Evolutionary history of a desert perennial Arnebia szechenyi (Boraginaceae): Intraspecific divergence, regional expansion and asymmetric gene flow

doi:10.1016/j.pld.2021.04.002

Plant Diversity ›› 2021, Vol. 43 ›› Issue (06): 462-471.DOI: 10.1016/j.pld.2021.04.002

Evolutionary history of a desert perennial Arnebia szechenyi (Boraginaceae): Intraspecific divergence, regional expansion and asymmetric gene flow

Meng-Jiao Fu^a, Hai-Yang Wu^a, Dong-Rui Jia^b, Bin Tian^a,c

a Key Laboratory for Forest Resources Conservation and Utilization in the Southwest Mountains of China, Ministry of Education, Southwest Forestry University, Kunming 650224, China;
b School of Ecology and Environmental Science&Yunnan Key Laboratory for Plateau Mountain Ecology and Restoration of Degraded Environments, Yunnan University, Kunming 650091, China;
c CAS Key Laboratory for Plant Diversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650204, China

收稿日期:2021-02-07 修回日期:2021-04-07 出版日期:2021-12-25 发布日期:2022-01-11
通讯作者: Dong-Rui Jia, Bin Tian
基金资助:
We are grateful to Dr. Jun-Wei Ye for assistant on data analysis. We thank Dr. Yuan-Wen Duan for help during the field survey. This study was supported by the National Natural Science Foundation of China (41861008), Science Foundation of Yunnan Education Department (2018JS347), and the Ten-thousand Talents Program of Yunnan Province (YNWR-QNBJ-2020).

Evolutionary history of a desert perennial Arnebia szechenyi (Boraginaceae): Intraspecific divergence, regional expansion and asymmetric gene flow

Meng-Jiao Fu^a, Hai-Yang Wu^a, Dong-Rui Jia^b, Bin Tian^a,c

a Key Laboratory for Forest Resources Conservation and Utilization in the Southwest Mountains of China, Ministry of Education, Southwest Forestry University, Kunming 650224, China;
b School of Ecology and Environmental Science&Yunnan Key Laboratory for Plateau Mountain Ecology and Restoration of Degraded Environments, Yunnan University, Kunming 650091, China;
c CAS Key Laboratory for Plant Diversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650204, China

Received:2021-02-07 Revised:2021-04-07 Online:2021-12-25 Published:2022-01-11
Contact: Dong-Rui Jia, Bin Tian
Supported by:
We are grateful to Dr. Jun-Wei Ye for assistant on data analysis. We thank Dr. Yuan-Wen Duan for help during the field survey. This study was supported by the National Natural Science Foundation of China (41861008), Science Foundation of Yunnan Education Department (2018JS347), and the Ten-thousand Talents Program of Yunnan Province (YNWR-QNBJ-2020).

摘要/Abstract

摘要： The complex interactions of historical, geological and climatic events on plant evolution have been an important research focus for many years. However, the role of desert formation and expansion in shaping the genetic structures and demographic histories of plants occurring in arid areas has not been well explored. In the present study, we investigated the phylogeography of Arnebia szechenyi, a desert herb showing a near-circular distribution surrounding the Tengger Desert in Northwest China. We measured genetic diversity of populations using three maternally inherited chloroplast DNA (cpDNA) fragments and seven bi-paternally inherited nuclear DNA (nDNA) loci that were sequenced from individuals collected from 16 natural populations across its range and modelled current and historical potential habitats of the species. Our data indicated a considerably high level of genetic variation within A. szechenyi and noteworthy asymmetry in historical migration from the east to the west. Moreover, two nuclear genetic groups of populations were revealed, corresponding to the two geographic regions separated by the Tengger Desert. However, analysis of cpDNA data did not show significant geographic structure. The most plausible explanation for the discrepancy between our findings based on cpDNA and nDNA data is that A. szechenyi populations experienced long periods of geographic isolation followed by range expansion, which would have promoted generalized recombination of the nuclear genome. Our findings further highlight the important role that the Tengger Desert, together with the Helan Mountains, has played in the evolution of desert plants and the preservation of biodiversity in arid Northwest China.

