Abstract
Maintenance of standing genetic diversity and effective population size (Ne) in trees is essential for sustainability, adaptation, and evolution, especially for dioecious tree species under changed climatic conditions. We examined the gene pool of Taxus baccata along latitudinal gradients in the Hyrcanian forest from west to east using 15 simple sequence repeat markers (SSR). A high level of genetic diversity and a significant level of fixation index was observed, and the populations showed spatial genetic structure. The fixation index ranged from 0.027 to 0.197. In six out of eleven populations inbreeding was the significant factor influencing deviation from the Hardy–Weinberg equilibrium. There was no bottleneck effect in any of the analysed populations and the global Fst with ENA correction was 0.044. The average total number of migrants per generation ranged from 4.93 to 2.14. Under the six tested scenarios, the DIYABC analysis showed that the eastern and western parts of the Hyrcanian yew forests split about 134 generations ago but these two pools meet in the central part of these forests about 49 generations ago. Although the genetic diversity of T. baccata in the Hyrcanian forest is relatively high, it is expected that the inbreeding depression will increase over time, causing the accumulation of destructive alleles and intensifying the extinction process. This process is caused by anthropogenic activities, habitat fragmentations, the age of the trees, low regenerations, the existence of high geographical barriers, and a significant reduction in gene flow among the habitats.
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References
Ahmadi K, Alavi SJ, Amiri GZ, Hosseini SM, Serra-Diaz JM, Svenning JC (2020a) The potential impact of future climate on the distribution of European yew (Taxus baccata L.) in the Hyrcanian Forest region (Iran). Int J Biometeorol 649(64):1451–1462. https://doi.org/10.1007/S00484-020-01922-Z
Ahmadi K, Jalil Alavi S, Zahedi Amiri G, Hosseini SM, Serra-Diaz JM, Svenning JC (2020b) Patterns of density and structure of natural populations of Taxus baccata in the Hyrcanian forests of Iran. Nord J Bot 38:njb02598. https://doi.org/10.1111/njb.02598
Akhani H, Djamali M, Ghorbanalizadeh A, Ramezani E (2010) Plant biodiversity of Hyrcanian relict forests, N Iran: an overview of the flora, vegetation, palaeoecology and conservation. Pak J Bot 42:231–258
Bassam BJ, Caetano-Anollés G, Gresshoff PM (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem 196:80–83. https://doi.org/10.1016/0003-2697(91)90120-I
Benham SE, Houston Durrant T, Caudullo G, de Rigo D (2016) Taxus baccata in Europe: distribution, habitat, usage and threats. Eur atlas For tree species e015921
Browicz K (1989) Chorology of the Euxinian and Hyrcanian element in the woody flora of Asia. Plant Syst Evol 162:305–314. https://doi.org/10.1007/BF00936923/METRICS
Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631. https://doi.org/10.1093/molbev/msl191
Cheng BB, Zheng YQ, Sun QW (2015) Genetic diversity and population structure of Taxus cuspidata in the Changbai Mountains assessed by chloroplast DNA sequences and microsatellite markers. Biochem Syst Ecol 63:157–164. https://doi.org/10.1016/j.bse.2015.10.009
Chybicki IJ, Oleksa A, Burczyk J (2011) Increased inbreeding and strong kinship structure in Taxus baccata estimated from both AFLP and SSR data. Heredity 107:589–600. https://doi.org/10.1038/hdy.2011.51
Cornuet J-M, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, Marin J-M, Estoup A (2014) DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30:1187–1189. https://doi.org/10.1093/bioinformatics/btt763
Delahunty JL (2007) The ethnobotanical history and holocene extent of yew (Taxus baccata L.) on the Irish landscape. J Ethnobiol 27:204–217. https://doi.org/10.2993/0278-0771(2007)27[204:TEHAHE]2.0.CO;2
Dhar A, Ruprecht H, Vacik H (2008) Population viability risk management (PVRM) for in situ management of endangered tree species—a case study on a Taxus baccata L. population. For Ecol Manag 255:2835–2845. https://doi.org/10.1016/j.foreco.2008.01.059
Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci 91:3166–3170. https://doi.org/10.1073/PNAS.91.8.3166
Dubreuil M, Sebastiani F, Mayol M, González-Martínez SC, Riba M, Vendramin GG (2008) Isolation and characterization of polymorphic nuclear microsatellite loci in Taxus baccata L. Conserv Genet 9:1665–1668. https://doi.org/10.1007/s10592-008-9515-3
