Abstract
Understanding the population genetic structure and demographic history helps in the management and restoration of endangered species. Cycas panzhihuaensis (Panzihihua sago palm) is narrowly distributed in the eastern Sichuan Basin of China. The only extant population is in the Panzhihua Cycad Nature Reserve (PCNR), which is close to Panzhihua City, and is threatened by the mining industry and slash-and-burn agriculture. To protect this rare species, the local government implemented an ex situ conservation project. In this study, amplified fragment length polymorphism (AFLP) was used to explore the genetic diversity of wild and cultivated populations. Two evolutionarily significant units (ESUs) in PCNR were determined based on significant differences in genetic diversity and demographic histories. The western ESU has low genetic diversity and shares common genotypes with a part of the eastern ESU. The founder effect is suggested as the best-fit scenario to explain the current genetic distribution among the eastern and western ESUs. Small carrying capacity limits both census and effective population sizes, and the gene surfing hypothesis explains the high frequency of fixed alleles without private alleles in multiple loci in the western subpopulation. Every cultivated population, established for either conservation or horticultural purposes, has only genotypes from a single ESU. Supplementary collection for ex situ conservation is suggested to preserve the genetic features of C. panzhihuaensis.
Similar content being viewed by others
References
Alvarez-Yepiz JC, Dovciak M, Burquez A (2011) Persistence of a rare ancient cycad: effects of environment and demography. Biol Conserv 144:122–130. doi:10.1016/j.biocon.2010.08.007
Bacles CFE, Ennos RA (2008) Paternity analysis of pollen-mediated gene flow for Fraxinus excelsior L. in a chronically fragmented landscape. Heredity 101:368–380. doi:10.1038/Hdy.2008.66
Beerli P (2004) Effect of unsampled populations on the estimation of population sizes and migration rates between sampled populations. Mol Ecol 13:827–836. doi:10.1111/j.1365-294X.2004.02101.x
Bensch S, Akesson M (2005) Ten years of AFLP in ecology and evolution: why so few animals? Mol Ecol 14:2899–2914. doi:10.1111/j.1365-294X.2005.02655.x
Bertorelle G, Benazzo A, Mona S (2010) ABC as a flexible framework to estimate demography over space and time: some cons, many pros. Mol Ecol 19:2609–2625. doi:10.1111/j.1365-294X.2010.04690.x
Chiang YC et al (2009) Paraphyly of organelle DNAs in Cycas Sect. Asiorientales due to ancient ancestral polymorphisms. BMC Evol Biol 9:161. doi:10.1186/1471-2148-9-161
Chiang YC, Huang BH, Chang CW, Wan YT, Lai SJ, Huang S, Liao PC (2013) Asymmetric introgression in the horticultural living fossil Cycas Sect. Asiorientales using a genome-wide scanning approach. Int J Mol Sci 14:8228–8251. doi:10.3390/Ijms14048228
Dehgan B, Yuen CKKH (1983) Seed morphology in relation to dispersal, evolution, and propagation of Cycas L. Bot Gaz 144:412–418. doi:10.1086/337391
Donaldson JS, Dehgan B, Vovides AP, Tang W (2003) Chapter 7: cycads in trade and sustainable use of cycad populations. In: Donaldson JS (ed) Cycads: status survey and conservation action plan. IUCN/SSC Cycad Specialist Group. IUCN, Gland, Switzerland and Cambridge, pp 39–47
Doyle J, Doyle J (1987) Genomic plant DNA preparation from fresh tissue-CTAB method. Phytochem Bull 19:11–15
Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192. doi:10.1093/molbev/msi103
Duan L, Min Q, Zhang H, Li H, Zhang Z (2013) Research progress of landslide dam events of Jinsha River and its geomorphologic and environmental effects. Adv Geosci 3:8–17
Earl DA, Vonholdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. doi:10.1007/s12686-011-9548-7
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. doi:10.1111/j.1365-294X.2005.02553.x
Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578. doi:10.1111/j.1471-8286.2007.01758.x
Fay JC, Wu CI (2000) Hitchhiking under positive Darwinian selection. Genetics 155:1405–1413
Fayard J, Klein EK, Lefevre F (2009) Long distance dispersal and the fate of a gene from the colonization front. J Evol Biol 22:2171–2182. doi:10.1111/j.1420-9101.2009.01832.x
