Gene Introgression among Closely Related Species in Sympatric Populations: A Case Study of Three Walnut (Juglans) Species

Dang Dang,Zhang Zhang,Zhao Zhao,Yue Yue

doi:10.3390/f10110965

Abstract

Gene introgression usually results from natural hybridization occurring among closely related species in sympatric populations. In this study, we discussed two rare and frequent gene flow phenomena between three species of Juglans plants and analyzed the possible causes for the difference. We collected 656 individuals from 40 populations of Persian walnut (Juglans regia L.), Chinese walnut (J. cathayensis Dode), and Iron walnut (J. sigillata Dode) that were genotyped at 17 expressed sequence tag simple sequence repeat (EST-SSR) loci to analyze the introgressions between J. regia and J. cathayensis, and J. regia and J. sigillata. Our study compared the spatial patterns of expected heterozygosity (HE), allelic richness (Rs), and private allele richness (PAR) so as to vividly infer the biogeographic history of related species of Juglans in the two regions. The results of the PCoA, UPGMA, and STRUCTURE analyses showed that all J. regia and J. sigillata populations clustered into one group, and the J. cathayensis populations clustered into the other group. The results of the historical gene flow analysis indicated that J. regia and J. sigillata have no genetic barriers, and the directional gene flow is mainly from J. regia to J. sigillata. For the three species of Juglans, all the above results indicated that gene flow was common among the same group of Juglans, and only rare and low-level gene flow appeared in distinct groups. Therefore, our study revealed multiple phenomena of gene flow and introgression among closely related species in sympatric populations, thereby providing a theoretical basis for the genetic evolution of the genus Juglans.

Highlights

Interspecies introgression can cause base substitution and deletion of DNA fragments, leading to a decrease in species specificity, which is likely to promote adaptive evolution of the infiltrated species [1,2,3]
Genetic diversity estimates varied among the microsatellite loci (Table S1) and among the population (Table 1)
The results of the STRUCTURE analysis (Figures 4 and 5), the unweighted pair-group method with an arithmetic means (UPGMA) tree (Figure 4c), principal coordinate analysis (PCoA) (Figure 4e), and the historical gene flow analysis (Table 3) indicate that gene introgression is common among the same groups of Juglans, as only rare and low-level gene introgression appears in distinct groups

Summary

Introduction

Interspecies introgression can cause base substitution and deletion of DNA fragments, leading to a decrease in species specificity, which is likely to promote adaptive evolution of the infiltrated species [1,2,3]. Interspecific hybridization occurs frequently in sympatric forest trees. Nuclear DNA sequences can be used to differentiate among closely related lineages, to clarify cases of sympatric speciation, and to identify hybrid individuals [4,5,6,7]. Studies have shown that hybridization and gene flow between species occur extensively in the genus Populus [8,9,10,11,12]. One of these studies showed that Populus × jrtyschensis is typical of F1 dominated hybrid zones between the distantly related species, P. nigra and P. laurifolia [12].

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Discussion

Conclusion