Distinct hybridization modes in wide- and narrow-ranged lineages of Causonis (Vitaceae)
Abstract Background Explaining contrasting patterns of distribution between related species is crucial for understanding the dynamics of biodiversity. Despite instances where hybridization and whole genome duplication (WGD) can yield detrimental outcomes, a role in facilitating the expansion of dist...
| Main Authors: | , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2023-10-01
|
| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-023-01718-8 |
| _version_ | 1797556433271652352 |
|---|---|
| author | Jinren Yu Hong Zhao Yanting Niu Yichen You Russell L. Barrett Rindra Manasoa Ranaivoson Romer Narindra Rabarijaona Gaurav Parmar Langxing Yuan Xiaofeng Jin Pan Li Jianhua Li Jun Wen Zhiduan Chen Limin Lu |
| author_facet | Jinren Yu Hong Zhao Yanting Niu Yichen You Russell L. Barrett Rindra Manasoa Ranaivoson Romer Narindra Rabarijaona Gaurav Parmar Langxing Yuan Xiaofeng Jin Pan Li Jianhua Li Jun Wen Zhiduan Chen Limin Lu |
| author_sort | Jinren Yu |
| collection | DOAJ |
| description | Abstract Background Explaining contrasting patterns of distribution between related species is crucial for understanding the dynamics of biodiversity. Despite instances where hybridization and whole genome duplication (WGD) can yield detrimental outcomes, a role in facilitating the expansion of distribution range has been proposed. The Vitaceae genus Causonis exhibits great variations in species’ distribution ranges, with most species in the derived lineages having a much wider range than those in the early-diverged lineages. Hybridization and WGD events have been suggested to occur in Causonis based on evidence of phylogenetic discordance. The genus, therefore, provides us with an opportunity to for explore different hybridization and polyploidization modes in lineages with contrasting species’ distribution ranges. However, the evolutionary history of Causonis incorporating potential hybridization and WGD events remains to be explored. Results With plastid and nuclear data from dense sampling, this study resolved the phylogenetic relationships within Causonis and revealed significant cyto-nuclear discordance. Nuclear gene tree conflicts were detected across the genus, especially in the japonica-corniculata clade, which were mainly attributed to gene flow. This study also inferred the allopolyploid origin of the core Causonis species, which promoted the accumulation of stress-related genes. Causonis was estimated to have originated in continental Asia in the early Eocene, and experienced glaciation in the early Oligocene, shortly after the divergence of the early-divergent lineages. The japonica-corniculata clade mainly diversified in the Miocene, followed by temperature declines that may have facilitated secondary contact. Species distribution modeling based on current climate change predicted that the widespread C. japonica tends to be more invasive, while the endemic C. ciliifera may be at risk of extinction. Conclusions This study presents Causonis, a genus with complex reticulate evolutionary history, as a model of how hybridization and WGD modes differ in lineages of contrasting species’ geographic ranges. It is important to consider specific evolutionary histories and genetic properties of the focal species within conservation strategies. |
| first_indexed | 2024-03-10T17:01:50Z |
| format | Article |
| id | doaj.art-56d0a49b0acd4584a8ed89cbd666a9e1 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-03-10T17:01:50Z |
| publishDate | 2023-10-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-56d0a49b0acd4584a8ed89cbd666a9e12023-11-20T10:55:46ZengBMCBMC Biology1741-70072023-10-0121112110.1186/s12915-023-01718-8Distinct hybridization modes in wide- and narrow-ranged lineages of Causonis (Vitaceae)Jinren Yu0Hong Zhao1Yanting Niu2Yichen You3Russell L. Barrett4Rindra Manasoa Ranaivoson5Romer Narindra Rabarijaona6Gaurav Parmar7Langxing Yuan8Xiaofeng Jin9Pan Li10Jianhua Li11Jun Wen12Zhiduan Chen13Limin Lu14State Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, Chinese Academy of SciencesSchool of Life Science, Shanxi Normal UniversityChina National Botanical GardenState Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, Chinese Academy of SciencesNational Herbarium of New South Wales, Australian Botanic GardenState Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, Chinese Academy of SciencesState Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, Chinese Academy of SciencesNational Botanical GardenTropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural SciencesZhejiang Provincial Key Laboratory of Forest Aromatic Plants-Based Healthcare Functions/School of Forestry and Bio-Technology, Zhejiang A&F UniversityLaboratory of Systematic & Evolutionary Botany and Biodiversity, College of Life Sciences, Zhejiang UniversityBiology Department, Hope CollegeDepartment of Botany, National Museum of Natural History, MRC166, Smithsonian