Skip to main content

Cytoplasmic DNA variation does not support a recent contribution of Pinus sylvestris L. from the Caucasus to the main range

Abstract

The history of the interaction between the boreal floras of northern Eurasia and those from the mountain areas located at intermediate latitudes remains insufficiently studied. Twenty-four population samples of 4 to 34 trees were analyzed with eight mitochondrial DNA (mtDNA) markers and four chloroplast DNA (cpDNA) microsatellite loci to study the history of Scots pine in the Black Sea region, and infer migration routes and genetic relationships with populations of the northern part of the range. These new data were combined with data previously obtained from Eastern Europe and North Asia. Scots pine past geographic range was also reconstructed using environmental niche modeling. Both mtDNA and cpDNA revealed a common origin of populations in the eastern Black Sea region (EBS), i.e., Crimea, Caucasus, and Asia Minor, and deep divergence from the main range of Scots pine, reminiscent of the isolation of enclaves in Iberian and Apennine Peninsulas. Mitochondrial DNA haplotypes (mitotypes) endemic to Western Caucasus are genetically intermediate between mitotypes from Eastern Europe and other mitotypes from the EBS region, indicating a recombinant origin likely due to migration to the Caucasus from the north and hybridization with local trees. Environmental niche modeling shows the possibility of such migration events during the last glacial maximum.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Arslanov KA, Dolukhanov PM, Gei NA (2007) Climate, Black Sea levels and human settlements in Caucasus Littoral 50,000-9000 BP. Quat Int 167:121–127. https://doi.org/10.1016/j.quaint.2007.02.013

    Article  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenics. Mol Biol Evol 16:37–48

    CAS  Article  Google Scholar 

  • Belletti P, Ferrazzini D, Piotti A, Monteleone I, Ducci F (2012) Genetic variation and divergence in Scots pine (Pinus sylvestris L.) within its natural range in Italy. Eur J For Res 131:1127–1138. https://doi.org/10.1007/s10342-011-0584-3

    Article  Google Scholar 

  • Bernhardsson C, Floran V, Ganea SL, Garcia-Gil MR (2016) Present genetic structure is congruent with the common origin of distant Scots pine populations in its Romanian distribution. For Ecol Manag 361:131–143. https://doi.org/10.1016/j.foreco.2015.10.047

    Article  Google Scholar 

  • Binney HA, Willis KJ, Edwards ME, Bhagwat SA, Anderson PM, Andreev AA, Blaauw M, Damblon F, Haesaerts P, Kienast F, Kremenetski KV, Krivonogov SK, Lozhkin AV, MacDonald GM, Novenko EY, Oksanen P, Sapelko TV, Valiranta M, Vazhenina L (2009) The distribution of late-Quaternary woody taxa in northern Eurasia: evidence from a new macrofossil database. Quat Sci Rev 28:2445–2464. https://doi.org/10.1016/j.quascirev.2009.04.016

    Article  Google Scholar 

  • Buchovska J, Danusevicius D, Baniulis D, Stanys V, Siksnianiene JB, Kavaliauskas D (2013) The location of the northern glacial refugium of Scots pine based on mitochondrial DNA markers. Balt For 19:2–12

    Google Scholar 

  • Burban C, Petit RJ, Carcreff E, Jactel H (1999) Rangewide variation of the maritime pine bast scale Matsucoccus feytaudi Duc. (Homoptera: Matsucoccidae) in relation to the genetic structure of its host. Mol Ecol 8:1593–1602. https://doi.org/10.1046/j.1365-294x.1999.00739.x

    CAS  Article  PubMed  Google Scholar 

  • Cheddadi R, Vendramin GG, Litt T, Francois L, Kageyama M, Lorentz S, Laurent JM, de Beaulieu JL, Sadori L, Jost A, Lunt D (2006) Imprints of glacial refugia in the modern genetic diversity of Pinus sylvestris. Glob Ecol Biogeogr 15:271–282. https://doi.org/10.1111/j.1466-822x.2006.00226.x

    Article  Google Scholar 

  • Cornuet JM, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, Marin JM, 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

