Genomic insights into local adaptation and vulnerability of Quercus longinux to climate change.

BACKGROUND: Climate change is expected to alter the factors that drive changes in adaptive variation. This is especially true for species with long life spans and limited dispersal capabilities. Rapid climate changes may disrupt the migration of beneficial genetic variations, making it challenging for them to keep up with changing environments. Understanding adaptive genetic variations in tree species is crucial for conservation and effective forest management. Our study used landscape genomic analyses and phenotypic traits from a thorough sampling across the entire range of Quercus longinux, an oak species native to Taiwan, to investigate the signals of adaptation within this species. RESULTS: Using ecological data, phenotypic traits, and 1,933 single-nucleotide polymorphisms (SNPs) from 205 individuals, we classified three genetic groups, which were also phenotypically and ecologically divergent. Thirty-five genes related to drought and freeze resistance displayed signatures of natural selection. The adaptive variation was driven by diverse environmental pressures such as low spring precipitation, low annual temperature, and soil grid sizes. Using linear-regression-based methods, we identified isolation by environment (IBE) as the optimal model for adaptive SNPs. Redundancy analysis (RDA) further revealed a substantial joint influence of demography, geology, and environments, suggesting a covariation between environmental gradients and colonization history. Lastly, we utilized adaptive signals to estimate the genetic offset for each individual under diverse climate change scenarios. The required genetic changes and migration distance are larger in severe climates. Our prediction also reveals potential threats to edge populations in northern and southeastern Taiwan due to escalating temperatures and precipitation reallocation. CONCLUSIONS: We demonstrate the intricate influence of ecological heterogeneity on genetic and phenotypic adaptation of an oak species. The adaptation is also driven by some rarely studied environmental factors, including wind speed and soil features. Furthermore, the genetic offset analysis predicted that the edge populations of Q. longinux in lower elevations might face higher risks of local extinctions under climate change.

Ghost introgression facilitates genomic divergence of a sympatric cryptic lineage in Cycas revoluta.

A cryptic lineage is a genetically diverged but morphologically unrecognized variant of a known species. Clarifying cryptic lineage evolution is essential for quantifying species diversity. In sympatric cryptic lineage divergence compared with allopatric divergence, the forces of divergent selection and mating patterns override geographical isolation. Introgression, by supplying preadapted or neutral standing genetic variations, can promote sympatric cryptic lineage divergence via selection. However, most studies concentrated on extant species introgression, ignoring the genetic legacy of introgression from extinct or unsampled lineages ("ghost introgression"). Cycads are an ideal plant for studying the influence of ghost introgression because of their common interspecific gene flow and past high extinction rate. Here, we utilized reference-based ddRADseq to clarify the role of ghost introgression in the evolution of a previously identified sympatric cryptic lineage in Cycas revoluta. After re-evaluating the evolutionary independency of cryptic lineages, the group-wise diverged single-nucleotide polymorphisms among sympatric and allopatric lineages were compared and functionally annotated. Next, we employed an approximate Bayesian computation method for hypothesis testing to clarify the cryptic lineage evolution and ghost introgression effect. SNPs with the genomic signatures of ghost introgression were further annotated. Our results reconfirmed the evolutionary independency of cryptic lineage among C. revoluta and demonstrated that ghost introgression to the noncryptic lineage facilitated their divergence. Gene function related to heat stress and disease resistance implied ecological adaptation of the main extant populations of C. revoluta.

Unravelling the dynamics of soil microbial communities under the environmental selection and range shift process in afforestation ecosystems.

The process of forest range shift not only affects the vegetation aboveground but also influences the dynamics of belowground microbial communities. To investigate the changes in soil under forest range shift, we examined the natural forest soil microbiome along with its corresponding physicochemical properties, as well as the afforestation of natural forest by seedlings and sowing. By utilizing natural forests and employing different afforestation methods, we simulated the three stages of forest range shift: the staging stage, regeneration, and colonization. We employed network analysis and phylogenetic assemblages to examine the structure of soil microbial communities during these three stages in a macro-environmental change context. Ordination and regression analyses were also used to explore the correlation between microorganisms, environmental factors, and changes in their niches. The findings revealed that different afforestation (range shift) types led to distinct microbial compositions. Seedling afforestation exhibited similarities to mature forests, suggesting a significant influence on below-ground microorganisms. In contrast, sowing-based afforestation resulted in small changes in soil microbes, indicating a legacy effect on grassland soils. The impact of the rhizosphere on microbial composition remained consistent across the three forest types. Overall, this study underscores the significance of forest range shift in shaping soil microbial communities and emphasizes the need to consider these dynamics in forest management and restoration endeavours.

