively or passively accumulate seeds. Additionally, we found SGS was also affected by pollination and marker type used. Our study highlights the importance of vector behaviour on SGS even in the presence of variance created by other factors. Thus, more detailed information on the behaviour of seed dispersers would contribute to better understand which factors shape the spatial scale of gene flow in animal-dispersed plant species.
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Flujo Génico , Genética de Población , Plantas/genética , Dispersión de Semillas , Animales , Aves , Variación Genética , Polinización , Análisis EspacialRESUMEN
Sakis (genus Pithecia) are frugivorous primates with a preference for seeds that complete their diet with leaves and insects. Fruit pulp and seeds are known to have different nutritional characteristics that change during the process of ripening. The consumption of seeds can be an adaptation to changes in resource availability, as unripe seeds are a more steadily available resource than ripe pulp or young leaves. Here, we present the first study of the feeding ecology of monk sakis (Pithecia monachus). We investigated dietary composition and identified important feeding plants in a seasonally flooded forest within the Área de Conservación Regional Comunal Tamshiyacu-Tahuayo in Peruvian Amazonia. Throughout 20 months, we followed groups of monk sakis by foot and canoe and recorded 459 feeding events. Seeds were the most frequently consumed food item (49%), followed by pulp (mesocarp, pericarp or aril; 25%) and arthropods (22%). Leaves, bark, and flowers were ingested only sporadically. The importance of ripe seeds and arthropods in the diet of the monk sakis differed from other studies: we recorded the consumption of mostly ripe seeds and the share of arthropods was relatively high.
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Artrópodos , Pitheciidae , Animales , Conducta Alimentaria , Ecología , Frutas , Dieta , BosquesRESUMEN
PREMISE OF THE STUDY: We developed a set of microsatellite markers for broad utility across the species-rich pantropical tree genus Ficus (fig trees). The markers were developed to study population structure, hybridization, and gene flow in neotropical species. METHODS AND RESULTS: We developed seven novel primer sets from expressed sequence tag (EST) libraries of F. citrifolia and F. popenoei (subgen. Urostigma sect. Americana) and optimized five previously developed anonymous loci for cross-species amplification. The markers were successfully tested on four species from the basal subgenus Pharmacosycea sect. Pharmacosycea (F. insipida, F. maxima, F. tonduzii, and F. yoponensis) and seven species of the derived subgenus Urostigma (F. citrifolia, F. colubrinae, F. costaricana, F. nymphaeifolia, F. obtusifolia, F. pertusa, and F. popenoei). The 12 markers amplified consistently and displayed polymorphism in all the species. CONCLUSIONS: This set of microsatellite markers is transferable across the phylogenetic breadth of Ficus, and should therefore be useful for studies of population structure and gene flow in approximately 750 fig species worldwide.
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Cartilla de ADN/genética , Ficus/genética , Repeticiones de Microsatélite/genética , Polimorfismo Genético , Alelos , Secuencia de Bases , ADN de Plantas/genética , Etiquetas de Secuencia Expresada , Ficus/clasificación , Flujo Génico , Biblioteca de Genes , Sitios Genéticos , Marcadores Genéticos , Heterocigoto , Datos de Secuencia Molecular , Hojas de la Planta/clasificación , Hojas de la Planta/genética , Análisis de Secuencia de ADN , Especificidad de la EspecieRESUMEN
Rapid human-induced environmental changes like climate warming represent a challenge for forest ecosystems. Due to their biological complexity and the long generation time of their keystone tree species, genetic adaptation in these ecosystems might not be fast enough to keep track with conditions changing at such a fast pace. The study of adaptation to environmental change and its genetic mechanisms is therefore key for ensuring a sustainable support and management of forests. The 4-day conference of the European Research Group EvolTree (https://www.evoltree.eu) on the topic of "Genomics and Adaptation in Forest Ecosystems" brought together over 130 scientists to present and discuss the latest developments and findings in forest evolutionary research. Genomic studies in forest trees have long been hampered by the lack of high-quality genomics resources and affordable genotyping methods. This has dramatically changed in the last few years; the conference impressively showed how such tools are now being applied to study past demography, adaptation and interactions with associated organisms. Moreover, genomic studies are now finally also entering the world of conservation and forest management, for example by measuring the value or cost of interspecific hybridization and introgression, assessing the vulnerability of species and populations to future change, or accurately delineating evolutionary significant units. The newly launched conference series of EvolTree will hopefully play a key role in the exchange and synthesis of such important investigations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s11295-022-01542-1.
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The question whether or not tropical lianas infest host trees randomly or they exert host selection has implications for the structure and dynamics of tropical rainforests, particularly if colonization by lianas impacts host fitness. In this study, we present evidence that the Neotropical liana Marcgravia longifolia (Marcgraviaceae) infests host trees non-randomly. We identified host trees to species or genus level for 87 of the 100 M. longifolia individuals found in the study area of the Estación Biológica Quebrada Blanco (EBQB) in north-eastern Peruvian Amazonia. Data on host availability were taken from two 1-ha plots sampled at EBQB as part of a large-scale tree inventory in western Amazonia. Of the total of 88 tree genera with two or more individuals present in the inventory, 18 were represented amongst hosts. Host genera with a probability of colonization higher than expected by chance were Eschweilera (Lecythidaceae), Pouteria (Sapotaceae), Brosimum (Moraceae), and Hymenaea (Fabaceae). These findings suggest that M. longifolia exerts some level of host selectivity, but the mechanisms for this are completely unknown. Given the large number of animal species (41 bird species, three primate species) that are dispersing the seeds of M. longifolia and that have diverse ecological strategies, directed seed dispersal is unlikely to account for the observed patterns of host infestation.