    CAS  Article  PubMed  Google Scholar 

  • Dering M, Kosiński P, Wyka TP, Pers-Kamczyc E, Boratyński A, Boratyńska K, Reich PB, Romo A, Zadworny M, Żytkowiak R, Oleksyn J (2017) Tertiary remnants and Holocene colonizers: genetic structure and phylogeography of Scots pine reveal higher genetic diversity in young boreal than in relict Mediterranean populations and a dual colonization of Fennoscandia. Divers Distrib 23:540–555. https://doi.org/10.1111/ddi.12546

    Article  Google Scholar 

  • Devey ME, Bell JC, Smith DN, Neale DB, Moran GF (1996) A genetic linkage map for Pinus radiata based on RFLP, RAPD, and microsatellite markers. Theor Appl Genet 92:673–679. https://doi.org/10.1007/Bf00226088

    CAS  Article  PubMed  Google Scholar 

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581. https://doi.org/10.1046/j.1365-294X.2002.01650.x

    CAS  Article  PubMed  Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree (Argania spinosa (L) Skeels) endemic to Morocco. Theor Appl Genet 92:832–839

    Article  Google Scholar 

  • Excoffier L, Lischer HEL (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. https://doi.org/10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  • Gernandt DS, Lopez GG, Garcia SO, Liston A (2005) Phylogeny and classification of Pinus. Taxon 54:29–42. https://doi.org/10.2307/25065300

    Article  Google Scholar 

  • Goldstein DB, Linares AR, Cavallisforza LL, Feldman MW (1995) An evaluation of genetic distances for use with microsatellite loci. Genetics 139:463–471

    CAS  Article  Google Scholar 

  • Goncharenko GG, Silin AE, Padutov VE (1995) Intraspecific and interspecific genetic differentiation in closely related pines from Pinus subsection sylvestris (Pinaceae) in the former Soviet Union. Plant Syst Evol 194:39–54. https://doi.org/10.1007/bf00983215

    Article  Google Scholar 

  • Grossheim AA (1936) Analysis of the flora of the Caucasus. The Azerbaijan branch of the Academy of Sciences of the USSR press, Baku (In Russian)

    Google Scholar 

  • Gulisashvili VZ (1955) Regularities in the distribution of forest vegetation and the main tree species in the Transcaucasus. Bot. Zhurn. (Moscow & Leningrad) 40:18–32. (In Russian)

  • Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467. https://doi.org/10.1111/j.1461-0248.2005.00739.x

    Article  PubMed  Google Scholar 

  • Haesaerts P, Borziac I, Chekha VP, Chirica V, Drozdov NI, Koulakovska L, Orlova LA, van der Plicht J, Damblon F (2010) Charcoal and wood remains for radiocarbon dating Upper Pleistocene loess sequences in Eastern Europe and Central Siberia. Paleogeogr Paleoclimatol Paleoecol 291:106–127. https://doi.org/10.1016/j.palaeo.2010.03.034

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp 41:95–98

    CAS  Google Scholar 

  • Hantemirova EV, Heinze B, Knyazeva SG, Musaev AM, Lascoux M, Semerikov VL (2017) A new Eurasian phylogeographical paradigm? Limited contribution of southern populations to the recolonization of high latitude populations in Juniperus communis L.(Cupressaceae). J Biogeogr 44:271–282. https://doi.org/10.1111/jbi.12867

    Article  Google Scholar 

  • Hrivnak M, Paule L, Krajmerova D, Kulac S, Sevik H, Turna I, Tvauri I, Gomory D (2017) Genetic variation in tertiary relics: the case of eastern-Mediterranean Abies (Pinaceae). Ecol Evol 7:10018–10030. https://doi.org/10.1002/ece3.3519

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaramillo-Correa JP, Beaulieu J, Bousquet J (2004) Variation in mitochondrial DNA reveals multiple distant glacial refugia in black spruce (Picea mariana), a transcontinental North American conifer. Mol Ecol 13:2735–2747. https://doi.org/10.1111/j.1365-294X.2004.02258.x

    CAS  Article  PubMed  Google Scholar 

  • Jaramillo-Correa JP, Bousquet J (2005) Mitochondrial genome recombination in the zone of contact between two hybridizing conifers. Genetics 171:1951–1962. https://doi.org/10.1534/genetics.105.042770

