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Recent increase in species-wide diversity after interspecies introgression in the highly endangered Iberian lynx

Nature Ecology & Evolution volume 8, pages 282–292 (2024)Cite this article

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Abstract

Genetic diversity is lost in small and isolated populations, affecting many globally declining species. Interspecific admixture events can increase genetic variation in the recipient species’ gene pool, but empirical examples of species-wide restoration of genetic diversity by admixture are lacking. Here we present multi-fold coverage genomic data from three ancient Iberian lynx (Lynx pardinus) approximately 2,000–4,000 years old and show a continuous or recurrent process of interspecies admixture with the Eurasian lynx (Lynx lynx) that increased modern Iberian lynx genetic diversity above that occurring millennia ago despite its recent demographic decline. Our results add to the accumulating evidence for natural admixture and introgression among closely related species and show that this can result in an increase of species-wide genetic diversity in highly genetically eroded species. The strict avoidance of interspecific sources in current genetic restoration measures needs to be carefully reconsidered, particularly in cases where no conspecific source population exists.

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Fig. 1: Geographic distribution, genetic structure and genetic diversity of ancient and contemporary Iberian lynx genomes.
Fig. 2: Genetic diversity across genomic features and check for purifying selection.
Fig. 3: D statistics for different combinations of Iberian and Eurasian lynx genomes.
Fig. 4

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Data availability

Merged and R1 and R2 reads sequence data are available for download at the European Nucleotide Archive (ENA) repository under study number PRJEB58855. Other data files supporting the results can be downloaded at figshare https://doi.org/10.6084/m9.figshare.24512722 (structure and diversity analyses) and https://doi.org/10.6084/m9.figshare.24486640 (admixture analyses).

Code Availability

Scripts used for diversity, structure and admixture analyses are available at Figshare: https://doi.org/10.6084/m9.figshare.24512722 (structure and diversity analyses) and https://doi.org/10.6084/m9.figshare.24486640 (admixture analyses).

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Acknowledgements

This research was funded by the Spanish Dirección General de Investigación Científica y Técnica through projects CGL2013-47755-P and CGL2017-84641-P to J.A.G and is an extension of a project on ancient lynx genetics granted to Miguel Delibes de Castro by the Fundación BBVA. M.L.-P. was supported by a PhD contract from Programa Internacional de Becas ‘La Caixa-Severo Ochoa’. J.N. received financial support through projects HAR2014- 55131 from the Ministerio de Ciencia e Innovación and SGR2014-108 from the Generalitat de Catalunya. We acknowledge support from Science for Life Laboratory, the Knut and Alice Wallenberg Foundation, the National Genomics Infrastructure funded by the Swedish Research Council and Uppsala Multidisciplinary Center for Advanced Computational Science for assistance with massively parallel sequencing and access to the UPPMAX computational infrastructure. We also acknowledge the support of the Supercomputing Wales project, which is part-funded by the European Regional Development Fund via the Welsh Government. Logistical support was provided by the Laboratorio de Ecología Molecular certified to ISO9001:2015 and ISO14001:2015 quality and environmental management systems. Data processing and most calculations and analyses were carried out in the Genomics servers of Doñana’s Singular Scientific-Technical Infrastructure, with additional computing and storage resources provided by Fundación Pública Galega, Centro Tecnolóxico de Supercomputación de Galicia. Logistical laboratory support was provided by the Laboratorio de Ecología Molecular certified to ISO9001:2015 and ISO14001:2015 quality and environmental management systems. Data processing and most calculations and analyses were carried out in the Genomics servers of Doñana’s Singular Scientific-Technical Infrastructure, with additional computing and storage resources provided by Fundación Pública Galega Centro Tecnolóxico de Supercomputación de Galicia.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolution, Estación Biológica de Doñana, CSIC, Seville, Spain

    Maria Lucena-Perez & José A. Godoy

  2. Evolutionary Adaptive Genomics, University of Potsdam, Potsdam, Germany

    Johanna L. A. Paijmans & Michael Hofreiter

  3. Department of Zoology, University of Cambridge, Cambridge, UK

    Johanna L. A. Paijmans

  4. Grupo de Investigación MIDAS, Departamento Historia I (Prehistoria), Universidad de Huelva, Huelva, Spain

    Francisco Nocete

  5. SERP, Departament de Prehistoria, Historia Antiga i Arqueologia, Universitat de Barcelona, Barcelona, Spain

    Jordi Nadal

  6. UNIARQ – Centro de Arqueologia da Faculdade de Letras da Universidade de Lisboa, Alameda da Universidade, Lisbon, Portugal

