A complex interplay of genetic introgression and local adaptation during the evolutionary history of three closely related spruce species

doi:10.1016/j.pld.2025.04.007

Plant Diversity ›› 2025, Vol. 47 ›› Issue (04): 620-632.DOI: 10.1016/j.pld.2025.04.007

• Articles • Previous Articles Next Articles

A complex interplay of genetic introgression and local adaptation during the evolutionary history of three closely related spruce species

Shuo Feng (封烁)^a, Haixia Ma (马海霞)^a, Yu Yin (殷钰)^a, Wei Wan (万薇)^a, Kangshan Mao (毛康珊)^b, Dafu Ru (汝大福)^c

a. State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining 810016, China;
b. Key Laboratory of Bio-Resources and Eco-Environment of Ministry of Education, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu 610065, China;
c. State Key Laboratory of Herbage Improvement and Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou 730000, China

Received:2024-11-30 Revised:2025-04-23 Online:2025-08-13 Published:2025-08-13
Contact: Shuo Feng (封烁),E-mail:fengshuo8894@126.com;Dafu Ru (汝大福),E-mail:rudf@lzu.edu.cn
Supported by:
This work was supported by the Project of Qinghai provincial central government guides local funds for science and technology development (2024ZY005).

A complex interplay of genetic introgression and local adaptation during the evolutionary history of three closely related spruce species

Shuo Feng (封烁)^a, Haixia Ma (马海霞)^a, Yu Yin (殷钰)^a, Wei Wan (万薇)^a, Kangshan Mao (毛康珊)^b, Dafu Ru (汝大福)^c

a. State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining 810016, China;
b. Key Laboratory of Bio-Resources and Eco-Environment of Ministry of Education, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu 610065, China;
c. State Key Laboratory of Herbage Improvement and Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou 730000, China

通讯作者: Shuo Feng (封烁),E-mail:fengshuo8894@126.com;Dafu Ru (汝大福),E-mail:rudf@lzu.edu.cn
基金资助:
This work was supported by the Project of Qinghai provincial central government guides local funds for science and technology development (2024ZY005).

Abstract

Abstract: As climate change triggers unprecedented ecological shifts, it becomes imperative to understand the genetic underpinnings of species’ adaptability. Adaptive introgression significantly contributes to organismal adaptation to new environments by introducing genetic variation across species boundaries. However, despite growing recognition of its importance, the extent to which adaptive introgression has shaped the evolutionary history of closely related species remains poorly understood. Here we employed population genetic analyses of high-throughput sequencing data to investigate the interplay between genetic introgression and local adaptation in three species of spruce trees in the genus Picea (P. asperata, P. crassifolia, and P. meyeri). We find distinct genetic differentiation among these species, despite a substantial gene flow. Crucially, we find bidirectional adaptive introgression between allopatrically distributed species pairs and unearthed dozens of genes linked to stress resilience and flowering time. These candidate genes most likely have promoted adaptability of these spruces to historical environmental changes and may enhance their survival and resilience to future climate changes. Our findings highlight that adaptive introgression could be prevalent and bidirectional in a topographically complex area, and this could have contributed to rich genetic variation and diverse habitat usage by tree species.

Key words: Adaptation, Introgression, Picea, Population transcriptome

摘要： As climate change triggers unprecedented ecological shifts, it becomes imperative to understand the genetic underpinnings of species’ adaptability. Adaptive introgression significantly contributes to organismal adaptation to new environments by introducing genetic variation across species boundaries. However, despite growing recognition of its importance, the extent to which adaptive introgression has shaped the evolutionary history of closely related species remains poorly understood. Here we employed population genetic analyses of high-throughput sequencing data to investigate the interplay between genetic introgression and local adaptation in three species of spruce trees in the genus Picea (P. asperata, P. crassifolia, and P. meyeri). We find distinct genetic differentiation among these species, despite a substantial gene flow. Crucially, we find bidirectional adaptive introgression between allopatrically distributed species pairs and unearthed dozens of genes linked to stress resilience and flowering time. These candidate genes most likely have promoted adaptability of these spruces to historical environmental changes and may enhance their survival and resilience to future climate changes. Our findings highlight that adaptive introgression could be prevalent and bidirectional in a topographically complex area, and this could have contributed to rich genetic variation and diverse habitat usage by tree species.

关键词: Adaptation, Introgression, Picea, Population transcriptome

Shuo Feng (封烁), Haixia Ma (马海霞), Yu Yin (殷钰), Wei Wan (万薇), Kangshan Mao (毛康珊), Dafu Ru (汝大福). A complex interplay of genetic introgression and local adaptation during the evolutionary history of three closely related spruce species[J]. Plant Diversity, 2025, 47(04): 620-632.

