1 Introduction

Eucommia ulmoides, commonly known as the Hardy Rubber Tree, is a dioecious tree species endemic to China and the sole extant species of the family Eucommiaceae. This species is of significant ecological and economic importance due to its medicinal properties and industrial applications. Traditionally, E. ulmoides has been utilized in Chinese herbal medicine (He et al., 2014; Wang et al., 2019), and its bark is a source of gutta-percha, a material used in various industrial applications (Zhang et al., 2013). Despite its value, the natural populations of E. ulmoides have been declining due to overharvesting and habitat destruction, making its conservation a priority (Zhang et al., 2016; Wang et al., 2023).

Population genetics plays a crucial role in the conservation of E. ulmoides by providing insights into its genetic diversity, population structure, and evolutionary history. Understanding the genetic variation within and among populations is essential for developing effective conservation strategies. Studies have shown that E. ulmoides exhibits high genetic diversity within populations, which is likely due to its outcrossing mating system and long-distance gene flow facilitated by seed exchange among local farmers (Yu et al., 2015; Wang et al., 2018). However, there is also evidence of genetic bottlenecks and reduced genetic diversity in certain populations, particularly those that are artificially cultivated (Wu et al., 2011; Yu et al., 2015). These findings underscore the need for targeted conservation efforts to preserve the genetic resources of this endangered species.

This study is to synthesize current knowledge on the population genetics of Eucommia ulmoides and to discuss the implications for its conservation. This study will cover various aspects of genetic diversity, population structure, and phenotypic variation in E. ulmoides, drawing on data from multiple genetic studies employing different molecular markers such as microsatellites, ISSR, SRAP, and SNPs. By integrating these findings, we aim to provide a comprehensive understanding of the genetic landscape of E. ulmoides and to propose informed conservation strategies that can help mitigate the risks of genetic erosion and ensure the long-term survival of this valuable species.

2 Biology and Ecology of Eucommia ulmoides

2.1 Description of the species: morphology, distribution, and habitat preferences

Eucommia ulmoides is commonly known as the Hardy Rubber Tree. Morphologically, it is characterized by its broad, ovate leaves, which exhibit significant phenotypic variation in traits such as leaf thickness and size (Wang et al., 2023). The tree produces small, inconspicuous flowers, with male and female inflorescences that greatly vary (Figure 1) (Du et al., 2023). E. ulmoides is typically found in mountainous regions, with its natural populations primarily distributed across the Wuling Mountains and other northern mountainous areas in China. The species shows a preference for temperate climates with adequate rainfall, which significantly influences its phenotypic traits such as leaf, fruit, and seed size (Deng et al., 2021).

Figure 1 Morphological characteristic of Eucommia ulmoides (Adopted from Du et al., 2023) Image caption: (A) Mature plant, (B) male inflorescence, (C) female inflorescence, (D) fruit (Adopted from Du et al., 2023)

2.2 Reproductive biology and life cycle

E. ulmoides is a dioecious species, meaning that individual trees are either male or female (Wang and Zhang, 2017), and their sexes can be identified by flower traits (Figure 2) (Wang et al., 2020). This reproductive strategy necessitates cross-pollination for seed production, contributing to the high genetic diversity observed within populations. The life cycle of E. ulmoides begins with seed germination, followed by a prolonged juvenile phase before reaching reproductive maturity. The species exhibits high longevity, which, along with its outcrossing mating system, supports substantial genetic variation within populations. The development of high-density genetic maps and the identification of quantitative trait loci (QTLs) associated with growth traits have provided insights into the genetic mechanisms underlying its growth and reproductive traits (Liu et al., 2022).

Figure 2 Male (♂) and female (♀) individuals of Eucommia ulmoides distinguished by flowers (Zhao et al. unpublish data)

2.3 Ecological roles and interactions within its native environment

E. ulmoides plays a significant ecological role in its native habitats. It contributes to the stability of mountainous ecosystems by providing wind shelter and aiding in sand fixation, which helps prevent soil erosion (Jin et al., 2020). The tree also supports local biodiversity by offering habitat and food resources for various animal species. Additionally, E. ulmoides has been widely cultivated for its medicinal and industrial value, which has led to extensive gene flow and seed exchange among local farmers, further enhancing its genetic diversity (Zhang et al., 2013). The species’ ecological interactions and its role in traditional Chinese medicine underscore its importance in both natural and human-modified environments (Wang et al., 2018).

