Past climate changes, population dynamics and the origin of Bison in Europe

Abstract

Background

Climatic and environmental fluctuations as well as anthropogenic pressure have led to the extinction of much of Europe's megafauna. The European bison or wisent (Bison bonasus), one of the last wild European large mammals, narrowly escaped extinction at the onset of the 20th century owing to hunting and habitat fragmentation. Little is known, however, about its origin, evolutionary history and population dynamics during the Pleistocene.

Results

Through ancient DNA analysis we show that the emblematic European bison has experienced several waves of population expansion, contraction, and extinction during the last 50,000 years in Europe, culminating in a major reduction of genetic diversity during the Holocene. Fifty-seven complete and partial ancient mitogenomes from throughout Europe, the Caucasus, and Siberia reveal that three populations of wisent (Bison bonasus) and steppe bison (B. priscus) alternately occupied Western Europe, correlating with climate-induced environmental changes. The Late Pleistocene European steppe bison originated from northern Eurasia, whereas the modern wisent population emerged from a refuge in the southern Caucasus after the last glacial maximum. A population overlap during a transition period is reflected in ca. 36,000-year-old paintings in the French Chauvet cave. Bayesian analyses of these complete ancient mitogenomes yielded new dates of the various branching events during the evolution of Bison and its radiation with Bos, which lead us to propose that the genetic affiliation between the wisent and cattle mitogenomes result from incomplete lineage sorting rather than post-speciation gene flow.

Conclusion

The paleogenetic analysis of bison remains from the last 50,000 years reveals the influence of climate changes on the dynamics of the various bison populations in Europe, only one of which survived into the Holocene, where it experienced severe reductions in its genetic diversity. The time depth and geographical scope of this study enables us to propose temperate Western Europe as a suitable biotope for the wisent compatible with its reintroduction.

ancientdna parameter [48]. Merged reads were then mapped to modern Bison bison and Bison bonasus mitogenomes using bwa as described previously [37]. The first 100 nt of each linearized reference mitogenome used for mapping was duplicated at the 3? end to allow mapping of fragments overlapping the junction. Mapped read duplicates were then removed using samtools rmdup as previously described [37]. The resulting bam files were then imported into Geneious 6.1.8 [43] and remapped onto the appropriate mitogenome sequence without the 100 nt duplication (B. bison for B. priscus sequences, B. bonasus for the Bb1 and Bb2 sequences). Consensus sequences were generated in Geneious and verified by visual inspection of the aligned reads. Geneious was used to measure coverage depth and the number of covered bases displayed in Additional file 1: Table S4.

Phylogenetic analyses

Sequence alignments were performed using the Muscle algorithm and were visually inspected and adjusted using Geneious 6.1.8 [43]. The maximum likelihood analyses presented in Fig. 1 were computed using PHYML 3.0, using an HKY substitution model with a gamma-distributed rate of variation among sites (+G) and invariant sites (+I) [49]. Robustness of the nodes was estimated using 500 bootstraps. RaXML 8.2.3 was used to generate the maximum likelihood bootstrap support values for the complete mitogenome alignment shown in Fig. 3 [50].