InstitutionState Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, Chinese Academy of SciencesState Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, Chinese Academy of SciencesAbstract Background Explaining contrasting patterns of distribution between related species is crucial for understanding the dynamics of biodiversity. Despite instances where hybridization and whole genome duplication (WGD) can yield detrimental outcomes, a role in facilitating the expansion of distribution range has been proposed. The Vitaceae genus Causonis exhibits great variations in species’ distribution ranges, with most species in the derived lineages having a much wider range than those in the early-diverged lineages. Hybridization and WGD events have been suggested to occur in Causonis based on evidence of phylogenetic discordance. The genus, therefore, provides us with an opportunity to for explore different hybridization and polyploidization modes in lineages with contrasting species’ distribution ranges. However, the evolutionary history of Causonis incorporating potential hybridization and WGD events remains to be explored. Results With plastid and nuclear data from dense sampling, this study resolved the phylogenetic relationships within Causonis and revealed significant cyto-nuclear discordance. Nuclear gene tree conflicts were detected across the genus, especially in the japonica-corniculata clade, which were mainly attributed to gene flow. This study also inferred the allopolyploid origin of the core Causonis species, which promoted the accumulation of stress-related genes. Causonis was estimated to have originated in continental Asia in the early Eocene, and experienced glaciation in the early Oligocene, shortly after the divergence of the early-divergent lineages. The japonica-corniculata clade mainly diversified in the Miocene, followed by temperature declines that may have facilitated secondary contact. Species distribution modeling based on current climate change predicted that the widespread C. japonica tends to be more invasive, while the endemic C. ciliifera may be at risk of extinction. Conclusions This study presents Causonis, a genus with complex reticulate evolutionary history, as a model of how hybridization and WGD modes differ in lineages of contrasting species’ geographic ranges. It is important to consider specific evolutionary histories and genetic properties of the focal species within conservation strategies.https://doi.org/10.1186/s12915-023-01718-8Distribution rangeCausonisHybridizationWhole genome duplicationAllopolyploidizationReticulate evolution |
| spellingShingle | Jinren Yu Hong Zhao Yanting Niu Yichen You Russell L. Barrett Rindra Manasoa Ranaivoson Romer Narindra Rabarijaona Gaurav Parmar Langxing Yuan Xiaofeng Jin Pan Li Jianhua Li Jun Wen Zhiduan Chen Limin Lu Distinct hybridization modes in wide- and narrow-ranged lineages of Causonis (Vitaceae) BMC Biology Distribution range Causonis Hybridization Whole genome duplication Allopolyploidization Reticulate evolution |
| title | Distinct hybridization modes in wide- and narrow-ranged lineages of Causonis (Vitaceae) |
| title_full | Distinct hybridization modes in wide- and narrow-ranged lineages of Causonis (Vitaceae) |
| title_fullStr | Distinct hybridization modes in wide- and narrow-ranged lineages of Causonis (Vitaceae) |
| title_full_unstemmed | Distinct hybridization modes in wide- and narrow-ranged lineages of Causonis (Vitaceae) |
| title_short | Distinct hybridization modes in wide- and narrow-ranged lineages of Causonis (Vitaceae) |
| title_sort | distinct hybridization modes in wide and narrow ranged lineages of causonis vitaceae |
| topic | Distribution range Causonis Hybridization Whole genome duplication Allopolyploidization Reticulate evolution |
| url | https://doi.org/10.1186/s12915-023-01718-8 |
| work_keys_str_mv | AT jinrenyu distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae AT hongzhao distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae AT yantingniu distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae AT yichenyou distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae AT russelllbarrett distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae AT rindramanasoaranaivoson distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae AT romernarindrarabarijaona distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae AT gauravparmar distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae AT langxingyuan distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae AT xiaofengjin distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae AT panli distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae AT jianhuali distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae AT junwen distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae AT zhiduanchen distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae AT liminlu distincthybridizationmodesinwideandnarrowrangedlineagesofcausonisvitaceae |