Feng XY, Wang YH, Gong X (2014) Genetic diversity, genetic structure and demographic history of Cycas simplicipinna (Cycadaceae) assessed by DNA sequences and SSR markers. BMC Plant Biol 14:187. doi:10.1186/1471-2229-14-187
Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Genet Res 66:95–107
Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, red list criteria and population viability analyses. Biol Conserv 170:56–63. doi:10.1016/j.biocon.2013.12.036
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Gaston KJ (2009) Geographic range limits: achieving synthesis. P Roy Soc B Biol Sci 276:1395–1406. doi:10.1098/rspb.2008.1480
Geertsema M, Pojar JJ (2007) Influence of landslides on biophysical diversity—a perspective from British Columbia. Geomorphology 89:55–69
Griffith MP et al (2015) Can a botanic garden cycad collection capture the genetic diversity in a wild population? Int J Plant Sci 176:1–10. doi:10.1086/678466
Guillot G, Santos F (2010) Using AFLP markers and the Geneland program for the inference of population genetic structure. Mol Ecol Resour 10:1082–1084. doi:10.1111/j.1755-0998.2010.02864.x
Guillot G, Mortier F, Estoup A (2005) GENELAND: a computer package for landscape genetics. Mol Ecol Notes 5:712–715. doi:10.1111/j.1471-8286.2005.01031.x
Guillot G, Santos F, Estoup A (2008) Analysing georeferenced population genetics data with Geneland: a new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics 24:1406–1407. doi:10.1093/bioinformatics/btn136
Guimaraes PR, Galetti M, Jordano P (2008) Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate. PLoS ONE 3, e1745. doi:10.1371/Journal.Pone.0001745
Hall JA, Walter GH (2014) Relative seed and fruit toxicity of the Australian cycads Macrozamia miquelii and Cycas ophiolitica: further evidence for a megafaunal seed dispersal syndrome in cycads, and its possible antiquity. J Chem Ecol 40:860–868. doi:10.1007/s10886-014-0490-5
Hallatschek O, Nelson DR (2008) Gene surfing in expanding populations. Theor Popul Biol 73:158–170. doi:10.1016/j.tpb.2007.08.008
Hill KD, Chen CJ, Loc PK (2003) Chapter 5: regional overview: Asia. In: Donaldson JS (ed) Cycads: status survey and conservation action plan. IUCN/SSC Cycad Specialist Group. IUCN, Gland, Switzerland and Cambridge, pp 25–30
Hoebee SE, Arnold U, Duggelin C, Gugerli F, Brodbeck S, Rotach P, Holderegger R (2007) Mating patterns and contemporary gene flow by pollen in a large continuous and a small isolated population of the scattered forest tree Sorbus torminalis. Heredity 99:47–55. doi:10.1038/sj.hdy.6800962
Holsinger KE, Lewis PO, Dey DK (2002) A Bayesian approach to inferring population structure from dominant markers. Mol Ecol 11:1157–1164. doi:10.1046/j.1365-294X.2002.01512.x
Holt RD (1987) Population dynamics and evolutionary processes: the manifold roles of habitat selection. Evol Ecol 1:331–347. doi:10.1007/Bf02071557
Huang S, Chiang YC, Schaal BA, Chou CH, Chiang TY (2001) Organelle DNA phylogeography of Cycas taitungensis, a relict species in Taiwan. Mol Ecol 10:2669–2681. doi:10.1046/j.0962-1083.2001.01395.x
Huang B-H, Ruan Y, Li J-Q, Liao P-C (2015) Applying effective population size estimates of Kandelia obovata Sheue, Liu & Yong to conservation and restoration management. Forest 6:1439–1453. doi:10.3390/f6051439
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332. doi:10.1111/j.1755-0998.2009.02591.x
Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914. doi:10.2307/2640449
Jensen JD, Kim Y, DuMont VB, Aquadro CF, Bustamante CD (2005a) Distinguishing between selective sweeps and demography using DNA polymorphism data. Genetics 170:1401–1410. doi:10.1534/genetics.104.038224
Jensen JL, Bohonak AJ, Kelley ST (2005b) Isolation by distance, web service. BMC Genet 6:13. doi:10.1186/1471-2156-6-13
Jian SG, Zhong Y, Liu N, Gao ZZ, Wei Q, Xie ZH, Ren H (2006) Genetic variation in the endangered endemic species Cycas fairylakea (Cycadaceae) in China and implications for conservation. Biodivers Conserv 15:1681–1694. doi:10.1007/s10531-004-5017-x
Jiarui C, Stevenson DW (1999) Cycadaceae. In: Wu ZY, Raven PH (eds) Flora of China, vol. 4. Science Press and Missouri Botanical Garden Press, Beijing, pp 1–7
Jorde PE, Palm S, Ryman N (1999) Estimating genetic drift and effective population size from temporal shifts in dominant gene marker frequencies. Mol Ecol 8:1171–1178. doi:10.1046/j.1365-294x.1999.00676.x