References

Abdirad, S., Wu, Y.Q., Ghorbanzadeh, Z., et al., 2022. Proteomic analysis of the meristematic root zone in contrasting genotypes reveals new insights in drought tolerance in rice. Proteomics 22, e2200100.
Aguillon, S.M., Dodge, T.O., Preising, G.A., et al., 2022. Introgression. Curr. Biol. 32, R865-R868.
Alexander, D.H., Novembre, J., Lange, K., 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655-1664.
Amraee, L., Rahmani, F., 2020. Modified CTAB protocol for RNA extraction from Lemon balm (Melissa officinalis L.). Acta Agric. Slov. 115, 53-57.
Barton, N.H., 2001. Speciation. Trends Ecol. Evol. 16, 325.
Bi, H., Yue, W., Wang, X., et al., 2016. Pleistocene climate change promoted divergence between Picea asperata and P. crassifolia on the Qinghai-Tibet Plateau through recent bottlenecks. Ecol. Evol. 6, 4435-4444.
Bouille, M., Bousquet, J., 2005. Trans-species shared polymorphisms at orthologous nuclear gene loci among distant species in the conifer Picea (Pinaceae):implications for the long-term maintenance of genetic diversity in trees. Am. J. Bot. 92, 63-73.
Brancourt-Hulmel, M., 2000, Selecting the right varieties for the environment and taking account of genotype/environment interactions. Ocl-Ol. Corps Gras Li. 7, 504-511.
Brunton, A.J., Farleigh, K., Ogbourne, S.M., et al., 2024. The geno-geo-climate nexus:contributions of geographic and ecological factors in shaping the genomic divergence of two closely related threatened rainforest species of Fontainea Heckel (Euphorbiaceae). Landscape Ecol. 39, 11.
Buchfink, B., Xie, C., Huson, D.H., 2015. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59-60.
Cantalapiedra, C.P., Hernandez-Plaza, A., Letunic, I., et al., 2021. EggNOG-mapper v2:functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol. Biol. Evol. 38, 5825-5829.
Chen, C.J., Chen, H., Zhang, Y., et al., 2020. TBtools:an integrative toolkit developed for interactive analyses of big biological data. Mol. Plant 13, 1194-1202.
Chen, N.B., Cai, Y.D., Chen, Q.M., et al., 2018a. Whole-genome resequencing reveals world-wide ancestry and adaptive introgression events of domesticated cattle in East Asia. Nat. Commun. 9, 2337.
Chen, S.F., Zhou, Y.Q., Chen, Y.R., et al., 2018b. fastp:an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, 884-890.
Cingolani, P., Platts, A., Wang, L.L., et al., 2012. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly 6, 80-92.
Cote, I.M., Darling, E.S., 2010. Rethinking ecosystem resilience in the face of climate change. PLoS Biology 8, e1000438.
Danecek, P., Auton, A., Abecasis, G., et al., 2011. The variant call format and VCFtools. Bioinformatics 27, 2156-2158.
De Lafontaine, G., Prunier, J., Gerardi, S., et al., 2015. Tracking the progression of speciation:variable patterns of introgression across the genome provide insights on the species delimitation between progenitor-derivative spruces (Picea mariana×P. rubens). Mol. Ecol. 24, 5229-5247.
Delhomme, N., Sundstrom, G., Zamani, N., et al., 2015. Serendipitous meta-transcriptomics:the fungal community of Norway spruce (Picea abies). PLoS One 10, e0139080.
DePristo, M.A., Banks, E., Poplin, R., et al., 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491.
Dixon, P., 2003. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927-930.
Dormann, C.F., Elith, J., Bacher, S., et al., 2013. Collinearity:a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 27-46.
Duan, B.L., Lu, Y.W., Yin, C.Y., et al., 2005. Physiological responses to drought and shade in two contrasting Picea asperata populations. Physiol. Plantarum 124, 476-484.
Duan, B.L., Yang, Y.Q., Lu, Y.W., et al., 2007. Interactions between water deficit, ABA, and provenances in Picea asperata. J. Exp. Bot. 58, 3025-3036.
Durand, E.Y., Patterson, N., Reich, D., et al., 2011. Testing for ancient admixture between closely related populations. Mol. Bio. Evol. 28, 2239-2252.