3 Genetic Diversity in Eucommia ulmoides

3.1 Overview of population genetics and its relevance to conservation

Population genetics is a field of biology that studies the distribution and changes of allele frequencies within populations, as influenced by evolutionary processes such as mutation, natural selection, genetic drift, and gene flow (Ottenburghs et al., 2019). Understanding the genetic diversity within and among populations of a species is crucial for conservation efforts, as it provides insights into the species' ability to adapt to environmental changes and resist diseases (Ghani et al., 2022). For endangered species like Eucommia ulmoides, which is valued for its medicinal and industrial uses, maintaining genetic diversity is essential to ensure its long-term survival and adaptability (Wang et al., 2023).

3.2 Studies on genetic diversity in Eucommia ulmoides populations

Several studies have investigated the genetic diversity of Eucommia ulmoides using various molecular markers. For instance, microsatellite markers revealed a high level of genetic diversity within populations (HE = 0.716) and slight differentiation among populations (FST = 0.063), suggesting significant gene flow mediated by seed exchange among local farmers (Zhang et al., 2013). Another study using RAPD analysis found a high percentage of polymorphic loci (96.36%), indicating substantial genetic variation within the species (Wang et al., 2006). ISSR and SRAP markers also demonstrated high genetic diversity at the species level (PPB = 85.54%) but lower diversity at the population level (PPB = 36.99%) (Wu et al., 2011). These findings highlight the importance of both intraspecific and interspecific genetic diversity for the conservation of E. ulmoides (Yu et al., 2015).

3.3 Factors influencing genetic diversity

Genetic diversity in Eucommia ulmoides is influenced by several factors, including habitat fragmentation, population size, and human activities. Habitat fragmentation can lead to smaller, isolated populations, which may reduce genetic diversity due to inbreeding and genetic drift. For example, a study on the genetic diversity of cultivated E. ulmoides in Guizhou Province found that genetic differentiation within populations was greater than among populations, suggesting that habitat fragmentation and limited gene flow could be contributing factors (Xiao et al., 2014). Additionally, the exchange of seeds among local farmers has been shown to play a significant role in maintaining genetic diversity and reducing genetic differentiation among populations. Population size also affects genetic diversity; smaller populations are more susceptible to genetic bottlenecks, which can reduce genetic variation and increase the risk of extinction (Wu et al., 2011).

4 Molecular Markers and Genetic Analysis

4.1 Types of molecular markers USED in Eucommia ulmoides genetic studies

In genetic studies of Eucommia ulmoides, various molecular markers have been employed to assess genetic diversity and population structure, with microsatellites (SSRs), single nucleotide polymorphisms (SNPs), inter-simple sequence repeats (ISSRs), sequence-related amplified polymorphism (SRAP), and amplified fragment length polymorphism (AFLP) being the primary types. Microsatellites, or SSRs, are highly polymorphic and widely used; for instance, 1 568 SSRs were identified using next-generation sequencing, leading to the development of 16 polymorphic SSR markers (Zhang et al., 2016). Another study successfully developed 23 microsatellite markers, with 19 proving to be polymorphic. SNP markers have been instrumental in constructing high-density genetic maps, with a study identifying 191 095 SNPs and using 10 103 SNP markers to cover 90% of the E. ulmoides genome.

ISSR markers have been utilized to analyze genetic diversity and structure, revealing significant genetic variation within and among populations (Wu et al., 2011). Additionally, SRAP markers have been employed to study genetic diversity and relationships among E. ulmoides populations, while AFLP markers, often used in conjunction with other markers, have estimated genetic diversity and relationships among cultivars (Li et al., 2014). These diverse molecular markers have collectively advanced our understanding of the genetic landscape of E. ulmoides.

