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.

Aspidistradaibuensis var. longkiauensis, a new variety of Aspidistra (Asparagaceae) from Taiwan, identified through morphological and genetic analyses.

Aspidistra Ker Gawl. is one of the the most diverse and fastest-growing genera of angiosperm. Most Aspidistra species have been discovered in a limited area or a single site through morphological comparison. Because of the lack of population studies, morphological variation within species and the boundaries of some species remain unclear. In recent years, combining genetic and morphological markers has become a powerful approach for species delimitation. In this study, we performed population sampling and integrated morphometrics and microsatellite genetic diversity analyses to determine the species diversity of Aspidistra in Taiwan. We identified three species, namely Aspidistraattenuata Hayata; A.daibuensisHayatavar.daibuensis; A.mushaensisHayatavar.mushaensis; and reduced A.longiconnectiva C.T.Lu, K.C.Chuang & J.C.Wang to the variety level, and described a new variety, A.daibuensisHayatavar.longkiauensis. The description, diagnosis, distribution, and photographs of this new variety as well as a key to the known Taiwanese Aspidistra are provided.

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.

Local adaptation and migratory habits balance spatial-genetic structure between continental and insular chestnut tiger butterflies in East Asia.

Geographic and climatic differences between islands and continents may affect the evolution of their biota, and promote divergent selection in species distributed in both landscapes. To assess spatial-genetic structure, we genotyped 18 expressed sequence tag-simple sequence repeat (EST-SSR) loci and sequenced two mtDNA markers (ND5 and COI) and one nuclear marker (EF1α) in two subspecies of the butterfly Parantica sita. Compared with nuclear markers, mtDNA had a stronger signal of population structure. Approximate Bayesian computation (ABC) suggested that a continuous-gene-flow model best described the data. According to this model, the two subspecies diverged approximately 23.1 kya, with 10 times more introgression from the continental (ssp. sita) to the insular subspecies (ssp. niphonica) than vice versa. Ecological niche modelling was performed to predict the paleo- and current potential distributions and elucidate the geohistorical process, which revealed a northeastern, insular origin. Winter precipitation and annual temperature range were the main determinants of the subspecies distributions. Maximum-likelihood population-effects models showed that the population differentiation of the insular and continental subspecies was primarily affected by environmental resistance and local climate. Sex-biased migration capacity and long-term precipitation-driven divergence between the continental and insular lineages shaped the current genetic structure of P. sita. Evidence from the nuclear markers confirmed intersubspecific gene flow despite adaptive divergence between the subspecies. These results imply that the continental subspecies is still capable of returning to the island and introgressing with the insular subspecies.

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.].

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.

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.

Niche partitioning among three snail-eating snakes revealed by dentition asymmetry and prey specialisation.

The level of dentition asymmetry in snail-eating snakes may reflect their prey choice and feeding efficiency on asymmetric land snails. The three species of Pareas snakes (Squamata: Pareidae) in Taiwan, which form partially sympatric distribution on the island, provide a potential case to test the hypothesis of niche partitioning and character displacement with regard to dentition asymmetry and specialisation in feeding behaviour. In this study, behavioural experiments confirmed that P. formosensis feeds exclusively on slugs, whereas P. atayal and P. komaii consumed both. However, P. atayal more efficiently preys on land snails than P. komaii, exhibiting a shorter handling time and fewer mandibular retractions. Micro-CT and ancestral character reconstruction demonstrated the lowest asymmetry in P. formosensis (the slug specialist), the highest dentition asymmetry in P. atayal (the land snail specialist) and flexibility in P. komaii (the niche switcher): increased dentition asymmetry when sympatrically distributed with the slug eater (character displacement), and decreased asymmetry when living alone (ecological niche release). Ecological niche modelling showed that the distribution of P. formosensis is associated with the presence of slugs, while that of P. atayal could be explained by the land snails. Combining the results from morphology, phylogeny, behavioural experiments and ecological niche modelling, we showed that competition in the sympatric region might have facilitated character displacement among congeners, while the absence of competition in allopatric region has led to ecological niche release.