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Jaramillo-Correa JP, Grivet D, Terrab A, Kurt Y, de-Lucas AI, Wahid N, Vendramin GG, Gonzalez-Martinez SC (2010) The Strait of Gibraltar as a major biogeographic barrier in Mediterranean conifers: a comparative phylogeographic survey. Mol Ecol 19:5452–5468. https://doi.org/10.1111/j.1365-294X.2010.04912.x

    CAS  Article  PubMed  Google Scholar 

  • Korshikov II, Podgorny DY, Lisnichuk AN (2012) Population-genetic differences between the Koch pine (Pinus koсhiana Klotzsch ex Koch) of the Mountain Crimea and the Scots pine (Pinus sylvestris L.) of the Kremenetsky hills. Bulletin of the Nikitsky Botanical Garden 104:23–27 (In Russian)

    Google Scholar 

  • Maleev VP (1941) Tertiary relics in the flora of the Western Caucasus and the principal stages of the quaternary history of vegetation. In: Komarov V. L. (ed), Materials of the history of the flora and vegetation of the USSR, fasc. 1. The USSR Academy of Sciences press, Moscow – Leningrad, pp. 61-144. (In Russian)

  • Naydenov K, Senneville S, Beaulieu J, Tremblay F, Bousquet J (2007) Glacial vicariance in Eurasia: mitochondrial DNA evidence from Scots pine for a complex heritage involving genetically distinct refugia at mid-northern latitudes and in Asia Minor. BMC Evol Biol 7:233. https://doi.org/10.1186/1471-2148-7-233

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia Univ, Press, N.Y

    Book  Google Scholar 

  • Pearl SA, Welch ME, McCauley DE (2009) Mitochondrial heteroplasmy and paternal leakage in natural populations of Silene vulgaris, a gynodioecious plant. Mol Biol Evol 26:537–545. https://doi.org/10.1093/molbev/msn273

    CAS  Article  PubMed  Google Scholar 

  • Petit RJ, Aguinagalde I, de Beaulieu JL, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Muller-Starck GM, Demesure-Musch B, Palme A, Martin JP, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565. https://doi.org/10.1126/science.1083264

    CAS  Article  PubMed  Google Scholar 

  • Petrova I, Bolshakov V, Sannikov S, Farzaliev V, Yegorov E (2013) Genetic differentiation of Pinus sylvestris L. populations in the Caucasus and adjacent regions. International Caucasian Forestry Symposium. 24–26 October 2013. 305–310

  • Petrova IV, Sannikov SN, Tembotova FI, Sannikova NS, Farzaliev VS, Mollaeva MZ, Egorov EV (2017) Genogeography of Pinus sylvestris L. populations in the Greater Caucasus and Crimea. Russ J Ecol 48:524–531. https://doi.org/10.1134/s106741361706008x

    Article  Google Scholar 

  • Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026

    Article  Google Scholar 

  • Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245

    CAS  Article  Google Scholar 

  • Pravdin LF (1969) Scots pine. Variation, intraspecific taxonomy and selection. Israel Program of Scientific Translations, Jerusalem

  • Pyhäjärvi T, Salmela MJ, Savolainen O (2008) Colonization routes of Pinus sylvestris inferred from distribution of mitochondrial DNA variation. Tree Genet Genomes 4:247–254. https://doi.org/10.1007/s11295-007-0105-1

    Article  Google Scholar 

  • Provan J, Soranzo N, Wilson NJ, Goldstein DB, Powell W (1999) A low mutation rate for chloroplast microsatellites. Genetics 153:943–947

    CAS  Article  Google Scholar 

  • Ren GP, Abbott RJ, Zhou YF, Zhang LR, Peng YL, Liu JQ (2012) Genetic divergence, range expansion and possible homoploid hybrid speciation among pine species in Northeast China. Heredity 108:552–562. https://doi.org/10.1038/hdy.2011.123

    CAS  Article  PubMed  Google Scholar 

  • Rohlf EJ (1988) Numerical taxonomy and multivariate analysis system. Exter Publ, LTD, N.Y

