Conservation genetics and geographic patterns of genetic variation of the vulnerable officinal herb Fritillaria walujewii (Liliaceae)
Zhihao Su A D , Borong Pan A , Stewart C. Sanderson B , Xiaojun Shi A and Xiaolong Jiang CA Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China.
B Shrub Sciences Laboratory, Intermountain Research Station, Forest Service, US Department of Agriculture, Utah 84601, USA.
C Shanghai Chenshan Plant Science Research Center, Shanghai Chenshan Botanical Garden, Chinese Academy of Sciences, Shanghai 201602, China.
D Corresponding author. Email: suzh@ms.xjb.ac.cn
Australian Journal of Botany 63(6) 467-476 https://doi.org/10.1071/BT14172
Submitted: 3 July 2014 Accepted: 19 April 2015 Published: 21 May 2015
Abstract
The Chinese herb Fritillaria walujewii Regel is an important officinal species that is vulnerable because of over-harvesting. Here, we examined the geographic pattern of genetic variation across the species entire range, to study its evolution process and give implication needed for the conservation. Nine haplotypes were detected on the basis of three chloroplast spacers. The most common haplotype was central in the haplotype network and was distributed widely from the Yili Valley to the eastern Tianshan Mountains. Genetic variation primarily occurred among populations and SAMOVA groups and the analysis of genetic structure showed a significant correlation between genetic and geographical distance. The fragmented distribution of F. walujewii in deep valleys may cause gene-flow barriers among distant populations and, along with genetic drift, has caused high genetic structure in the species. We identified Xinyuan County as the centre of diversification of F. walujewii, and speculated that populations in the eastern Tianshan Mountains were colonised from the Yili Valley. In relation to conservation management, we identified Xinyuan and Zhaosu County as having a high degree of genetic diversity and these should be the areas of the greatest focus for conservation.
Additional keywords: conservation implications, genetic diversity, genetic structure.
References
Aris-Brosou S, Excoffier L (1996) The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Molecular Biology and Evolution 13, 494–504.| The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xht1Kgurs%3D&md5=67cb80d86b2928215960e921c2bf1ed6CAS | 8742638PubMed |
Avise JC (2000) ‘Phylogeography: the history and formation of species.’ (Harvard University Press: Cambridge, MA)
Avise JC, Walker D (1998) Pleistocene phylogeographic effects on avian populations and the speciation process. Proceedings of the Royal Society of London 265, 457–463.
| Pleistocene phylogeographic effects on avian populations and the speciation process.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3jtFWhsQ%3D%3D&md5=268d8d7bdd6c95a0e61dcb9518a37735CAS |
Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual Review of Ecology and Systematics 18, 489–522.
Bohonak AJ (2002) IBD (isolation by distance): a program for analyses of isolation by distance. The Journal of Heredity 93, 153–154.
| IBD (isolation by distance): a program for analyses of isolation by distance.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zptVSlug%3D%3D&md5=734985461de106226467aee604f8c6e5CAS | 12140277PubMed |
Byrne M (2008) Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography. Quaternary Science Reviews 27, 2576–2585.
| Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography.Crossref | GoogleScholarGoogle Scholar |
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
| TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvV2gtbw%3D&md5=460412404d7cfe32448a1b8ba47d22b5CAS | 11050560PubMed |
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 from small quantities of fresh leaf tissues. Phytochemical Bulletin 19, 11–15.
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 | 1:STN:280:DC%2BD38nptlaksw%3D%3D&md5=ea953a53749a4b44c48b05652b557201CAS | 12453240PubMed |
Excoffier L, Ray N (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends in Ecology & Evolution 23, 347–351.
| Surfing during population expansions promotes genetic revolutions and structuration.Crossref | GoogleScholarGoogle Scholar |
Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: applications to human mitochondrial DNA restriction data. Genetics 131, 479–491.
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1, 47–50.
Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annual Review of Ecology Evolution and Systematics 40, 481–501.
| Genetic consequences of range expansions.Crossref | GoogleScholarGoogle Scholar |
Fehlberg SD, Ranker TA (2009) Evolutionary history and phylogeography of Encelia farinosa (Asteraceae) from the Sonoran, Mojave, and Peninsular Deserts. Molecular Phylogenetics and Evolution 50, 326–335.
| Evolutionary history and phylogeography of Encelia farinosa (Asteraceae) from the Sonoran, Mojave, and Peninsular Deserts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVGqsQ%3D%3D&md5=059233441313d633079a0de62210d619CAS | 19059351PubMed |
Fischer M, Matthies D (1997) Mating structure and inbreeding and outbreeding depression in the rare plant Gentianella germanica (Gentianaceae). American Journal of Botany 84, 1685–1692.
| Mating structure and inbreeding and outbreeding depression in the rare plant Gentianella germanica (Gentianaceae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MnjvVCktg%3D%3D&md5=bd13e95057ccb03ab1345c609efb727bCAS | 21708572PubMed |
Forester BR, DeChaine EG, Bunn AG (2013) Integrating ensemble species distribution modelling and statistical phylogeography to inform projections of climate change impacts on species distributions. Diversity & Distributions 19, 1480–1495.
| Integrating ensemble species distribution modelling and statistical phylogeography to inform projections of climate change impacts on species distributions.Crossref | GoogleScholarGoogle Scholar |
Frankel OH (1983) The place of management in conservation. In ‘Genetics and conservation’. (Eds CM Schonewald-Cox, SM Chambers, B MacBryde, L Thomas L) pp. 1–14. (Benjamin-Cummings: Menlo Park, CA)
Frankham R, Ballou JD, Briscoe DA (2002) ‘Introduction to conservation genetics.’ (Cambridge University Press: Cambridge, UK)
Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology 10, 2741–2752.
| Adaptive evolutionary conservation: towards a unified concept for defining conservation units.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387mvFOjtw%3D%3D&md5=2412fdbcf0eba629adc9ac843bb49889CAS | 11903888PubMed |
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking, and background selection. Genetics 147, 915–925.
Ge XJ, Hwang CC, Liu ZH, Huang CC, Huang WH, Hung KH, Wang WK, Chiang TY (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 | 1:CAS:528:DC%2BC3MXosVOjsw%3D%3D&md5=5595c4cc0b2089ff617f6274550e8705CAS | 21205287PubMed |
Hasumi H, Emori S (2004) ‘K-1 coupled GCM (MIROC) description.’ (Center for Climate System Research, University of Tokyo: Tokyo)
Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of The Royal Society of London Series B, Biologic 359, 183–195.
| Genetic consequences of climatic oscillations in the Quaternary.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c3gsVSjuw%3D%3D&md5=7fc74baf0aae4e0d2eefed0e14b5ba72CAS |
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 1965–1978.
| Very high resolution interpolated climate surfaces for global land areas.Crossref | GoogleScholarGoogle Scholar |
Hu RJ (1998) ‘Physical geography of the Tianshan Mountains in China.’ (China Environmental Science Press: Beijing)
Huelsenbeck JP, Ronquist F (2001) MrBayes: a program for the Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
| MrBayes: a program for the Bayesian inference of phylogeny.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvotV2isw%3D%3D&md5=458690d9a9603af201694797b3e38b1bCAS | 11524383PubMed |
Jaeger JR, Riddle BR, Bradford DF (2005) Cryptic neogene vicariance and Quaternary dispersal of the red-spotted toad (Bufo punctatus): insights on the evolution of North American warm desert biotas. Molecular Ecology 14, 3033–3048.
| Cryptic neogene vicariance and Quaternary dispersal of the red-spotted toad (Bufo punctatus): insights on the evolution of North American warm desert biotas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGltLbP&md5=72b85b88192abb25a901b7e8893db851CAS | 16101772PubMed |
Jia DR, Abbott RJ, Liu TL, Mao KS, Bartish IV, Liu JQ (2012) Out of the Qinghai–Tibet Plateau: evidence for the origin and dispersal of Eurasian temperate plants from a phylogeographic study of Hippophaë rhamnoides (Elaeagnaceae). New Phytologist 194, 1123–1133.
