Genetic structure of the endangered, relict shrub Amygdalus mongolica (Rosaceae) in arid northwest China
Song Mei Ma A G H , Ying Bin Nie B H , Xiao Long Jiang C D , Zhe Xu E and Wan Quan Ji F G
+ Author Affiliations
- Author Affiliations
A College of Science, Shihezi University, Shihezi 832000, Xinjiang, China.
B Institute of Crop Research, Xinjiang Academy of Agri-Reclamation Sciences, Shihezi 832000, Xinjiang, China.
C Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Botanical Garden, Shanghai 201602, China.
D Shanghai Chenshan Plant Science Research Center, Chinese Academy of Sciences, Shanghai 201602, China.
E The Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, Xinjiang, China.
F State Key Laboratory of Crop Stress Biology for Arid Areas, College of Agronomy (Northwest A&F University), Yangling 712100, China.
G Corresponding authors. Email: shzmsm@126.com; jiwanquan2008@126.com
H *These author contributed equally to this work.
Australian Journal of Botany 67(2) 128-139 https://doi.org/10.1071/BT18188
Submitted: 5 October 2018 Accepted: 18 March 2019 Published: 3 May 2019
Abstract
In the present study we selected the endangered species Amygdalus mongolica to investigate the influence of climatic fluctuations on the spatial genetic patterns and evolutionary history of organisms in arid northwest China. The intraspecific genetic variation and demographic history of A. mongolica were investigated using two cpDNA sequences (psbK-psbI and trnL-trnF) from 174 individuals in 15 populations across most of its covered range. Significant genetic differentiation among populations was identified, which resulted from fragmented populations coupled with the enhanced aridification and desertification of the Pleistocene. Twelve haplotypes clustered into two clades, corresponding to the Western region (northernmost Gansu, Hexi Corridor and Alxa Left Banner) and the Eastern region (Urad Houqi, Yinshan Mountains, Urad Zhongqi and Daqing Mountains) respectively. Five independent Pleistocene refugia in different mountainous areas were identified. Amygdalus mongolica has likely experienced westward shifts from refugia along the margins of the Ulanbuhe and Tengger deserts, and also postglacial re-colonisation northward along the Hexi Corridor.
Additional keywords: demography, genetic differentiation, refugia.
References
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.| Median-joining networks for inferring intraspecific phylogenies.Crossref | GoogleScholarGoogle Scholar | 10331250PubMed |
Bennett K (2004) Continuing the debate on the role of quaternary environmental change for macroevolution. Philosophical Transactions of the Royal Society Biological Sciences 359, 295–303.
| Continuing the debate on the role of quaternary environmental change for macroevolution.Crossref | GoogleScholarGoogle Scholar | 15101585PubMed |
Broadhurst LM, Mellick R, Knerr N, Li L, Supple MA (2018) Land availability may be more important than genetic diversity in the range shift response of a widely distributed eucalypt, Eucalyptus melliodora. Forest Ecology and Management 409, 38–46.
| Land availability may be more important than genetic diversity in the range shift response of a widely distributed eucalypt, Eucalyptus melliodora.Crossref | GoogleScholarGoogle Scholar |
Chen DM, Zhang XX, Kang HZ, Sun X, Yin S, Du HM, Yamanaka N, Gapare W, Wu HX, Liu CJ (2012) Phylogeography of Quercus variabilis based on chloroplast DNA sequence in East Asia: multiple glacial refugia and mainland-migrated island populations. PLoS One 7, e47268
| Phylogeography of Quercus variabilis based on chloroplast DNA sequence in East Asia: multiple glacial refugia and mainland-migrated island populations.Crossref | GoogleScholarGoogle Scholar |
Clegg MT, Gaut BS, Learn GH, Morton BR (1994) Rates and patterns of chloroplast DNA evolution. Proceedings of the National Academy of Sciences of the United States of America 91, 6795–6801.
| Rates and patterns of chloroplast DNA evolution.Crossref | GoogleScholarGoogle Scholar | 8041699PubMed |
Collins WD, Bitz CM, Blackmon ML, Bonan GB, Bretherton CS, Carton JA, Chang P, Doney SC, Hack JJ, Henderson TB, Kiehl JT, Large WG, McKenna DS, Santer BD, Smith RD (2006) The community climate system model version 3 (CCSM3). Journal of Climate 19, 2122–2143.
| The community climate system model version 3 (CCSM3).Crossref | GoogleScholarGoogle Scholar |
Comes HP, Kadereit JW (1998) The effect of quaternary climatic changes on plant distribution and evolution. Trends in Plant Science 3, 432–438.
| The effect of quaternary climatic changes on plant distribution and evolution.Crossref | GoogleScholarGoogle Scholar |
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf material. Phytochemical Bulletin 19, 11–15.