    Cleia Detry

  7. Centre for Palaeogenetics, Stockholm, Sweden

    Love Dalén

  8. Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden

    Love Dalén

  9. School of Environmental and Natural Sciences, Bangor University, Bangor, Gwynedd, UK

    Axel Barlow

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  1. Maria Lucena-Perez
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Contributions

J.A.G. conceived the project. A.B., J.A.G. and M.L.-P. designed the study. C.D., F.N. and J.N. provided ancient samples and critical input on archaeological context. M.L.-P. performed the laboratory work under the supervision of J.L.A.P. and M.H. A.B., J.L.A.P. and M.L.-P. analysed the data. A.B., J.A.G., J.L.A.P. and M.L.-P. interpreted the results, with critical input from M.H. and L.D. M.L.-P. drafted the manuscript with support from A.B. and J.A.G. and input by J.L.A.P., C.D., J.N., M.H. and L.D. All authors approved the final version of the manuscript.

Corresponding author

Correspondence to José A. Godoy.

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Extended data

Extended Data Fig. 1 Authentication of ancient DNA data using MapDamage.

On the left, cytosine deamination patterns. X axis indicates the relative nucleotide position of the reads. Plots show the proportion of T where the reference genome possesses a C (red) and proportion of A where the reference possesses a G (blue). Increased C to T substitutions towards the ends of the read are typical damage patterns for ancient data, although the single-stranded library preparation with UDG (uracil–DNA glycosylase) treatment reduced this pattern. Plot on the right represents the fragment length distribution. Minimum read length for mapping used was 30 bp, resulting in a truncation of the plot.

Extended Data Fig. 2 Additional clustering analyses results.

Alternative clustering patterns obtained in five runs of NGSadmix for K = 4 and K = 5. Population names on top, with number of samples within parentheses.

Extended Data Fig. 3 Genetic diversity in ancient and contemporary populations.

Diversity of the ancient population (n = 3) and different random subsamples (n = 3) of individuals from the contemporary populations, Andújar and Doñana, considering both transitions and transversions (a) and transversion only (b). Points represent the mean and bars, although not always visible, and represent the standard deviation calculated over 10 kb windows using 100 iterations.

Extended Data Fig. 4 D statistics calculated for tree topologies relating different genome trios.

On the left, the different tree topologies tested (a–g). IL= Iberian lynx, EL= Eurasian lynx. Western EL included genomes sampled in Kirov, Caucasus, Balkans and Carpathians, while Eastern EL genomes were sampled in Primorsky Krai and Yakutia. All topologies were tested using the domestic cat as the outgroup. Red and white points show significant and non-significant D values, respectively. The seven different tree topologies tested (a–g) are displayed for each category of D values shown, with double-headed arrows indicating the admixing lineages supported by significant tests. a shows similar introgression in different contemporary IL individuals. b and c show similar and non-significant d-stat when different eastern and western Eurasian lynx individuals are compared. d and e show higher admixture signal from contemporary Eurasian lynx than from a single ancient Eurasian lynx from the Iberian Peninsula, whereas ancient Iberian lynx is less admixed with ancient EL than contemporary Western EL (F) and similarly than Eastern EL (G).

Extended Data Fig. 5 Results of phylogenetic tests of gene flow direction.

The schematic at the top of the figure shows topologies informative on gene flow from Eurasian into Iberian lynx. An excess of genomic windows returning topologies where the ancient Iberian lynx is in a basal position relative to the number of genomic windows retuning topologies where the contemporary Iberian lynx is basal indicates gene flow from Eurasian lynx onto the modern Iberian lynx population, above that occurring into the ancient Iberian lynx population. The lower part of the figure shows individual results (points) generated using each combination of one contemporary Iberian lynx (30 individuals total) and one of the two Eurasian lynx as representative for the two main Eurasian clades. An excess (mean 1.84-fold higher) of topologies with the ancient Iberian lynx in the basal position in all comparisons indicates that the admixture inferred using D statistics can be attributed, at least in part, to gene flow from Eurasian lynx into ancestors of contemporary Eurasian lynx.

Extended Data Table 1 List of ancient Iberian lynx samples used in this study
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Extended Data Table 2 Observed individual heterozygosity of Iberian lynx ancient and modern samples
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Extended Data Table 3 Genetic diversity in ancient and modern populations
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Extended Data Table 4 List of contemporary Iberian lynx and Eurasian lynx samples used in this study
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Extended Data Table 5 Statistics of ancient read mapping to Iberian lynx and domestic cat reference genome
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Lucena-Perez, M., Paijmans, J.L.A., Nocete, F. et al. Recent increase in species-wide diversity after interspecies introgression in the highly endangered Iberian lynx. Nat Ecol Evol 8, 282–292 (2024). https://doi.org/10.1038/s41559-023-02267-7

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  • DOI: https://doi.org/10.1038/s41559-023-02267-7

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