Keller LF, Jeffery KJ, Arcese P, Beaumont MA, Hochachka WM, Smith JNM, Bruford MW (2001) Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers. P Roy Soc B Biol Sci 268:1387–1394
Keppel G, Lee SW, Hodgskiss PD (2002) Evidence for long isolation among populations of a pacific cycad: genetic diversity and differentiation in Cycas seemannii A.B..r. (Cycadaceae). J Hered 93:133–139. doi:10.1093/jhered/93.2.133
Kono M, Tobe H (2007) Is Cycas revoluta (Cycadaceae) wind- or insect-pollinated? Am J Bot 94:847–855. doi:10.3732/Ajb.94.5.847
Krauss SL (2000) Accurate gene diversity estimates from amplified fragment length polymorphism (AFLP) markers. Mol Ecol 9:1241–1245. doi:10.1046/j.1365-294x.2000.01001.x
Li CL, Wang Q, Jiang SY, Ge S, Wang KQ (1999) Genetic diversity of allozymes in populations of Cycas panzhihuaensis L. Zhou & S.Y. Yang. Paper presented at the biology and conservation of cycads. Proceedings of the Fourth International Conference on Cycad Biology. Panzhihua
Mekanawakul M, Thongtham M, Chalermglin P, Srifah P, Juntawong N (2003) Diversity and genetic variation among population of Thai cycads revealed by AFLP markers. Suranaree J Sci Technol 10:317–328
Min L, Yin Z, Zhang J (1990) The formation time and paleoenvironment of the Longjie silt bed. Quat Sci 10:354–362
Nagalingum NS, Marshall CR, Quental TB, Rai HS, Little DP, Mathews S (2011) Recent synchronous radiation of a living fossil. Science 334:796–799. doi:10.1126/science.1209926
Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155. doi:10.1111/j.1365-294X.2004.02141.x
Opgen-Rhein R, Fahrmeir L, Strimmer K (2005) Inference of demographic history from genealogical trees using reversible jump Markov chain Monte Carlo. BMC Evol Biol 5:6. doi:10.1186/1471-2148-5-6
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539. doi:10.1093/bioinformatics/bts460
Pierce AA et al (2014) Serial founder effects and genetic differentiation during worldwide range expansion of monarch butterflies. Proc R Soc B Biol Sci 281. doi:10.1098/Rspb.2014.2230
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Pybus OG, Harvey PH (2000) Testing macro-evolutionary models using incomplete molecular phylogenies. P Roy Soc B Biol Sci 267:2267–2272
Rabosky DL (2006) Likelihood methods for detecting temporal shifts in diversification rates. Evolution 60:1152–1164
Radha P, Singh R (2011) Amplified fragment length polymorphism (AFLP) studies on Indian Cycas species. Afr J Biotechnol 10:6381–6386
Reinartz JA, Les DH (1994) Bottleneck-induced dissolution of self-incompatibility and breeding system consequences in Aster Furcatus (Asteraceae). Am J Bot 81:446–455. doi:10.2307/2445494
Reisch C, Bernhardt-Romermann M (2014) The impact of study design and life history traits on genetic variation of plants determined with AFLPs. Plant Ecol 215:1493–1511. doi:10.1007/s11258-014-0409-9
Robledo-Arnuncio JJ, Klein EK, Muller-Landau HC, Santamaría L (2014) Space, time and complexity in plant dispersal ecology. Mov Ecol 2:16
Rosenberg NA, Nordborg M (2002) Genealogical trees, coalescent theory and the analysis of genetic polymorphisms. Nat Rev Genet 3:380–390. doi:10.1038/Nrg795
Ruan Y, Huang BH, Lai SJ, Wan YT, Li JQ, Huang S, Liao PC (2013) Population genetic structure, local adaptation, and conservation genetics of Kandelia obovata. Tree Genet Genomes 9:913–925. doi:10.1007/s11295-013-0605-0
Salas-Leiva DE et al (2013) Phylogeny of the cycads based on multiple single-copy nuclear genes: congruence of concatenated parsimony, likelihood and species tree inference methods. Ann Bot Lond 112:1263–1278. doi:10.1093/Aob/Mct192
Schutkowski H (2006) Chapter 5: population development and regulation. In: Czeschlik D (ed) Human ecology: biocultural adaptations in human communities. Ecological studies, vol. 182. Springer-Verlag Berlin Heidelberg, Germany, pp 183–250
Selwood KE, McGeoch MA, Mac Nally R (2014) The effects of climate change and land-use change on demographic rates and population viability. Biol Rev. doi:10.1111/brv.12136
Shellnutt JG, Jahn BM (2010) Formation of the late Permian Panzhihua plutonic-hypabyssal-volcanic igneous complex: implications for the genesis of Fe-Ti oxide deposits and A-type granites of SW China. Earth Planet Sci Lett 289:509–519. doi:10.1016/j.epsl.2009.11.044