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214
| BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar | 17996036PubMed |
Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Molecular Ecology 11, 2571–2581.
| A simulated annealing approach to define the genetic structure of populations.Crossref | GoogleScholarGoogle Scholar | 12453240PubMed |
Dutech C, Maggia L, Joly H (2000) Chloroplast diversity in Vouacapoua Americana (Caesalpiniaceae), a neotropical forest tree. Molecular Ecology 9, 1427–1432.
| Chloroplast diversity in Vouacapoua Americana (Caesalpiniaceae), a neotropical forest tree.Crossref | GoogleScholarGoogle Scholar | 10972782PubMed |
Elith J, Phillips SJ, Hastie T, Dudik M (2011) A statistical explanation of MaxEnt for ecologists. Diversity & Distributions 17, 43–57.
| A statistical explanation of MaxEnt for ecologists.Crossref | GoogleScholarGoogle Scholar |
Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
| Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar | 21565059PubMed |
Falchi A, Paolini J, Desjobert JM, Melis A, Costa J, Varesi L (2009) Phylogeography of Cistus creticus L. on Corsica and Sardinia inferred by the trnL-F and rpl32-trnL sequences of cpDNA. Molecular Phylogenetics and Evolution 52, 538–543.
| Phylogeography of Cistus creticus L. on Corsica and Sardinia inferred by the trnL-F and rpl32-trnL sequences of cpDNA.Crossref | GoogleScholarGoogle Scholar | 19364536PubMed |
Fielding AH, Bell JF (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environmental Conservation 24, 38–49.
| A review of methods for the assessment of prediction errors in conservation presence/absence models.Crossref | GoogleScholarGoogle Scholar |
Fu L (1992) ‘China plant red data book rare and endangered plants.’ (Science Press: Beijing)
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking, and background selection. Genetics 147, 915–925.
Futuyma DJ (2010) Evolutionary constraint and ecological consequences. Evolution 64, 1865–1884.
| Evolutionary constraint and ecological consequences.Crossref | GoogleScholarGoogle Scholar | 20659157PubMed |
Gao XY, Meng HH, Zhang ML (2014) Diversification and vicariance of desert plants: Evidence inferred from chloroplast DNA sequence variation of Lagochilus ilicifolius (Lamiaceae). Biochemical Systematics and Ecology 55, 93–100.
| Diversification and vicariance of desert plants: Evidence inferred from chloroplast DNA sequence variation of Lagochilus ilicifolius (Lamiaceae).Crossref | GoogleScholarGoogle Scholar |
Ge X-J, Hwang C-C, Liu Z-H, Huang C-C, Huang W-H, Hung K-H, Wang W-K, Chiang T-Y (2011) Conservation genetics and phylogeography of endangered and endemic shrub Tetraena mongolica (Zygophyllaceae) in Inner Mongolia, China. BMC Genetics 12, 1
| Conservation genetics and phylogeography of endangered and endemic shrub Tetraena mongolica (Zygophyllaceae) in Inner Mongolia, China.Crossref | GoogleScholarGoogle Scholar | 21205287PubMed |
Guan QY, Pan BT, Li N, Zhang JD, Xue LJ (2011) Timing and significance of the initiation of present day deserts in the northeastern Hexi Corridor, China. Palaeogeography, Palaeoclimatology, Palaeoecology 306, 70–74.
| Timing and significance of the initiation of present day deserts in the northeastern Hexi Corridor, China.Crossref | GoogleScholarGoogle Scholar |
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405, 907–913.