4.2 Applications of molecular markers in assessing genetic diversity and structure

Molecular markers have played a crucial role in assessing the genetic diversity and structure of Eucommia ulmoides populations. Studies utilizing microsatellite markers have revealed significant genetic diversity within these populations, with expected heterozygosity values ranging from 0.054 to 0.874. Additionally, ISSR and SRAP markers have demonstrated high polymorphism rates, underscoring the substantial genetic variation present (Yu et al., 2015). In terms of population structure analysis, molecular markers, such as ISSR, have shown significant differentiation among populations, with AMOVA indicating that the majority of genetic variation exists within populations. Moreover, SNP markers have been employed to construct genetic maps and identify quantitative trait loci (QTLs) associated with growth traits, offering deeper insights into the genetic structure of E. ulmoides.

The genetic data obtained from these molecular marker studies are also pivotal for informing conservation strategies for E. ulmoides. The identification of genetic bottlenecks and the observation of high genetic diversity within populations are particularly important for preserving the genetic resources of this species. These findings provide essential guidance for developing effective conservation strategies aimed at maintaining the genetic integrity of E. ulmoides (Zhang et al., 2013; Yu et al., 2015).

4.3 Case Examples of genetic studies in Eucommia ulmoides

Several studies have highlighted the use of molecular markers in genetic research on Eucommia ulmoides. For instance, researchers developed 16 polymorphic SSR markers using next-generation sequencing to assess genetic diversity and population structure in E. ulmoides. Additionally, another study developed 23 microsatellite markers, 19 of which were polymorphic, providing essential tools for genetic studies. Furthermore, research using eight microsatellite markers revealed high genetic diversity within populations and slight differentiation among populations, suggesting long-distance gene flow mediated by seed exchange. Conversely, another study using ISSR markers found lower genetic diversity in artificial populations compared to wild populations, highlighting the impact of human activities on genetic variation.

In more in-depth research, the researchers updated the genetic linkage map of Eucommia ulmoides using single nucleotide polymorphism (SNP) markers and conducted quantitative trait loci (QTL) analysis related to growth traits. This study revealed multiple QTLs associated with tree height, ground diameter, and crown diameter, providing new insights into the genetic mechanisms underlying growth traits in Eucommia ulmoides (Jin et al., 2020). Additionally, Wang and Zhang (2017) conducted a study on the sexual dimorphism and genetic mechanisms of sex determination in Eucommia ulmoides. They validated and annotated all assembled single genes. Through comparative transcriptome analysis, they detected 116 differentially expressed genes (DEGs) between males and females, including 73 male-biased genes and 43 female-biased genes.

5 Population Structure and Gene Flow

5.1 Analysis of population structure in Eucommia ulmoides

The population structure of Eucommia ulmoides has been extensively studied using various molecular markers (Wang et al., 2023). Studies utilizing microsatellite markers have revealed that populations of E. ulmoides exhibit high genetic diversity within populations (HE = 0.716) and low differentiation among populations (FST = 0.063). This pattern is supported by analysis of molecular variance (AMOVA), which indicates that 94.05% of the total genetic variation resides within populations (Zhang et al., 2013). Similarly, research using inter-simple sequence repeat (ISSR) and sequence-related amplified polymorphism (SRAP) markers has shown that a significant portion of genetic variation is found within populations, with 88.8% and 92.4% of the total variation residing within populations, respectively. These findings suggest that E. ulmoides populations are not highly structured and that there is substantial genetic exchange among them.

5.2 Gene flow and its role in maintaining genetic diversity

Gene flow plays a crucial role in maintaining the genetic diversity of E. ulmoides. The high level of genetic diversity observed within populations can be attributed to factors such as the species' highly outcrossed mating system, high longevity, and seed admixture. Long-distance gene flow, likely mediated by the exchange of seeds by local farmers, has been identified as a significant factor contributing to the genetic homogeneity among populations (Yu et al., 2015). This extensive gene flow helps to prevent genetic drift and inbreeding, thereby maintaining the overall genetic health and adaptability of the species.

