Evidence for two types of Aquilegia ecalcarata and its implications for adaptation to new environments

doi:10.1016/j.pld.2021.06.006

Plant Diversity ›› 2022, Vol. 44 ›› Issue (02): 153-162.DOI: 10.1016/j.pld.2021.06.006

Evidence for two types of Aquilegia ecalcarata and its implications for adaptation to new environments

Lei Huang, Fang-Dong Geng, Jing-Jing Fan, Wei Zhai, Cheng Xue, Xiao-Hui Zhang, Yi Ren, Ju-Qing Kang

National Engineering Laboratory for Resource Development of Endangered Crude Drugs in Northwest China, College of Life Sciences, Shaanxi Normal University, Xi'an, Shaanxi 710119, China

收稿日期:2021-02-06 修回日期:2021-06-17 出版日期:2022-04-25 发布日期:2022-04-24
通讯作者: Yi Ren,E-mail:renyi@snnu.edu.cn;Ju-Qing Kang,E-mail:kangjq@snnu.edu.cn
基金资助:
We thank Li Sun, Xiao-peng Chang for sample collection and other members of Ren's group for technical assistance. We are grateful to Professor Hong-zhi Kong and Professor Song Ge (Institute of Botany, Chinese Academy of Science) for their valuable advice. We also thank professor Elena Kramer (Harvard University) for polishing this manuscript. This work was supported by the National Natural Science Foundation of China (31700180 and 31330007), and the fundamental Research Funds for the Central Universities of Shaanxi Normal University (GK202002011).

Evidence for two types of Aquilegia ecalcarata and its implications for adaptation to new environments

Lei Huang, Fang-Dong Geng, Jing-Jing Fan, Wei Zhai, Cheng Xue, Xiao-Hui Zhang, Yi Ren, Ju-Qing Kang

National Engineering Laboratory for Resource Development of Endangered Crude Drugs in Northwest China, College of Life Sciences, Shaanxi Normal University, Xi'an, Shaanxi 710119, China

Received:2021-02-06 Revised:2021-06-17 Online:2022-04-25 Published:2022-04-24
Contact: Yi Ren,E-mail:renyi@snnu.edu.cn;Ju-Qing Kang,E-mail:kangjq@snnu.edu.cn
Supported by:
We thank Li Sun, Xiao-peng Chang for sample collection and other members of Ren's group for technical assistance. We are grateful to Professor Hong-zhi Kong and Professor Song Ge (Institute of Botany, Chinese Academy of Science) for their valuable advice. We also thank professor Elena Kramer (Harvard University) for polishing this manuscript. This work was supported by the National Natural Science Foundation of China (31700180 and 31330007), and the fundamental Research Funds for the Central Universities of Shaanxi Normal University (GK202002011).

摘要/Abstract

摘要： Spurs have played an important role in the radiation of the genus Aquilegia, but little is known about how the spurless state arose in A. ecalcarata. Here we aim to characterize the genetic divergence within A. ecalcarata and gain insights into the origin of this species. A total of 19 populations from A. ecalcarata and 23 populations from three of its closest relatives (Aquilegia kansuensis, Aquilegia rockii and Aquilegia yabeana) were sampled in this study. We sequenced fifteen nuclear gene fragments across the genome and three chloroplast loci to conduct phylogenetic, PCoA and STRUCTURE analyses.
Our analyses indicate that A. ecalcarata may not be monophyletic and can be divided into two distinct lineages (A. ecalcarata I and A. ecalcarata II). A. ecalcarata I is genetically close to A. kansuensis, whereas A. ecalcarata II is close to A. rockii. Isolation-with-migration analysis suggested that historical gene flow was low between A. ecalcarata I and A. rockii, as well as between A. ecalcarata II and A. kansuensis. The two distinct lineages of A. ecalcarata show significant divergence in 13 floral traits and also have distinct distributions. In addition, both A. ecalcarata I and II are adapted to a stony environment that differs from that of their closest relatives, indicating a habitat shift may have driven new adaptations. Our findings enrich the understanding of how floral evolution contributes to species diversification.