Dubreuil M, Riba M, González-Martínez SC, Vendramin GG, Sebastiani F, Mayol M (2010) Genetic effects of chronic habitat fragmentation revisited: strong genetic structure in a temperate tree, Taxus baccata (Taxaceae), with great dispersal capability. Am J Bot 97:303–310. https://doi.org/10.3732/ajb.0900148
Dumolin S, Demesure B, Petit RJ (1995) Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method. Theoret Appl Genet 91:1253–1256. https://doi.org/10.1007/BF00220937
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
El-Kassaby YA, Yanchuk AD (1994) Genetic diversity, differentiation, and inbreeding in Pacific Yew from British Columbia. J Hered 85:112–117. https://doi.org/10.1093/oxfordjournals.jhered.a111407
Esmailzadeh O, Hosseini SM (2007) A phytosociological study of English Yew (Taxus Baccata L.) In Afratakhteh reserve. Pajouhesh Sazandegi 20:17–24
Esmailzadeh O, Soofi M (2022) Syntaxonomy and gradient analysis of common yew ( Taxus baccata L.) communities in eastern Hyrcanian forests, northern Iran. Ecol Res 37:325–343. https://doi.org/10.1111/1440-1703.12291
Esmailzadeh O, Hosseini SM, Asadi H, Ghadiripour P, Ahmadi A (2012) Plant biodiversity in relation to physiographical factors in Afratakhteh Yew (Taxus baccata L.) Habitat, NE Iran. Iranian J Plant Biol 4:1–12
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Garbarino M, Weisberg PJ, Bagnara L, Urbinati C (2015) Sex-related spatial segregation along environmental gradients in the dioecious conifer, Taxus baccata. For Ecol Manag 358:122–129. https://doi.org/10.1016/J.FORECO.2015.09.009
Gargiulo R, Saubin M, Rizzuto G, West B, Fay MF, Kallow S, Trivedi C (2019) Genetic diversity in British populations of Taxus baccata L.: is the seedbank collection representative of the genetic variation in the wild? Biol Conserv 233:289–297. https://doi.org/10.1016/j.biocon.2019.01.014
Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318. https://doi.org/10.1046/j.1365-294x.2001.01190.x
Gholizadeh H, Naqinezhad A, Chytrý M (2020) Classification of the Hyrcanian forest vegetation, Northern Iran. Appl Veg Sci 23:107–126. https://doi.org/10.1111/AVSC.12469
Gholizadeh H, Friedman MS, McMillan NA, Hammond WM, Hassani K, Sams AV, Charles MD, Garrett DR, Joshi O, Hamilton RG, Fuhlendorf SD, Trowbridge AM, Adams H (2022) Mapping invasive alien species in grassland ecosystems using airborne imaging spectroscopy and remotely observable vegetation functional traits. Remote Sens Environ 271:112887. https://doi.org/10.1016/j.rse.2022.112887
González-Martínez SC, Dubreuil M, Riba M, Vendramin GG, Sebastiani F, Mayol M (2010) Spatial genetic structure of Taxus baccata L. in the western Mediterranean Basin: past and present limits to gene movement over a broad geographic scale. Mol Phylogenet Evol 55:805–815. https://doi.org/10.1016/j.ympev.2010.03.001
Goudet J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html
Hamrigk JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc B 351:1291–1298. https://doi.org/10.1098/rstb.1996.0112
Hensen I, Cierjacks A, Hirsch H et al (2012) Historic and recent fragmentation coupled with altitude affect the genetic population structure of one of the world’s highest tropical tree line species. Glob Ecol Biogeogr 21:455–464. https://doi.org/10.1111/j.1466-8238.2011.00691.x
Hosseinzadeh S, Esmailzadeh O (2017) Floristic study of Buxus hyrcana stands in the Western forests of Haraz District, Amol. Iran J Appl Ecol 6:1–13. https://doi.org/10.18869/acadpub.ijae.6.1.1
Iszkuło G, Jasińska AK, Giertych MJ, Boratyński A (2009) Do secondary sexual dimorphism and female intolerance to drought influence the sex ratio and extinction risk of Taxus baccata? Plant Ecol 200:229–240. https://doi.org/10.1007/s11258-008-9447-5
Iszkuło G, Kosiński P, Hajnos M (2013) Sex influences the taxanes content in Taxus baccata. Acta Physiol Plant 35:147–152. https://doi.org/10.1007/s11738-012-1057-0
Jalili A, Jamzad Z (1999) Red data book of plant species of Iran
Karami-Kordalivand P, Esmailzadeh O, Willner W, Noroozi J, Alavi SJ (2021) Classification of forest communities (co-)dominated by Taxus baccata in the Hyrcanian forests (northern Iran) and their comparison with southern Europe. Eur J For Res 1402(140):463–476. https://doi.org/10.1007/S10342-020-01343-Y
