Mar 2024, Volume 62 Issue 3
    

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  • Research Article
    Xu-Long Yang, Qing-Hui Sun, Diego F. Morales-Briones, Jacob B. Landis, Da-Juan Chen, Hong-Xin Wang, Jun Wen, Hua-Feng Wang
    2024, 62(3): 333-357. https://doi.org/10.1111/jse.13014
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    The discontinuous geographic distribution pattern of plants in the north temperate zone has been a focus of biogeographic research, especially concerning the mechanisms behind the formation of such a pattern and the spatial and temporal evolution of this intermittent distribution pattern. Hypotheses of boreotropical origin, land bridge migration, and out-of-Tibet have been proposed to explain the formation of the discontinuous distribution pattern. The distribution of Lonicera shows a typical Europe–Asia–North America discontinuous distribution, which makes for a good case study to investigate the above three hypotheses. In this study, we inferred the phylogeny based on plastid genomes and a nuclear data set with broad taxon sampling, covering 83 species representing two subgenera and four sections. Both nuclear and plastid phylogenetic analyses found section Isika polyphyletic, while sections Nintooa, Isoxylosteum, and Coelxylosteum were monophyletic in subgenus Chamaecerasus. Based on the nuclear and chloroplast phylogeny, we suggest transferring Lonicera maximowiczii and Lonicera tangutica into section Nintooa. Reconstruction of ancestral areas suggests that Lonicera originated in the Qinghai–Tibetan Plateau (QTP) and/or Asia, and subsequently dispersed to other regions. The aridification of the Asian interior may have facilitated the rapid radiation of Lonicera in the region. At the same time, the uplifts of the Tibetan Plateau appear to have triggered the spread and recent rapid diversification of the genus on the QTP and adjacent areas. Overall, our results deepen the understanding of the evolutionary diversification history of Lonicera.

  • Research Article
    Jia-Fu Chen, Yong-Chao Xu, Juan Jiang, Xiao-Min Niu, Xing-Hui Hou, Zhi-Qin Zhang, Ya-Long Guo
    2024, 62(3): 358-367. https://doi.org/10.1111/jse.13002
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    Transposable elements (TEs) are prevalent components of diverse genomes, and play an important role on the genomic stability and expression regulation of their adjacent genes. It is interesting to know the variation of TE expression and the effects of the presence/absence of TEs on gene expression after hybridization. Here we assessed the expression variation of TEs and the impacts of TEs on expression of nearby genes after hybridization based on comparisons of three pairs of reciprocal F1 hybrids and four parents in Capsella rubella. Of the 480 TE families expressed in all the four parents and six F1 hybrids, 7–23 (1.5%–4.2%) TE families were significantly differentially expressed between in silico and real F1 hybrids, indicating the expression levels of these TE families were affected during hybridization. In particular, there was a Copia TE superfamily and a non-long terminal repeat (non-LTR) TE differentially expressed between the reciprocal F1 hybrids of 879 and 86IT1, indicating maternal effects may have impacts on expression of TEs in these F1 hybrids. Besides the impacts on the expression of TE families of the hybridization, genes adjacent to polymorphic TEs tended to show a higher proportion (24.83%) of allele-specific expression (ASE) in F1 hybrids. Overall, our results highlight the impacts of hybridization on the expression level variation of TEs, and the effects of TEs on ASE after hybridization.

  • Research Article
    Jorge Cruz-Nicolás, Norberto Martínez-Méndez, Erika Aguirre-Planter, Luis E. Eguiarte, Juan P. Jaramillo-Correa
    2024, 62(3): 368-383. https://doi.org/10.1111/jse.13000
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    Interspecific trait divergence may reflect adaptation and reproductive isolation, particularly after the rapid differentiation that may follow the colonization of new environments. Although new lineages are generally expected to be morphologically and ecologically similar to their ancestors, environmental forces can also drive adaptive differentiation along specific phenotypic axes. We used climate niche models and comparative analyses based on a previously inferred phylogeny to examine the history of ecological and morphological divergence of Neotropical firs (Abies Mill., Pinaceae), a group of conifers that have recently colonized and diversified in the mountains of Mexico and northern Central America. We inferred past secondary contact zones by comparing current and past climate niche projections and looked for evidence of recent interspecific gene flow using genomic data. Neotropical firs have similar niches to each other and show a strong phylogenetic signal for most evaluated morphological traits. Analyses based on individual variables suggested a random walk model of differentiation. However, early adaptation to tropical conditions is inferred in the ancestor of the southernmost firs, as all modern southern taxa are differentiated climatically from Abies concolor, the northernmost species. In addition, observed autapomorphic traits for soil properties and the number of resin ducts in needles are consistent with possible species-specific adaptations. Thus, a combination of nonadaptive and adaptive processes along different phenotypic axes, some related to the environment, likely operated after the southward migration of this plant lineage from North America and its subsequent radiation in the Neotropics.