关键词: Aquilegia ecalcarata, Phylogeny, Population structure, Gene flow, Spur loss

Abstract: Spurs have played an important role in the radiation of the genus Aquilegia, but little is known about how the spurless state arose in A. ecalcarata. Here we aim to characterize the genetic divergence within A. ecalcarata and gain insights into the origin of this species. A total of 19 populations from A. ecalcarata and 23 populations from three of its closest relatives (Aquilegia kansuensis, Aquilegia rockii and Aquilegia yabeana) were sampled in this study. We sequenced fifteen nuclear gene fragments across the genome and three chloroplast loci to conduct phylogenetic, PCoA and STRUCTURE analyses.
Our analyses indicate that A. ecalcarata may not be monophyletic and can be divided into two distinct lineages (A. ecalcarata I and A. ecalcarata II). A. ecalcarata I is genetically close to A. kansuensis, whereas A. ecalcarata II is close to A. rockii. Isolation-with-migration analysis suggested that historical gene flow was low between A. ecalcarata I and A. rockii, as well as between A. ecalcarata II and A. kansuensis. The two distinct lineages of A. ecalcarata show significant divergence in 13 floral traits and also have distinct distributions. In addition, both A. ecalcarata I and II are adapted to a stony environment that differs from that of their closest relatives, indicating a habitat shift may have driven new adaptations. Our findings enrich the understanding of how floral evolution contributes to species diversification.

Key words: Aquilegia ecalcarata, Phylogeny, Population structure, Gene flow, Spur loss

Lei Huang, Fang-Dong Geng, Jing-Jing Fan, Wei Zhai, Cheng Xue, Xiao-Hui Zhang, Yi Ren, Ju-Qing Kang. Evidence for two types of Aquilegia ecalcarata and its implications for adaptation to new environments[J]. Plant Diversity, 2022, 44(02): 153-162.

