Comparative evolutionary history of two closely related desert plant, Convolvulus tragacanthoide and Convolvulus gortschakovii (Convolvulaceae) from northwest China

Abstract Desert ecosystems are one of the most fragile ecosystems on Earth. The study of the effects of paleoclimatic and geological changes on genetic diversity, genetic structure, and species differentiation of desert plants is not only helpful in understanding the strategies of adaptation of plants to arid habitats, but can also provide reference for the protection and restoration of vegetation in desert ecosystem. Northwest China is an important part of arid regions in the northern hemisphere. Convolvulus tragacanthoides and Convolvulus gortschakovii are closely related and have similar morphology. Through our field investigation, we found that the annual precipitation of the two species distribution areas is significantly different. Thus, C. tragacanthoides and C. gortschakovii provide an ideal comparative template to investigate the evolutionary processes of closely related species, which have adapted to different niches in response to changes in paleogeography and paleoclimate in northwest China. In this study, we employed phylogeographical approaches (two cpDNA spacers: rpl14–rpl36 and trnT–trnY) and species distribution models to trace the demographic history of C. tragacanthoides and C. gortschakovii, two common subshrubs and small shrubs in northwest China. The results showed the following: (1) Populations of C. tragacanthoides in northwest China were divided into three groups: Tianshan Mountains—Ili Valley, west Yin Mountains—Helan Mountains‐Qinglian Mountains, and Qinling Mountains—east Yin Mountains. There was a strong correlation between the distribution of haplotypes and the floristic subkingdom. The three groups corresponded to the Eurasian forest subkingdom, Asian desert flora subkingdom, and Sino‐Japanese floristic regions, respectively. Thus, environmental differences among different flora may lead to the genetic differentiation of C. tragacanthoides in China. (2) The west Yin Mountains—Helan Mountains‐Qinglian Mountains, and Qinling Mountains—east Yin Mountains were thought to form the ancestral distribution range of C. tragacanthoides. (3) C. tragacanthoides and C. gortschakovii adopted different strategies to cope with the Pleistocene glacial cycle. Convolvulus tragacanthoides contracted to the south during the glacial period and expanded to the north during the interglacial period; and there was no obvious north–south expansion or contraction of C. gortschakovii during the glacial cycle. (4) The interspecific variation of C. tragacanthoides and C. gortschakovii was related to the orogeny in northwest China caused by the uplift of the Tibetan Plateau during Miocene. (5) The 200 mm precipitation line formed the dividing line between the niches occupied by C. tragacanthoides and C. gortschakovii, respectively. In this study, from the perspective of precipitation, the impact of the formation of the summer monsoon limit line on species divergence and speciation is reported, which provides a new perspective for studying the response mechanism of species to the formation of the summer monsoon line, and also provides a clue for predicting how desert plants respond to future environmental changes.

[1]  Hong‐xiang Zhang,et al.  Population Genetic Structure and Biodiversity Conservation of a Relict and Medicinal Subshrub Capparis spinosa in Arid Central Asia , 2022, Diversity.

[2]  Kyoko Sugai,et al.  Genetic Distinctiveness but Low Diversity Characterizes Rear-Edge Thuja standishii (Gordon) Carr. (Cupressaceae) Populations in Southwest Japan , 2021, Diversity.

[3]  Yi-Gang Song,et al.  Biodiversity arks in the Anthropocene , 2021, Regional Sustainability.

[4]  S. Jia,et al.  Introgression of phylogeography lineages of Convolvulus gortschakovii (Convolvulaceae) in the northwest China , 2021, Plant Systematics and Evolution.

[5]  F. Leprieur,et al.  Patterns of phylogenetic beta diversity measured at deep evolutionary histories across geographical and ecological spaces for angiosperms in China , 2020, Journal of Biogeography.

[6]  Hong‐xiang Zhang,et al.  Genomic Phylogeography of Gymnocarpos przewalskii (Caryophyllaceae): Insights into Habitat Fragmentation in Arid Northwestern China , 2020, Diversity.

[7]  Ming-Li Zhang,et al.  Pleistocene climate change and phylogeographic structure of the Gymnocarpos przewalskii (Caryophyllaceae) in the northwest China: Evidence from plastid DNA, ITS sequences, and Microsatellite , 2019, Ecology and evolution.

[8]  D. Zheng,et al.  Neogene Expansion of the Qilian Shan, North Tibet: Implications for the Dynamic Evolution of the Tibetan Plateau , 2019, Tectonics.

[9]  Cindy Q. Tang,et al.  Identifying long-term stable refugia for relict plant species in East Asia , 2018, Nature Communications.

[10]  M. Suchard,et al.  Posterior summarisation in Bayesian phylogenetics using Tracer , 2022 .

[11]  Stephen A. Smith,et al.  Evolutionary history of the angiosperm flora of China , 2018, Nature.

[12]  Juan C. Sánchez-DelBarrio,et al.  DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets. , 2017, Molecular biology and evolution.

[13]  H. Jian,et al.  The impact of major geological events on Chinese flora , 2017 .

[14]  S. Jia,et al.  Evolutionary history of Gymnocarpos (Caryophyllaceae) in the arid regions from North Africa to Central Asia , 2016 .

[15]  Junqiang Yao,et al.  Precipitation trend–Elevation relationship in arid regions of the China , 2016 .

[16]  W. Lu,et al.  Phylogeographical patterns of two closely related desert shrubs, Nitraria roborowskii and N. sphaerocarpa (Nitrariaceae), from arid north‐western China , 2016 .

[17]  T. Yamashiro,et al.  Long-term persisting hybrid swarm and geographic difference in hybridization pattern: genetic consequences of secondary contact between two Vincetoxicum species (Apocynaceae–Asclepiadoideae) , 2016, BMC Evolutionary Biology.

