Divergence and reticulation in the Mexican white oaks: ecological and phylogenomic evidence on species limits and phylogenetic networks in the Quercus laeta complex (Fagaceae).

BACKGROUND AND AIMS: Introgressive hybridization poses a challenge to taxonomic and phylogenetic understanding of taxa, particularly when there are high numbers of co-occurring, intercrossable species. The genus Quercus exemplifies this situation. Oaks are highly diverse in sympatry and cross freely, creating syngameons of interfertile species. Although a well-resolved, dated phylogeny is available for the American oak clade, evolutionary relationships within many of the more recently derived clades remain to be defined, particularly for the young and exceptionally diverse Mexican white oak clade. Here, we adopted an approach bridging micro- and macroevolutionary scales to resolve evolutionary relationships in a rapidly diversifying clade endemic to Mexico. METHODS: Ecological data and sequences of 155 low-copy nuclear genes were used to identify distinct lineages within the Quercus laeta complex. Concatenated and coalescent approaches were used to assess the phylogenetic placement of these lineages relative to the Mexican white oak clade. Phylogenetic network methods were applied to evaluate the timing and genomic significance of recent or historical introgression among lineages. KEY RESULTS: The Q. laeta complex comprises six well-supported lineages, each restricted geographically and with mostly divergent climatic niches. Species trees corroborated that the different lineages are more closely related to other species of Mexican white oaks than to each other, suggesting that this complex is polyphyletic. Phylogenetic networks estimated events of ancient introgression that involved the ancestors of three present-day Q. laeta lineages. CONCLUSIONS: The Q. laeta complex is a morphologically and ecologically related group of species rather than a clade. Currently, oak phylogenetics is at a turning point, at which it is necessary to integrate phylogenetics and ecology in broad regional samples to figure out species boundaries. Our study illuminates one of the more complicated of the Mexican white oak groups and lays groundwork for further taxonomic study.

Ancient tree genomes for old questions.

Most foundational work on the evolution and migration of plant species relies on genomic data from contemporary samples. Ancient plant samples can give us access to allele sequences and distributions on the landscape dating back to the mid Holocene or earlier (Gugerli et al., 2005). Nuclear DNA from ancient wood, however, has been mostly inaccessible until now. In a From the Cover article in this issue of Molecular Ecology, Wagner et al. (2023) present the first resequenced nuclear genomes from ancient oak wood, including two samples dated to the 15th century and one that dates to more than 3500 years ago. These ancient tree genomes open the possibility for investigating species adaptation, migration, divergence, and hybridisation in the deep past. They pave the way for what we hope will be a new era in the use of paleogenomics to study Holocene tree histories.

Echoes of ancient introgression punctuate stable genomic lineages in the evolution of figs.

Studies investigating the evolution of flowering plants have long focused on isolating mechanisms such as pollinator specificity. Some recent studies have proposed a role for introgressive hybridization between species, recognizing that isolating processes such as pollinator specialization may not be complete barriers to hybridization. Occasional hybridization may therefore lead to distinct yet reproductively connected lineages. We investigate the balance between introgression and reproductive isolation in a diverse clade using a densely sampled phylogenomic study of fig trees (Ficus, Moraceae). Codiversification with specialized pollinating wasps (Agaonidae) is recognized as a major engine of fig diversity, leading to about 850 species. Nevertheless, some studies have focused on the importance of hybridization in Ficus, highlighting the consequences of pollinator sharing. Here, we employ dense taxon sampling (520 species) throughout Moraceae and 1,751 loci to investigate phylogenetic relationships and the prevalence of introgression among species throughout the history of Ficus. We present a well-resolved phylogenomic backbone for Ficus, providing a solid foundation for an updated classification. Our results paint a picture of phylogenetically stable evolution within lineages punctuated by occasional local introgression events likely mediated by local pollinator sharing, illustrated by clear cases of cytoplasmic introgression that have been nearly drowned out of the nuclear genome through subsequent lineage fidelity. The phylogenetic history of figs thus highlights that while hybridization is an important process in plant evolution, the mere ability of species to hybridize locally does not necessarily translate into ongoing introgression between distant lineages, particularly in the presence of obligate plant-pollinator relationships.