Turfgrass-dependent mycotrophic change enhances soil deterioration in dry, cold and high-alkali environments.

AIMS: Soil quality is undergoing severe degradation under anthropogenic effects. Different methods of land management have been implemented for soil reclamation, such as turfing. Although widely accepted to improve soil quality, turfing in specific environments may also culminate in soil deterioration. We aim to know how turfing impacts soils by changing mycobiomes. METHODS AND RESULTS: The soil physicochemical properties and ITS metabarcoding were used to investigate mycobiome diversity and eco-function differences between the eudicot Dianthus plumarius and the monocot Poa pratensis in dry, cold, and high-alkali soil. The effects of plantation and the rhizosphere (e.g. root exudates) were tested. We showed that the change in soil mycobiomes in different planted bulk soils and rhizospheres could mainly be attributed to species turnover, with minor nestedness. Unexpectedly, the soil deteriorates more following turfing. The increasing saprotrophs in planted bulk soil were more marked in the monocot than in the eudicot, even the rhizosphere effect alleviated saprotrophic risks in the rhizosphere. CONCLUSIONS: Turfing deteriorates the health of high-alkali soil by reducing nitrification, and upshift the soil saprotrophs in a dry and cold environment.

Parallel adaptation prompted core-periphery divergence of Ammopiptanthus mongolicus.

Range expansion requires peripheral populations to shift adaptive optima to breach range boundaries. Opportunities for range expansion can be assessed by investigating the associations of core-periphery environmental and genetic differences. This study investigates differences in the core-periphery adaptation of Ammopiptanthus mongolicus, a broad-leaved evergreen shrub species in a relatively homogeneous temperate Asian desert environment, to explore the environmental factors that limit the expansion of desert plants. Temperate deserts are characterized by severe drought, a large diurnal temperature range, and seasonality. Long-standing adaptation to the harsh desert environment may confine the genetic diversity of A. mongolicus, despite its distribution over a wide range of longitude, latitude, and altitude. Since range edges defined by climate niches may have different genetic responses to environmental extremes, we compared genome-wide polymorphisms between nine environmental core populations and ten fragmented peripheral populations to determine the "adaptive peripheral" populations. At least four adaptive peripheral populations had similar genetic-environmental association patterns. High elevations, summer drought, and winter cold were the three main determinants of converging these four adaptive peripheral populations. Elevation mainly caused similar local climates among different geographic regions. Altitudinal adaptation resulting from integrated environmental-genetic responses was a breakthrough in breaching niche boundaries. These peripheral populations are also located in relatively humid and warmer environments. Relaxation of the drought and cold constraints facilitated the genetic divergence of these peripheral populations from the core population's adaptive legacy. We conclude that pleiotropic selection synchronized adaptative divergence to cold and drought vs. warm and humid environments between the core and peripheral populations. Such parallel adaptation of peripheral populations relies on selection under a background of abundant new variants derived from the core population's standing genetic variation, i.e., integration of genetic surfing and local adaptation.

Divergence With Gene Flow and Contrasting Population Size Blur the Species Boundary in Cycas Sect. Asiorientales, as Inferred From Morphology and RAD-Seq Data.

The divergence process of incipient species is fascinating but elusive by incomplete lineage sorting or gene flow. Species delimitation is also challenging among those morphologically similar allopatric species, especially when lacking comprehensive data. Cycas sect. Asiorientales, comprised of C. taitungensis and C. revoluta in the Ryukyu Archipelago and Taiwan, diverged recently with continuous gene flow, resulting in a reciprocal paraphyletic relationship. Their previous evolutionary inferences are questioned from few genetic markers, incomplete sampling, and incomprehensive morphological comparison by a long-term taxonomic misconception. By whole range sampling, this study tests the geographic mode of speciation in the two species of Asiorientales by approximate Bayesian computation (ABC) using genome-wide single nucleotide polymorphisms (SNPs). The individual tree was reconstructed to delimit the species and track the gene-flow trajectory. With the comparison of diagnostic morphological traits and genetic data, the allopatric speciation was rejected. Alternatively, continuous but spatially heterogeneous gene flow driven by transoceanic vegetative dispersal and pollen flow with contrasting population sizes blurred their species boundary. On the basis of morphological, genetic, and evolutionary evidence, we synonymized these two Cycas species. This study highlights not only the importance of the Kuroshio Current to species evolution but also the disadvantage of using species with geographically structured genealogies as conservation units.