  • Research Article
    Xian-Lin Guo, Wei Gou, Megan Price, Qiu-Ping Jiang, Chang Peng, Song-Dong Zhou, Xing-Jin He
    2024, 62(3): 384-402. https://doi.org/10.1111/jse.12958
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    The classification of species in the genus Pterocyclus has been a topic of concern, as they were initially considered members of Pleurospermum (Apiaceae) in the Flora of China. However, the intergeneric and infrageneric classifications of Pterocyclus and its allies, such as Hymenidium and Pleurospermum, have been controversial. To address these issues, we performed phylogenetic analyses using one nuclear marker (nrITS) from 167 accessions, including 137 species (including five species of Pterocyclus), and 105 plastid genes from 82 accessions representing 82 species (including five species of Pterocyclus) of Apiaceae. We used both maximum likelihood and Bayesian approaches to deduce phylogenetic relationships of Pterocyclus and its allies. Furthermore, we conducted morphometric analyses that specifically targeted the mericarp morphology, and compared the structural differences in their plastid genomes. Based on these findings, we suggest the following revisions to the classification of Pterocyclus and its allies: (i) Pterocyclus should encompass five species (Pterocyclus angelicoides, Pterocyclus forrestii, Pterocyclus rotundatus, Pterocyclus tibeticus, and Pterocyclus wolffianus), all of which are all monophyletic and placed in the Komarovieae; (ii) Pterocyclus rivulorum shows both phylogenetic and mericarp morphological similarities to Hymenidium apiolens and Hymenidium dentatum, which belongs to the Hymenidium Clade, thus we provisionally transfer it to Hymenidium; (iii) Pleurospermum longicarpum is considered conspecific with Pterocyclus angelicoides based on morphological descriptions in the Flora Xizangica; (iv) we describe and illustrate Pterocyclus tibeticus as a new species; and (v) Pterocyclus wolffianus should be recognized as a valid species and not considered a synonym of Pterocyclus forrestii.

  • Research Article
    Yong-Xiu Song, Tian Hu, Shuai Peng, Yi-Yan Cong, Guang-Wan Hu
    2024, 62(3): 403-420. https://doi.org/10.1111/jse.12959
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    The genus Impatiens comprises more than 1000 species and displays enormous morphological diversity. As a taxon that is notoriously difficult to classify morphologically, the taxonomic significance of pollen morphology has been discussed in previous studies. However, there was only limited study on the evolution of palynological and macroscopic character in this genus before. In this paper, we observed pollen of 143 species of Impatiens, including all representatives of infrageneric groups and discussed their taxonomic value. Meanwhile, based on the reconstructed phylogenetic framework, we selected five pollen traits, and nine macroscopic traits including both vegetative and reproductive organs for evolutionary analysis. The character reconstruction showed that the morphology and number of aperture, granules in lumina, seed number of per capsule, number of sepals, lateral united petals connate, spur length, and phyllotaxy could be identified as unambiguous, while other characters were ambiguous in the last common ancestor of Impatiens. The results of comprehensively macroscopic characters and palynological evidence suggest that these traits experienced a complicated evolution, exhibit high levels of instability and variability and occur character multiple reversals in the evolutionary processes of Impatiens due to different selection pressures. In addition, we found that there is an evident mosaic evolution in this genus. Pollen and macroscopic character are conserved with a slower evolutionary rate in the I. subgen. Clavicarpa, however, these characters showed higher diversity with a rapid rate of evolution in the I. subgen. Impatiens. Furthermore, the relationship between floral morphology and pollinators was discussed.

