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Genome-wide analyses of introgression between two sympatric Asian oak species

Abstract

Introgression can be an important source of new alleles for adaption under rapidly changing environments, perhaps even more important than standing variation. Though introgression has been extensively studied in many plants and animals, key questions on the underlying mechanisms of introgression still remain unanswered. In particular, we are yet to determine the genomic distribution of introgressed regions along the genome; whether the extent and patterns of introgression are influenced by ecological factors; and when and how introgression contributes to adaptation. Here, we generated high-quality genomic resources for two sympatric widespread Asian oak species, Quercus acutissima and Q. variabilis, sampled in multiple forests to study introgression between them. We show that introgressed regions are broadly distributed across the genome. Introgression was affected by genetic divergence between pairs of populations and by the similarity of the environments in which they live—populations occupying similar ecological sites tended to share the same introgressed regions. Introgressed genomic footprints of adaptation were preferentially located in regions with suppressed recombination rate. Introgression probably confers adaptation in these oak populations by introducing allelic variation in cis-regulatory elements, in particular through transposable element insertions, thereby altering the regulation of genes related to stress. Our results provide new avenues of research for uncovering mechanisms of adaptation due to hybridization in sympatric species.

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Fig. 1: The distribution ranges, phylogenetic and admixture analyses and demographic inference.
Fig. 2: The distributions of genome-wide introgression for two sympatric oak species and its correlation with geographic and environmental distances.
Fig. 3: The distribution of adaptive introgressed SNPs across the genome and its correlation with population recombination rate.
Fig. 4: The numbers of adaptive introgressed SNPs and genes harbouring them associated with different environmental factors and their functions in GO terms.

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Data availability

All sequencing data used in this study have been deposited in NCBI SRA database with the Bioproject number PRJNA763710 for the reference genome, PRJNA765790 for population resequencing libraries and PRJNA762601 for the RNA-seq libraries. The reference genome and gene annotations have also been deposited in the Genome Warehouse in National Genomics Data Center (https://ngdc.cncb.ac.cn/gwh) under the accession number GWHBGBO00000000. Figures 14 have associated source data at https://github.com/cjevol/protocols-for-introgression-in-oaks. There are no restrictions on data availability.

Code availability

All codes used for main analyses in this paper are available for download from https://github.com/cjevol/protocols-for-introgression-in-oaks and zenodo (https://doi.org/10.5281/zenodo.5726659).

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Acknowledgements

This project was supported by National Natural Science Foundation of China (31972946) and the Fundamental Research Funds for the Central Universities 2-2050205-21-688 granted to J.C.

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Contributions

J.C. conceived the research. All analyses were performed by R.F., with contributions to chromosome inversion analysis and gene expression analysis from Y.Z. and Y. Liu, respectively. Y.Z., Y.F., R.-S.L., Y. Li. and P.L. contributed plant material collection. R.F., J.C., A.K. and M.L. wrote the manuscript.

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Correspondence to Jun Chen.

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Extended data

Extended Data Fig. 1

Admixture plots with K values from 2 to 4.

Extended Data Fig. 2 The correlation between environmental distance and geographic distance.

Shaded areas represent 95% confidence intervals. Each dot represents one population pairs. Statistical significance was determined by Mantel test based on Pearson’s product-moment correlation with two-sided and multiple comparisons was performed. Adjusted R2 and significance of the correlation (p-value) are shown for plot.

Extended Data Fig. 3 FST distribution for allopatric (red) and sympatric (blue) Q. acutissima -Q. variabilis pairs examined in ABBA analyses.

Populations were labelled in ((P1, P2), P3) order. Significance shows introgression has lowered the genetic divergence between sympatric species. Statistical significance was determined by T-test with two-sided and multiple comparisons was performed (p-values: * ≤ 0.05, **≤ 0.01, ***≤ 0.001, **** ≤ 0.0001). Specifically, Adjusted P-values = 8.9E-249, 1.9E-134, 4.6E-249, 1.1E-128, 0, 0.58, 1.1E-4, 0, 4.1E-5, 0 from BWL_KYS_KY to LFS_TBS_TB, respectively. The box plots were based on n=72,866 sliding windows for all Q. acutissima -Q. variabilis pairs (from BWL_KYS_KY to LFS_TBS_TB). The central lines, box limits, whiskers and the top and bottom ends show the median values, upper and lower quartiles, 1.5× the interquartile ranges, and the maximum and minimum values, respectively.

Extended Data Fig. 4

The distribution of population recombination rate (rho = 4Ner) for all chromosomes.

Extended Data Fig. 5

The cross-validation errors against K values in Admixture analysis.

Extended Data Fig. 6 The comparison of FST matrix and covariance matrix for Q. acutissima.

FST matrix of Q. acutissima populations (left) and the covariance matrix of Q. acutissima populations (right).

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Fu, R., Zhu, Y., Liu, Y. et al. Genome-wide analyses of introgression between two sympatric Asian oak species. Nat Ecol Evol 6, 924–935 (2022). https://doi.org/10.1038/s41559-022-01754-7

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