Genomic hotspots of chromosome rearrangements explain conserved synteny despite high rates of chromosome evolution in a holocentric lineage.

Holocentric organisms, unlike typical monocentric organisms, have kinetochore activity distributed along almost the whole length of the chromosome. Because of this, chromosome rearrangements through fission and fusion are more likely to become fixed in holocentric species, which may account for the extraordinary rates of chromosome evolution that many holocentric lineages exhibit. Long blocks of genome synteny have been reported in animals with holocentric chromosomes despite high rates of chromosome rearrangements. Nothing is known from plants, however, despite the fact that holocentricity appears to have played a key role in the diversification of one of the largest angiosperm genera, Carex (Cyperaceae). In the current study, we compared genomes of Carex species and a distantly related Cyperaceae species to characterize conserved and rearranged genome regions. Our analyses span divergence times ranging between 2 and 50 million years. We also compared a C. scoparia chromosome-level genome assembly with a linkage map of the same species to study rearrangements at a population level and suppression of recombination patterns. We found longer genome synteny blocks than expected under a null model of random rearrangement breakpoints, even between very distantly related species. We also found repetitive DNA to be non-randomly associated with holocentromeres and rearranged regions of the genome. The evidence of conserved synteny in sedges despite high rates of chromosome fission and fusion suggests that conserved genomic hotspots of chromosome evolution related to repetitive DNA shape the evolution of recombination, gene order and crossability in sedges. This finding may help explain why sedges are able to maintain species cohesion even in the face of high interspecific chromosome rearrangements.

Drought response strategies are coupled with leaf habit in 35 evergreen and deciduous oak (Quercus) species across a climatic gradient in the Americas.

Distinct survival strategies can result from trade-offs in plant function under contrasting environments. Investment in drought resistance mechanisms can enhance survivorship but result in conservative growth. We tested the hypothesis that the widespread oaks (Quercus spp.) of the Americas exhibit an interspecific trade-off between drought resistance and growth capacity. Using experimental water treatments, we isolated adaptive trait associations among species in relation to their broad climates of origin and tested for correlated evolution between plant functional responses to water availability and habitat. Across all lineages, oaks displayed plastic drought responses - typically acclimating through osmolyte accumulation in leaves and/or employing conservative growth. Oaks from xeric climates had higher osmolytes and reduced stomatal pore area index, which allows for moderated gas exchange and limits tissue loss. Patterns suggest drought resistance strategies are convergent and under strong adaptive pressure. Leaf habit, however, mediates the growth and drought resistance strategies of oaks. Deciduous species, and evergreen species from xeric climates, have increased drought tolerance through osmoregulation, which allows for continuous, conservative growth. Evergreen mesic species show limited drought resistance but could enhance growth under well-watered conditions. Consequently, evergreen species from mesic environments are especially vulnerable to chronic drought and climate change.

Evolutionary history shapes grassland productivity through opposing effects on complementarity and selection.

Phylogenetic diversity (PD), the evolutionary history of the organisms comprising a community, is increasingly recognized as an important driver of ecosystem function. However, biodiversity-ecosystem function experiments have rarely included PD as an a priori treatment. Thus, PD's effects in existing experiments are often confounded by covarying differences in species richness and functional trait diversity (FD). Here we report an experimental demonstration of strong PD effects on grassland primary productivity that are independent of FD, which was separately manipulated, and species richness, which was planted uniformly high to mimic diverse natural grasslands. Partitioning diversity effects demonstrated that higher PD increased complementarity (niche partitioning and/or facilitation) but lowered selection effects (probability of sampling highly productive species). Specifically, for every 5% increase in PD, complementarity increased by 26% on average (±8% SE), while selection effects decreased more modestly (8 ± 16%). PD also shaped productivity through clade-level effects on functional traits, that is, trait values associated with particular plant families. This clade effect was most pronounced in the Asteraceae (sunflower family), which, in tallgrass prairies, generally comprises tall, high-biomass species with low phylogenetic distinctiveness. FD also reduced selection effects but did not alter complementarity. Our results show that PD, independent of richness and FD, mediates ecosystem function through contrasting effects on complementarity and selection. This adds to growing evidence that consideration of phylogenetic dimensions of biodiversity can advance ecological understanding and inform conservation and restoration.

