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Plastid phylogenomics and biogeographic analysis support a trans-Tethyan origin and rapid early radiation of Cornales in the Mid-Cretaceous.
Mol Phylogenet Evol. 2019 11; 140:106601.MP

Abstract

The Cornales is a relatively small but morphologically diverse order in the basal position of the Asterids clade. Previous study hypothesized that the order might have undergone ancient rapid radiation during the Cretaceous when major angiosperm lineages were established. We conducted the phylogenomic analysis of Cornales using 81 plastid genome sequences with 67 newly generated in this study to test the hypothesis. This sampling represents all the families and 31 out of 48 genera in the order. Phylogenetic analyses were conducted using different datasets to examine the effects of different coding positions and character coding methods. We further conducted divergence time, diversification rate, and biogeographic analyses to understand the early evolutionary history of Cornales in space and time. Our phylogenetic analyses of four datasets (the amino acid characters, the 1st and 2nd codon positions of protein coding genes, nucleotide characters with degenerated coding method, and noncoding regions) resulted in a robust phylogeny congruent with results of previous studies, showing (((Cornaceae-Alangiaceae)-(Curtisiaceae-Grubbiaceae))-(((Nyssaceae-Davidiaceae)-Mastixiaceae)-((Hydrostachyaceae-(Hydrangeaceae-Loasaceae)))). Phylogenetic relationships within families were also well resolved. Conflicts in the placement of Hydrostachyaceae were found from analyses of two datasets, the nucleotide characters of all codon position and the 3rd codon positions, where the family was united with Loasaceae, but not strongly supported. Results from divergence time analyses suggested a mid-Cretaceous origin of Cornales followed by rapid early diversification into major clades/families within 10 million years. The early diversification of Cornales may have been facilitated by divergence in habitat and morphology following geographic dispersals. The ancestral distribution of the order was inferred as a widespread range covering Asia, Europe, North America, and Africa when including fossils in the analyses, suggesting an origin of the order likely along the Tethys Seaway where the areas were connected in the mid-Cretaceous. Inferred geographic origins of each family differed to some extent between analyses including fossils vs excluding fossils. In the analysis with extant and fossil species, the origins of the African Hydrostachyaceae and Grubbiaceae-Curtisiaceae clade were inferred to have involved two independent events, an intercontinental dispersal from the northern hemisphere to Africa and an intercontinental vicariance between the northern hemisphere and Africa, respectively. Other families were inferred to have evolved in the northern hemisphere with subsequent intercontinental dispersal(s) to other areas including to Central and South America, during their subsequent diversification. Net diversification rate analysis based on treePL dated phylogeny using MEDUSA detected a nearly 5-fold decrease in the African endemic Curtisiaceae-Grubbiaceae (CuG) clade and an increase of rate in the Hydrangeaceae-Loasaceae (HL) clade. Within HL, a decrease in the Fendlera-Jamesia clade and an increase in the Philadelphus clade were also detected. The findings are also consistent with the level of present species diversity in these lineages. Our study demonstrated the value of plastid genome in phylogenomic study, but posed an old challenge of biogeographic study with fossil data and raised caution for the synonymous substitution sites of plastid genome in phylogenomics studies.

Authors+Show Affiliations

CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China; Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China; Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, Yunnan 650201, China.CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China; Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, Yunnan 650201, China.Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China.Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangdong 510650, China.CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China; Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China; Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, Yunnan 650201, China. Electronic address: dzl@mail.kib.ac.cn.Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC 27695, USA. Electronic address: qyxiang@ncsu.edu.CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China. Electronic address: gaolm@mail.kib.ac.cn.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