关键词: Asymmetric gene flow, Cytonuclear discordance, Desert growth, Intraspecific divergence

Abstract: The complex interactions of historical, geological and climatic events on plant evolution have been an important research focus for many years. However, the role of desert formation and expansion in shaping the genetic structures and demographic histories of plants occurring in arid areas has not been well explored. In the present study, we investigated the phylogeography of Arnebia szechenyi, a desert herb showing a near-circular distribution surrounding the Tengger Desert in Northwest China. We measured genetic diversity of populations using three maternally inherited chloroplast DNA (cpDNA) fragments and seven bi-paternally inherited nuclear DNA (nDNA) loci that were sequenced from individuals collected from 16 natural populations across its range and modelled current and historical potential habitats of the species. Our data indicated a considerably high level of genetic variation within A. szechenyi and noteworthy asymmetry in historical migration from the east to the west. Moreover, two nuclear genetic groups of populations were revealed, corresponding to the two geographic regions separated by the Tengger Desert. However, analysis of cpDNA data did not show significant geographic structure. The most plausible explanation for the discrepancy between our findings based on cpDNA and nDNA data is that A. szechenyi populations experienced long periods of geographic isolation followed by range expansion, which would have promoted generalized recombination of the nuclear genome. Our findings further highlight the important role that the Tengger Desert, together with the Helan Mountains, has played in the evolution of desert plants and the preservation of biodiversity in arid Northwest China.

Key words: Asymmetric gene flow, Cytonuclear discordance, Desert growth, Intraspecific divergence

Meng-Jiao Fu, Hai-Yang Wu, Dong-Rui Jia, Bin Tian. Evolutionary history of a desert perennial Arnebia szechenyi (Boraginaceae): Intraspecific divergence, regional expansion and asymmetric gene flow[J]. Plant Diversity, 2021, 43(06): 462-471.