Niche evolution in a northern temperate tree lineage: biogeographical legacies in cork oaks (Quercus section Cerris).

BACKGROUND AND AIMS: Cork oaks (Quercus section Cerris) comprise 15 extant species in Eurasia. Despite being a small clade, they display a range of leaf morphologies comparable to the largest sections (>100 spp.) in Quercus. Their fossil record extends back to the Eocene. Here, we explore how cork oaks achieved their modern ranges and how legacy effects might explain niche evolution in modern species of section Cerris and its sister section Ilex, the holly oaks. METHODS: We inferred a dated phylogeny for cork and holly oaks using a reduced-representation next-generation sequencing method, restriction site-associated DNA sequencing (RAD-seq), and used D-statistics to investigate gene flow hypotheses. We estimated divergence times using a fossilized birth-death model calibrated with 47 fossils. We used Köppen profiles, selected bioclimatic parameters and forest biomes occupied by modern species to infer ancestral climatic and biotic niches. KEY RESULTS: East Asian and Western Eurasian cork oaks diverged initially in the Eocene. Subsequently, four Western Eurasian lineages (subsections) differentiated during the Oligocene and Miocene. Evolution of leaf size, form and texture was correlated, in part, with multiple transitions from ancestral humid temperate climates to mediterranean, arid and continental climates. Distantly related but ecologically similar species converged on similar leaf traits in the process. CONCLUSIONS: Originating in temperate (frost-free) biomes, Eocene to Oligocene ranges of the primarily deciduous cork oaks were restricted to higher latitudes (Siberia to north of Paratethys). Members of the evergreen holly oaks (section Ilex) also originated in temperate biomes but migrated southwards and south-westwards into then-(sub)tropical southern China and south-eastern Tibet during the Eocene, then westwards along existing pre-Himalayan mountain ranges. Divergent biogeographical histories and deep-time phylogenetic legacies (in cold and drought tolerance, nutrient storage and fire resistance) thus account for the modern species mosaic of Western Eurasian oak communities, which are composed of oaks belonging to four sections.

Improving species delimitation for effective conservation: a case study in the endemic maple-leaf oak (Quercus acerifolia).

Species delimitation is challenging in lineages that exhibit both high plasticity and introgression. This challenge can be compounded by collection biases, which may downweight specimens morphologically intermediate between traditional species. Additionally, mismatch between named species and observable phenotypes can compromise species conservation. We studied the species boundaries of Quercus acerifolia, a tree endemic to Arkansas, U.S. We performed morphometric analyses of leaves and acorns from 527 field and 138 herbarium samples of Q. acerifolia and its close relatives, Q. shumardii and Q. rubra. We employed two novel approaches: sampling ex situ collections to detect phenotypic plasticity caused by environmental variation and comparing random field samples with historical herbarium samples to identify collection biases that might undermine species delimitation. To provide genetic evidence, we also performed molecular analyses on genome-wide SNPs. Quercus acerifolia shows distinctive morphological, ecological, and genomic characteristics, rejecting the hypothesis that Q. acerifolia is a phenotypic variant of Q. shumardii. We found mismatches between traditional taxonomy and phenotypic clusters. We detected underrepresentation of morphological intermediates in herbarium collections, which may bias species discovery and recognition. Rare species conservation requires considering and addressing taxonomic problems related to phenotypic plasticity, mismatch between taxonomy and morphological clusters, and collection biases.

Tree species and genetic diversity increase productivity via functional diversity and trophic feedbacks.