  • Research Article
    Ivón M. Ramírez-Morillo, Laura A. Espinosa-Barrera, Carolina Granados Mendoza, Sandra I. Vera-Paz, Daniel D. Díaz Contreras Díaz, Katya J. Romero-Soler
    2024, 62(3): 421-437. https://doi.org/10.1111/jse.13004
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    Full plastomes have recently proven to be a valuable data source for resolving recalcitrant phylogenetic relationships in the flowering plant family Bromeliaceae. The study of complete plastomes has additionally led to the discovery of new structural rearrangements and advanced our understanding of bromeliad plastome diversity and evolution. Here, we focus on the study of full plastomes of the bromeliad subfamily Hechtioideae to assess phylogenetic relationships, marker informativeness, and plastome structure and evolution. Using whole-genome sequencing data, we de novo assembled and annotated new plastid genomes of 19 Hechtioideae species plus one representative each from the Pitcairnioideae and Puyoideae subfamilies and compared them with four additional available plastomes from other bromeliad subfamilies. Our phylogenetic analysis using complete plastome sequences not only recovered the three currently recognized genera of Hechtioideae as monophyletic, strongly supporting Mesoamerantha as sister of Bakerantha and Hechtia, but also improved statistical support at different phylogenetic depths within the subfamily. We identified a set of highly informative loci, some of them explored for the first time in Hechtioideae. Structural rearrangements, including expansions and contractions of the inverted repeats, large inversions, and gene loss and potential pseudogenization were detected mainly within the genus Hechtia. Evolutionary trait rate shifts were associated with the size and guanine–cytosine content of the small single copy and inverted repeats.

  • Research Article
    Zhi-Hua Zeng, Qian Yu, Qing-Hong Feng, Xin-Jia Wang, Li Zhong, Hua-Ying Sun, Hong Wang, De-Zhu Li, Spencer C.H. Barrett, Wei Zhou
    2024, 62(3): 438-448. https://doi.org/10.1111/jse.12960
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    The adaptive significance of phenotypic differences between females and males can provide insights into sex-specific selection and the evolution of sexual dimorphism. Dioecious plants commonly exhibit sexual dimorphism in height, although its ecological and evolutionary significance have rarely been examined experimentally. Here, we investigate the functional consequences of the temporal reversal of height dimorphism for pollen and seed dispersal in dioecious Rumex hastatulus Baldw., a species in which males are taller than females at flowering and the reverse pattern occurs at fruiting. Populations of this colonizing weed are wind-pollinated and seeds are wind-dispersed. In a glasshouse experiment we manipulated the height of pollen donors and using sex-specific genetic markers compared the paternal success of males of contrasting height and investigated whether seed families showed evidence of sexual dimorphism in early life-history traits. In a second glasshouse experiment using fruiting plants we also examined how female height influenced the distance that seeds were dispersed. We found that taller males had significantly higher siring success than males of equivalent height to flowering females. Similarly, taller females dispersed fruit to greater distances than shorter females. Female seeds were significantly heavier than male seeds and germinated more rapidly, although early seedling growth was greater in males. Our study suggests that the striking sex reversal of height in R. hastatulus likely functions to optimize the contrasting reproductive functions of the sexes by promoting increased pollen and seed dispersal distances. Improved dispersal quality could limit inbreeding and reduce local mate and resource competition within populations.

  • Research Article
    Xie-Ting Wu, Jun-Wu Shu, Su-Xin Yin, Eva-Maria Sadowski, Gong-Le Shi
    2024, 62(3): 449-456. https://doi.org/10.1111/jse.13001
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    Parrotia C. A. Meyer (Hamamelidaceae) is a relictual genus with only two extant species disjunctly distributed in the subtropical forests of East China and temperate forests of North Iran. Fossil records suggest that Parrotia was widespread in Europe and Asia during the Miocene, but its fossils are predominantly based on pollen and leaves. In this paper we describe the first fossil flower of Parrotia based on an exceptionally well-preserved amber inclusion from the middle Miocene of Zhangpu, Southeast China. The fossil flower was investigated with light microscope and microcomputed tomography techniques. Parrotia zhiyanii sp. nov. is a small apetalous staminate flower subtended by a pair of prominent bracts. The androecium consists of 12 stamens, and each stamen consists of a short, slender filament and a prominent, elongated anther. The anthers with short simple trichomes on the outer surface and a prominent apical connective extension are opened by longitudinal slits. Unlike its living relatives, the new Parrotia from Zhangpu grew in a Miocene seasonal tropical rainforest.