参考文献

Avise, J.C., 2004. Molecular Markers, Natural History, and Evolution. Sinauer Associates, Sunderland, MA.
Avise, J.C., Arnold, J., Ball, R.M., et al., 1987. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu. Rev. Ecol. Systemat. 18, 489-522.
Barrett, R.D.H., Schluter, D., 2008. Adaptation from standing genetic variation. Trends Ecol. Evol. 23, 38-44.
Barrett, S.C.H., Jesson, L.K., Baker, A.M., 2000. The evolution and function of stylar polymorphisms in flowering plants. Ann. Bot. 85, 253-265.
Beerli, P., 2006. Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22, 341-345.
Beheregaray, L.B., 2008. Twenty years of phylogeography: the state of the field and the challenges for the Southern Hemisphere. Mol. Ecol. 17, 3754-3774.
Bouckaert, R., Heled, J., Kühnert, D., et al., 2014. Beast 2: a software Platform for bayesian evolutionary analysis. PLoS Comput. Biol. 10, e1003537.
Comes, H.P., Kadereit, J.W., 1998. The effect of Quaternary climatic changes on plant distribution and evolution. Trends Plant Sci. 3, 432-438.
Comes, H.P., Kadereit, J.W., 2003. Spatial and temporal patterns in the evolution of the flora of the European Alpine System. Taxon 52, 451-462.
Darriba, D., Taboada, G.L., Doallo, R., et al., 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772-772.
Dellicour, S., Mardulyn, P., 2014. Spads 1.0: a toolbox to perform spatial analyses on DNA sequence data sets. Mol. Ecol. Resour. 14, 647-651.
Després, L., 2019. One, two or more species? Mitonuclear discordance and species delimitation. Mol. Ecol. 28, 3845-3847.
Drouin, G., Daoud, H., Xia, J.N., 2008. Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol. Phylogenet. Evol. 49, 827-831.
Du, F.K., Petit, R.J., Liu, J.Q., 2009. More introgression with less gene flow: chloroplast vs. mitochondrial DNA in the Picea asperata complex in China, and comparison with other Conifers. Mol. Ecol. 18, 1396-1407.
Excoffier, L., Lischer, H.E.L., 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564-567.
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.
Falush, D., Stephens, M., Pritchard, J.K., 2007. Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol. Ecol. Notes 7, 574-578.
Fawcett, T., 2006. An introduction to ROC analysis. Pattern Recogn. Lett. 27, 861-874.
Field, C.B., Behrenfeld, M.J., Randerson, J.T., et al., 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237-240.
Fu, Y., He, C.Z., Tian, B., 2016. Development of low copy nuclear gene primers for Arnebia szechenyi based on transcriptome. J. S. W. Forest. Univ. 36, 86-90.
Fu, Y.X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915-925.
Fu, Y.X., Li, W.H., 1993. Statistical tests of neutrality of mutations. Genetics 133, 693-709.
Funk, D.J., Omland, K.E., 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu.Rev. Ecol. Evol. Syst. 34, 397-423.
Hewitt, G., 2000. The genetic legacy of the Quaternary ice ages. Nature 405, 907-913.
Hewitt, G.M., 1996. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. Lond. 58, 247-276.
Hewitt, G.M., 1999. Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. Lond. 68, 87-112.
Hickerson, M.J., Carstens, B.C., Cavender-Bares, J., et al., 2010. Phylogeography's past, present, and future: 10 years after Avise, 2000. Mol. Phylogenet. Evol. 54, 291-301.
Hinojosa, J.C., Koubínová, D., Szenteczki, M.A., et al., 2019. A mirage of crypticspecies: genomics uncover striking mitonuclear discordance in the butterfly Thymelicus sylvestris. Mol. Ecol. 28, 3857-3868.
Jia, D., Abbott, R., Liu, T., et al., 2012. Out of the Qinghai-Tibet plateau: evidence for the origin and dispersal of Eurasian temperate plants from a phylogeographic study of Hippophae rhamnoides (Elaeagnaceae). New Phytol. 194, 1123-1133.
Kay, K.M., Whittall, J.B., Hodges, S.A., 2006. A survey of nuclear ribosomal internal transcribed spacer substitution rates across angiosperms: an approximate molecular clock with life history effects. BMC Evol. Biol. 6, 1-9.
Kier, G., Mutke, J., Dinerstein, E., et al., 2005. Global patterns of plant diversity and floristic knowledge. J. Biogeogr. 32, 1107-1116.