[18]  J. R. Wood,et al.  How the temperate world was colonised by bindweeds: biogeography of the Convolvuleae (Convolvulaceae) , 2016, BMC Evolutionary Biology.

[19]  David C. Tank,et al.  Shifts in diversification rates linked to biogeographic movement into new areas: An example of a recent radiation in the Andes. , 2015, American journal of botany.

[20]  Robert W. Scotland,et al.  A foundation monograph of Convolvulus L. (Convolvulaceae) , 2015, PhytoKeys.

[21]  Y. Yu,et al.  RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography. , 2015, Molecular phylogenetics and evolution.

[22]  Zhe Xu,et al.  Phylogeography of the arid shrub Atraphaxis frutescens (Polygonaceae) in northwestern China: evidence from cpDNA sequences. , 2015, The Journal of heredity.

[23]  Xiaoyang Gao,et al.  Plant phylogeography in arid Northwest China: Retrospectives and perspectives , 2015 .

[24]  Ming‐Li Zhang,et al.  Phylogeographical structure inferred from cpDNA sequence variation of Zygophyllum xanthoxylon across north-west China , 2015, Journal of Plant Research.

[25]  Xiaoyang Gao,et al.  Diversification and vicariance of desert plants: Evidence inferred from chloroplast DNA sequence variation of Lagochilus ilicifolius (Lamiaceae) , 2014 .

[26]  Jason L. Brown SDMtoolbox: a python‐based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses , 2014 .

[27]  R. Jarret,et al.  Phylogenetics and diversification of morning glories (tribe Ipomoeeae, Convolvulaceae) based on whole plastome sequences. , 2014, American journal of botany.

[28]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

[29]  Hong‐xiang Zhang,et al.  Retreating or Standing: Responses of Forest Species and Steppe Species to Climate Change in Arid Eastern Central Asia , 2013, PloS one.

[30]  David C. Tank,et al.  A Southern Hemisphere origin for campanulid angiosperms, with traces of the break-up of Gondwana , 2013, BMC Evolutionary Biology.

[31]  Hong‐xiang Zhang,et al.  Identifying a contact zone between two phylogeographic lineages of Clematis sibirica (Ranunculeae) in the Tianshan and Altai Mountains , 2012 .

[32]  S. Sanderson,et al.  Phylogeography of the rare Gymnocarpos przewalskii (Caryophyllaceae): indications of multiple glacial refugia in north-western China , 2012 .

[33]  M. Suchard,et al.  Bayesian Phylogenetics with BEAUti and the BEAST 1.7 , 2012, Molecular biology and evolution.

[34]  Xingjin He,et al.  S-DIVA (Statistical Dispersal-Vicariance Analysis): A tool for inferring biogeographic histories. , 2010, Molecular phylogenetics and evolution.

[35]  A. Graham Late Cretaceous and Cenozoic History of Latin American Vegetation and Terrestrial Environments , 2010 .

[36]  Wang Li The uplift history of south-western Tianshan—Implications from AFT analysis of detrital samples , 2010 .

[37]  E. Zavaleta,et al.  Biodiversity management in the face of climate change: A review of 22 years of recommendations , 2009 .

[38]  Richard H. Ree,et al.  Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. , 2008, Systematic biology.

[39]  J. Muller Fossil pollen records of extant angiosperms , 2008, The Botanical Review.

[40]  Zhang Jie,et al.  Characteristics of Water Cycle in the Qilian Mountains and the Oases in Hexi Inland River Basins , 2008 .

[41]  M. Möller,et al.  High variation and strong phylogeographic pattern among cpDNA haplotypes in Taxus wallichiana (Taxaceae) in China and North Vietnam , 2007, Molecular ecology.

[42]  Joey Shaw,et al.  Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. , 2007, American journal of botany.

[43]  Laurent Excoffier,et al.  Arlequin (version 3.0): An integrated software package for population genetics data analysis , 2005, Evolutionary bioinformatics online.

[44]  Jianquan Liu,et al.  Radiation and diversification within the Ligularia-Cremanthodium-Parasenecio complex (Asteraceae) triggered by uplift of the Qinghai-Tibetan Plateau. , 2006, Molecular phylogenetics and evolution.

[45]  Hongwen Huang,et al.  Development and characterization of polymorphic microsatellite loci in endangered fern Adiantum reniforme var. sinense , 2006, Conservation Genetics.

[46]  X. Jiong-xin Precipitation¿vegetation coupling and its influence on erosion on the Loess Plateau, China , 2005 .

[47]  J. Shaw,et al.  The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. , 2005, American journal of botany.

[48]  J. Bowler,et al.  Timing of the Tianshan Mountains uplift constrained by magnetostratigraphic analysis of molasse deposits , 2004 .

[49]  K. Niklas,et al.  The role of Quaternary environmental change in plant macroevolution: the exception or the rule? , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[50]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[51]  Xiangtao Fan,et al.  The variability of NDVI over northwest China and its relation to temperature and precipitation , 2003, IGARSS 2003. 2003 IEEE International Geoscience and Remote Sensing Symposium. Proceedings (IEEE Cat. No.03CH37477).

[52]  L. Excoffier,et al.  A simulated annealing approach to define the genetic structure of populations , 2002, Molecular ecology.

[53]  G. Hewitt The genetic legacy of the Quaternary ice ages , 2000, Nature.

[54]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[55]  H. Bandelt,et al.  Median-joining networks for inferring intraspecific phylogenies. , 1999, Molecular biology and evolution.

[56]  R. Petit,et al.  Measuring and testing genetic differentiation with ordered versus unordered alleles. , 1996, Genetics.

[57]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[58]  E. Pahlich,et al.  A rapid DNA isolation procedure for small quantities of fresh leaf tissue , 1980 .