Addressing global biodiversity loss requires an expanded focus on multiple dimensions of biodiversity. While most studies have focused on the consequences of plant interspecific diversity, our mechanistic understanding of how genetic diversity within plant species affects plant productivity remains limited. Here, we use a tree species × genetic diversity experiment to disentangle the effects of species diversity and genetic diversity on tree productivity, and how they are related to tree functional diversity and trophic feedbacks. We found that tree species diversity increased tree productivity via increased tree functional diversity, reduced soil fungal diversity, and marginally reduced herbivory. The effects of tree genetic diversity on productivity via functional diversity and soil fungal diversity were negative in monocultures but positive in the mixture of the four tree species tested. Given the complexity of interactions between species and genetic diversity, tree functional diversity and trophic feedbacks on productivity, we suggest that both tree species and genetic diversity should be considered in afforestation.

Biodiversity, the richness of species in a given ecosystem, is essential for maintaining ecological functions. This is supported by many long-term biodiversity experiments where researchers manipulated the numbers of tree species they planted in a forest and then evaluated both its productivity (how much biological material the forest produced in a given timeframe) and the health of its trees. This work contributed to our understanding of forest ecology and paved the way for better reforestation approaches. The most important observation was that diverse forests, which contain several tree species, are more productive and healthier than monocultures where a single tree species dominates. However, it remained unclear what the role of genetic diversity within individual tree species is in determining productivity and health of forests. Tang, Zhang et al. set out to improve on previous studies on tree genetic diversity and community productivity by looking at two possible mechanisms that might affect the productivity of a forest ecosystem using publicly available data. First, they looked at the diversity of traits found within a tree population, which determines what resources in the ecosystem the trees can exploit; for example, trees with varied specific leaf areas (that is the ratio between a leaf's area and its dry mass) have more access to different intensities of sunlight for photosynthesis, allowing the whole forest to gain more biomass. Second, they considered interactions with other organisms such as herbivore animals and soil fungi that affect tree growth by either consuming their leaves or competing for the same resources. Tang, Zhang et al. used a mathematical model to interpret a complex dataset that includes multiple parameters for each of four types of forest: a forest with a single tree species seeded from a single parent tree (which will have low species and genetic diversity), a forest with a single tree species seeded from several parent trees (low species diversity and high genetic diversity, due to the diversity of parents), a forest with four tree species each seeded from a single parent tree (high species diversity and low genetic diversity), and a forest with four tree species each seeded from several parent trees (high species and genetic diversity). Using their model, Tang, Zhang et al. determined that species diversity promotes productivity because the increased diversity of traits allows trees to exploit more of the surrounding resources. Genetic diversity, on the other hand, did not seem to have a direct effect on overall productivity. However, greater genetic diversity did coincide with an increase in the diversity of traits in forests with a single tree species, which led to a decrease in damage to tree leaves by herbivores. This suggests that high genetic diversity in species-rich forests is likely also beneficial as herbivores are less able to damage tree foliage. As expected, in single-species forests with both low and high genetic diversity, higher soil fungi diversity was associated with a loss in productivity. Interestingly, in forests that had high species and genetic diversity, this effect was reversed, and higher genetic diversity reduced the loss of productivity caused by soil fungi, resulting in higher productivity overall. These results should be considered in reforestation projects to promote genetic diversity of trees on top of species diversity when replanting. How genetic diversity leads to downstream mechanisms that benefit community productivity is not fully understood and future research could look at what specific genetic features matter most to help select the ideal mixture of trees to maximize productivity and increase the land's ecological and economic value.

A snapshot of progenitor-derivative speciation in Iberodes (Boraginaceae).