| Out of the Qinghai–Tibet Plateau: evidence for the origin and dispersal of Eurasian temperate plants from a phylogeographic study of Hippophaë rhamnoides (Elaeagnaceae).Crossref | GoogleScholarGoogle Scholar | 22432741PubMed |
Li N, Fu L (1997) Notes on gymnosperms I. Taxonomic treatment of some Chinese conifers. Novon 7, 261–264.
| Notes on gymnosperms I. Taxonomic treatment of some Chinese conifers.Crossref | GoogleScholarGoogle Scholar |
Mellick R, Lowe A, Allen C, Hill RS, Rossetto M (2012) Palaeodistribution modelling and genetic evidence highlight differential post-glacial range shifts of a rain forest conifer distributed across a latitudinal gradient. Journal of Biogeography 39, 2292–2302.
| Palaeodistribution modelling and genetic evidence highlight differential post-glacial range shifts of a rain forest conifer distributed across a latitudinal gradient.Crossref | GoogleScholarGoogle Scholar |
Moritz C (1994) Applications of mitochondrial DNA analysis in conservation: a critical review. Molecular Ecology 3, 401–411.
| Applications of mitochondrial DNA analysis in conservation: a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtlyktrw%3D&md5=3ed54e2fbad7cdcd4f7ae8dd486fbbf3CAS |
Nei M (1987) ‘Molecular evolutionary genetics.’ (Columbia University Press: NewYork)
Nichols RA, Hewitt GM (1994) The genetic consequences of long distance dispersal during colonization. Heredity 72, 312–317.
| The genetic consequences of long distance dispersal during colonization.Crossref | GoogleScholarGoogle Scholar |
Osborne MJ, Norman JA, Christidis L, Murray ND (2000) Genetic distinctness of isolated populations of an endangered marsupial, the mountain pygmy-possum, Burramys parvus. Molecular Ecology 9, 609–613.
| Genetic distinctness of isolated populations of an endangered marsupial, the mountain pygmy-possum, Burramys parvus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3lt12msw%3D%3D&md5=750358bf2773a25a7f5422fda90b86bcCAS | 10792703PubMed |
Oxelman B, Lidén M, Berglund D (1997) Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Plant Systematics and Evolution 206, 393–410.
| Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae).Crossref | GoogleScholarGoogle Scholar |
Peterson AT, Nakazawa Y (2008) Environmental data sets matter in ecological niche modelling: an example with Solenopsis invicta and Solenopsis richteri. Global Ecology and Biogeography 17, 135–144.
Phillips SJ, Dudík M (2008) Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31, 161–175.
| Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation.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 |
Pope LC, Sharp A, Moritz C (1998) The genetic diversity and distinctiveness of the yellow-footed rock-wallaby Petrogale xanthopus (Gray, 1854) in New South Wales Pacific. Conservation Biology 4, 164–169.
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 | 1:CAS:528:DyaK1MXktlCltw%3D%3D&md5=efc7af3b0c4019e31f1e57d17909accbCAS | 9918953PubMed |
Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conservation Biology 17, 230–237.
| Correlation between fitness and genetic diversity.Crossref | GoogleScholarGoogle Scholar |
Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant-tissues. Plant Molecular Biology Reporter 5, 69–76.
| Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant-tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlvFalsrk%3D&md5=a7e0a8a60b027d468527b4073c285419CAS |
Rogers A, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552–569.
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=6d0dbb2a0d91e525d9f9009ea3f38ec7CAS | 12912839PubMed |
Rosenberg MS (2001) ‘PASSAGE: pattern analysis, spatial statistics and geographic exegesis. Ver. 1.1.’ (Department of Biology, Arizona State University: Tucson, AZ)
Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends in Ecology & Evolution 1, 9–10.
| Species conservation and systematics: the dilemma of subspecies.Crossref | GoogleScholarGoogle Scholar |
Sang T, Crawford DJ, Stuessy TF (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 | 1:CAS:528:DyaK2sXlvFejuro%3D&md5=9603f08b07b09255549c5f69a93ff820CAS | 21708667PubMed |
Shaw J, Lickey E, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. American Journal of Botany 92, 142–166.