31445202

Citation

Fu, Chao-Nan, et al. "Plastid Phylogenomics and Biogeographic Analysis Support a trans-Tethyan Origin and Rapid Early Radiation of Cornales in the Mid-Cretaceous." Molecular Phylogenetics and Evolution, vol. 140, 2019, p. 106601.
Fu CN, Mo ZQ, Yang JB, et al. Plastid phylogenomics and biogeographic analysis support a trans-Tethyan origin and rapid early radiation of Cornales in the Mid-Cretaceous. Mol Phylogenet Evol. 2019;140:106601.
Fu, C. N., Mo, Z. Q., Yang, J. B., Ge, X. J., Li, D. Z., Xiang, Q. J., & Gao, L. M. (2019). Plastid phylogenomics and biogeographic analysis support a trans-Tethyan origin and rapid early radiation of Cornales in the Mid-Cretaceous. Molecular Phylogenetics and Evolution, 140, 106601. https://doi.org/10.1016/j.ympev.2019.106601
Fu CN, et al. Plastid Phylogenomics and Biogeographic Analysis Support a trans-Tethyan Origin and Rapid Early Radiation of Cornales in the Mid-Cretaceous. Mol Phylogenet Evol. 2019;140:106601. PubMed PMID: 31445202.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Plastid phylogenomics and biogeographic analysis support a trans-Tethyan origin and rapid early radiation of Cornales in the Mid-Cretaceous. AU - Fu,Chao-Nan, AU - Mo,Zhi-Qiong, AU - Yang,Jun-Bo, AU - Ge,Xue-Jun, AU - Li,De-Zhu, AU - Xiang,Qiu-Yun Jenny, AU - Gao,Lian-Ming, Y1 - 2019/08/21/ PY - 2019/01/15/received PY - 2019/08/17/revised PY - 2019/08/20/accepted PY - 2019/8/25/pubmed PY - 2020/3/7/medline PY - 2019/8/25/entrez KW - Biogeography KW - Character coding KW - Cornales KW - Phylogenomics KW - Plastid genome SP - 106601 EP - 106601 JF - Molecular phylogenetics and evolution JO - Mol. Phylogenet. Evol. VL - 140 N2 - The Cornales is a relatively small but morphologically diverse order in the basal position of the Asterids clade. Previous study hypothesized that the order might have undergone ancient rapid radiation during the Cretaceous when major angiosperm lineages were established. We conducted the phylogenomic analysis of Cornales using 81 plastid genome sequences with 67 newly generated in this study to test the hypothesis. This sampling represents all the families and 31 out of 48 genera in the order. Phylogenetic analyses were conducted using different datasets to examine the effects of different coding positions and character coding methods. We further conducted divergence time, diversification rate, and biogeographic analyses to understand the early evolutionary history of Cornales in space and time. Our phylogenetic analyses of four datasets (the amino acid characters, the 1st and 2nd codon positions of protein coding genes, nucleotide characters with degenerated coding method, and noncoding regions) resulted in a robust phylogeny congruent with results of previous studies, showing (((Cornaceae-Alangiaceae)-(Curtisiaceae-Grubbiaceae))-(((Nyssaceae-Davidiaceae)-Mastixiaceae)-((Hydrostachyaceae-(Hydrangeaceae-Loasaceae)))). Phylogenetic relationships within families were also well resolved. Conflicts in the placement of Hydrostachyaceae were found from analyses of two datasets, the nucleotide characters of all codon position and the 3rd codon positions, where the family was united with Loasaceae, but not strongly supported. Results from divergence time analyses suggested a mid-Cretaceous origin of Cornales followed by rapid early diversification into major clades/families within 10 million years. The early diversification of Cornales may have been facilitated by divergence in habitat and morphology following geographic dispersals. The ancestral distribution of the order was inferred as a widespread range covering Asia, Europe, North America, and Africa when including fossils in the analyses, suggesting an origin of the order likely along the Tethys Seaway where the areas were connected in the mid-Cretaceous. Inferred geographic origins of each family differed to some extent between analyses including fossils vs excluding fossils. In the analysis with extant and fossil species, the origins of the African Hydrostachyaceae and Grubbiaceae-Curtisiaceae clade were inferred to have involved two independent events, an intercontinental dispersal from the northern hemisphere to Africa and an intercontinental vicariance between the northern hemisphere and Africa, respectively. Other families were inferred to have evolved in the northern hemisphere with subsequent intercontinental dispersal(s) to other areas including to Central and South America, during their subsequent diversification. Net diversification rate analysis based on treePL dated phylogeny using MEDUSA detected a nearly 5-fold decrease in the African endemic Curtisiaceae-Grubbiaceae (CuG) clade and an increase of rate in the Hydrangeaceae-Loasaceae (HL) clade. Within HL, a decrease in the Fendlera-Jamesia clade and an increase in the Philadelphus clade were also detected. The findings are also consistent with the level of present species diversity in these lineages. Our study demonstrated the value of plastid genome in phylogenomic study, but posed an old challenge of biogeographic study with fossil data and raised caution for the synonymous substitution sites of plastid genome in phylogenomics studies. SN - 1095-9513 UR - https://www.unboundmedicine.com/medline/citation/31445202/Plastid_phylogenomics_and_biogeographic_analysis_support_a_trans_Tethyan_origin_and_rapid_early_radiation_of_Cornales_in_the_Mid_Cretaceous_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S1055-7903(19)30024-7 DB - PRIME DP - Unbound Medicine ER -