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Bosque Lluvioso , Clima Tropical , Animales , Probabilidad , Semillas , PerúRESUMEN
Vertical stratification (VS) is a widespread phenomenon in plant and animal communities in forests and a key factor for structuring their species richness and biodiversity, particularly in tropical forests. The organisms composing forest communities adjust and shape the complex three-dimensional structure of their environment and inhabit a large variety of niches along the vertical gradient of the forest. Even though the degree of VS varies among different vertebrate groups, patterns of compositional stratification can be observed across taxa. Communities of birds, bats, primates, and non-flying small mammals are vertically stratified in terms of abundance, species richness, diversity, and community composition. Frugivorous members of these taxa play important roles as seed dispersers and forage on fruit resources that, in turn, vary in quantity and nutritional value along the vertical gradient. As a consequence, plant-seed disperser interaction networks differ among strata, which is manifested in differences in interaction frequencies and the degree of mutual specialization. In general, the canopy stratum is composed of strong links and generalized associations, while the lower strata comprise weaker links and more specialized interactions. Investigating the VS of communities can provide us with a better understanding of species habitat restrictions, resource use, spatial movement, and species interactions. Especially in the face of global change, this knowledge will be important as these characteristics can imply different responses of species and taxa at a fine spatial scale.
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Ecosistema , Bosques , Animales , Aves , Plantas , SemillasRESUMEN
Global warming is predicted to exert negative impacts on plant growth due to the damaging effect of high temperatures on plant physiology. Revealing the genetic architecture underlying the heat stress response is therefore crucial for the development of conservation strategies, and for breeding heat-resistant plant genotypes. Here we investigated the transcriptional changes induced by heat in Nothofagus pumilio, an emblematic tree species of the sub-Antarctic forests of South America. Through the performance of RNA-seq of leaves of plants exposed to 20°C (control) or 34°C (heat shock), we generated the first transcriptomic resource for the species. We also studied the changes in protein-coding transcripts expression in response to heat. We found 5,214 contigs differentially expressed between temperatures. The heat treatment resulted in a down-regulation of genes related to photosynthesis and carbon metabolism, whereas secondary metabolism, protein re-folding and response to stress were up-regulated. Moreover, several transcription factor families like WRKY or ERF were promoted by heat, alongside spliceosome machinery and hormone signaling pathways. Through a comparative analysis of gene regulation in response to heat in Arabidopsis thaliana, Populus tomentosa and N. pumilio we provide evidence of the existence of shared molecular features of heat stress responses across angiosperms, and identify genes of potential biotechnological application.
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Fagales/genética , Perfilación de la Expresión Génica/métodos , Proteínas de Plantas/genética , Regulación de la Expresión Génica de las Plantas , Redes Reguladoras de Genes , Respuesta al Choque Térmico , Hojas de la Planta/genética , Análisis de Secuencia de ARN , América del SurRESUMEN
Knowledge on the adaptation of trees to rapid environmental changes is essential to preserve forests and their ecosystem services under climate change. Treeline populations are particularly suitable for studying adaptation processes in trees, as environmental stress together with reduced gene flow can enhance local adaptation. We investigated white spruce (Picea glauca) populations in Alaska on one moisture-limited and two cold-limited treeline sites with a paired plot design of one forest and one treeline population each, resulting in six plots. Additionally, one forest plot in the middle of the distribution range complements the study design. We combined spatial, climatic and dendrochronological data with neutral genetic marker of 2203 trees to investigate population genetic structure and drivers of tree growth. We used several individual-based approaches including random slope mixed-effects models to test the influence of genetic similarity and microenvironment on growth performance. A high degree of genetic diversity was found within each of the seven plots associated with high rates of gene flow. We discovered a low genetic differentiation between the three sites which was better explained by geographic distances than by environmental differences, indicating genetic drift as the main driver of population differentiation. Our findings indicated that microenvironmental features had an overall larger influence on growth performances than genetic similarity among individuals. The effects of climate on growth differed between sites but were smaller than the effect of tree size. Overall, our results suggest that the high genetic diversity of white spruce may result in a wider range of phenotypes which enhances the efficiency of selection when the species is facing rapid climatic changes. In addition, the large intra-individual variability in growth responses may indicate the high phenotypic plasticity of white spruce which can buffer short-term environmental changes and, thus, allow enduring the present changing climate conditions.
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Picea , Cambio Climático , Ecosistema , Bosques , Humanos , Picea/genética , ÁrbolesRESUMEN
Bisulfite sequencing is a widely used technique for determining DNA methylation and its relationship with epigenetics, genetics, and environmental parameters. Various techniques were implemented for epigenome-wide association studies (EWAS) to reveal meaningful associations; however, there are only very few plant studies available to date. Here, we developed the EpiDiverse EWAS pipeline and tested it using two plant datasets, from P. abies (Norway spruce) and Q. lobata (valley oak). Hence, we present an EWAS implementation tested for non-model plant species and describe its use.