| The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Klsbc%3D&md5=5327a0aa93d73519dee5791af9ac7e3cCAS | 21652394PubMed |
Shi YF, Cui ZJ, Su Z (2005) ‘The quaternary glaciations and environmental variations in China.’ (Hebei Science and Technology Publishing House: Hebei, China)
Simmons MP, Ochoterena H (2000) Gaps as characters in sequencebased phylogenetic analyses. Systematic Biology 49, 369–381.
| Gaps as characters in sequencebased phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zntlKjtg%3D%3D&md5=a96b4f815a87e4f7e4f9201e5ce5adfaCAS | 12118412PubMed |
Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129, 555–562.
Smith CI, Farrell BD (2005) Range expansions in the flightless longhorn cactus beetles, Moneilema gigas and Moneilema armatum, in response to Pleistocene climate changes. Molecular Ecology 14, 1025–1044.
| Range expansions in the flightless longhorn cactus beetles, Moneilema gigas and Moneilema armatum, in response to Pleistocene climate changes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsFalt78%3D&md5=4aa229683fdff3bff4906a24ed353e1aCAS | 15773934PubMed |
Su ZH, Zhang ML (2013) Evolutionary response to Quaternary climate aridification and oscillations in northwestern China revealed by chloroplast phylogeography of 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 northwestern China revealed by chloroplast phylogeography of Nitraria sphaerocarpa (Nitrariaceae).Crossref | GoogleScholarGoogle Scholar |
Swets JA (1988) Measuring the accuracy of diagnostic systems. Science 240, 1285–1293.
| Measuring the accuracy of diagnostic systems.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c3jsF2jtQ%3D%3D&md5=51a58dd2d33300420a84b196e4767d5cCAS | 3287615PubMed |
Taberlet P, Cheddadi R (2002) Quaternary refugia and persistence of biodiversity. Science 297, 2009–2010.
| Quaternary refugia and persistence of biodiversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVehtr4%3D&md5=3c68507efe9bf8e354e5e66669c48dd3CAS | 12242431PubMed |
Tajima F (1983) Evolutionary relationships of DNA sequences in finite populations. Genetics 105, 437–460.
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.
Tajima F (1996) The amount of DNA polymorphism maintained in a finite population when the neutral mutation rate varies among sites. Genetics 143, 1457–1465.
Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619–633.
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 | 1:CAS:528:DyaK2MXitlSgu74%3D&md5=7a346316d0bceda10425a7c114233981CAS | 7984417PubMed |
Wang FZ, Tang J (1980) Liliaceae. In ‘Flora of China, vol 14’. (Eds ZY Wu, PH Raven) p. 102. (Science Press: Beijing)
Wei WS, Hu RJ (1990) Precipitation and climate conditions of Tianshan Mountains. Arid Land Geography 13, 29–36.
Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAS. Proceedings of The National Academy of Sciences, USA 84, 9054–9058.
| Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXovVyktQ%3D%3D&md5=1dfc57a799216a8f750f0a0d3375a0c4CAS |
Wu LL, Cui XK, Milne RI, Sun YS, Liu JQ (2010a) Multiple autopolyploidizations and range expansion of Allium przewalskianum Regel. (Alliaceae) in the Qinghai–Tibetan Plateau. Molecular Ecology 19, 1691–1704.
| Multiple autopolyploidizations and range expansion of Allium przewalskianum Regel. (Alliaceae) in the Qinghai–Tibetan Plateau.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtlGisr8%3D&md5=f53e1132958d50f8eb045ba4214b99c9CAS | 20345685PubMed |
Yin LK, Tan LX, Wang B (2006) ‘Rare endanged endemic higher plants in XinJiang of China.’ (Science Press: Urumqi, China)
Zhang JM (2006) Studies on the geological structures and characteristic of terrain and landform in Yili river basin. Journal of Shihezi University 24, 442–445.
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 | 1:CAS:528:DC%2BC3sXmslSjs74%3D&md5=ffc859cc7a809e702699877dee0238fdCAS | 23596532PubMed |