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Comparative phylogeography of Juglans regia and J. mandshurica combining organellar and nuclear DNA markers to assess genetic diversity and introgression in regions of sympatry

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By comparing the phylogeography of Juglans regia and J. mandshurica, we found that two walnut species, even when sympatric, rarely introgress, suggesting that strong hybridization barriers exist between these species.

Abstract

The biogeographic investigation of temperate walnut (Juglans) trees is of great interest because of their ecological and economical importance. Our goal was to perform an in-depth investigation of the genetic and phylogeographic history of J. regia and J. mandshurica, two walnut species that are sympatric in parts of their ranges, including tests for gene flow and incomplete lineage sorting. We employed a 234 bp locus of mitochondrial DNA, a 1.8 Kbp locus of chloroplast DNA, 3 nuclear loci totaling 1740 bp in length, and 17 EST-SSRs. We sampled 559 individuals, 332 of J. regia and 227 of J. mandshurica, from 69 locations. We found that J. regia and J. mandshurica, even when sympatric, rarely introgress, suggesting that strong barriers to hybridization exist between these species. Niche overlap analyses for the two species found that they occupy distinct ecological niches and that the sympatric populations may be the result of recent postglacial population expansion.

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Acknowledgements

We thank Nan Hou, Yiheng Hu, Tao Zhou, and Lei Wang for assisting with sampling. Mention of a trademark, proprietary product, or vendor does not constitute a guarantee or warranty of the product by the U.S. Department of Agriculture and does not imply its approval to the exclusion of other products or vendors that also may be suitable.

Funding

This work was supported by the National Natural Science Foundation of China (32,070,372, 41,471,038, and 31,200,500), Shaanxi Academy of Science Research Funding Project (2019 K-06), the Natural Science Foundation of Shaanxi Province of China (2019JM-008), the Opening Foundation of the Key Laboratory of Resource Biology and Biotechnology in Western China (Northwest University), the Ministry of Education (ZSK2018009), and the Program for Excellent Young Academic Backbones, funded by Northwest University.

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  1. Meng Dang and Hui-Juan Zhou contributed equally to this paper.

Authors and Affiliations

  1. Key Laboratory of Resource Biology and Biotechnology in Western China, Ministry of Education, College of Life Sciences, Northwest University, Xi’an, 710069, Shaanxi, China

    Meng Dang, Ming Yue, Yi Zhang, Gui-Fang Zhao & Peng Zhao

  2. College of Forestry, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Hui-Juan Zhou & Shuo-Xin Zhang

  3. USDA Forest Service Hardwood Tree Improvement and Regeneration Center (HTIRC), Department of Forestry and Natural Resources, Purdue University, 715 West State Street, West Lafayette, Indiana, 47907, USA

    Keith E. Woeste

  4. Xi’an Botanical Garden of Shaanxi Province, Xi’an, Shaanxi, People’s Republic of China

    Ming Yue

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  1. Meng Dang
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Correspondence to Peng Zhao.

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Supplementary Information

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468_2021_2167_MOESM1_ESM.tif

Supplementary Fig. S1 Geographic distribution of sequence in variation in J. regia and J. mandshurica at the (nuclear) 15R-8 sequence. a Locations where more than one allele per population was encountered are represented as pie charts that show the proportion of each allele. We added a black border to the pie chart of J. mandshurica. b The network of genealogical relationships for the 81 alleles at 15R-8 found among all samples in this study. The black lines show the connections inferred between the alleles, based on parsimonious mutation models. The size of the circles is roughly proportional to the number of alleles of that type encountered; the smallest circles represent one tree each. Abbreviations for samples, numbers of populations, and sampling details are in Table 1. (TIF 14115 KB)