  • Research Article
    Han-Jing Liu, Ming-Hui Li, Zhen Wang, Ting Wang, Ying-Juan Su
    2024, 62(3): 457-474. https://doi.org/10.1111/jse.12999
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    Having a comprehensive understanding of genetic differentiation, responses to environmental change and demographic history is critical for genetic improvement and conservation efforts. Forest trees are an excellent resource for understanding population differentiation and adaptive genetic variation due to their ability to adapt to different climates and environments. Cephalotaxus oliveri is a relict conifer endemic to China. In this study, we generated transcriptome data and identified 17 728 high-quality single-nucleotide polymorphisms (SNPs) from 18 populations. We found significant negative correlations between expression diversity and nucleotide diversity within and among populations, suggesting that gene expression and nucleotide diversity have a reciprocal relationship when the species adapts to the environment. The analyses of population structure showed that C. oliveri displayed a striking genetic structure with four groups. BayeScEnv and RDA methods detected the signatures of local adaptation, and identified that 738 outlier SNPs were associated with precipitation, temperature and soil conditions across heterogeneous environmental conditions. Approximate Bayesian computation analyses showed that the first and second divergence occurred in the late Miocene (c. 10.075 million years ago [Ma]) and the middle Pleistocene transition (c. 0.815 Ma), respectively. Ecological niche modeling of C. oliveri revealed signs of westward expansion after the last glacial maximum, while it was predicted to experience significant range contractions in future climate change scenarios. Geographical factors and environmental factors in southern China have played a critical role in establishing the current genetic diversity and population structure of C. oliveri. This study provides an important reference for forest resource management and conservation for C. oliveri.

  • Research Article
    Eva Mikulášková, Tomáš Peterka, Jakub Šmerda, Michal Hájek
    2024, 62(3): 475-488. https://doi.org/10.1111/jse.13005
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    The recent development of genetic methods has facilitated the identification of cryptic species across different groups of organisms, including plants. However, next-generation sequencing has rarely been used to study cryptic speciation in plants, especially in bryophytes, organisms with a dominant haploid life phase. The ability to capture variation across the whole genome makes this method an effective tool for distinguishing cryptic lineages. We have focused on the genetic structure of the moss Meesia triquetra along the Alps-to-Scandinavia transect. We detected the presence of the two genetically critically different lineages of M. triquetra in Europe. These lineages overlap in both morphological characters of the gametophyte and distribution ranges. However, they considerably differ in ecological preferences to groundwater pH. While lineage 1 occupied alkaline to subneutral fens, lineage 2 occurred in fens saturated with neutral to acidic water. We consider the entities cryptic species with respect to genetic and ecological differences but the absence of morphological features necessary for determining the entities. We hypothesize that fragmentation of the ancestral population of the moss in geographically isolated refugia differing in the commonness of acidic and alkaline substrates led to consequent long-term adaptation to different environmental conditions, then drove diversification in M. triquetra.

  • Research Article
    Jian-Shuang Shen, Lan Lan, Sheng-Long Kan, He-Feng Cheng, Dan Peng, Zi-Yun Wan, Yue Hu, Xiao-Ling Huang, Xue-Qin Li, Yuan-Jun Ye, Luke R. Tembrock, Zhi-Qiang Wu, Song-Heng Jin
    2024, 62(3): 489-504. https://doi.org/10.1111/jse.13007
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    Rhododendron is the largest genus in Ericaceae and is well known for its diversity and beauty of flowers present in different species, making it a much-revered lineage of ornamental plants. Many species of Rhododendron are intolerant of high temperatures, which are becoming more common and intense in urban areas under global climate change. Therefore, the discovery and description of genes from heat-tolerant Rhododendron lineages are essential in the development of new climate-resilient cultivars. One such species known to be heat tolerant is Rhododendron × pulchrum Sweet. To better understand the genomics of heat tolerance in this species, we assembled a haplotype-resolved and chromosome-scale genome for R. × pulchrum, which had a genome size of 509 Mb; a scaffold N50 of 37 251 370 bp; and contained 35 610 genes. In addition, based on the same reannotation pipeline, we conducted pan-genomic analyses for all seven available chromosome-scale Rhododendron genomes and found 14 415 gene groups shared across all species and 18 018 gene groups distributed in the other species, including 1879 gene groups found in only a single species. Finally, we analyzed the transcriptomic data from heat-treated and non-heat-treated R. × pulchrum plants to quantify the genes that are most important during heat stress in an effort to inform the development of climate-resilient cultivars. This study provides insight into the genome diversity in Rhododendron and targets several genes related to agronomic traits that may help in further analysis.