Koç DE, Svenning JC, Avcı M (2018) Climate change impacts on the potential distribution of Taxus baccata L. in the Eastern Mediterranean and the Bolkar Mountains (Turkey) from last glacial maximum to the future. Euras J For Sci 6:69–82. https://doi.org/10.31195/ejejfs.435962
Komárková M, Novotný P, Cvrčková H, Máchová P (2022) The genetic differences and structure of selected important populations of the endangered Taxus baccata in the Czech Republic. Forests 13:137. https://doi.org/10.3390/f13020137
Kýpeťová M, Walas Ł, Jaloviar P, Iszkuło G (2018) Influence of herbivory pressure on the growth rate and needle morphology of Taxus baccata L. juveniles. Dendrobiology 79:10–19. https://doi.org/10.12657/denbio.079.002
Litkowiec M, Plitta-michalak BP, Lewandowski A (2015) Homogenous genetic structure in populations of Taxus baccata with varied proportions of male and female individuals. Silva Fennica 49:1–14
Litkowiec M, Lewandowski A, Wachowiak W (2018) Genetic variation in Taxus baccata L.: a case study supporting Poland’s protection and restoration program. For Ecol Manag 409:148–160. https://doi.org/10.1016/j.foreco.2017.11.026
Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247. https://doi.org/10.1093/JHERED/89.3.238
Mahmoodi P, Khayam Nekouei SM, Mardi M, Pirseyedi SM, Ghaffari MR, Ramroodi M, Siahsar BA (2010) Isolation and characterization of new microsatellite marker in Taxus baccata L. Conserv Genet Resour 2:195–199. https://doi.org/10.1007/s12686-009-9133-5
Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190. https://doi.org/10.1353/hub.2004.0034
Maroso F, Vera M, Ferreiro J, Mayol M, Riba M, Ramil-Rego P, Martínez P, Bouza C (2021) Genetic diversity and structure of Taxus baccata from the Cantabrian-Atlantic area in northern Spain: a guide for conservation and management actions. For Ecol Manag 482:118844. https://doi.org/10.1016/J.FORECO.2020.118844
Mayol M, Riba M, González-Martínez SC, Bagnoli F, de Beaulieu JL, Berganzo E, Burgarella C, Dubreuil M, Krajmerová D, Paule L, Romšáková I, Vettori C, Vincenot L, Vendramin GG (2015) Adapting through glacial cycles: insights from a long-lived tree (Taxus baccata). New Phytol 208:973–986. https://doi.org/10.1111/nph.13496
Merril CR, Goldman D, Sedman SA, Ebert MH (1981) Ultrasensitive stain for proteins in polyacrylamide gels shows regional variation in cerebrospinal fluid proteins. Science 212:1437–1438. https://doi.org/10.1126/science.6162199
Myking T, Vakkari P, Skrøppa T (2009) Genetic variation in northern marginal Taxus baccata L. populations. Implications for conservation. Forestry 82:529–539. https://doi.org/10.1093/forestry/cpp022
Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155. https://doi.org/10.1111/j.1365-294X.2004.02141.x
Ohsawa T, Ide Y (2008) Global patterns of genetic variation in plant species along vertical and horizontal gradients on mountains. Glob Ecol Biogeogr 17:152–163. https://doi.org/10.1111/j.1466-8238.2007.00357.x
Ohsawa T, Tsuda Y, Saito Y, Sawada H, Ide Y (2007) Altitudinal genetic diversity and differentiation of Quercus crispula in the Chichibu Mountains, central Japan. Int J Plant Sci 168:333–340. https://doi.org/10.1086/510413
Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population*. Genet Res 22:201–204. https://doi.org/10.1017/S0016672300012994
Olsson S, Pinosio S, González-Martínez SC, Abascal F, Mayol M, Grivet D, Vendramin GG (2018) De novo assembly of English yew (Taxus baccata) transcriptome and its applications for intra- and inter-specific analyses. Plant Mol Biol 97:337–345. https://doi.org/10.1007/s11103-018-0742-9
Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420. https://doi.org/10.1093/bioinformatics/btp696
Peakall ER, Smouse PE (2006) genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
Piovesan G, Saba EP, Biondi F, Alessandrini A, Di Filippo A, Schirone B (2009) Population ecology of yew (Taxus baccata L.) in the central Apennines: spatial patterns and their relevance for conservation strategies. Plant Ecol 205:23–46. https://doi.org/10.1007/s11258-009-9596-1
Piry S, Luikart G, Cornuet JM (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered 90:502–503. https://doi.org/10.1093/JHERED/90.4.502
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1093/genetics/155.2.945