Traditional classification of speciation modes has focused on physical barriers to gene flow. Allopatric speciation with complete reproductive isolation is viewed as the most common mechanism of speciation. Parapatry and sympatry, by contrast, entail speciation in the face of ongoing gene flow, making them more difficult to detect. The genus Iberodes (Boraginaceae, NW Europe) comprises five species with contrasting morphological traits, habitats and species distributions. Based on the predominance of narrow and geographically distant endemic species, we hypothesized that geographical barriers were responsible for most speciation events in Iberodes. We undertook an integrative study including: (i) phylogenomics through restriction-site-associated DNA sequencing (RAD-seq), (ii) genetic structure analyses, (iii) demographic modelling, (iv) morphometrics, and (v) climatic niche modelling and niche overlap analysis. The results revealed a history of recurrent progenitor-derivative speciation manifested by a paraphyletic pattern of nested species differentiation. Budding speciation mediated by ecological differentiation is suggested for the coastal lineage, deriving from the inland widespread Iberodes linifolia during the Late Pliocene. Meanwhile, geographical isolation followed by niche shifts are suggested for the more recent differentiation of the coastland taxa. Our work provides a model for distinguishing speciation via ecological differentiation of peripheral, narrowly endemic I. kuzinskyanae and I. littoralis from a widespread extant ancestor, I. linifolia. Ultimately, our results illustrate a case of Pliocene speciation in the probable absence of geographical barriers and get away from the traditional cladistic perspective of speciation as producing two species from an extinct ancestor, thus reminding us that phylogenetic trees tell only part of the story.

Phylogenetic distance and resource availability mediate direction and strength of plant interactions in a competition experiment.

Phylogenetic ecology uses evolutionary history to improve understanding of plant interactions. Phylogenetic distance can mediate plant interactions such as competition (e.g., via limiting similarity) and facilitation (e.g., via niche complementarity), influencing community assembly patterns. Previous research has found evidence both for and against a relationship between phylogenetic distance and the strength of plant interactions, and has found that other factors, such as trait differences, may be more influential. In addition to phylogenetic distance and species' traits, environmental conditions can also influence competition, with facilitative interactions-particularly among distantly related species-potentially becoming more pronounced under stressful, resource-limited conditions. We tested the prediction that greater phylogenetic distance is associated with decreased competition in a greenhouse experiment using plant species of the North American tallgrass prairie. We calculated the Relative Interaction Index for 81 species pairs using plant height, leaf length, and biomass as indicators of performance. We found that phylogenetic distance alone did not significantly affect competition. However, the interaction between phylogenetic distance and stressful conditions (sandier soils with low nutrient availability and water retention vs. resource-rich potting soil) altered plant traits and competition. Under stressful conditions, more distantly related species competed more strongly, leading to smaller plants. Conversely, under benign conditions more distantly related species pairs competed less and were larger. These results were contrary to our expectations that distant relatives would compete less under stressful conditions. Our experiment provides evidence that, while relatedness alone may not drive competition, phylogenetic distance can nonetheless be influential through interactions with environmental conditions.

Leaf shape and size variation in bur oaks: an empirical study and simulation of sampling strategies.

PREMISE: Leaf shape and size figure strongly in plants' adaptation to their environments. Among trees, oaks are notoriously variable in leaf morphology. Our study examines the degree to which within-tree, among-tree, and among-site variation contribute to latitudinal variation in leaf shape and size of bur oak (Quercus macrocarpa: Fagaceae), one of North America's most geographically widespread oak species. METHODS: Samples were collected from four sites each at northern, central, and southern latitudes of the bur oak range. Ten leaf size traits were measured, and variance in these traits and eight ratios based on these traits was partitioned into tree and population components. Population means were regressed on latitude. We then parameterized a series of leaf collection simulations using empirical covariance among leaves on trees and trees at sites. We used the simulations to assess the efficiency of different collecting strategies for estimating among-population differences in leaf shape and size. RESULTS: Leaf size was highly responsive to latitude. Site contributed more than tree to total variation in leaf shape and size. Simulations suggest that power to detect among-site variance in leaf shape and size increases with either more leaves per tree (10-11 leaves from each of 5 trees) or more trees per site (5 leaves from each of 10+ trees). CONCLUSIONS: Our study demonstrates the utility of simulating sampling and controlling for variance in sampling for leaf morphology, whether the questions being addressed are ecological, evolutionary, or taxonomic. Simulation code is provided as an R package (traitsPopSim) to help researchers plan morphological sampling strategies.

Application of remote sensing technology to estimate productivity and assess phylogenetic heritability.

