Advertisement

Tree Genetics & Genomes

, 12:93 | Cite as

Pollen-mediated gene flow promotes low nuclear genetic differentiation among populations of Cycas debaoensis (Cycadaceae)

  • Yi-Qing Gong
  • Xun GongEmail author
Original Article
First Online:
Part of the following topical collections:
  1. Population structure

Abstract

Cycas debaoensis is a critically endangered cycad species endemic to China. This species is found on two kinds of habitats according to the edaphic differences, sand and karst. A previous chloroplast DNA (cpDNA) study indicated that C. debaoensis had low genetic variation within populations and high genetic differentiation among populations. Because maternally inherited cpDNA does not fully characterize genetic structure of the species, we screened seven low-copy nuclear genes and 17 nuclear microsatellite loci to detect the nuclear genetic diversity, differentiation, and the population structure of C. debaoensis. The nuclear genes revealed higher level of genetic diversity. There were both the same and region-specific haplotypes or alleles between the karst and sand regions. Nuclear gene flow among all the populations was much greater than that of cpDNA, which indicated that pollen-mediated gene flow was much greater than seed-mediated gene flow. This promoted low nuclear genetic differentiation among populations of C. debaoensis. The study suggests that both genetic and anthropogenic disturbances have resulted in the critically endangered status of C. debaoensis.

Keywords

Cycas debaoensis Genetic differentiation Population structure Gene flow Conservation 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

The authors thank Prof. Yu-Chung Chiang from National Sun Yat-sen University, Taiwan for sharing the primers information of low-copy nuclear genes. This research was supported by the United Fund of the NSFC and the Yunnan Natural Science Foundation (U1136602 to X.G.).

Data archiving statement

Our nuclear sequences have been deposited in GenBank, and their accession numbers are KT761200–KT761289, and the details were in Supplemental File 7 Table S5. Primer sequences of the SSR markers used in this study are provided in Supplementary File 2 Table S2.

Supplementary material

11295_2016_1051_MOESM1_ESM.docx (19 kb)
ESM 1 (DOCX 18 kb)
11295_2016_1051_MOESM2_ESM.docx (19 kb)
ESM 2 (DOCX 18 kb)
11295_2016_1051_MOESM3_ESM.docx (21 kb)
ESM 3 (DOCX 20 kb)
11295_2016_1051_MOESM4_ESM.docx (18 kb)
ESM 4 (DOCX 18 kb)
11295_2016_1051_MOESM5_ESM.tiff (73 kb)
ESM 5 (TIFF 73 kb)
11295_2016_1051_MOESM6_ESM.tiff (31 kb)
ESM 6 (TIFF 31 kb)
11295_2016_1051_MOESM7_ESM.docx (18 kb)
ESM 7 (DOCX 18 kb)