5.3 Implications of restricted gene flow on population viability

Restricted gene flow can have detrimental effects on the viability of E. ulmoides populations. When gene flow is limited, populations may become genetically isolated, leading to reduced genetic diversity and increased genetic differentiation. This can result in inbreeding depression and a decreased ability to adapt to environmental changes. Studies have shown that artificial populations of E. ulmoides exhibit decreased genetic diversity and increased genetic differentiation compared to wild populations, highlighting the negative impact of restricted gene flow (Wu et al., 2011). Conservation strategies should therefore focus on promoting gene flow among populations to ensure the long-term viability and resilience of E. ulmoides.

6 Threats to Eucommia ulmoides Populations

6.1 Habitat loss and degradation

Habitat loss and degradation pose significant threats to Eucommia ulmoides populations. The natural habitats of this species are increasingly being encroached upon by human activities such as urbanization, agriculture, and industrial development. These activities lead to the fragmentation of habitats, which in turn reduces the available space for E. ulmoides to grow and reproduce. The degradation of habitat quality, including soil erosion and pollution, further exacerbates the challenges faced by this species. The phenotypic variation observed in different populations of E. ulmoides is influenced by geographic and climatic factors, indicating that habitat changes can significantly impact the genetic diversity and adaptability of the species (Wang et al., 2023).

6.2 Overharvesting and its impact on population dynamics

Overharvesting is another critical threat to Eucommia ulmoides. This species has been extensively harvested for its medicinal properties and industrial uses, particularly in the late 20th century. The widespread and long-term harvesting has led to a decline in natural populations, making the species endangered. The genetic diversity studies reveal that while there is a high level of genetic variation within populations, the overharvesting has caused a genetic bottleneck in some populations, reducing their resilience and adaptability (Zhang et al., 2013). The exchange of seeds by local farmers has facilitated long-distance gene flow, which has somewhat mitigated the genetic differentiation among populations, but the overall impact of overharvesting remains a significant concern (Zhang et al., 2013).

6.3 Climate change and other environmental stressors

Climate change and other environmental stressors are increasingly threatening Eucommia ulmoides populations. Changes in temperature and precipitation patterns can alter the growth conditions for this species, affecting its phenotypic traits such as leaf, fruit, and seed size (Wang et al., 2023). The genetic studies indicate that average annual temperature and rainfall are major factors influencing phenotypic variation among populations (Wang et al., 2023). Additionally, environmental stressors such as pollution and invasive species can further strain the already vulnerable populations of E. ulmoides. The genetic structure analysis shows significant differentiation among populations, suggesting that environmental changes could lead to further genetic isolation and reduced genetic diversity (Wu et al., 2011). The development of molecular markers and genetic maps can aid in understanding the genetic mechanisms underlying these stress responses and inform conservation strategies (Wang et al., 2018; Liu et al., 2022).

7 Case Study: Conservation Genetics of Eucommia ulmoides in a Specific Region

7.1 Overview of the selected region and its significance for Eucommia ulmoides

The Wuling Mountains region in China is a significant area for the conservation of Eucommia ulmoides, a relict tree species endemic to China. This region is characterized by its unique geoclimatic conditions, which have contributed to the phenotypic variation observed in natural populations of E. ulmoides. The Wuling Mountains are home to several natural populations of this species, making it a critical area for studying genetic diversity and implementing conservation strategies (Wang et al., 2023).

7.2 Genetic studies conducted in this region

Several genetic studies have been conducted in the Wuling Mountains to understand the genetic diversity and structure of E. ulmoides populations. One study analyzed phenotypic variation in leaf, fruit, and seed traits across ten natural populations, revealing significant phenotypic differentiation correlated with geographic and climatic distances (Figure 3) (Wang et al., 2023). Another study utilized microsatellite markers to investigate genetic diversity in both semi-wild and cultivated populations, finding high genetic diversity within populations and slight differentiation among them, likely due to long-distance gene flow mediated by seed exchange (Zhang et al., 2013). Additionally, inter-simple sequence repeat (ISSR) markers were used to analyze genetic diversity and structure, revealing low genetic diversity at the population level but high diversity at the species level, with significant differentiation among populations (Wu et al., 2011).