Edelman, N.B., Frandsen, P.B., Miyagi, M., et al., 2019. Genomic architecture and introgression shape a butterfly radiation. Science 366, 594.
Edmands, S., 2007. Between a rock and a hard place:evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol. Ecol. 16, 463-475.
Excoffier, L., Lischer, H.E., 2010. Arlequin suite ver 3.5:a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564-567.
Feng, S., Ru, D.F., Sun, Y.S., et al., 2019. Trans-lineage polymorphism and nonbifurcating diversification of the genus Picea. New Phytol. 222, 576-587.
Feng, S., Xi, E.R., Wan, W., et al., 2023a. Genomic signals of local adaptation in Picea crassifolia. BMC Plant Biol. 23, 534.
Feng, S., Wan, W., Li, Y., et al., 2023b. Transcriptome-based analyses of adaptive divergence between two closely related spruce species on the Qinghai-Tibet plateau and adjacent regions. Mol. Ecol. 32, 476-491.
Flanagan, S.P., Forester, B.R., Latch, E.K., et al., 2018. Guidelines for planning genomic assessment and monitoring of locally adaptive variation to inform species conservation. Evol. Appl. 11, 1035-1052.
Flores, A., Rodriguez, E.B., Ojeda, T.P., et al., 2023. Genetic conservation and use of genetic resources of 18 Mexican pine species. Diversity 15, 735.
Forester, B.R., Lasky, J.R., Wagner, H.H., et al., 2018. Comparing methods for detecting multivariate adaptation with multivariate genotype-environment associations. Mol. Ecol. 27, 2215-2233.
Freitas, S., Gazda, M.A., Rebelo, M.A., et al., 2021. Pervasive hybridization with local wild relatives in Western European grapevine varieties. Sci. Adv. 7, eabi8584.
Fu, R.R., Zhu, Y.X., Liu, Y., et al., 2022. Genome-wide analyses of introgression between two sympatric Asian oak species. Nat. Ecol. Evol. 6, 924-935.
Fu, R.R., Zhu, Y.X., Liu, Y., et al., 2024. Shared xerophytic genes and their re-use in local adaptation to aridity in the desert plant Gymnocarpos przewalskii. Mol. Ecol. 33, e17380.
Gagalova, K.K., Warren, R.L., Coombe, L., et al., 2022. Spruce giga-genomes:structurally similar yet distinctive with differentially expanding gene families and rapidly evolving genes. Plant J. 111, 1469-1485.
Gao, Y.D., Harris, A.J., Li, H.C., et al., 2020. Hybrid speciation and introgression both underlie the genetic structures and evolutionary relationships of three morphologically distinct species of Lilium (Liliaceae) forming a hybrid zone along an elevational gradient. Front. Plant Sci. 11, 576407.
Genner, M.J., Turner, G.F., 2012. Ancient hybridization and phenotypic novelty within lake Malawi's cichlid fish radiation. Mol. Bio. Evol. 29, 195-206.
Gerardi, S., Jaramillo-Correa, J.P., Beaulieu, J., et al., 2010. From glacial refugia to modern populations:new assemblages of organelle genomes generated by differential cytoplasmic gene flow in transcontinental black spruce. Mol. Ecol. 19, 5265-5280.
Gilbert-Norton, L., Wilson, R., Stevens, J.R., et al., 2010. A meta-analytic review of corridor effectiveness. Conserv Biol. 24, 660-668.
Goyal, K., Walton, L.J., Tunnacliffe, A., 2005. LEA proteins prevent protein aggregation due to water stress. Biochem. J. 388, 151-157.
Green, R.E., Krause, J., Briggs, A.W., et al., 2010. A draft sequence of the Neandertal genome. Science 328, 710-722.
Gregory, S.D., Ancrenaz, M., Brook, B.W., et al., 2014. Forecasts of habitat suitability improve habitat corridor efficacy in rapidly changing environments. Divers. Distrib. 20, 1044-1057.
Gugger, P.F., Sugita, S., Cavender-Bares, J., 2010. Phylogeography of Douglas-fir based on mitochondrial and chloroplast DNA sequences:testing hypotheses from the fossil record. Mol. Ecol. 19, 1877-1897.
Harrison, R.G., Larson, E.L., 2014. Hybridization, introgression, and the nature of species boundaries. J. Hered. 105, 795-809.
Hamilton, K.L., Miller, B.F., 2016. What is the evidence for stress resistance and slowed aging? Exp. Gerontol. 82, 67-72.
Hamilton, J.A., Lexer, C., Aitken, S.N., 2013. Differential introgression reveals candidate genes for selection across a spruce (Picea sitchensis×P. glauca) hybrid zone. New Phytol. 197, 927-938.