References

  1. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics 9:323CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bader E (2005) ArcGIS server administrator and developer guide: ArcGIS 9. ESRI Press 1:1–100Google Scholar
  3. Bai WN, Wang WT, Zhang DY (2014) Contrasts between the phylogeographic patterns of chloroplast and nuclear DNA highlight a role for pollen-mediated gene flow in preventing population divergence in an East Asian temperate tree. Mol Phylogenet Evol 81:37–48, doi:10.1016/j.ympev.2014.08.024
  4. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
  5. Barrett SCH, Kohn JR (1991) Genetic and evolutionary consequences of small population size in plants: implications for conservation. In: Falk DA, Holsinger KE (eds) Genetics and conservation of rare plants. Oxford University Press 1:3–30 Google Scholar
  6. Cantrill D (2000) A petrified cycad trunk from the Late Cretaceous of the Larsen Basin, Antarctica. Alcheringa 24:307–318CrossRefGoogle Scholar
  7. Chaw SM, Walters TW, Chang CC, Hu SH, Chen SH (2005) A phylogeny of cycads (Cycadales) inferred from chloroplast matK gene, trnK intron, and nuclear rDNA ITS region. Mol Phylogenet Evol 37:214–234CrossRefPubMedGoogle Scholar
  8. Chen JR, Zhong YC (1997) Cycas debaoensis Y.C. ZHONG et C.J. Chen—a new cycad from China. Acta Phytotaxon Sin 6:013Google Scholar
  9. Cibrián-Jaramillo A, Daly A, Brenner E, Desalle R, Marler T (2010) When North and South don’t mix: genetic connectivity of a recently endangered oceanic cycad, Cycas micronesica, in Guam using EST-microsatellites. Mol Ecol 19:2364–2379PubMedGoogle Scholar
  10. Cibrián-Jaramillo A, Marler TE (2011) Novel tools for an old lineage: population genomics for cycads. Commun Integr Biol 4:466–468. doi: 10.4161/cib.4.4.15546 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cibrián-Jaramillo A, Marler TE, DeSalle R, Brenner ED (2008) Development of EST-microsatellites from the cycad Cycas rumphii, and their use in the recently endangered Cycas micronesica. Conserv Genet 9:1051–1054CrossRefGoogle Scholar
  12. Cinget B, Gerardi S, Beaulieu J, Bousquet J (2015) Less pollen-mediated gene flow for more signatures of glacial lineages: congruent evidence from balsam fir cpDNA and mtDNA for multiple refugia in eastern and central North America. PLoS One 10:e0122815. doi: 10.1371/journal.pone.0122815 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedPubMedCentralGoogle Scholar
  14. Dehgan B, Yuen C (1983) Seed morphology in relation to dispersal, evolution, and propagation of Cycas L. Botanical Gazette 144:412–418Google Scholar
  15. Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169CrossRefGoogle Scholar
  16. Donaldson JS (2003) Cycads: status survey and conservation action plan. IUCN/SSC Cycad Specialist Group, IUCN, Gland and CambridgeGoogle Scholar
  17. Earl DA (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  18. Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445CrossRefPubMedGoogle Scholar
  19. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  20. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47–50Google Scholar
  21. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515CrossRefGoogle Scholar
  22. 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 14:187CrossRefPubMedPubMedCentralGoogle Scholar
  23. Frankham R, Bradshaw CJ, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63CrossRefGoogle Scholar
  24. Gao Z, Barry AT (1989) A review of fossil cycad megasporophylls, with new evidence of Crossozamia pomel and its associated leaves from the lower permian of Taiyuan, China. Rev Palaeobot Palynol 60:205–223CrossRefGoogle Scholar
  25. Garza J, Williamson E (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318CrossRefPubMedGoogle Scholar
  26. Gong YQ, Zhan QQ, Nguyen KS, Nguyen HT, Wang YH, Gong X (2015) The historical demography and genetic variation of the endangered Cycas multipinnata (Cycadaceae) in the Red River Region, examined by chloroplast DNA sequences and microsatellite markers. PloS one 10 doi:  10.1371/journal.pone.0117719
  27. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9. 3)Google Scholar
  28. Harpending H (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600PubMedGoogle Scholar
  29. Hermsen EJ, Taylor TN, Taylor EL, Stevenson DW (2006) Cataphylls of the Middle Triassic cycad Antarcticycas schopfii and new insights into cycad evolution. Am J Bot 93:724–738CrossRefPubMedGoogle Scholar
  30. Huang XX, Wu M, Song JJ, Liu N, Xing FW (2002) Karyotype analysis of Cycas debaoensis. J Trop Subtrop Bot 11:260–262Google Scholar
  31. Jamieson IG, Allendorf FW (2012) How does the 50/500 rule apply to MVPs? Trends Ecol Evol 27:578–584CrossRefPubMedGoogle Scholar
  32. Ju LP, Kuo CC, Chao YS, Cheng YP, Gong X, Chiang YC (2011) Microsatellite primers in the native perennial cycad Cycas taitungensis (Cycadaceae). Am J Bot 98:e84–e86CrossRefPubMedGoogle Scholar