Isolation-by-environment as a driver of genetic differentiation among populations of the only broad-leaved evergreen shrub Ammopiptanthus mongolicus in Asian temperate deserts.

Whether the effect of migration-selection-drift equilibrium on population structure is governed by spatial or environmental differences is usually elucidated by isolation-by-distance (IBD), isolation-by-environment (IBE), and isolation-by-resistance (IBR) tests. The population structure of Ammopiptanthus mongolicus, a broad-leaved evergreen psammophyte in eastern Central Asia, was previously thought to follow an isolation by distance pattern. However, recent studies have emphasized the effects of environmental factors on its growth and distribution, suggesting an important influence of local adaptation on the genetic structure of the species. Using inter-simple sequence repeat (ISSR) markers, we verified the previously inferred low intra-population variation and high inter-population differentiation. However, in contrast to previous studies, the results of partial Mantel tests and a maximum likelihood population effects mixed model (MLPE) suggested that local climate differences, rather than geographic distances or resistance distances, are the main factor affecting population differentiation. Further analysis with removal of multicollinear climatic variables and univariate MLPE found that summer and winter precipitation were crucial for shaping the current population genetic structure. Since local precipitation is related to the regeneration, colonization, and overwintering survival of A. mongolicus, its influence on demographic change may explain its effect on the population genetic structure. In addition, precipitation is related to terrain despite westward decreases, which explains the independence of genetic difference and geographic distance. The identified role of IBE suggests that collecting germplasm resources from genetically differentiated populations could be a more effective strategy to preserve the overall genetic diversity of the species than the establishment of corridors to enhance gene flow among populations.

Differential genetic responses to the stress revealed the mutation-order adaptive divergence between two sympatric ginger species.

BACKGROUND: Divergent genetic responses to the same environmental pressures may lead sympatric ecological speciation possible. Such speciation process possibly explains rapid sympatric speciation of island species. Two island endemic ginger species Zingiber kawagoii and Z. shuanglongensis was suggested to be independently originated from inland ancestors, but their island endemism and similar morphologies and habitats lead another hypothesis of in situ ecological speciation. For understanding when and how these two species diverged, intraspecific variation was estimated from three chloroplast DNA fragments (cpDNA) and interspecific genome-wide SNPs and expression differences after saline treatment were examined by transcriptomic analyses. RESULTS: Extremely low intraspecific genetic variation was estimated by cpDNA sequences in both species: nucleotide diversity π = 0.00002 in Z. kawagoii and no nucleotide substitution but only indels found in Z. shuanglongensis. Nonsignificant inter-population genetic differentiation suggests homogenized genetic variation within species. Based on 53,683 SNPs from 13,842 polymorphic transcripts, in which 10,693 SNPs are fixed between species, Z. kawagoii and Z. shuanglongensis were estimated to be diverged since 218~ 238 thousand generations ago (complete divergence since 41.5~ 43.5 thousand generations ago). This time is more recent than the time of Taiwan Island formation. In addition, high proportion of differential expression genes (DEGs) is non-polymorphic or non-positively selected, suggesting key roles of plastic genetic divergence in broaden the selectability in incipient speciation. While some positive selected DEGs were mainly the biotic and abiotic stress-resistance genes, emphasizing the importance of adaptive divergence of stress-related genes in sympatric ecological speciation. Furthermore, the higher proportional expression of functional classes in Z. kawagoii than in Z. shuanglongensis explains the more widespread distribution of Z. kawagoii in Taiwan. CONCLUSIONS: Our results contradict the previous hypothesis of independent origination of these two island endemic ginger species from SE China and SW China. Adaptive divergent responses to the stress explain how these gingers maintain genetic differentiation in sympatry. However, the recent speciation and rapid expansion make extremely low intraspecific genetic variation in these two species. This study arise a more probable speciation hypothesis of sympatric speciation within an island via the mutation-order mechanism underlying the same environmental pressure.