Han, Y.J., Li, S.H., Wang, J.C., et al., 2023. Responses of Picea meyeri to climatic factors revealed by tree ring isotopes and water use efficiency on Luya Mountain of North-Central China. Atmosphere 14, 615.
Hendry, A.P., Nosil, P., Rieseberg, L.H., 2007. The speed of ecological speciation. Funct. Ecol. 21, 455-464.
Hendry, A.P., Taylor, E.B., 2004. How much of the variation in adaptive divergence can be explained by gene flow? An evaluation using lake-stream stickleback pairs. Evolution 58, 2319-2331.
Hosius, B., Leinemann, L., Bergmann, F., et al., 2001. Species diversity and genetic diversity-Is there any relationship? Allg. Forst Jagdztg. 172, 87-91.
Hoskin, C.J., Higgie, M., McDonald, K.R., et al., 2005. Reinforcement drives rapid allopatric speciation. Nature 437, 1353-1356.
Ingram, J., Bartels, D., 1996. The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. Mol. Bio. 47, 377-403.
Jang, M.J., Cho, H.J., Park, Y.S., et al., 2024. Haplotype-resolved genome assembly and resequencing analysis provide insights into genome evolution and allelic imbalance in Pinus densiflora. Nat. Genet. 56, 2551-2561.
Jones, T.H., Steane, D.A., Jones, R.C., et al., 2006. Effects of domestication on genetic diversity in Eucalyptus globulus. Forest Ecol. Manag. 234, 78-84.
Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., et al., 2017. ModelFinder:fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587-589.
Kijowska-Oberc, J., Staszak, A.M., Kaminski, J., et al., 2020. Adaptation of forest trees to rapidly changing climate. Forests 11, 123.
Kim, H.S., Hwang, D.S., Lee, B.Y., et al., 2016. De novo assembly and annotation of the marine mysid (Neomysis awatschensis) transcriptome. Mar. Genom. 28, 41-43.
Kimmitt, A.A., Pegan, T.M., Jones, A.W., et al., 2023. Genetic evidence for widespread population size expansion in North American boreal birds prior to the Last Glacial Maximum. Proc. Roy. Soc. B-Biol. Sci. 290, 20221334.
Kiwuka, C., Goudsmit, E., Tournebize, R., et al., 2021. Genetic diversity of native and cultivated Ugandan Robusta coffee (Coffea canephora Pierre ex A. Froehner):Climate influences, breeding potential and diversity conservation. PLoS One 16, e0245965.
Korznikov, K., Petrenko, T., Kislov, D., et al., 2023. Predicting spruce taiga distribution in Northeast Asia using species distribution models:glacial refugia, mid-Holocene expansion and future predictions for global warming. Forests 14, 219.
Leroy, S.A.G., Arpe, K., Mikolajewicz, U., et al., 2020. Climate simulations and pollen data reveal the distribution and connectivity of temperate tree populations in eastern Asia during the Last Glacial Maximum. Clim. Past 16, 2039-2054.
Li, H., Durbin, R., 2009a. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760.
Li, H., Handsaker, B., Wysoker, A., et al., 2009b. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079.
Li, L.F., Chen, X.L., Fang, D.M., et al., 2022. Genomes shed light on the evolution of Begonia, a mega-diverse genus. New Phytol. 234, 295-310.
Li, M.Z., Tian, S.L., Jin, L., et al., 2013. Genomic analyses identify distinct patterns of selection in domesticated pigs and Tibetan wild boars. Nat. Genet. 45, 1431-1438.
Liu, Y.F., Xiao, W.F., Wang, F.D., et al., 2024. Adaptive divergence, historical population dynamics, and simulation of suitable distributions for Picea Meyeri and P. Mongolica at the whole-genome level. BMC Plant Biol. 24, 479.
Lockwood, J.D., Aleksic, J.M., Zou, J.B., et al., 2013. A new phylogeny for the genus Picea from plastid, mitochondrial, and nuclear sequences. Mol. Phylogenet. Evol. 69, 717-727.
Lu, S.M., Liu, L., Lei, W.X., et al., 2024. Cryptic divergence in and evolutionary dynamics of endangered hybrid Picea brachytyla sensu stricto in the Qinghai-Tibet Plateau. BMC Plant Biol. 24, 1202.