Different Roles of Introgression on the Demographic Change in Two Snakebark Maples, Acer caudatifolium and A. morrisonense, with Contrasted Postglacial Expansion Routes.

Hybridization frequently occurs in plant species. With repeated backcross, the introgression may influence evolutionary trajectories through the entry of foreign genes. However, the genetic admixture via hybridization events is often confused with the ancestral polymorphism, especially in closely related species that have experienced similar evolutionary events. In Taiwan, two independent-originated endemic snakebark maples have contrasted postglacial range expansion routes: northward and upward expansion in Acer caudatifolium and downward expansion in A. morrisonense. The range expansion causes the current parapatric distribution, increasing the possibility of introgression. This study elucidates how their genetic variation reflects introgression and historical demography. With 17 EST-SSR markers among the intensely sampled 657 individuals, we confirmed that the genetic admixture between species mainly was attributed to recent introgression instead of common ancestral polymorphism. The secondary contact scenario inferred by approximate Bayesian computation suggested that A. morrisonense received more genetic variations from A. caudatifolium. Introgression occurred in colonized Taiwan around the early Last Glacial Period. Furthermore, the demography of A. caudatifolium was more severely affected by introgression than A. morrisonense, especially in the wavefront populations with high altitude range expansion, implying an altitude-related adaptive introgression. In contrast, A. morrisonense exhibited ubiquitous introgression independent of postglacial expansion, suggesting that introgression in A. morrisonense was neutral. In terms of different genetic consequences, introgression had different demographic impacts on species with different altitude expansion directions even under the same climate-change conditions within an island.

Physicochemical and Biotic Changes and the Phylogenetic Evenness of Microbial Community in Soil Subjected to Phytoreclamation.

Phytoreclamation is the intervention of plants to improve degraded soil quality, changing soil biotic and abiotic properties. Many studies have focused on microbial composition and bioactivity, but few explored the changes in phylogenetic assemblages of soil microbiota after phytoreclamation. This study compared microbiomes of bare land to those of planted soils and investigated how the rhizosphere environment affects microbial assemblages from monocot Poa pratensis and eudicot Dianthus plumarius plantings using 16S rRNA metabarcoding. The results showed that the biotic susceptibility of soil to the rhizosphere environment was higher than that of the abiotic. A noticeable change was in some soil physicochemical properties like Na, P, Zn, Cu, C, and sand-to-silt proportion before and after phytoreclamation, but not between the rhizosphere and bulk soil of plantings. Contrastingly, microbial composition and diversity were significantly affected by both turfing and rhizosphere effects and were more susceptible to differences in turfing or not than in planting species. In the turfgrass, the microbiome differences between plants were greater in the rhizosphere than in the surrounding bulk soil, indicating the proximal influence of root exudates. We also found that the main abiotic factors that influenced microbial composition were Na, Zn, NOx, N, and S; as for the phylogenetic assemblages, were by K levels and the increase of silt. Turfgrass decomposes soil aggregates and changes the physicochemical properties, thereby evens the phylogenetic clustering of the soil microbial community. We demonstrated that the deterministic process affects the microbial assemblage and acts as a selective agent of the soil microbiota in fundamental and realized niches. Phytoreclamation may lead to abiotic soil changes that reallocate resources to microbes. This could affect the phylogeny of the microbial assemblages and increase microbial richness.

Corrigendum: Divergence with gene flow and contrasting population size blur the species boundary in Cycas Sect. Asiorientales, as inferred from morphology and RAD-seq data.

[This corrects the article DOI: 10.3389/fpls.2022.824158.].

Evolution of floral characters and biogeography of Heloniadeae (Melanthiaceae): an example of breeding system shifts with inflorescence change.