| The genetic legacy of the Quaternary ice ages.Crossref | GoogleScholarGoogle Scholar | 10879524PubMed |
Jiang XL, Deng M, Li Y (2016) Evolutionary history of subtropical evergreen broad-leaved forest in Yunnan Plateau and adjacent areas: an insight from Quercus schottkyana (Fagaceae). Tree Genetics & Genomes 12, 104
| Evolutionary history of subtropical evergreen broad-leaved forest in Yunnan Plateau and adjacent areas: an insight from Quercus schottkyana (Fagaceae).Crossref | GoogleScholarGoogle Scholar |
Li WC (1998) ‘The Chinese Quaternary vegetation and environment.’ (Science Press: Beijing)
Li ZH, Chen J, Zhao GF, Guo YP, Kou YX, Ma YZ, Wang G, Ma XF (2012) Response of a desert shrub to past geological and climatic change: a phylogeographic study of Reaumuria soongarica (Tamaricaceae) in western China. Journal of Systematics and Evolution 50, 351–361.
| Response of a desert shrub to past geological and climatic change: a phylogeographic study of Reaumuria soongarica (Tamaricaceae) in western China.Crossref | GoogleScholarGoogle Scholar |
Ma SM, Zhang ML, Sanderson SC (2012a) Phylogeography of the rare Gymnocarpos przewalskii (Caryophyllaceae): indications of multiple glacial refugia in north-western China. Australian Journal of Botany 60, 20–31.
| Phylogeography of the rare Gymnocarpos przewalskii (Caryophyllaceae): indications of multiple glacial refugia in north-western China.Crossref | GoogleScholarGoogle Scholar |
Ma SM, Zhang ML, Sanderson SC (2012b) Phylogeography and conservation genetics of the relic Gymnocarpos przewalskii (Caryophyllaceae) restricted to northwestern China. Conservation Genetics 13, 1531–1541.
| Phylogeography and conservation genetics of the relic Gymnocarpos przewalskii (Caryophyllaceae) restricted to northwestern China.Crossref | GoogleScholarGoogle Scholar |
Ma SM, Nie YB, Duan X, Yu CS, Wang RX (2015) The potential distribution and population protection priority of Amygdalus mongolica. Acta Ecologica Sinica 35, 2960–2966.
Mellick R, Wilson PD, Rossetto M (2014) Demographic history and niche conservatism of tropical rainforest trees separated along an altitudinal gradient of a biogeographic barrier. Australian Journal of Botany 62, 438–450.
| Demographic history and niche conservatism of tropical rainforest trees separated along an altitudinal gradient of a biogeographic barrier.Crossref | GoogleScholarGoogle Scholar |
Meng HH, Zhang ML (2011) Phylogeography of Lagochilus ilicifolius (Lamiaceae) in relation to Quaternary climatic oscillation and aridification in northern China. Biochemical Systematics and Ecology 39, 787–796.
| Phylogeography of Lagochilus ilicifolius (Lamiaceae) in relation to Quaternary climatic oscillation and aridification in northern China.Crossref | GoogleScholarGoogle Scholar |
Meng HH, Gao XY, Huang JF, Zhang ML (2015) Plant phylogeography in arid Northwest China: retrospectives and perspectives. Journal of Systematics and Evolution 53, 33–46.
| Plant phylogeography in arid Northwest China: retrospectives and perspectives.Crossref | GoogleScholarGoogle Scholar |
Newman D, Pilson D (1997) Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution 51, 354–362.
| Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella.Crossref | GoogleScholarGoogle Scholar | 28565367PubMed |
Petit RJ, Grivet D (2002) Optimal randomization strategies when testing the existence of a phylogeographic structure. Genetics 161, 469–471.
Petit RJ, Aguinagalde I, Beaulieu JL, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Muller-Starck GM, Demesure-Musch B, Palme A, Martin P, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300, 1563–1565.
| Glacial refugia: hotspots but not melting pots of genetic diversity.Crossref | GoogleScholarGoogle Scholar |
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecological Modelling 190, 231–259.
| Maximum entropy modeling of species geographic distributions.Crossref | GoogleScholarGoogle Scholar |
Pons O, Petit R (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144, 1237–1245.
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
| Modeltest: testing the model of DNA substitution.Crossref | GoogleScholarGoogle Scholar | 9918953PubMed |
Raes N, Roos MC, Slik J, Van Loon EE, Steege H (2009) Botanical richness and endemicity patterns of Borneo derived from species distribution models. Ecography 32, 180–192.
| Botanical richness and endemicity patterns of Borneo derived from species distribution models.Crossref | GoogleScholarGoogle Scholar |
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552–569.