Ma, T., Wang, K., Hu, Q.J., et al., 2018. Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex. Proc. Natl. Acad. Sci. U.S.A. 115, E236-E243.
Ma, Y.Z., Wang, J., Hu, Q.J., et al., 2019. Ancient introgression drives adaptation to cooler and drier mountain habitats in a cypress species complex. Commun. Bio. 2, 213.
Ma, Z.H., Huang, B.L., Xu, S.S., et al., 2015. Isolation of High-Quality Total RNA from Chinese Fir (Cunninghamia lanceolata (Lamb.) Hook). PLoS One 10, e0130234.
Malinsky, M., Challis, R.J., Tyers, A.M., et al., 2015. Genomic islands of speciation separate cichlid ecomorphs in an East African crater lake. Science 350, 1493-1498.
Malinsky, M., Matschiner, M., Svardal, H., 2021. Dsuite-Fast D-statistics and related admixture evidence from VCF files. Mol. Ecol. Resour. 21, 584-595.
Mallet, J., 2005. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20, 229-237.
Martin, B.P., Brandon, C.J., Stewart, J.J.P., et al., 2015. Accuracy issues involved in modeling in vivo protein structures using PM7. Proteins 83, 1427-1435.
Martin, S.H., Dasmahapatra, K.K., Nadeau, N.J., et al., 2013. Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Res. 23, 1817-1828.
Nakayama, D., Makino, T., 2024. Convergent accelerated evolution of mammal-specific conserved non-coding elements in hibernators. Sci. Rep. 14, 11754.
Nguyen, L.T., Schmidt, H.A., Von, Haeseler, A., et al., 2015. IQ-TREE:a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268-274.
Nolan, R.H., Drew, D.W., O'Grady, A.P., et al., 2018. Safeguarding reforestation efforts against changes in climate and disturbance regimes. Forest Ecol. Manag. 424, 458-467.
Nosil, P., 2008. Ernst Mayr and the integration of geographic and ecological factors in speciation. Biol. J. Linn. Soc. 95, 26-46.
Novella, I.S., Zarate, S., Metzgar, D., et al., 2004. Positive selection of synonymous mutations in vesicular stomatitis virus. J. Mol. Biol. 342, 1415-1421.
Novikova, P.Y., Hohmann, N., Nizhynska, V., et al., 2016. Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism. Nat. Genet. 48, 1077-1082.
Numaguchi, K., Akagi, T., Kitamura, Y., et al., 2020. Interspecific introgression and natural selection in the evolution of Japanese apricot (Prunus mume). Plant J. 104, 1551-1567.
Nystedt, B., Street, N.R., Wetterbom, A., et al., 2013. The Norway spruce genome sequence and conifer genome evolution. Nature 497, 579-584.
Oberhuber, W., Thomaser, G., Mayr, S., et al., 1999. Radial growth of Norway spruce infected by Chrysomyxa rhododendri. Phyton-Ann. Rei Bot. A. 39, 147-154.
Oziolor, E.M., Reid, N.M., Yair, S., et al., 2019. Adaptive introgression enables evolutionary rescue from extreme environmental pollution. Science 364, 455-457.
Patterson, N., Moorjani, P., Luo, Y.T., et al., 2012. Ancient admixture in human history. Genetics 192, 1065-1093.
Pease, J.B., Hahn, M.W., 2015. Detection and polarization of introgression in a five-taxon phylogeny. Syst. Biol. 64, 651-662.
Petit, R.J., Hampe, A., 2006. Some evolutionary consequences of being a tree. Annu. Rev. Ecol. Evol. Syst. 37, 187-214.
Phillips, S.J., Dudik, M., 2008. Modeling of species distributions with Maxent:new extensions and a comprehensive evaluation. Ecography 31, 161-175.
Pickrell, J.K., Pritchard, J.K., 2012. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genetics 8, e1002967.
Potts, S.G., Biesmeijer, J.C., Kremen, C., et al., 2010. Global pollinator declines:trends, impacts and drivers. Trends Ecol. Evol. 25, 345-353.
Price, A.L., Patterson, N.J., Plenge, R.M., et al., 2006. Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38, 904-909.
Prunier, J., Gerardi, S., Laroche, J., et al., 2012. Parallel and lineage-specific molecular adaptation to climate in boreal black spruce. Mol. Ecol. 21, 4270-4286.
Purcell, S., Neale, B., Todd-Brown, K., et al., 2007. PLINK:a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559-575.
Racimo, F., Sankararaman, S., Nielsen, R., et al., 2015. Evidence for archaic adaptive introgression in humans. Nat. Rev. Genet. 16, 359-371.