Shellnutt JG, Zhou MF (2007) Permian peralkaline, peraluminous and metaluminous A-type granites in the Panxi district, SW China: their relationship to the Emeishan mantle plume. Chem Geol 243:286–316. doi:10.1016/j.chemgeo.2007.05.022
Shen HH, Chiang YC (2014) Phylogenetic relationships and divergence time estimation in section Asiorentales, Panzhihuaensis, Stangerioides and Wadeanae. In: The 6th China National Cycad Symposium. Cycad Conservation Committee of China Wild Plant Conservation Association, Panzhihua City 21–23
Vos P et al (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414. doi:10.1093/nar/23.21.4407
Vucetich JA, Waite TA, Nunney L (1997) Fluctuating population size and the ratio of effective to census population size. Evolution 51:2017–2021. doi:10.2307/2411022
Waters JM, Fraser CI, Hewitt GM (2013) Founder takes all: density-dependent processes structure biodiversity. Trends Ecol Evol 28:78–85. doi:10.1016/j.tree.2012.08.024
White GM, Boshier DH, Powell W (2002) Increased pollen flow counteracts fragmentation in a tropical dry forest: an example from Swietenia humilis Zuccarini. Proc Natl Acad Sci U S A 99:2038–2042. doi:10.1073/pnas.042649999
Wu Q, Zheng PP, Hu YB, Wei FW (2014) Genome-scale analysis of demographic history and adaptive selection. Protein Cell 5:99–112. doi:10.1007/s13238-013-0004-1
Xiao LQ, Gong X (2006) Genetic differentiation and relationships of populations in the Cycas balansae complex (Cycadaceae) and its conservation implications. Ann Bot Lond 97:807–812. doi:10.1093/Aob/Mcl039
Xiao LQ, Ge XJ, Gong X, Hao G, Zheng SX (2004) ISSR variation in the endemic and endangered plant Cycas guizhouensis (Cycadaceae). Ann Bot Lond 94:133–138. doi:10.1093/Aob/Mch119
Zhong H, Zhu WG, Hu RZ, Xie LW, He DF, Liu F, Chu ZY (2009) Zircon U-Pb age and Sr-Nd-Hf isotope geochemistry of the Panzhihua A-type syenitic intrusion in the Emeishan large igneous province, southwest China and implications for growth of juvenile crust. Lithos 110:109–128. doi:10.1016/j.lithos.2008.12.006
Acknowledgments
Our deepest gratitude goes to Dr. Shong Huang for his valuable assistance and helpful suggestions. We also thank Dr. J.G. Shellnutt for providing geological information of Panzhihua areas. This research is finically supported by the Society of Subtropical Ecology, Sichuan Panzhihua Cycad National Nature Reserve Administration, and National Science Council in Taiwan (NSC 102-2621-B-003-005-MY3). This article was also subsidized by the National Taiwan Normal University (NTNU), Taiwan.
Conflict of interest
The authors declare that they have no competing interest.
Compliance with ethical standards
The authors declare that all experiments described herein comply with the law of government in which they were carried out.
Data archiving statement
Data used in this study are publically available in Supplemental File 4.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P. Ingvarsson
This article is part of the Topical Collection on Gene Conservation
Yong-Qiong Yang, Bing-Hong Huang and Zhi-Xiang Yu contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Fig. S1
Distribution of allele frequency of each population shown in a normal quantile plot and bar plot. Thin lines in the normal quantile plot are distribution of expectations. Population Wuding is excluded in this analysis because of small sample size (only two samples) (PDF 426 kb)
Fig. S2
Correlation between the genetic distance (number of differences) and geographic distance (km2) of sampled individuals in the PCNR of C. panzhihuaensis in Panzhihua City, Sichuan Province in China (PDF 324 kb)
Table S1
Sampling information (DOCX 30 kb)
Table S2
AFLP primers information (DOCX 15 kb)
Table S3
Model test for the diversification rate of C. panzhihuaensis lineages. The best-fit models were marked in bold (DOCX 19 kb)
ESM 6
The AFLP data used in this study (TXT 56 kb)
Rights and permissions
About this article
Cite this article
Yang, YQ., Huang, BH., Yu, ZX. et al. Inferences of demographic history and fine-scale landscape genetics in Cycas panzhihuaensis and implications for its conservation. Tree Genetics & Genomes 11, 78 (2015). https://doi.org/10.1007/s11295-015-0894-6
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11295-015-0894-6