Korner, C., 2000. Biosphere responses to CO₂ enrichment. Ecol. Appl. 10, 1590-1619.
Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874.
Le Houérou, H.N., 1996. Climate change, drought and desertification. J. Arid Environ. 34, 133-185.
Li, Y., Zhang, X.N., Lv, G.H., 2019. Phylogeography of Ixiolirion songaricum, a spring ephemeral species endemic to Northwest China. Plant Systemat. Evol. 305, 205-221.
Li, Z., Sun, D., Chen, F., et al., 2014. Chronology and paleoenvironmental records of a drill core in the central Tengger Desert of China. Quat. Sci. Rev. 85, 85-98.
Li, Z.J., 2013. Formation and Paleo-Environmental Evolution of the Tengger Desert Revealed by Drilling Holes in the Hinterland of the Tengger Desert (Doctoral Dissertation. Lanzhou University.
Librado, P., Rozas, J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451-1452.
Liu, J.Q., Sun, Y.S., Ge, X.J., et al., 2012. Phylogeographic studies of plants in China:advances in the past and directions in the future. J. Systemat. Evol. 50, 267-275.
Lloyd, D.G., Webb, C.J., 1992. The Evolution of Heterostyly. Evolution and Function of Heterostyly. Springer, Berlin, Heidelberg, pp. 151-178.
Maestre, F.T., Salguero-Gomez, R., Quero, J.L., 2012. It is getting hotter in here:determining and projecting the impacts of global environmental change on drylands. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 3062-3075.
Meng, H.H., Gao, X.Y., Huang, J.F., et al., 2015. Plant phylogeography in arid Northwest China: retrospectives and perspectives. J. Systemat. Evol. 53, 33-46.
Meng, H.H., Zhang, M.L., 2011. Phylogeography of Lagochilus ilicifolius (Lamiaceae) in relation to Quaternary climatic oscillation and aridification in northern China. Biochem. Systemat. Ecol. 39, 787-796.
Morris, A.B., Shaw, J., 2018. Markers in time and space: a review of the last decade of plant phylogeographic approaches. Mol. Ecol. 27, 2317-2333.
Muscarella, R., Galante, P.J., Soley-Guardia, M., et al., 2014. ENM eval: an R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods Ecol. Evol. 5, 1198-1205.
Phillips, S.J., Anderson, R.P., Schapire, R.E., 2006. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190, 231-259.
Pons, O., Petit, R.J., 1996. Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144, 1237-1245.
Qiu, Y.X., Fu, C.X., Comes, H.P., 2011. Plant molecular phylogeography in China and adjacent regions: tracing the genetic imprints of Quaternary climate and environmental change in the world's most diverse temperate flora. Mol. Phylogenet. Evol. 59, 225-244.
R Core Team, 2013. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Rambaut, A., Drummond, A.J., Xie, D., et al., 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901.
Reynolds, J.F., Maestre, F.T., Kemp, P.R., et al., 2007. Natural and human dimensions of land degradation in drylands: causes and consequences. In: Terrestrial Ecosystems in a Changing World. Springer, Berlin, Heidelberg, pp. 247-257.
Rock, C.D., Barkan, A., Taylor, W.C., 1987. The maize plastid psbB-psbF-petB-petD gene cluster: spliced and unspliced petB and petD RNAs encode alternative products. Curr. Genet. 12, 69-77.
Rogers, A.R., Harpending, H., 1992. Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol. 9, 552-569.
Sala, O.E., Chapin, F.S., Armesto, J.J., et al., 2000. Global biodiversity scenarios for the year 2100. Science 287, 1770-1774.
Sang, T., Crawford, D.J., Stuessy, T.F., 1997. Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). Am. J. Bot. 84, 1120-1136.
Sloan, D.B., Havird, J.C., Sharbrough, J., 2017. The on-again, off-again relationship between mitochondrial genomes and species boundaries. Mol. Ecol. 26, 2212-2236.
Taberlet, P., Gielly, L., Pautou, G., et al., 1991. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol. Biol. 17, 1105-1109.
Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585-595.
Tian, B., Fu, Y., Milne, R.I., et al., 2020. A complex pattern of post-divergence expansion, contraction, introgression, and asynchronous responses to Pleistocene climate changes in two Dipelta sister species from western China. J. Systemat. Evol. 58, 247-262.