Richards, E.J., Servedio, M.R., Martin, C.H., 2019. Searching for sympatric speciation in the genomic era. Bioessays 41, 1900047.
Rieseberg, L.H., 2001. Chromosomal rearrangements and speciation. Trends Ecol. Evol. 16, 351-358.
Ru, D.F., Mao, K.S., Zhang, L., et al., 2016. Genomic evidence for polyphyletic origins and interlineage gene flow within complex taxa:a case study of Picea brachytyla in the Qinghai-Tibet Plateau. Mol. Ecol. 25, 2373-2386.
Ru, D.F., Sun, Y.S., Wang, D.L., et al., 2018. Population genomic analysis reveals that homoploid hybrid speciation can be a lengthy process. Mol. Ecol. 27, 4875-4887.
Savolainen, O., Lascoux, M., Merila, J., 2013. Ecological genomics of local adaptation. Nat. Rev. Genet. 14, 807-820.
Savolainen, O., Pyhajarvi, T., 2007. Genomic diversity in forest trees. Curr. Opin. Plant Biol. 10, 162-167.
Sexton, J.P., Hangartner, S.B., Hoffmann, A.A., 2014. Genetic isolation by environment or distance:which pattern of gene flow is most common? Evolution 68, 1-15.
Shi, C.Y., Xie, Y.J., Guan, D.L., et al., 2024. Transcriptomic analysis reveals adaptive evolution and conservation implications for the endangered Magnolia lotungensis. Genes 15, 787.
Siitonen, P., Lehtinen, A., Siitonen, M., 2005. Effects of forest edges on the distribution, abundance, and regional persistence of wood-rotting fungi. Conserv. Biol. 19, 250-260.
Slatkin, M., Pollack, J.L., 2008. Subdivision in an ancestral species creates asymmetry in gene trees. Mol. Biol. Evol. 25, 2241-2246.
Slatkin, M., Racimo, F., 2016. Ancient DNA and human history. Proc. Natl. Acad. Sci. U.S.A. 113, 6380-6387.
Sochacki, D., Marciniak, P., Zajaczkowska, M., et al., 2024. In situ and ex situ conservation of ornamental geophytes in Poland. Sustainability 16, 5375.
Statham, M.J., Aylward, C.M., Barthman-Thompson, L., et al., 2022. Landscape genetics of an endangered salt marsh endemic:Identifying population continuity and barriers to dispersal. Conserv. Genet. 23, 759-771.
Stewart, C.N., Halfhill, M.D., Warwick, S.I., 2003. Transgene introgression from genetically modified crops to their wild relatives. Nat. Rev. Genet. 4, 806-817.
Suarez-Gonzalez, A., Hefer, C.A., Lexer, C., et al., 2018. Introgression from Populus balsamifera underlies adaptively significant variation and range boundaries in P. trichocarpa. New Phytol. 217, 416-427.
Sun, Y.S., Abbott, R.J., Li, L.L., et al., 2014. Evolutionary history of Purple cone spruce (Picea purpurea) in the Qinghai-Tibet Plateau:homoploid hybrid origin and Pleistocene expansion. Mol. Ecol. 23, 343-359.
Than, C., Ruths, D., Nakhleh, L., 2008. PhyloNet:a software package for analyzing and reconstructing reticulate evolutionary relationships. BMC Bioinformatics 9, 322.
Thibert-Plante, X., Hendry, A.P., 2011. Factors influencing progress toward sympatric speciation. J. Evolution Biol. 24, 2186-2196.
Tolleter, D., Hincha, D.K., Macherel, D., 2010. A mitochondrial late embryogenesis abundant protein stabilizes model membranes in the dry state. BBA-Biomembranes 1798, 1926-1933.
Twyford, A.D., Ennos, R.A., 2012. Next-generation sequencing as a tool for plant ecology and evolution. Plant Ecol. Divers. 5, 411-413.
Wang, B., Chen, T., Li, C.J., et al., 2020a. Radial growth of Qinghai spruce (Picea crassifolia Kom.) and its leading influencing climate factor varied along a moisture gradient. For. Ecol. Manage. 476, 118474.
Wang, D.L., Sun, Y.S., Lei, W.X., et al., 2023a. Backcrossing to different parents produced two distinct hybrid species. Heredity 131, 145-155.
Wang, G.H., Zhao, H.W., An, M., et al., 2020b. Detecting the driving forces underlying the divergence of spruce forests in China:evidence from phytocoenology, morphology and phylogenetics. J. Plant Ecol. 13, 59-69.
Wang, J.C., Ma, J.W., OuYang, F.Q., et al., 2021. Instrinsic relationship among needle morphology, anatomy, gas exchanges and tree growth across 17 Picea species. New Forest. 52, 509-535.