Saihangerel S (2012) The analysis of allozymic variation and genetic diversity in different Prunus mongolica population. Journal of Chinese Medicinal Materials 35, 195–199.
Sang T, Crawford D, Stuessy T (1997) Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). American Journal of Botany 84, 1120–1136.
| Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae).Crossref | GoogleScholarGoogle Scholar | 21708667PubMed |
Schönswetter P, Stehlik I, Holderegger R, Tribsch A (2005) Molecular evidence for glacial refugia of mountain plants in the European Alps. Molecular Ecology 14, 3547–3555.
| Molecular evidence for glacial refugia of mountain plants in the European Alps.Crossref | GoogleScholarGoogle Scholar | 16156822PubMed |
Shaw J, Small RL (2005) Chloroplast DNA phylogeny and phylogeography of the North American plums (Prunus subgenus Prunus section Prunocerasus, Rosaceae). American Journal of Botany 92, 2011–2030.
| Chloroplast DNA phylogeny and phylogeography of the North American plums (Prunus subgenus Prunus section Prunocerasus, Rosaceae).Crossref | GoogleScholarGoogle Scholar | 21646120PubMed |
Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. American Journal of Botany 94, 275–288.
| Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III.Crossref | GoogleScholarGoogle Scholar | 21636401PubMed |
Shen L, Chen XY, Li YY (2002) Glacial refugia and postglacial recolonization patterns of organisms. Acta Ecologica Sinica 22, 1983–1990.
Shi XJ, Zhang ML (2015) Phylogeographical structure inferred from cpDNA sequence variation of Zygophyllum xanthoxylon across north-west China. Journal of Plant Research 128, 269–282.
| Phylogeographical structure inferred from cpDNA sequence variation of Zygophyllum xanthoxylon across north-west China.Crossref | GoogleScholarGoogle Scholar | 25626403PubMed |
Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology 49, 369–381.
| Gaps as characters in sequence-based phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 12118412PubMed |
Su ZH, Zhang ML (2013) Evolutionary response to quaternary climate aridification and oscillations in north-western China revealed by chloroplast phylogeography of the desert shrub Nitraria sphaerocarpa (Nitrariaceae). Biological Journal of the Linnean Society. Linnean Society of London 109, 757–770.
| Evolutionary response to quaternary climate aridification and oscillations in north-western China revealed by chloroplast phylogeography of the desert shrub Nitraria sphaerocarpa (Nitrariaceae).Crossref | GoogleScholarGoogle Scholar |
Su ZH, Zhang ML, Sanderson SC (2011) Chloroplast phylogeography of Helianthemum songaricum (Cistaceae) from northwestern China: implications for preservation of genetic diversity. Conservation Genetics 12, 1525–1537.
| Chloroplast phylogeography of Helianthemum songaricum (Cistaceae) from northwestern China: implications for preservation of genetic diversity.Crossref | GoogleScholarGoogle Scholar |
Su ZH, Lu W, Zhang ML (2016) Phylogeographical patterns of two closely related desert shrubs, Nitraria roborowskii and N. sphaerocarpa (Nitrariaceae), from arid north-western China. Botanical Journal of the Linnean Society 180, 334–347.
| Phylogeographical patterns of two closely related desert shrubs, Nitraria roborowskii and N. sphaerocarpa (Nitrariaceae), from arid north-western China.Crossref | GoogleScholarGoogle Scholar |
Sun JM, Ding ZL, Liu TS (1998) Desert distributions during the glacial maximum and climatic optimum: example of China. Episodes 21, 28–31.
Taberlet P, Fumagalli L, Wust A, Cosson J (1998) Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology 7, 453–464.
| Comparative phylogeography and postglacial colonization routes in Europe.Crossref | GoogleScholarGoogle Scholar | 9628000PubMed |
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.
| MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0.Crossref | GoogleScholarGoogle Scholar | 17488738PubMed |
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
| CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 7984417PubMed |
Vandergast AG, Perry WM, Lugo RV, Hathaway SA (2011) Genetic landscapes GIS Toolbox: tools to map patterns of genetic divergence and diversity. Molecular Ecology Resources 11, 158–161.
| Genetic landscapes GIS Toolbox: tools to map patterns of genetic divergence and diversity.Crossref | GoogleScholarGoogle Scholar | 21429115PubMed |
Wang Q, Abbott RJ, Yu QS, Lin K, Liu JQ (2013) Pleistocene climate change and the origin of two desert plant species, Pugionium cornutum and Pugionium dolabratum (Brassicaceae), in northwest China. New Phytologist 199, 277–287.