Figure 3 The correlation between Eucommia ulmoides phenotypes and geographic and climatic distances (Adapted from Wang et al., 2023) Image caption: A: The relationships of the pairwise geographic (a) and climatic distances (b) with the phenotypic differences among populations; B: Correlation analysis among climate and PCs. Blue and maroon color represent positive and negative correlation. The darker the color, the stronger the correlation (* p < 0.05; ** p < 0.01; *** p < 0.001); C: Visual representation of sampled fruit and measured morphometric traits: FVD - Fruit vertical diameter; FHD - Fruit horizontal diameter; FLD - Fruit lateral diameter. (B) Visual representation of sampled seed and measured morphometric traits: SVD - Seed vertical diameter; SHD - Seed horizontal diameter; SLD - Seed lateral diameter. (C) Visual representation of sampled leaf and measured morphometric traits: LL - Leaf length; LW - Leaf width; PL - Petiole length (Adopted from Wang et al., 2023)

7.3 Conservation challenges and strategies implemented in the region

The primary conservation challenges for E. ulmoides in the Wuling Mountains include habitat fragmentation, genetic bottlenecks, and the impact of artificial cultivation on genetic diversity. The high level of genetic variation within populations suggests that conservation efforts should focus on maintaining this diversity to ensure the species’ long-term survival (Zhang et al., 2013). Strategies implemented in the region include the use of molecular markers to monitor genetic diversity and structure, the development of high-density genetic maps to facilitate breeding programs, and the identification of quantitative trait loci (QTLs) associated with growth traits to improve genetic improvement efforts (Jin et al., 2020; Liu et al., 2022). Additionally, conservation strategies emphasize the importance of protecting natural habitats and promoting sustainable harvesting practices to mitigate the impact of human activities on genetic diversity.

8 Conservation Strategies for Eucommia ulmoides

8.1 In situ conservation

In situ conservation involves protecting and managing Eucommia ulmoides within its natural habitat. This strategy is crucial for maintaining the genetic diversity and ecological interactions of the species (Xie et al., 2023). Studies have shown significant phenotypic variation within and among natural populations of E. ulmoides, which is influenced by geographic and climatic factors (Wang et al., 2023). By preserving these natural habitats, we can ensure the continued evolution and adaptation of the species to changing environmental conditions (Deng et al., 2022). Additionally, in situ conservation helps maintain the ecological balance and supports other species that coexist with E. ulmoides.

8.2 Ex situ conservation

Ex situ conservation strategies involve the preservation of Eucommia ulmoides outside its natural habitat. This can include the establishment of seed banks, botanical gardens, and controlled cultivation programs (Fant et al., 2016). The high genetic diversity observed within populations of E. ulmoides, despite a genetic bottleneck in one population, underscores the importance of ex situ conservation to safeguard against potential threats in the wild (Zhang et al., 2013). By maintaining a diverse genetic pool in controlled environments, we can facilitate future reintroduction and restoration efforts if natural populations decline (Ensslin et al., 2011).

8.3 The role of community involvement and sustainable use practices

Community involvement and sustainable use practices are essential for the long-term conservation of Eucommia ulmoides. Local communities play a vital role in the conservation of this species through traditional knowledge and sustainable harvesting practices. The exchange of seeds by local farmers has been identified as a key factor in maintaining genetic diversity and facilitating long-distance gene flow (Calvet-Mir et al., 2012; Zhang et al., 2013). Encouraging sustainable use practices, such as controlled harvesting and cultivation, can help reduce the pressure on wild populations while providing economic benefits to local communities (Tian, 2015). Education and awareness programs can further enhance community participation in conservation efforts, ensuring the protection and sustainable use of E. ulmoides for future generations.