Rannala B, Zhu T, Yang Z (2012) Tail Paradox, partial identifiability, and influential priors in Bayesian branch length inference. Mol Biol Evol 29:325–335. https://doi.org/10.1093/molbev/msr210
Rivers M (2019) European red list of trees. Eur Red List Trees. https://doi.org/10.2305/IUCN.CH.2019.ERL.1.EN
Romo A, Iszkuło G, Seghir Taleb M, Walas Ł, Boratyński A (2017) Taxus baccata in Morocco: a tree in regression in its southern extreme. Dendrobiology 78:63–74. https://doi.org/10.12657/denbio.078.007
Rostami Shahraji T, Yousefpour Rashti M (2003) The study of natural regeneration of Taxus Baccata L. in Dorfak Forest region in Gilan province. 15:15–19
Sagheb-Talebi K, Pourhashemi M, Sajedi T (2014) Forests of Iran: a treasure from the past, a hope for the future. Springer, New York
Scharnweber T, Rietschel M, Manthey M (2007) Degradation stages of the Hyrcanian forests in southern Azerbaijan. Arch Für Naturschutz Und Landschaftsforsch 46:133–156
Senneville S, Beaulieu J, Daoust G, Deslauriers M, Bousquet J (2001) Evidence for low genetic diversity and metapopulation structure in Canada yew (Taxus canadensis): considerations for conservation. Can J For Res 31:110–116. https://doi.org/10.1139/x00-152
Shin S, Lee SG, Kang H (2017) Spatial distribution patterns of old-growth forest of dioecious tree Torreya nucifera in rocky gotjawal terrain of Jeju Island, South Korea. J Ecol Environ 41:1–12. https://doi.org/10.1186/s41610-017-0050-3
Thomas PA, Garcia-Martí X (2015) Response of European yews to climate change: a review. For Syst 24:1–11. https://doi.org/10.5424/fs/2015243-07465
Thomas PA, Polwart A (2003) Taxus baccata L. J Ecol 91:489–524
Vranckx G, Jacquemyn H, Mergeay J, Cox K, Kint V, Muys B, Honnay O (2014) Transmission of genetic variation from the adult generation to naturally established seedling cohorts in small forest stands of pedunculate oak (Quercus robur L.). For Ecol Manag 312:19–27. https://doi.org/10.1016/j.foreco.2013.10.027
Vu DD, Bui TTX, Nguyen MT, Vu DG, Nguyen MD, Bui VT, Huang X, Zhang Y (2017) Genetic diversity in two threatened species in Vietnam: Taxus chinensis and Taxus wallichiana. J For Res 28:265–272. https://doi.org/10.1007/s11676-016-0323-1
Wheeler NC, Jech KS, Masters SA, O’brien CJ, Stonecypher RW, Timmons DW, Lupkes A (1995) Genetic variation and parameter estimates in Taxus brevifolia (Pacific yew). Can J For Res 25:1913–1927. https://doi.org/10.1139/x95-207
Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191. https://doi.org/10.1093/genetics/163.3.1177
Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 395–420
Yousefzadeh H, Amirchakhmaghi N, Naseri B, Shafizadeh F, Kozlowski G, Walas Ł (2022) The impact of climate change on the future geographical distribution range of the endemic relict tree Gleditsia caspica (Fabaceae) in Hyrcanian forests. Ecol Inform 71:101773. https://doi.org/10.1016/J.ECOINF.2022.101773
Zhang DQ, Zhou N (2013) Genetic diversity and population structure of the endangered conifer Taxus wallichiana var. mairei (Taxaceae) revealed by Simple Sequence Repeat (SSR) markers. Biochem Syst Ecol 49:107–114. https://doi.org/10.1016/j.bse.2013.03.030
Acknowledgements
The authors would like to thank Mr. Mohammad-Reza Abbaszadeh and Mr. Malek Nasiri Mehr for their kind help in the sampling and technical laboratory, respectively.
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This work was supported by Research Council of Tarbiat Modares University (TMU) and Iran National Science Foundation (Grant no. 97020110).
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This research was conceived and designed by all authors. AH and OE carried out field sampling and collected plant material. Conceptualization, methodology, investigation and preparing original draft was done by AH, OE and HY were in charge of supervision, methodology, validation, formal analysis, writing review and editing. MHM and SGJ provided critical feedback and contributed substantially to manuscript revision. Statistical analysis of the manuscript was performed by ŁW
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Hematzadeh, A., Esmailzadeh, O., Jalali, S.G. et al. Genetic diversity and structure of English yew (Taxus baccata L.) as a tertiary relict and endangered tree in the Hyrcanian forests. Biodivers Conserv 32, 1733–1753 (2023). https://doi.org/10.1007/s10531-023-02573-3
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DOI: https://doi.org/10.1007/s10531-023-02573-3