  • Research Article
    Yong Shi, Biao-Feng Zhou, Yi-Ye Liang, Baosheng Wang
    2024, 62(3): 505-519. https://doi.org/10.1111/jse.13008
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    A fundamental question in speciation genomics is how evolutionary processes shape the genomic landscape of differentiation between species. Regions of elevated differentiation, referred to as genomic islands, could be shared among closely related species (shared islands) or specific to a lineage (lineage-specific islands). Shared islands are typically assumed to result from background selection. However, simulations and empirical studies have suggested that positive selection contributes to both shared and lineage-specific islands. Here, we utilized comparative population genomics to examine the contributions of different evolutionary processes to patterns of genetic differentiation when gene flow and incomplete lineage sorting are minimal. We used whole-genome resequencing data for 135 individuals from four oak species, including two independent species pairs, Quercus variabilis Blume and Quercus acutissima Carruth. in the subgenus Cerris, and Quercus dentata Thunb. and Quercus griffithii Hook.f. & Thomson ex Miq. in the subgenus Quercus. We found that both shared and subgenus-specific islands were caused by positive selection, including selective sweeps in current populations and in their most recent common ancestors. Moreover, the recombination rate was a better predictor of genomic differentiation than gene density. Overall, our results reveal that recombination and positive selection impacted genomic differentiation considerably and provide a more precise grasp of how genomic islands formed in Quercus.

  • Research Article
    Alexander V. Agafonov, Elena V. Shabanova, Maria V. Emtseva, Sergey V. Asbaganov, Igor V. Morozov, Alexander A. Bondar, Olga V. Dorogina
    2024, 62(3): 520-533. https://doi.org/10.1111/jse.13006
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    We represent a comparative analysis of GBSS1 gene fragment sequences for a number of species related to Elymus caninus: Elymus prokudinii, Elymus viridiglumis, Elymus goloskokovii, as well as a number of morphologically deviating biotypes, inhabiting Russia and Kazakhstan. Microevolutionary relationships between species were assessed from dendrograms derived from sequences of exons and introns. In all taxa, the St subgenome was represented by St2 variants, rather typical of the North American ancestral line of Pseudoroegneria spicata than of the Asian line descending from Pseudoroegneria strigosa. All putative relatives of E. caninus had H1 subgenome variants linked around the Asian diploid carrier of the H genome from Hordeum jubatum and were divided into two subclades. One of them (H1-1) contained most of the closely related E. caninus clones, including Elymus uralensis. Another subclade (H1-2) consisted of five variants phylogenetically related to Elymus mutabilis. We have also studied reproductive relationships between species E. goloskokovii, E. prokudinii, and E. viridiglumis and the degree of their integration into the E. caninus complex. Biotypes included in sexual hybridization formed a single recombination gene pool, within which slight differences in reproductive compatibility were observed. A comprehensive study of microevolutionary differentiation of taxa showed the expediency of taxonomic revision. The species mentioned should probably be relegated to the infraspecific rank within E. caninus s. l.