    Google Scholar 

  • Sannikov SN, Petrova IV (2012) Phylogenogeography and genotaxonomy of Pinus sylvestris L. populations. Russ J Ecol 43:273–280. https://doi.org/10.1134/S1067413612040145

    Article  Google Scholar 

  • Semerikov VL, Podogas AV, Shurkhal AV (1993) Variability of allozyme loci in populations of common pine. Russ J Ecol 24:14–20

    Google Scholar 

  • Semerikov VL, Lascoux M (2003) Nuclear and cytoplasmic variation within and between Eurasian Larix (Pinaceae) species. Am J Bot 90:1113–1123. https://doi.org/10.3732/ajb.90.8.1113

    CAS  Article  PubMed  Google Scholar 

  • Semerikov VL, Semerikova SA, Polezhaeva MA, Kosintsev PA, Lascoux M (2013) Southern montane populations did not contribute to the recolonization of West Siberian Plain by Siberian larch (Larix sibirica): a range-wide analysis of cytoplasmic markers. Mol Ecol 22:4958–4971. https://doi.org/10.1111/mec.12433

    CAS  Article  PubMed  Google Scholar 

  • Semerikov VL, Semerikova SA, Dymshakova OS, Zatsepina KG, Tarakanov VV, Tikhonova IV, Ekart AK, Vidyakin AI, Jamiyansuren S, Rogovtsev RV, Kalchenko LI (2014) Microsatellite loci polymorphism of chloroplast DNA of Scots pine (Pinus sylvestris L.) in Asia and Eastern Europe. Russ J Genet 50:577–585. https://doi.org/10.1134/S1022795414040127

    CAS  Article  Google Scholar 

  • Semerikov VL, Putintseva YA, Oreshkova NV, Semerikova SA, Krutovsky KV (2015) Development of new mitochondrial DNA markers in Scots pine (Pinus sylvestris L.) for population and phylogeographic studies. Russ J Genet 51:1199–1203. https://doi.org/10.1134/S1022795415120108

    CAS  Article  Google Scholar 

  • Semerikov VL, Semerikova SA, Putintseva YA, Tarakanov VV, Tikhonova IV, Vidyakin AI, Oreshkova NV, Krutovsky KV (2018) Colonization history of Scots pine in Eastern Europe and North Asia based on mitochondrial DNA variation. Tree Genet Genomes 14. 10.1007/s11295-017-1222-0

  • Semerikova SA, Semerikov VL (2014) Mitochondrial DNA variation and reticulate evolution of the genus Abies. Russ J Genet 50:366–377. https://doi.org/10.1134/s1022795414040139

    CAS  Article  Google Scholar 

  • Semerikova SA, Khrunyk YY, Lascoux M, Semerikov VL (2018) From America to Eurasia: a multigenomes history of the genus Abies. Mol Phylogenet Evol 125:14–28. https://doi.org/10.1016/j.ympev.2018.03.009

    CAS  Article  PubMed  Google Scholar 

  • Shatilova I, Mchedlishvili N, Rukhadze L, Kvavadze E (2011) The history of the flora and vegetation of Georgia. Georgian National Museum, Institute of Paleobiology, Tbilisi

  • Soranzo N, Alia R, Provan J, Powell W (2000) Patterns of variation at a mitochondrial sequence-tagged-site locus provides new insights into the postglacial history of European Pinus sylvestris populations. Mol Ecol 9:1205–1211. https://doi.org/10.1046/j.1365-294x.2000.00994.x

    CAS  Article  PubMed  Google Scholar 

  • Tarasov PE, Volkova VS, Webb T, Guiot J, Andreev AA, Bezusko LG, Bezusko TV, Bykova GV, Dorofeyuk NI, Kvavadze EV, Osipova IM, Panova NK, Sevastyanov DV (2000) Last glacial maximum biomes reconstructed from pollen and plant macrofossil data from northern Eurasia. J Biogeogr 27:609–620. https://doi.org/10.1046/j.1365-2699.2000.00429.x