PREMISE: Measuring plant productivity is critical to understanding complex community interactions. Many traditional methods for estimating productivity, such as direct measurements of biomass and cover, are resource intensive, and remote sensing techniques are emerging as viable alternatives. METHODS: We explore drone-based remote sensing tools to estimate productivity in a tallgrass prairie restoration experiment and evaluate their ability to predict direct measures of productivity. We apply these various productivity measures to trace the evolution of plant productivity and the traits underlying it. RESULTS: The correlation between remote sensing data and direct measurements of productivity varies depending on vegetation diversity, but the volume of vegetation estimated from drone-based photogrammetry is among the best predictors of biomass and cover regardless of community composition. The commonly used normalized difference vegetation index (NDVI) is a less accurate predictor of biomass and cover than other equally accessible vegetation indices. We found that the traits most strongly correlated with productivity have lower phylogenetic signal, reflecting the fact that high productivity is convergent across the phylogeny of prairie species. This history of trait convergence connects phylogenetic diversity to plant community assembly and succession. DISCUSSION: Our study demonstrates (1) the importance of considering phylogenetic diversity when setting management goals in a threatened North American grassland ecosystem and (2) the utility of remote sensing as a complement to ground measurements of grassland productivity for both applied and fundamental questions.

Climate and phylogenetic history structure morphological and architectural trait variation among fine-root orders.

Fine roots mediate below-ground resource acquisition, yet understanding of how fine-root functional traits vary along environmental gradients, within branching orders and across phylogenetic scales remains limited. Morphological and architectural fine-root traits were measured on individual root orders of 20 oak species (genus Quercus) from divergent climates of origin that were harvested after three growing seasons in a glasshouse. These were then compared with similar measurements obtained from a phylogenetically diverse dataset of woody species from the Fine-Root Ecology Database (FRED). For the oaks, only precipitation seasonality and growing season moisture availability were correlated to aspects of root diameter and branching. Strong correlations among root diameters and architecture of different branch orders were common, while correlations between diameter and length were weakly negative. By contrast, the FRED dataset showed strong positive correlations between diameter and length and fewer correlations between root diameter and architectural traits. Our findings suggest that seasonal patterns of water availability are more important drivers of root adaptation in oaks than annual averages in precipitation and temperature. Furthermore, contrasting patterns of trait relationships between the oak and FRED datasets suggest that branching patterns are differentially constrained at narrow vs broad phylogenetic scales.

Biogeography and phylogeny of masting: do global patterns fit functional hypotheses?

Interannual variability of seed crops (CVp) has profound consequences for plant populations and food webs, where high CVp is termed 'masting'. Here we ask: is global variation in CVp better predicted by plant or habitat differences consistent with adaptive economies of scale, in which flower and seed benefits increase disproportionately during mast years; or by passive mechanisms, in which seed production responds to variation in resource availability associated with climate variability? To address this question, we compiled a dataset for phylogenetic comparative analysis of long-term fruit/seed production for plants comprising 920 time series spanning 311 plant species. Factors associated with both adaptive benefits of CVp (wind pollination and seed dispersal) and climatic variability (variability of summer precipitation) were among the best predictors of global variation in CVp. We observed a hump-shaped relationship between CVp and latitude and intermediate phylogenetic and geographic signals in CVp. CVp is patterned nonrandomly across the globe and over the plant tree of life, where high CVp is associated with species benefiting from economies of scale of seed or flower production and with species that experience variable rainfall over summer months when seeds usually mature.

Taxonomic similarity does not predict necessary sample size for ex situ conservation: a comparison among five genera.