Heloniadeae (Melanthiaceae) presents an East Asia-North America disjunct distribution. Different molecular and morphological data nevertheless support the tribe as a monophyletic group. However, their phylogenetic relationships and biogeographic history, together with the character evolution, are not clear. Therefore, we constructed a Bayesian phylogenetic tree for Heloniadeae using cpDNA and inferred the historical biogeography and floral character evolution. The results revealed that Heloniadeae was distributed in high-latitudes of East Asia and North America, originating since 22.2 mya. The East Asia clade migrated into southwest China, and subsequently colonized the Korean Peninsula, Taiwan, the Ryukyus, and spread northward to Japan and southern Sakhalin. The evolution of the inflorescence and number of flowers were phylogenetically conserved, associated with the historical biogeography of Heloniadeae. The inflorescences transferred from raceme to sub-umbel, and the number of flowers decreased during the dispersal process, which may be accompanied by changes in the breeding system. Besides, the anthesis period was more affected by the habitat environment than phylogenetic constraints. The flowering temperature of was below 20 °C in most species, except H. kawanoi. Such a low temperature might not be conductive to pollinator activities, but it could be compensated by sustaining seed production with long-lasting flowers.

Environmental Heterogeneity Leads to Spatial Differences in Genetic Diversity and Demographic Structure of Acer caudatifolium.

Under climate fluctuation, species dispersal may be disturbed by terrain and local climate, resulting in uneven spatial-genetic structure. In addition, organisms at different latitudes may be differentially susceptible to climate change. Here, we tracked the seed dispersal of Acer caudatifolium using chloroplast DNA to explore the relationships of terrain and local climate heterogeneity with range shifts and demography in Taiwan. Our results showed that the extant populations have shifted upward and northward to the mountains since the Last Glacial Maximum. The distributional upshift of A. caudatifolium is in contrast to the downward expansion of its closest relative in Taiwan, A. morrisonense. The northern populations of A. caudatifolium have acquired multiple-source chlorotypes and harbor high genetic diversity. However, effective gene flow between the north and south is interrupted by topography, geographic distance, north-south differences in October rainfall, and other climate heterogeneities, blocking southward genetic rescue. In addition, winter monsoon-driven rainfall may cause regional differences in the phenological schedule, resulting in adaptive effects on the timing of range shift and the genetic draft of chlorotype distribution. Terrain, distance, and local climate also differentiate the northernmost populations from the others, supporting the previous taxonomic treatment of Acer kawakamii var. taitonmontanum as an independent variety.

Taxonomic notes on Scutellaria taipeiensis (Lamiaceae) from morphological and molecular data.

The genus Scutellaria comprises eight species distributed from 50 to 2000 m in Taiwan. Amongst them, S. barbata and S. taipeiensis are very similar on the basis of morphological and plastid DNA sequence information. Therefore, a comprehensive study of the taxonomic status of S. taipeiensis is necessary. We reviewed the herbarium sheets, related literature and protologues and compared morphologies of these two species, as well as their phylogenetic relationships. All evidence, including the diagnostic characters between S. taipeiensis and S. barbata, suggest that they belonged to a single species rather than two. As a result, S. taipeiensis is treated as a synonym of S. barbata.

Local Climate Heterogeneity Shapes Population Genetic Structure of Two Undifferentiated Insular Scutellaria Species.

Spatial climate heterogeneity may not only affect adaptive gene frequencies but could also indirectly shape the genetic structure of neutral loci by impacting demographic dynamics. In this study, the effect of local climate on population genetic variation was tested in two phylogenetically close Scutellaria species in Taiwan. Scutellaria taipeiensis, which was originally assumed to be an endemic species of Taiwan Island, is shown to be part of the widespread species S. barbata based on the overlapping ranges of genetic variation and climatic niches as well as their morphological similarity. Rejection of the scenario of "early divergence with secondary contact" and the support for multiple origins of populations of S. taipeiensis from S. barbata provide strong evolutionary evidence for a taxonomic revision of the species combination. Further tests of a climatic effect on genetic variation were conducted. Regression analyses show nonlinear correlations among any pair of geographic, climatic, and genetic distances. However, significantly, the bioclimatic variables that represent the precipitation from late summer to early autumn explain roughly 13% of the genetic variation of our sampled populations. These results indicate that spatial differences of precipitation in the typhoon season may influence the regeneration rate and colonization rate of local populations. The periodic typhoon episodes explain the significant but nonlinear influence of climatic variables on population genetic differentiation. Although, the climatic difference does not lead to species divergence, the local climate variability indeed impacts the spatial genetic distribution at the population level.