Phylogenetic analyses conducted under the Bayesian framework were performed using the program BEAST v. 1.8.2, which allows estimation of mutation and population history parameters simultaneously from temporally spaced sequence data [51]. Nucleotide substitution models were chosen following comparisons performed with jModelTest 2.1.7 using the Bayesian Information Criteria [52]. The HVR analysis presented in Fig. 2 was performed considering a TN93 model for the nucleotide substitution model, a gamma-distributed rate of variation among sites (+G) with four rate categories and invariant sites (i.e., TN93?+?I?+?G model). For the complete mitogenome analysis presented in Fig. 3, we used four partitions, the HVR, the first and second positions of the codons within the coding region, the third position, and the RNA genes. We considered the HKY?+?I?+?G model for the first two partitions, and the TN93?+?G for the last two. Default priors were used for all parameters of the nucleotide substitution model. For the analysis of Fig. 2, we used a strict molecular clock with a lognormal prior for the substitution rate (mean?=?-15.0, stdev?=?1.4) corresponding to a median of 2?×?10-7 substitutions per site and per year (95 % HPD 1.3?×?10-8 to 3.2?×?10-6) based on the estimation for Bison HVR substitution rate [7]. For the various partitions of the mitogenome of Fig. 3, we used estimates for the human mitogenome substitution rate to set the priors [53]: lognormal priors: HVR, mean?=?-16.1 stdev?=?2.0, corresponding to a median of 1.0?×?10-7 (2?×?10-9 to 5?×?10-6); RNA, mean?=?-18.65 stdev?=?2.0, corresponding to a median of 8.0?×?10-9 (1.6?×?10-10 to 4?×?10-7); first and second positions, mean?=?-18.5 stdev?=?2.0, corresponding to a median of 9.0?×?10-9 (1.8?×?10-10 to 4.7?×?10-7); third position, mean?=?-17.7 stdev?=?2.0 corresponding to a median of 2.0?×?10-8 (4× 10-10 to 1?×?10-6). Finally, a standard coalescent model was considered for the tree prior with a Bayesian skyline plot to model populations (5 and 10 populations with default parameters for the HVR and the mitogenomes respectively). The prior for the tree height followed a log-normal distribution, mean?=?14.6 stdev?=?0.6, truncate to 8.0?×?106 and 1.0?×?105, corresponding to a median of 2.2?×?106 and a 95 % HPD of (6.3?×?106 to 6.7?×?105), which integrates the various fossil finds assumed to correspond to ancestors of cattle and bison [54, 55].

To estimate the posterior distribution of each parameter of interest, we used the Markov Chain Monte Carlo algorithm implemented in the BEAST software. We ran five independent chains with initial values sampled as described above and an input UPGMA tree constructed using a Juke-Cantor distance matrix. Each of these chains was run for 50,000,000 iterations and for each parameter of interest, 18,000 samples (one every 2500 generated ones) were drawn after discarding a 10 % burn-in period. The BEAST output was analyzed with the software Tracer v. 1.6 (http://tree.bio.ed.ac.uk/software/tracer/). Visual inspection of the traces and the estimated posterior distributions suggested that each MCMC had converged on its stationary distribution. Using Logcombiner v. 1.8.2, we further combined all the results from the five independent chains. The maximum clade credibility tree with the median height of the nodes was finally calculated using TreeAnnotator v. 1.8.2 and visualized using FigTree v. 1.4.2 (http://tree.bio.ed.ac.uk/software/figtree/).

Declarations

Acknowledgments

We thank G Baldacci for continuous support. We thank Lou Saïer for help with the production of HVR data for some samples. We like to thank Marie-Hélène Moncel, Camille Daujeard, and Marie-Anne Julien for providing samples that did not yield genetic results. We acknowledge the contribution to sampling of Myriam Boudadi-Maligne, Jean-Baptiste Mallye, Pierre Pétrequin, Sylvie Lourdaux, and René Rémond. We are grateful to the French ministry of culture, Centre national de Préhistoire for providing the image of the wall paintings of the Chauvet cave.

Funding

The study was supported by the French national research center CNRS. The paleogenomic facility obtained support from the University Paris Diderot within the program "Actions de recherche structurantes". The sequencing facility of the Institut Jacques Monod, Paris, is supported by grants from the University Paris Diderot, the Fondation pour la Recherche Médicale (DGE20111123014), and the Région Ile-de-France (11015901). MT acknowledges financial support through the "Biodiversity of East-European and Siberian large mammals on the level of genetic variation of populations (BIOGEAST)" project within the 7th European Framework Programme, Marie Curie Actions, that allowed sampling to take place in Russia.

Availability of data and material

The produced DNA sequences have been deposited at NCBI: From KX870126 to KX870182 and from KX898005 to KX898020.

Authors' contributions

EMG and TG designed and supervised the overall research with an initial input from MT. DM developed sequence capture and produced the mitogenome data. SG produced the HVR data. TG, EMG, DM, and SG analyzed and interpreted the data. TG, EMG, and EAB wrote the manuscript with inputs from DM and SG. JPB provided samples, discussed the data and corrected the manuscript. MT, RMA, GBa, GBo, JCC, SD, SM, OP, NS, and HPU provided samples and feedbacks on the manuscript. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Not applicable since no data from individuals were used.

Ethics approval and consent to participate

Not applicable since we did not use biological material.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Additional files

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