9 Future Directions in Research and Conservation

9.1 Advances in genomic tools and their application to conservation genetics

The advent of genomic tools has revolutionized the field of conservation genetics, providing unprecedented insights into the genetic diversity and evolutionary potential of species. The complete genome sequences from thousands of species will soon be available, transforming our understanding of genetic variation in natural populations and its functional significance (Allendorf et al., 2010). These advancements enable the identification of specific genomic regions associated with adaptive traits, which is crucial for the conservation of endangered species like Eucommia ulmoides. For instance, the development of high-density genetic maps using single-nucleotide polymorphism (SNP) markers has facilitated the identification of quantitative trait loci (QTLs) associated with growth traits in E. ulmoides, providing a solid foundation for future breeding and conservation efforts (Jin et al., 2020; Liu et al., 2022). Additionally, the use of whole-genome comparisons has revealed heterogeneous divergence and mutation hotspots in the chloroplast genome of E. ulmoides, highlighting potential molecular markers for population genetics studies (Wang et al., 2018).

9.2 The potential for genetic rescue and assisted gene flow

Genetic rescue, which involves introducing new alleles to increase population growth, has shown significant benefits in reversing population declines in various species. This approach can be particularly beneficial for small, isolated populations of E. ulmoides suffering from inbreeding depression. Genomic tools can enhance the implementation and monitoring of genetic rescue by identifying populations that would benefit most from augmented gene flow and by predicting the outcomes of such interventions (Fitzpatrick and Funk, 2021). Meta-analyses have demonstrated that outcrossing inbred populations results in substantial fitness benefits, with a median increase in composite fitness of 148% in stressful environments (Frankham, 2015). However, uncertainties remain regarding the magnitude and duration of these benefits, necessitating further research to optimize genetic rescue strategies (Bell et al., 2019).

9.3 The importance of integrating genetic data

Integrating genetic data into conservation strategies is essential for the effective management of endangered species like E. ulmoides. Studies have shown that genetic diversity within populations of E. ulmoides is high, likely due to its outcrossed mating system and long-distance gene flow mediated by seed exchange. This genetic diversity is crucial for the species' adaptability to environmental changes and should be a key consideration in conservation planning. Moreover, phenotypic variation in traits such as leaf, fruit, and seed size has been linked to geoclimatic factors, suggesting that conservation efforts should also account for environmental heterogeneity (Wang et al., 2023). By combining genetic and phenotypic data, conservationists can develop more targeted and effective strategies to preserve the genetic resources of E. ulmoides.

10 Concluding Remarks

This study has highlighted the intricate population genetics of Eucommia ulmoides and its significance in formulating effective conservation strategies. Key findings indicate that despite the high genetic diversity observed within populations, the species faces substantial threats from habitat loss, overharvesting, and climate change. The high levels of genetic diversity within populations, largely maintained through outcrossing and long-distance gene flow, underscore the species' resilience. However, the presence of genetic bottlenecks in some populations points to the critical need for targeted conservation efforts to preserve this genetic richness.

The implications of these findings extend beyond E. ulmoides, providing valuable insights for the conservation of other species facing similar threats. The successful integration of molecular tools in identifying genetic diversity and population structure can serve as a model for broader conservation strategies. The importance of maintaining genetic diversity through both in situ and ex situ conservation methods, coupled with the promotion of sustainable use practices, is critical for the survival of endangered species in the face of ongoing environmental pressures.

To ensure the long-term survival of Eucommia ulmoides, it is imperative that conservation efforts are informed by comprehensive genetic data and are adaptive to the changing environmental landscape. By safeguarding its genetic diversity and promoting sustainable practices, we can enhance the species' resilience and secure its future. Continued research and monitoring are essential to refining these strategies, ensuring that E. ulmoides remains a viable component of its natural ecosystem and continues to provide its ecological and economic benefits for generations to come.

Acknowledgments

EcoEvo Publisher extends sincere thanks to two anonymous peer reviewers for their feedback on the manuscript.

Funding

This work was supported by Guizhou Academy of Agricultural Sciences Talent Special Project (No. 2023-02 and No. 2024-02), National High Tech nology Research and Development Program of China (“863” Program) [grant number 2013AA102605-05], National Major Project of Cultivating New Varieties of Genetically Modified Organisms [grant no. 2016ZX08010003009]. Talent Base for Germplasm Resources Utilization and Innovation of Characteristic Plant in Guizhou (RCJD2018-14).

Conflict of Interest Disclosure

The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

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