  • Research Article
    Shabir A. Rather, Josphat K. Saina, Arjun Adit, Hong-Mei Liu, Zhao-Yang Chang, Harald Schneider
    2024, 62(3): 534-547. https://doi.org/10.1111/jse.13009
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    Obtaining reliable species identification of the legume genus Caragana has been challenging. Until now, species identification was mostly carried out utilizing diagnostic morphological characteristics, in addition to some successful applications of secondary chemical compounds. This study was designed to establish a DNA barcoding protocol enabling unambiguous identification of 238 accessions belonging to 67 species of Caragana. The performance of four DNA barcoding regions nrITS, trnH-psbA, matK, and rbcL was explored using three analytical approaches, Pairwise Genetic Distance, Sequence Similarity and Phylogenetic Tree method. The chloroplast regions rbcL and matK showed lower discriminatory power compared with the nuclear region internal transcribed spacer (ITS) and the chloroplast region trnH-psbA. The nrITS outperformed the other regions in the resolution rate. The present study brings forth an efficient barcode locus for Caragana. A barcode based either on a single-locus nrITS or the combination of nrITS and trnH-psbA was found to be most suitable for species discrimination with distinctive barcoding gaps. An attempt has also been made to resolve taxonomic issues in the Caragana opulens complex. DNA barcoding tools when complemented with alpha taxonomic evidence can aid in solving complex systematic problems, especially when taxa are characterized by overlapping traits, such as species belonging to the Fabaceae family.

  • Research Article
    Wen-Juan Lan, Fang-Yuan Wang, Spencer C. H. Barrett, Wen-Ting Wang, Yue Ma, Yang Yang, Nan Li, Jun-Chen Deng, Wei-Ning Bai
    2024, 62(3): 548-560. https://doi.org/10.1111/jse.12997
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    Quantifying the relative strength of isolating barriers is a major focus of research on plant speciation. Contrasting life histories and mating systems have the potential to limit gene exchange between closely related populations growing in sympatry. However, few studies have quantified reproductive isolating barriers between conspecific annual and perennial populations and their contributions to total reproductive isolation (RI). Incarvillea sinensis Lam. (Bignoniaceae) is an insect-pollinated herb with largely allopatric annual and perennial populations that differ in mating systems. The perennial populations are primarily outcrossing whereas annual populations are predominantly selfing. At a rare sympatric site in northern China we estimated prezygotic and postzygotic barriers to gene exchange between annual and perennial plants and found complete RI between the two life histories. Annuals exhibited significantly higher ecogeographic isolation than perennials whereas perennials experienced more isolation through pollen–pistil interactions than annuals. Crosses between annuals and perennials demonstrated that postzygotic barriers influencing fruit and seed formation, F1 germination and survival were negligible for annuals but played a small role for perennials. However, F1 hybrids of crosses between annuals and perennials produced no pollen and their ovules were largely sterile. Our study provides insight into the relative importance of prezygotic and postzygotic isolating barriers between closely related annual and perennial populations of I. sinensis and some of these barriers could have been involved with speciation. Annuals and perennials of I. sinensis represent two biological species and thus deserve to be recognized as distinct taxonomic species.

  • Research Article
    Bartosz Łabiszak, Witold Wachowiak
    2024, 62(3): 561-576. https://doi.org/10.1111/jse.13013
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    Scots pine (Pinus sylvestris L.) is one of the most important tree species of the temperate and boreal zones in Eurasia. Its wide distribution range and current patterns of genetic variation have been influenced by Quaternary climatic oscillations and the demographic processes connected to them. In order to better understand the relationship between evolutionary history and demographic factors in a widespread species with a large genome, we used the single-nucleotide polymorphism (SNP) array to genotype thousands of SNP markers across 62 natural populations (N = 686 trees) of Scots pine in Eurasia. This provides the largest range-wide SNPs' genetic diversity assessment of Scots pine to date. Our findings show evidence of past admixture events between genetic clusters that were retained despite the potential for effective pollen-mediated gene flow across the species' distribution range. We also examined the contemporary population structure of the species and analyzed the range-wide genetic diversity patterns. Phylogenetic analyses and demographic modeling suggest that the observed divergence patterns between genetic lineages likely predate the last glaciation events. Two of the most distinctive groups are represented by trees from the eastern parts of Fennoscandia and Eastern Russia, which have remained separated since the mid-Pleistocene. The patterns of genetic variation also confirm the dual colonization of Fennoscandia and the existence of an admixture zone in Central Europe that was formed during multiple waves of postglacial recolonization. This study provides insights into the genetic relationships of Scots pine populations from Europe and Asia and offers a more comprehensive understanding of the species' history.