Effectively conserving biodiversity with limited resources requires scientifically informed and efficient strategies. Guidance is particularly needed on how many living plants are necessary to conserve a threshold level of genetic diversity in ex situ collections. We investigated this question for 11 taxa across five genera. In this first study analysing and optimizing ex situ genetic diversity across multiple genera, we found that the percentage of extant genetic diversity currently conserved varies among taxa from 40% to 95%. Most taxa are well below genetic conservation targets. Resampling datasets showed that ideal collection sizes vary widely even within a genus: one taxon typically required at least 50% more individuals than another (though Quercus was an exception). Still, across taxa, the minimum collection size to achieve genetic conservation goals is within one order of magnitude. Current collections are also suboptimal: they could remain the same size yet capture twice the genetic diversity with an improved sampling design. We term this deficiency the 'genetic conservation gap'. Lastly, we show that minimum collection sizes are influenced by collection priorities regarding the genetic diversity target. In summary, current collections are insufficient (not reaching targets) and suboptimal (not efficiently designed), and we show how improvements can be made.

Genomic landscape of the global oak phylogeny.

The tree of life is highly reticulate, with the history of population divergence emerging from populations of gene phylogenies that reflect histories of introgression, lineage sorting and divergence. In this study, we investigate global patterns of oak diversity and test the hypothesis that there are regions of the oak genome that are broadly informative about phylogeny. We utilize fossil data and restriction-site associated DNA sequencing (RAD-seq) for 632 individuals representing nearly 250 Quercus species to infer a time-calibrated phylogeny of the world's oaks. We use a reversible-jump Markov chain Monte Carlo method to reconstruct shifts in lineage diversification rates, accounting for among-clade sampling biases. We then map the > 20 000 RAD-seq loci back to an annotated oak genome and investigate genomic distribution of introgression and phylogenetic support across the phylogeny. Oak lineages have diversified among geographic regions, followed by ecological divergence within regions, in the Americas and Eurasia. Roughly 60% of oak diversity traces back to four clades that experienced increases in net diversification, probably in response to climatic transitions or ecological opportunity. The strong support for the phylogeny contrasts with high genomic heterogeneity in phylogenetic signal and introgression. Oaks are phylogenomic mosaics, and their diversity may in fact depend on the gene flow that shapes the oak genome.

Uncovering the genomic signature of ancient introgression between white oak lineages (Quercus).

Botanists have long recognised interspecific gene flow as a common occurrence within white oaks (Quercus section Quercus). Historical allele exchange, however, has not been fully characterised and the complex genomic signals resulting from the combination of vertical and horizontal gene transmission may confound phylogenetic inference and obscure our ability to accurately infer the deep evolutionary history of oaks. Using anchored enrichment, we obtained a phylogenomic dataset consisting of hundreds of single-copy nuclear loci. Concatenation, species-tree and network analyses were carried out in an attempt to uncover the genomic signal of ancient introgression and infer the divergent phylogenetic topology for the white oak clade. Locus and site-level likelihood comparisons were then conducted to further explore the introgressed signal within our dataset. Historical, intersectional gene flow is suggested to have occurred between an ancestor of the Eurasian Roburoid lineage and Quercus pontica and North American Dumosae and Prinoideae lineages. Despite extensive time past, our approach proved successful in detecting the genomic signature of ancient introgression. Our results, however, highlight the importance of sampling and the use of a plurality of analytical tools and methods to sufficiently explore genomic datasets, uncover this signal, and accurately infer evolutionary history.

Oaks: an evolutionary success story.

The genus Quercus is among the most widespread and species-rich tree genera in the northern hemisphere. The extraordinary species diversity in America and Asia together with the continuous continental distribution of a limited number of European species raise questions about how macro- and microevolutionary processes made the genus Quercus an evolutionary success. Synthesizing conclusions reached during the past three decades by complementary approaches in phylogenetics, phylogeography, genomics, ecology, paleobotany, population biology and quantitative genetics, this review aims to illuminate evolutionary processes leading to the radiation and expansion of oaks. From opposing scales of time and geography, we converge on four overarching explanations of evolutionary success in oaks: accumulation of large reservoirs of diversity within populations and species; ability for rapid migration contributing to ecological priority effects on lineage diversification; high rates of evolutionary divergence within clades combined with convergent solutions to ecological problems across clades; and propensity for hybridization, contributing to adaptive introgression and facilitating migration. Finally, we explore potential future research avenues, emphasizing the integration of microevolutionary and macroevolutionary perspectives.