| Pleistocene climate change and the origin of two desert plant species, Pugionium cornutum and Pugionium dolabratum (Brassicaceae), in northwest China.Crossref | GoogleScholarGoogle Scholar | 23550542PubMed |
Wang Q, Zhang ML, Yin LK (2016) Phylogeographic structure of a Tethyan Relict Capparis spinosa (Capparaceae) traces Pleistocene geologic and climatic changes in the Western Himalayas, Tianshan Mountains, and adjacent desert regions. BioMed Research International 2016, art id 5792708
| Phylogeographic structure of a Tethyan Relict Capparis spinosa (Capparaceae) traces Pleistocene geologic and climatic changes in the Western Himalayas, Tianshan Mountains, and adjacent desert regions.Crossref | GoogleScholarGoogle Scholar | 28090537PubMed |
Ward DF (2007) Modelling the potential geographic distribution of invasive ant species in New Zealand. Biological Invasions 9, 723–735.
| Modelling the potential geographic distribution of invasive ant species in New Zealand.Crossref | GoogleScholarGoogle Scholar |
Xu Z, Zhang ML (2015) Phylogeography of the arid shrub Atraphaxis frutescens (Polygonaceae) in Northwestern China: evidence from cpDNA sequences. The Journal of Heredity 106, 184–195.
| Phylogeography of the arid shrub Atraphaxis frutescens (Polygonaceae) in Northwestern China: evidence from cpDNA sequences.Crossref | GoogleScholarGoogle Scholar | 25516612PubMed |
Yang D, Fang XM, Dong GR, Peng ZC, Li JJ (2006) Aeolian deposit evidence for formation and evolution of the Tengger Desert in the north of China since early Pleistocene. Haiyang Dizhi Yu Disiji Dizhi 26, 93–100.
Yazbek M, Oh SH (2013) Peaches and almonds: phylogeny of Prunus subg. Amygdalus (Rosaceae) based on DNA sequences and morphology. Plant Systematics and Evolution 299, 1403–1418.
| Peaches and almonds: phylogeny of Prunus subg. Amygdalus (Rosaceae) based on DNA sequences and morphology.Crossref | GoogleScholarGoogle Scholar |
Yu HB, Zhang YL, Gao JG, Qi W (2014) Visualizing patterns of genetic landscapes and species distribution of Taxus wallichiana (Taxaceae), based on GIS and ecological niche models. Journal of Resources and Ecology 5, 193–202.
| Visualizing patterns of genetic landscapes and species distribution of Taxus wallichiana (Taxaceae), based on GIS and ecological niche models.Crossref | GoogleScholarGoogle Scholar |
Yuan QJ, Zhang ZY, Peng H, Ge S (2008) Chloroplast phylogeography of Dipentodon (Dipentodontaceae) in southwest China and northern Vietnam. Molecular Ecology 17, 1054–1065.
| Chloroplast phylogeography of Dipentodon (Dipentodontaceae) in southwest China and northern Vietnam.Crossref | GoogleScholarGoogle Scholar | 18208489PubMed |
Zhang J, Wang J, Li HY, Zhang HR, Wang YC (2012) Genetic diversity of different eco-geographical populations in endangered plant Prunus mongolica by ISSR Markers. Acta Ecologica Sinica 32, 4443–4452.
| Genetic diversity of different eco-geographical populations in endangered plant Prunus mongolica by ISSR Markers.Crossref | GoogleScholarGoogle Scholar |
Zhang HX, Zhang ML, Sanderson SC (2013) Retreating or standing: responses of forest species and steppe species to climate change in arid Eastern Central Asia. PLoS One 8, e61954
| Retreating or standing: responses of forest species and steppe species to climate change in arid Eastern Central Asia.Crossref | GoogleScholarGoogle Scholar | 23734224PubMed |
Zhao YZ (1995) Study on floristic geographical distribution of Amygdalus mongolica. Acta Scientiarum Naturalium Universitatis NeiMonggol 26, 713–715.
Zhao YZ (1997) Endemic genera and their basic characteristics of the Mongolian Plateau plants. Acta Scientiarum Naturalium Universitatis NeiMongol 28, 547–552.