    Article  Google Scholar 

  • Tesakov AS, Titov VV, Baygusheva VS, Velichko AA et al. (2013) VIII All-Russian conference on quaternary research: basic problems of quaternary, research results, and the main trends of future studies. Field Excursions Guidebook (Rostov-on-Don, Russia, 10–15 June 2013). SSC RAS. Publishers, Rostov-on-Don. (In Russian)

  • Velichko AA, Catto NR, Kononov MY, Morozova TD, Novenko EY, Panin PG, Ryskov GY, Semenov VV, Timireva SN, Titov VV, Tesakov AS (2009) Progressively cooler, drier interglacials in southern Russia through the quaternary: evidence from the Sea of Azov region. Quat Int 98:204–219. https://doi.org/10.1016/j.quaint.2008.06.005

    Article  Google Scholar 

  • Vendramin GG, Lelli L, Rossi P, Morgante M (1996) A set of primers for the amplification of 20 chloroplast microsatellites in Pinaceae. Mol Ecol 5:595–598

    CAS  Article  Google Scholar 

  • Vidyakin AI, Semerikov VL, Polezhaeva MA, Dymshakova OS (2012) Spread of mitochondrial DNA haplotypes in population of scots pine (Pinus sylvestris L.) in northern European Russia. Russ J Genet 48:1267–1271. https://doi.org/10.1134/s1022795412120150

    CAS  Article  Google Scholar 

  • Wagner DB, Dong J, Carlson MR, Yanchuk AD (1991) Paternal leakage of mitochondrial DNA in Pinus. Theor Appl Genet 82:510–514. https://doi.org/10.1007/bf00588607

    CAS  Article  PubMed  Google Scholar 

  • Wang BS, Wang XR (2014) Mitochondrial DNA capture and divergence in Pinus provide new insights into the evolution of the genus. Mol Phylogenet Evol 80:20–30. https://doi.org/10.1016/j.ympev.2014.07.014

    CAS  Article  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  Google Scholar 

  • Willis KJ, van Andel TH (2004) Trees or not trees? The environments of central and eastern Europe during the Last Glaciation. Quat Sci Rev 23:2269–2287. https://doi.org/10.1016/j.quascirev.2004.06.002

    Article  Google Scholar 

  • Wojkiewicz B, Wachowiak W (2016) Substructuring of Scots pine in Europe based on polymorphism at chloroplast microsatellite loci. Flora 220:142–149. https://doi.org/10.1016/j.flora.2016.03.005

    Article  Google Scholar 

  • Zeb U, Dong WL, Zhang TT, Wang RN, Shahzad K, Ma XF, Li ZH (2020) Comparative plastid genomics of Pinus species: insights into sequence variations and phylogenetic relationships. J Syst Evol 58:118–132. https://doi.org/10.1111/jse.12492

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to the staff of the Caucasus Nature Reserve, Utrish Nature Reserve, Teberda Nature Reserve, Yalta mountain forest Reserve, Crimea Reserve, and Kastamonu University as well as to Farzaliev, V. S., Hantemirova, E. V., Hantemirov R. M., Cherepanova, O. E., and Sezgin, A. for help with sampling.

Data archiving statement

A list of the population samples including haplotype frequency is provided in Supplementary material - Table S1. Sequences used in the study were deposited in GenBank (MN725822, MN725820, MN725821, MN725828, MN725827, MN725829, MN725824, MN725826, MN725825, MN781407, MN781410, MN781408, and MN725819).

Funding

This study was supported by the Russian Foundation for Basic Research (grant no. 16-04-00607), by the State Contract of the Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences, and partly supported by the Program of the Ural Branch of Russian Academy of Sciences (project no 18-4-4-43).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vladimir L. Semerikov.

Additional information

Communicated by G. G. Vendramin

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 3284 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Semerikov, N.V., Petrova, I.V., Sannikov, S.N. et al. Cytoplasmic DNA variation does not support a recent contribution of Pinus sylvestris L. from the Caucasus to the main range. Tree Genetics & Genomes 16, 59 (2020). https://doi.org/10.1007/s11295-020-01458-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-020-01458-8

Keywords

  • Cytoplasmic DNA
  • Phylogeography
  • Caucasus
  • Pinus sylvestris
  • Refugia