参考文献

Abbott, R.J., 2017. Plant speciation across environmental gradients and the occurrence and nature of hybrid zones. J. Syst. Evol. 55, 238-258.
Ballerini, E.S., Min, Y., Edwards, M.B., et al., 2020. POPOVICH, encoding a C2H2 zincfinger transcription factor plays a central role in the development of a key innovation floral nectar spurs in Aquilegia. Proc. Natl. Acad. Sci. U.S.A. 117, 22552-22560.
Bastida, J.M., Alcantara, J.M., Rey, P.J., et al., 2010. Extended phylogeny of Aquilegia:the biogeographical and ecological patterns of two simultaneous but contrasting radiations. Plant Syst. Evol. 284, 171-185.
Bouckaert, R., Heled, J., Kühnert, D., et al., 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10, e1003537.
Cai, Z., Zhou, L., Ren, N.N., et al., 2019. Parallel speciation of wild rice associated with habitat shifts. Mol. Biol. Evol. 36, 875-889.
Duminil, J., Di Michele, M., 2009. Plant species delimitation: a comparison of morphological and molecular markers. Plant Biosyst. 143, 528-542.
Erst, A.S., Shaulo, D.N., Luferov, A.N., et al., 2014. On the taxonomical status of Aquilegia kansuensis (Ranunculaceae). Turczaninowia 17, 24-25.
Evanno, G., Regnaut, S., Goudet, J., 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611-2620.
Excoffier, L., Smouse, P.E., Quattro, J.M., 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479-491.
Farris, J.S., Kallersjo, M., Kluge, A.G., et al., 1994. Testing significance of incon-gruence. Cladistics 10, 315-319.
Filiault, D., Ballerini, E.S., Mandakova, T., et al., 2018. The Aquilegia genome: adaptive radiation and an extraordinarily polymorphic chromosome with a unique history. eLife 7, e36426.
Fior, S., Li, M., Oxelman, B., et al., 2013. Spatiotemporal reconstruction of the Aquilegia rapid radiation through next-generation sequencing of rapidly evolving cpDNA regions. New Phytol. 198, 579-592.
Fu, D., Robinson, O.R., 2001. Aquilegia L. In: Wu, Z.Y., Raven, P.H. (Eds.), Flora of China 6. Science Press, Beijing, pp. 278-281.
Fu, Y.X., Li, W.H., 1993. Statistical tests of neutrality of mutations. Genetics 133, 693-709.
Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95-98.
Hey, J., 2010. Isolation with migration models for more than two populations. Mol. Biol. Evol. 27, 905-920.
Hey, J., Nielsen, R., 2004. Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167, 747-760.
Hodges, S.A., 1997. Floral nectar spurs and diversification. Int. J. Plant Sci. 158, 81-88.
Hodges, S.A., Arnold, M.L., 1995. Spurring plant diversification: are floral nectar spurs a key innovation? Proc. Roy. Soc. B: Biol. Sci. 262, 343-348.
Hodges, S.A., Fulton, M., Yang, J.Y., et al., 2003. Verne grant and evolutionary studies of Aquilegia. New Phytol. 161, 113-120.
Hoekstra, H.E., Coyne, J.A., 2007. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61, 995-1016.
Huang, L., Geng, F.D., Fan, J.J., et al., 2018. Genetic diversity and evolutionary history of four closely related Aquilegia species revealed by ten nuclear gene fragments. J. Syst. Evol. 56, 129-138.
Huang, X., Kurata, N., Wei, X., et al., 2012. A map of rice genome variation reveals the origin of cultivated rice. Nature 490, 497-501.
Hudson, R.R., Kaplan, N.L., 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111, 147-164.
Hudson, R.R., Kreitman, M., Aguade, M., 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116, 153-159.
Huelsenbeck, J.P., Ronquist, F., 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755.
Kimura, M., 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111-134.
Kramer, E.M., 2009. Aquilegia: a new model for plant development, ecology, and evolution. Annu. Rev. Plant Biol. 60, 261-277.
Kramer, E.M., Hodges, S.A., 2010. Aquilegia as a model system for the evolution and ecology of petals. Phil. Trans. Biol. Sci. 365, 477-490.
Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874.
Librado, P., Rozas, J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451-1452.
Londo, J.P., Chiang, Y.C., Hung, K.H., et al., 2006. Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proc. Natl. Acad. Sci. U.S.A. 103, 9578-9583.
Mayr, E., 1942. Systematics and the origin of species. Columbia University Press, New York.
Nei, M., 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.
Perrier, X., Jacquemond-Collet, J.P., 2006. Darwin software. http://darwin.cirad.fr/darwin/.
Posada, D., Crandall, K.A., 2001. Intraspecific gene genealogies: trees grafting into networks. Trends Ecol. Evol. 16, 37-45.
Pritchard, J.K., Stephens, M., Donnelly, P., 2000. Inference of population structure using multilocus genotype data. Genetics 155, 945-959.
Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585-595.
Tenaillon, M.I., U'Ren, J., Tenaillon, O., Gaut, B.S., 2004. Selection versus demography: a multilocus investigation of the domestication process in maize. Mol. Biol. Evol. 21, 1214-1225.
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.G., 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24, 4876-4882.
Wang, W.S., Mauleon, R., Hu, Z.Q., et al., 2018. Genomic variation in 3010 diverse accessions of Asian cultivated rice. Nature 557, 43-49.
Watterson, G.A., 1975. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7, 256-276.
Whittall, J.B., Hodges, S.A., 2007. Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447, 706-712.
Woerner, A.E., Cox, M.P., Hammer, M.F., 2007. Recombination-filtered genomic datasets by information maximization. Bioinformatics 23, 1851-1853.
Xiao, P.K., 1979. Aquilegia. In: Delectis Florae Reipublicae Popularis Sinicae Agendae Academiae Sinicae Edita, Flora Reipublicae Popularis Sinicae 27. Science Press, Beijing, pp. 490-502.
Xue, C., Geng, F.D., Zhang, X.Y., et al., 2020. Pattern of variation in the morphological characteristics of Aquilegia ecalcarata and its closely related species. J. Syst. Evol. 58, 221-233.
Zhang, L.B., Ge, S., 2007. Multilocus analysis of nucleotide variation and speciation in Oryza officinalis and its close relatives. Mol. Biol. Evol. 24, 769-783.
Zhu, Q.H., Zheng, X.M., Luo, J.C., 2007. Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Mol. Biol. Evol. 24, 875-888.