Wang, F., Sun, D., Chen, F., et al., 2015. Formation and evolution of the Badain Jaran Desert, North China, as revealed by a drill core from the desert centre and by geological survey. Palaeogeogr. Palaeoclimatol. Palaeoecol. 426, 139-158.
Wang, L.L., Zhang, C., Tian, B., et al., 2015a. Reproductive isolation is mediated by pollen incompatibility in sympatric populations of two Arnebia species. Ecol. Evol. 5, 5838-5846.
Wang, P., Zhang, X., Tang, N., et al., 2016. Phylogeography of Libanotis buchtormensis(Umbelliferae) in disjunct populations along the deserts in Northwest China. PLoS One 11, e0159790.
Ward, D., 2016. The Biology of Deserts. Oxford University Press.
White, T.J., Bruns, T., Lee, S.J.W.T., et al., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J. (Eds.), PCR Protocols: A Guide to Methods and Applications. Academic Press, Inc., New York, pp. 315-322.
Wolfe, K.H., Li, W.H., Sharp, P.M., 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl. Acad. Sci. U.S.A. 84, 9054-9058.
Xie,K.Q.,Zhang, M.L.,2013. TheeffectofQuaternaryclimatic oscillationsonRibes meyeri(Saxifragaceae) in northwestern China. Biochem. Systemat. Ecol. 50, 39-47.
Yang, X., Scuderi, L.A., 2010. Hydrological and climatic changes in deserts of China since the late Pleistocene. Quat. Res. 73, 1-9.
Yin, H., Wang, L., Shi, Y., et al., 2020. The East Asian Winter Monsoon acts as a major selective factor in the intraspecific differentiation of drought-tolerant Nitraria tangutorum in Northwest China. Plants 9, 1100.
Yin, H.X., Yan, X., Shi, Y., et al., 2015. The role of East Asian monsoon system in shaping population divergence and dynamics of a constructive desert shrub Reaumuria soongarica. Sci. Rep. 5, 1-14.
Zamudio, K.R., Bell, R.C., Mason, N.A., 2016. Phenotypes in phylogeography: species'traits, environmental variation, and vertebrate diversification. Proc. Natl. Acad. Sci. U.S.A. 113, 8041.
Zeng, Y.F., Zhang, J.G., Abuduhamiti, B., et al., 2018. Phylogeographic patterns of the desert poplar in Northwest China shaped by both geology and climatic oscillations. BMC Evol. Biol. 18, 1-14.
Zhang, C., Vereecken, N.J., Wang, L., et al., 2017a. Are nectar guide colour changes a reliable signal to pollinators that enhances reproductive success? Plant Ecol. Divers. 10, 89-96.
Zhang, C., Wang, L.L., Lan, D., et al., 2014. Pollination ecology of Arnebia szechenyi(Boraginaceae), a Chinese endemic perennial characterized by distyly and heteromorphic self-incompatibility. Ann. Zool. Fenn. 51, 297-304.
Zhang, D.F., L, F.Q., B, J.M., 2000. Eco-environmental effects of the Qinghai-Tibet Plateau uplift during the quaternary in China. Environ. Geol. 39, 1352-1358.
Zhang, H.X., Zhang, M.L., Sanderson, S.C., 2017b. Spatial genetic structure of forest and xerophytic plant species in arid Eastern Central Asia: insights from comparative phylogeography and ecological niche modelling. Biol. J. Linn. Soc. Lond. 120, 612-625.
Zhang, Y., Yu, Q., Zhang, Q., et al., 2017. Regional-scale differentiation and phylogeography of a desert plant Allium mongolicum (Liliaceae) inferred from chloroplast DNA sequence variation. Plant Systemat. Evol. 303, 451-466.
Zhao, Y.F., Zhang, H.X., Pan, B.R., et al., 2019. Intraspecific divergences and phylogeography of Panzerina lanata (Lamiaceae) in northwest China. PeerJ 7, e6264.
Zhou, W., Wang, H., 2009. Heterostyly in angiosperms and its evolutionary significance. Ann. Bot. 44, 742.
Zhu, G.L., Riedl, H., Kamelin, R., 2005. Boraginaceae. In: Wu, Z.-Y., Raven, P.H. (Eds.), Flora of China. Science Press and Missouri Botanical Garden, Beijing and St Louis.

Evolutionary history of a desert perennial Arnebia szechenyi (Boraginaceae): Intraspecific divergence, regional expansion and asymmetric gene flow

Evolutionary history of a desert perennial Arnebia szechenyi (Boraginaceae): Intraspecific divergence, regional expansion and asymmetric gene flow

PDF (PC)

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 1

编辑推荐

Metrics

本文评价