Wang, M.H., Wang, J.R., Zhang, X.W., et al., 2019. Phenotypic plasticity of stomatal and photosynthetic features of four Picea species in two contrasting common gardens. AoB Plants 11, plz034.
Wang, Y., Liu, K., Liao, H., et al., 2008. The plant WNK gene family and regulation of flowering time in Arabidopsis. Plant Biol. 10, 548-562.
Wang, Y., Jiang, Z.P., Qin, A.L., et al., 2023b. Population structure, genetic diversity and candidate genes for the adaptation to environmental stress in Picea koraiensis. Plants 12, 1266.
Wang, Z., Zhang, X., Lei, W., et al. 2023c, Chromosome-level genome assembly and population genomics of Robinia pseudoacacia reveal the genetic basis for its wide cultivation. Commun. Biol. 6, 797.
Whitney, K.D., Broman, K.W., Kane, N.C., et al., 2015. Quantitative trait locus mapping identifies candidate alleles involved in adaptive introgression and range expansion in a wild sunflower. Mol. Ecol. 24, 2194-2211.
Xiao, H., Liu, Z.J., Wang, N., et al., 2023. Adaptive and maladaptive introgression in grapevine domestication. Proc. Natl. Acad. Sci. U.S.A. 120, e2222041120.
Xue, F., Jiang, Y., Dong, M.Y., et al., 2022. Seasonal and daily variations in stem water relations between co-occurring Larix principis-rupprechtii and Picea meyeri at different elevations. Forest Ecol. Manag. 504, 119821.
Xue, X., Wang, Y., Korpelainen, H., 2007. Genetic diversity of Picea asperata populations based on RAPDs. Plant Biol. 9, 101-108.
Yin, D.C., Gou, X.H., Liu, J., et al., 2024. Increasing deep soil water uptake during drought does not indicate higher drought resistance. J. Hydrol. 630, 130694.
Yu, G.H., Jiang, L.L., Ma, X.F., et al., 2014. A soybean C2H2-type zinc finger gene GmZF1 enhanced cold tolerance in transgenic Arabidopsis. PLoS One 9, e109399.
Zani, D., Lischke, H., Lehsten, V., 2023. Climate and dispersal limitation drive tree species range shifts in post-glacial Europe:results from dynamic simulations. Front. Ecol. Evol. 11, 1321104.
Zhao, W., Gao, J., Hall, D., et al., 2024. Evolutionary radiation of the Eurasian Pinus species under pervasive gene flow. New Phytol. 242, 2353-2368.
Zhang, H., Feng, B., Qi, D.W., et al., 2024. Habitat status and feasibility of constructing corridors for a vulnerable population of giant pandas. Glob. Ecol. Conserv. 54, e03190.
Zhang, H.L., Sun, Z., Feng, S., et al., 2022a. The C2H2-type zinc finger protein PhZFP1 regulates cold stress tolerance by modulating galactinol synthesis in Petunia hybrida. J. Exp. Bot. 73, 6434-6448.
Zhang, H.F., Wei, C.H., Yang, X.Z., et al., 2017. Genome-wide identification and expression analysis of calcium dependent protein kinase and its related kinase gene families in melon (Cucumis melo L.). PLoS One 12, e0176352.
Zhang, J.P., Zhang, F., Tay, W.T., et al., 2022b. Population genomics provides insights into lineage divergence and local adaptation within the cotton bollworm. Mol. Ecol. Resour. 22, 1875-1891.
Zhou, Y.F., Zhang, L.R., Liu, J.Q., et al., 2014a. Climatic adaptation and ecological divergence between two closely related pine species in Southeast China. Mol. Ecol. 23, 3504-3522.
Zhou, T.H., Wu, K.X., Qian, Z.Q., et al., 2014b. Genetic diversity of the threatened Chinese endemic plant, Sinowilsonia henryi Hemsi. (Hamamelidaceae), revealed by inter-simple sequence repeat (ISSR) markers. Biochem. Syst. Ecol. 56, 171-177.
Zhu, H., Lei, W.X., Lai, Q., et al., 2024. Comparative analysis shows high level of lineage sorting in genomic regions with low recombination in the extended Picea likiangensis species complex. Plant Divers. 46, 547-550.
Zhu, J.X., Wang, S., Zhang, B.E., et al., 2021. Adapting to changing labor productivity as a result of intensified heat stress in a changing climate. GeoHealth 5, e2020GH000313.
Zou, J.B., Sun, Y.S., Li, L., et al., 2013. Population genetic evidence for speciation pattern and gene flow between Picea wilsonii, P. morrisonicola and P. neoveitchii. Ann. Bot. 112, 1829-1844.