[1]	Xin-Mao Zhou, Li-Bing Zhang. Phylogeny, character evolution, and classification of Selaginellaceae(lycophytes)[J]. Plant Diversity, 2023, 45(06): 630-684.
[2]	Zhe Chen, Zhuo Zhou, Ze-Min Guo, Truong Van Do, Hang Sun, Yang Niu. Historical development of karst evergreen broadleaved forests in East Asia has shaped the evolution of a hemiparasitic genus Brandisia (Orobanchaceae)[J]. Plant Diversity, 2023, 45(05): 501-512.
[3]	Hai-Su Hu, Jiu-Yang Mao, Xue Wang, Yu-Ze Liang, Bei Jiang, De-Quan Zhang. Plastid phylogenomics and species discrimination in the “Chinese” clade of Roscoea (Zingiberaceae)[J]. Plant Diversity, 2023, 45(05): 523-534.
[4]	Cindy Q. Tang, Shi-Qian Yao, Peng-Bin Han, Jian-Ran Wen, Shuaifeng Li, Ming-Chun Peng, Chong-Yun Wang, Tetsuya Matsui, Yong-Ping Li, Shan Lu, Yuan He. Forest characteristics, population structure and growth trends of threatened relict Pseudotsuga forrestii in China[J]. Plant Diversity, 2023, 45(04): 422-433.
[5]	Yu-Feng Gu, Jiang-Ping Shu, Yi-Jun Lu, Hui Shen, Wen Shao, Yan Zhou, Qi-Meng Sun, Jian-Bing Chen, Bao-Dong Liu, Yue-Hong Yan. Insights into cryptic speciation of quillworts in China[J]. Plant Diversity, 2023, 45(03): 284-301.
[6]	Yi Jin, Hong Qian. U.PhyloMaker:An R package that can generate large phylogenetic trees for plants and animals[J]. Plant Diversity, 2023, 45(03): 347-352.
[7]	Xing Liu, Hui-Min Cai, Wen-Qiao Wang, Wei Lin, Zhi-Wei Su, Zhong-Hui Ma. Why is the beautyberry so colourful? Evolution, biogeography, and diversification of fruit colours in Callicarpa (Lamiaceae)[J]. Plant Diversity, 2023, 45(01): 6-19.
[8]	Mei-Zhen Wang, Xiao-Kai Fan, Yong-Hua Zhang, Jing Wu, Li-Mi Mao, Sheng-Lu Zhang, Min-Qi Cai, Ming-Hong Li, Zhang-Shi-Chang Zhu, Ming-Shui Zhao, Lu-Xian Liu, Kenneth M. Cameron, Pan Li. Phylogenomics and integrative taxonomy reveal two new species of Amana (Liliaceae)[J]. Plant Diversity, 2023, 45(01): 54-68.
[9]	Hong-Hu Meng, Can-Yu Zhang, Shook Ling Low, Lang Li, Jian-Yong Shen, Nurainas, Yu Zhang, Pei-Han Huang, Shi-Shun Zhou, Yun-Hong Tan, Jie Li. Two new species from Sulawesi and Borneo facilitate phylogeny and taxonomic revision of Engelhardia (Juglandaceae)[J]. Plant Diversity, 2022, 44(06): 552-564.
[10]	Xiaxia Li, Lijun Qiao, Birong Chen, Yujie Zheng, Chengchen Zhi, Siyu Zhang, Yupeng Pan, Zhihui Cheng. SSR markers development and their application in genetic diversity evaluation of garlic (Allium sativum) germplasm[J]. Plant Diversity, 2022, 44(05): 481-491.
[11]	Yi Jin, Hong Qian. V.PhyloMaker2：An updated and enlarged R package that can generate very large phylogenies for vascular plants[J]. Plant Diversity, 2022, 44(04): 335-339.
[12]	Jun-Hao Yu, Rui Zhang, Qiao-Ling Liu, Fa-Guo Wang, Xun-Lin Yu, Xi-Ling Dai, Yong-Bo Liu, Yue-Hong Yan. Ceratopteris chunii and Ceratopteris chingii (Pteridaceae), two new diploid species from China, based on morphological, cytological, and molecular data[J]. Plant Diversity, 2022, 44(03): 300-307.
[13]	Zheng-Yu Zuo, Ting Zhao, Xin-Yu Du, Yun Xiong, Jin-Mei Lu, De-Zhu Li. A revision of Dryopteris sect. Diclisodon (Dryopteridaceae) based on morphological and molecular evidence with description of a new species[J]. Plant Diversity, 2022, 44(02): 181-190.
[14]	Zhen-Yu Lv, Ziyoviddin Yusupov, Dai-Gui Zhang, Ya-Zhou Zhang, Xiao-Shuang Zhang, Nan Lin, Komiljon Tojibaev, Hang Sun, Tao Deng. Oreocharis xieyongii, an unusual new species of Gesneriaceae from western Hunan, China[J]. Plant Diversity, 2022, 44(02): 222-230.
[15]	Ying-Min Zhang, Li-Jun Han, Cong-Wei Yang, Zi-Li Yin, Xing Tian, Zi-Gang Qian, Guo-Dong Li. Comparative chloroplast genome analysis of medicinally important Veratrum (Melanthiaceae) in China: Insights into genomic characterization and phylogenetic relationships[J]. Plant Diversity, 2022, 44(01): 70-82.

Evidence for two types of Aquilegia ecalcarata and its implications for adaptation to new environments

Evidence for two types of Aquilegia ecalcarata and its implications for adaptation to new environments

PDF (PC)

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 15

编辑推荐

Metrics

本文评价