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Genetic structure of endangered species Adenophora liliifolia and footprints of postglacial recolonisation in Central Europe

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Abstract

Quaternary climatic fluctuations changed the floristic composition of large areas and forced biota to repeated movements following gradients of their ecological tolerance. Different and contrasting patterns of responses were reported for various species. In this study we focused on Adenophora liliifolia, a perennial herbaceous species representing a south Siberian floristic element in European flora, well adapted to a continental climate. We investigated the genetic diversity and phylogeography of the species within Europe. The results show the absence of stronger sequence differentiation across the investigated 3600 km long transect, which reflects the young evolutionary origin of the species and/or repeated population contractions/expansions accompanied by bottleneck during the Quaternary climatic fluctuations. Along with this, the results suggest several regions located in Carpathians, Alps-Dinarides, and in non-glaciated parts of Central Russia with high haplotype diversity, which probably served as refugia. Low genetic diversity, the prevalence of a single cpDNA haplotype, and the genetic composition of the investigated European sites suggest re-colonization of Central Europe from a refugium located in southern Europe. The distribution of genetic variation and moderate genetic differentiation of the investigated sites may indicate the process of fragmentation of the common genetic pool in Central Europe. Projections of ongoing climate change during the twenty-first century are not favorable for species persistence in Central Europe. In the case of ex-situ conservation actions, we recommend protection and proper management of rapidly vanishing populations and maintenance of genetic diversity, especially in regions with high haplotype diversity.

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Data availability

The AFLP data matrix is available upon request. DNA sequences: GenBank accessions MN530067-93, MN519409-16, MT299777-8, MT304671-2, and MT308772-3. Haplotype alignments of the three sequenced cpDNA loci and ITS region in ‘fasta’ format: SM 3. Climate data and Maxent input files: SM 4.

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Acknowledgements

We are grateful to all who helped to gather plant material and permissions necessary for this study; Austria: Renate Hoellriegl, Wolfgang Schleidt; Czech Republic: Roman Hamerský, Josef Mottl; Switzerland: Lorenzo Schmid; Germany: Martin Scheuerer; Hungary: Tünde Farkas; Italy: Cesare Lasen, Nicola Casarotto; Poland: Adam Rapa, Marek Ciosek; Romania: Victor Adrian Indreica; Slovakia: Drahoš Blanár, Štefánia Bryndzová, Peter Turis, Róbert Šuvada; Slovenia: Brane Vres. The BRNU herbarium samples were kindly provided by Jiří Danihelka (Masaryk University, Brno). We would like to thank the editor and reviewers for their valuable and constructive comments on the manuscript.

Funding

The study was supported by the Internal Grant Agency of Palacký University Olomouc (IGA_Prf_2021_001), the European Social Fund, The Education for Competitiveness Operational Programme (CZ.1.07/2.3.00/30.0004), and fund awarded by EEA/Norway and the Ministry of Environment of the Czech Republic (No. MGSII-17 in 2015–2017). Marco Thines and Tahir Ali received support from LOEWE in the Centre for Translational Biodiversity Genomics (TBG) framework. RFBR and Krasnodar Krai funded the reported study by Alexey P. Seregin according to the research project № 19-44-233012. Romana Prausová was supported by the funds of Specific research provided by the Ministry of Education of the Czech Republic No. 2117/2020. Computational resources were provided by the ELIXIR-CZ project (LM2018131), part of the international ELIXIR infrastructure, and by the project “e-Infrastruktura CZ” (e-INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures.

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Authors and Affiliations

  1. Faculty of Science, Department of Botany, Palacký University Olomouc, Šlechtitelů 27, 783 71, Olomouc-Holice, Czech Republic

    Lucie Vaculná, Ľuboš Majeský & Miloslav Kitner

  2. Senckenberg Biodiversity and Climate Research Center, Senckenberg Gesellschaft Für Naturforschung, Senckenberganlage 25, D-60325, Frankfurt, Germany

    Tahir Ali & Marco Thines

  3. Translational Biodiversity Genomics Centre (TBG), Georg-Voigt-Str. 14-16, 60325, Frankfurt, Germany

    Tahir Ali & Marco Thines

  4. Faculty of Biology, Herbarium (MW), M. V. Lomonosov Moscow State University, Moscow, Russia, 119991

    Alexey P. Seregin

  5. Faculty of Science, Department of Biology, University of Hradec Králové, 500 02, Hradec Králové, Czech Republic

    Romana Prausová

  6. PAS Botanical Garden – Center for Biological Diversity Conservation in Powsin, Prawdziwka 2, 02-973, Warsaw 76, Poland

    Adam Kapler

  7. Faculty of Biological Sciences, Department of Botany and Ecology, University of Zielona Góra, 65-516, Zielona Gora, Poland

    Dmytro Iakushenko

  8. Department of Biology, Institute of Ecology, Evolution, and Diversity, Goethe University, Campus Riedberg, Max-von-Laue-Str. 13, D-60439, Frankfurt, Germany

    Marco Thines

Authors
  1. Lucie Vaculná
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  2. Ľuboš Majeský
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  3. Tahir Ali
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  4. Alexey P. Seregin
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  5. Romana Prausová
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  6. Adam Kapler
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  7. Dmytro Iakushenko
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  8. Marco Thines
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  9. Miloslav Kitner
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Contributions

MK, LV, and LM designed experiments, performed statistical analyses, interpreted results, wrote the manuscript; LV performed the main part of laboratory analyses (with the assistance of MK, TA, and MT); RP, AK, DI, APS, and MT participated in sampling and manuscript preparation. All co-authors approved the final version of the manuscript.