468_2021_2167_MOESM2_ESM.tif

Supplementary Fig. S2 Geographic distribution of sequence in variation in J. regia and J. mandshurica based on Jr5680 sequence data. a Geographical distribution of the haplotypes of all sampled locations in China. The green and amber circles (single color and number inside) indicate the population contained only one haplotype. We added a black border to the pie chart of J. mandshurica. b The network of genealogical relationships among the 22 haplotypes found in this study. Black lines show the connections inferred between the haplotypes, based on parsimonious mutation models. The size of circles for haplotypes is roughly proportional to the number of samples with the indicated haplotype. The remaining haplotypes represent one tree each. (TIF 20723 KB)

468_2021_2167_MOESM3_ESM.tif

Supplementary Fig. S3 Using MEGA 6.0 (Tamura et al. 2013) to construct the maximum likelihood (ML) phylogenetic tree based on the nuclear DNA (ITS, 15R-8, and Jr5680) sequences, with 1,000 bootstrap replicates. (TIF 25337 KB)

468_2021_2167_MOESM4_ESM.tif

Supplementary Fig. S4 Mismatch distribution analysis using mtDNA a, b, cpDNA c, d, and data on three types of nuclear DNA e‒j. a Mismatch distribution results of J. regia from mtDNA data; b Mismatch distribution results of J. mandshurica from mtDNA data; c Mismatch distribution results of J. regia from cpDNA data; d Mismatch distribution results of J. mandshurica from cpDNA data; e, g, i Mismatch distribution results of J. regia from nrDNA data ITS, 15R-8, and Jr5680, respectively. f, h, j Mismatch distribution results of J. mandshurica from nrDNA data ITS, 15R-8, and Jr5680, respectively (TIF 25337 KB)

468_2021_2167_MOESM5_ESM.docx

Supplementary Table S1 Details of sample locations and sample sizes in 77 populations in this study, and the number of samples analyzed for multiple DNA fragments. (DOCX 31 KB)

468_2021_2167_MOESM6_ESM.docx

Supplementary Table S2 The nine mitochondrial DNA markers, 18 chloroplast DNA markers, and 17 microsatellite markers used to scan all samples in this study. (DOCX 19 KB)

468_2021_2167_MOESM7_ESM.docx

Supplementary Table S3 Details of sample location, sample size and descriptive statistics of genetic variability for eight Juglans regia L. populations and eight Juglans mandshurica M. populations in China based on EST-SSRs data. (DOCX 21 KB)

468_2021_2167_MOESM8_ESM.docx

Supplementary Table S4 Information related to primers and genetic characteristics of 17 EST-SSR primers for 16 walnut populations used in this study. (DOCX 19 KB)

468_2021_2167_MOESM9_ESM.pdf

Supplementary Table S5 Genetic variable sites of eleven haplotypes based on mitochondrial DNA marker 3-9 dataset. (PDF 62 KB)

468_2021_2167_MOESM10_ESM.pdf

Supplementary Table S6 Genetic variable sites of 11 haplotypes based on chloroplast DNA marker trnL-F and trnS-G dataset. (PDF 128 KB)

Supplementary Table S7 Genetic variable sites of 22 haplotypes based on nrDNA ITS dataset. (PDF 129 KB)

Supplementary Table S8 Genetically variable sites comprising 81 haplotypes based on nrDNA 15r-8 dataset. (PDF 148 KB)

Supplementary Table S9 Genetically variable sites comprising 39 haplotypes based on nrDNA Jr5680 dataset. (PDF 112 KB)

468_2021_2167_MOESM14_ESM.docx

Supplementary Table S10 Estimated gene flow between sympatric J. regia vs J. mandshurica populations by Migtate 3.6.4. (DOCX 15 KB)

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Dang, M., Zhou, HJ., Woeste, K.E. et al. Comparative phylogeography of Juglans regia and J. mandshurica combining organellar and nuclear DNA markers to assess genetic diversity and introgression in regions of sympatry. Trees 35, 1993–2007 (2021). https://doi.org/10.1007/s00468-021-02167-y

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