[1]	Fangdong Geng (耿方东), Miaoqing Liu (刘苗青), Luzhen Wang (王璐珍), Xuedong Zhang (张雪栋), Jiayu Ma (马佳雨), Hang Ye (叶航), Keith Woeste, Peng Zhao (赵鹏). Genomic introgression underlies environmental adaptation in three species of Chinese wingnuts, Pterocarya [J]. Plant Diversity, 2025, 47(03): 365-381.
[2]	Javier Hernández-Velasco, José Ciro Hernández-Díaz, Sergio Leonel Simental-Rodríguez, Juan P. Jaramillo-Correa, David S. Gernandt, José Jesús Vargas-Hernández, Ilga Porth, Roos Goessen, M. Socorro González-Elizondo, Matthias Fladung, Cuauhtémoc Sáenz-Romero, José Guadalupe Martínez-Ávalos, Artemio Carrillo-Parra, Eduardo Mendoza-Maya, Arnulfo Blanco-García, Christian Wehenkel. Causes of heterozygosity excess: The case of Mexican populations of Populus tremuloides [J]. Plant Diversity, 2025, 47(03): 415-428.
[3]	Miaomiao Shi, Ping Liang, Zhonglai Luo, Yu Zhang, Shiran Gu, Xiangping Wang, Xin Qian, Shuguang Jian, Kuaifei Xia, Shijin Li, Zhongtao Zhao, Tieyao Tu, Dianxiang Zhang. Genome compaction underlies the molecular adaptation of bay cedar (Suriana maritima) to the extreme habitat on the tropical coral islands [J]. Plant Diversity, 2025, 47(02): 337-340.
[4]	Tian-Rui Wang, Xin Ning, Si-Si Zheng, Yu Li, Zi-Jia Lu, Hong-Hu Meng, Bin-Jie Ge, Gregor Kozlowski, Meng-Xiao Yan, Yi-Gang Song. Genomic insights into ecological adaptation of oaks revealed by phylogenomic analysis of multiple species [J]. Plant Diversity, 2025, 47(01): 53-67.
[5]	Miao Liu, Tiancai Zhou, Quansheng Fu. Leaf nitrogen and phosphorus are more sensitive to environmental factors in dicots than in monocots, globally [J]. Plant Diversity, 2024, 46(06): 804-811.
[6]	Xiang-Zhou Hu, Cen Guo, Sheng-Yuan Qin, De-Zhu Li, Zhen-Hua Guo. Deep genome skimming reveals the hybrid origin of Pseudosasa gracilis (Poaceae: Bambusoideae) [J]. Plant Diversity, 2024, 46(03): 344-352.
[7]	Zhen Yang, Lisong Liang, Weibo Xiang, Lujun Wang, Qinghua Ma, Zhaoshan Wang. Conservation genomics provides insights into genetic resilience and adaptation of the endangered Chinese hazelnut, Corylus chinensis [J]. Plant Diversity, 2024, 46(03): 294-308.
[8]	Hong Qian. Patterns of phylogenetic relatedness of non-native plants across the introduction-naturalization-invasion continuum in China [J]. Plant Diversity, 2023, 45(02): 169-176.
[9]	Ting-Shen Han, Zheng-Yan Hu, Zhi-Qiang Du, Quan-Jing Zheng, Jia Liu, Thomas Mitchell-Olds, Yao-Wu Xing. Adaptive responses drive the success of polyploid yellowcresses (Rorippa, Brassicaceae) in the Hengduan Mountains, a temperate biodiversity hotspot [J]. Plant Diversity, 2022, 44(05): 455-467.
[10]	Ji-Hua Wang, Yan-Fei Cai, Shi-Feng Li, Shi-Bao Zhang. Differences in leaf physiological and morphological traits between Camellia japonica and Camellia reticulata [J]. Plant Diversity, 2020, 42(03): 181-188.
[11]	Yujin Li, Qingqing Ye, De He, Huixian Bai, Jianfan Wen. The ubiquity and coexistence of two FBPases in chloroplasts of photosynthetic eukaryotes and its evolutionary and functional implications [J]. Plant Diversity, 2020, 42(02): 120-125.
[12]	Aysajan Abdusalam, Qingjun Li. Morphological plasticity and adaptation level of distylous Primula nivalis in a heterogeneous alpine environment [J]. Plant Diversity, 2018, 40(06): 284-291.
[13]	Huai Ning, Jiaojun Yu, Xun Gong. Bidirectional natural hybridization between sympatric Ligularia vellerea and L. subspicata [J]. Plant Diversity, 2017, 39(04): 214-220.
[14]	Xiong Li,§, Yunqiang Yang,§, Shihai Yang,§, Xudong Sun, Xin Yin, . Comparative proteomics analyses of intraspecific differences in the response of Stipa purpurea to drought [J]. Plant Diversity, 2016, 38(02): 124-145.
[15]	LI Xiong-, YANG Shi-Hai-, YANG Yun-Qiang-, YIN Xin-, SUN Xu-Dong-, YANG Yong-Ping. Comparative Physiological and Molecular Analyses of Intraspecific Differences of Stipa purpurea (Poaceae) Response to Drought [J]. Plant Diversity, 2015, 37(4): 439-452.

A complex interplay of genetic introgression and local adaptation during the evolutionary history of three closely related spruce species

A complex interplay of genetic introgression and local adaptation during the evolutionary history of three closely related spruce species

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 15

Recommended Articles

Metrics

Comments