Corresponding author

Correspondence to Miloslav Kitner.

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Supplementary Information

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Supplementary file1 (DOCX 26 KB)

SM 1a. AFLP primer combinations, used for selective and pre-selective amplification. SM 1b. List of tested nuclear and chloroplast regions; F (forward primer), I (internal primer), R (reverse primer). SM 1c. PCR reaction conditions for the sequenced regions.

Supplementary file2 (XLSX 59 KB)

SM 2a. List of identified haplotypes/ribotypes in analysed A. liliifolia samples. SM 2b. Details on herbarium vouchers used in the study.

Supplementary file3 (TXT 28 KB)

SM 3. Haplotype alignments of three cpDNA loci and ITS region in ‘fasta’ format.

Supplementary file4 (DOCX 2351 KB)

SM 4a. Geographic coordinates of 78 A. liliifolia records used in Maxent modeling. SM 4b. Summary of selected WorldClim Global Circulation Models (GCM) and data resolution used for Maxent modeling. SM 4c. Bioclimatic and environmental variables used for Maxent modeling. SM 4d. Response of A. liliifolia to variables used in Maxent modeling. A) Temperature Seasonality (Coeff. of Var; bio_4), B) Max Temperature of Warmest Month (°C x 10; bio_5), C) Min Temperature of Coldest Month (°C x 10; bio_6), D) Precipitation Seasonality (Coeff. of Var, bio_15), E) Precipitation of Warmest Quarter (mm; bio_18), F) Available Soil Water Capacity (%; Awch1), G) Base Saturation (%; BS1), H) Deciduous Trees cover (%; vege_3), I) Cultived & Managed vegetation cover (%; vege_7).SM 4e. Maxent prediction of future habitat suitability for A. liliifolia populations based on ensemble models: A) rcp45 - 2050; B) rcp45 - 2070; C) rcp85 - 2050; D) rcp85 - 2070. Suitability is expressed between 0 and 1; higher values (represented by warmer colours) indicate an increased haitat suitability. Dots on the map represent verified populations sampled in the present study.

Supplementary file5 (PDF 825 KB)

SM 5a. Statistic based on AFLP and concatenated three cpDNA loci. nAFLP (number of samples used for AFLP analysis), PLP (percentage of polymorphic loci), nFB (fixed band number), nPB (private band number), nFPB (fixed private band number), Hj (Nei’s Gene Diversity), I (Shannon’s index), NE (number of effective alleles), DW (frequency-down-weighted marker value [rare fragments]), nSeq (number of samples sequenced for three cpDNA loci), NoH (number of different haplotypes), HD (haplotype diversity), Pi (nucleotide diversity), Tajima’s D[P] (Tajima’s D test, the significance of the test is shown as the superscript, ns = not significant), cpDNA (multilocus haplotype observed for the concatenated three intergenic spacers; + frequency of observed haplotype), SE (standard error), † (indicates populations with the presence of suggested ancestral haplotype. SM 5b. Visualization of A) the spatial distribution of Nei’s Gene Diversity (Hj), B) the frequency-down-weighted (DW) marker across the sampled populations (n >5). Coloured polygons show defined regions: Central Europe (magenta), Poland (red), Western Carpathians (orange), Alps - Dinarides (dark turquoise), Southeastern Carpathians (green), Russia (light blue). SM 5c. Result of Bayesian clustering performed in STRUCTURE and processed by STRUCTURE HARVESTER. The plot of mean likelihood L(K) and variance per each K value and plot of deltaK for detecting the number of K best fitting analysed data. SM 5d. Graphical output of STRUCTURE clustering analysis for K = 3, and K = 7. Individuals are represented by a single vertical line broken into colored segments representing different genetic groups, where the length of each shade (x-axis) is proportional to the assignment to particular cluster. SM 5e. Unrooted Neighbor-joining dendrogram based on 350 AFLP markers, showing the division of 213 samples into eight clusters. Branches colored according to the country of origin. Bootstrap values on all nodes were below 50% and are not shown. SM 5f. Unrooted Neighbor-joining dendrogram based on 350 AFLP markers, showing the division of 213 samples into eight clusters. Branches colored according to the samples’ affiliation between the six defined regions. Bootstrap values on all nodes were below 50% and are not shown.

Supplementary file6 (XLSX 21 KB)

SM 6a. Table of pairwise FST values based on AFLP data. Darker colour means lower pairwise FST. Sampling sites highlighted in pink indicate sites with less than 5 individuals. Significance levels: * (p < 0.05), *** (p < 0.001).

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Vaculná, L., Majeský, Ľ., Ali, T. et al. Genetic structure of endangered species Adenophora liliifolia and footprints of postglacial recolonisation in Central Europe. Conserv Genet 22, 1069–1084 (2021). https://doi.org/10.1007/s10592-021-01396-5

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