  33. Jump AS, Marchant R, Penuelas J (2009) Environmental change and the option value of genetic diversity. Trends Plant Sci 14:51–58CrossRefPubMedGoogle Scholar
  34. Keppel G, Hodgskiss PD, Plunkett GM (2008) Cycads in the insular South-west Pacific: dispersal or vicariance? J Biogeogr 35:1004–1015CrossRefGoogle Scholar
  35. Kovach W (1999) MVSP—a multivariate statistical package for Windows, ver. 3.1. Kovach Computing Services, Pentraeth, p 137Google Scholar
  36. Kramer AT, Havens K (2009) Plant conservation genetics in a changing world. Trends Plant Sci 14:599–607CrossRefPubMedGoogle Scholar
  37. Kuchma O, Vornam B, Finkeldey R (2011) Mutation rates in Scots pine (Pinus sylvestris L.) from the Chernobyl exclusion zone evaluated with amplified fragment-length polymorphisms (AFLPs) and microsatellite markers. Mutat Res Genet Toxicol Environ Mutagen 725:29–35CrossRefGoogle Scholar
  38. Li L, Wang ZF, Jian SG, Zhu P, Zhang M, Ye WH, Ren H (2009) Isolation and characterization of microsatellite loci in endangered Cycas changjiangensis (Cycadaceae). Conserv Genet 10:793–795CrossRefGoogle Scholar
  39. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  40. Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237CrossRefGoogle Scholar
  41. Nagalingum N, Marshall C, Quental T, Rai H, Little D, Mathews S (2011) Recent synchronous radiation of a living fossil. Science 334:796–799CrossRefPubMedGoogle Scholar
  42. Naumann J, Symmank L, Samain MS, Müller KF, Neinhuis C, Wanke S (2011) Chasing the hare-evaluating the phylogenetic utility of a nuclear single copy gene region at and below species level within the species rich group Peperomia (Piperaceae). BMC Evol Biol 11:357CrossRefPubMedPubMedCentralGoogle Scholar
  43. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  44. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  45. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  46. Osborne R, Calonje MA, Hill KD, Calonje MA, Hill KD, Stanberg L, Stevenson DW (2012) The world list of cycads. Mem N Y Bot Gard 106:480–510Google Scholar
  47. Sgro CM, Lowe AJ, Hoffmann AA (2011) Building evolutionary resilience for conserving biodiversity under climate change. Evol Appl 4:326–337CrossRefPubMedGoogle Scholar
  48. Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279CrossRefGoogle Scholar
  49. Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562PubMedPubMedCentralGoogle Scholar
  50. Spencer C, Neigel J, Leberg P (2000) Experimental evaluation of the usefulness of microsatellite DNA for detecting demographic bottlenecks. Mol Ecol 9:1517–1528CrossRefPubMedGoogle Scholar
  51. Stevenson DW (1981) Observations on ptyxis, phenology, and trichomes in the Cycadales and their systematic implications. Am J Bot 68:1104–1114. doi: 10.2307/2442720 CrossRefGoogle Scholar
  52. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  53. Terry I, Walter GH, Moore C, Roemer R, Hull C (2007) Odor-mediated push-pull pollination in cycads. Science 318:70CrossRefPubMedGoogle Scholar
  54. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefPubMedPubMedCentralGoogle Scholar
  55. Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO‐CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  56. Wang X, Li N, Wang YD, Zheng SL (2009) The discovery of whole-plant fossil cycad from the Upper Triassic in western Liaoning and its significance. Chin Sci Bull 54:3116–3119CrossRefGoogle Scholar
  57. Wang ZF, Ye WH, Cao HL, Li ZC, Peng SL (2008) Identification and characterization of EST-SSRs and cpSSRs in endangered Cycas hainanensis. Conserv Genet 9:1079–1081CrossRefGoogle Scholar
  58. Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756CrossRefPubMedGoogle Scholar
  59. Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562CrossRefGoogle Scholar
  60. Wolfe KH, Li W-H, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci U S A 84:9054–9058CrossRefPubMedPubMedCentralGoogle Scholar
  61. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159PubMedPubMedCentralGoogle Scholar
  62. Xiao LQ, Gong X (2006) Genetic differentiation and relationships of populations in the Cycas balansae complex (Cycadaceae) and its conservation implications. Ann Bot 97:807–812CrossRefPubMedPubMedCentralGoogle Scholar
  63. Xiao LQ, Möller M (2015) Nuclear ribosomal its functional paralogs resolve the phylogenetic relationships of a late-Miocene radiation cycad Cycas (Cycadaceae). PLoS One 10:e0117971. doi: 10.1371/journal.pone.0117971 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Xiao LQ, Möller M, Zhu H (2010) High nrDNA ITS polymorphism in the ancient extant seed plant Cycas: incomplete concerted evolution and the origin of pseudogenes. Mol Phylogenet Evol 55:168–177CrossRefPubMedGoogle Scholar
  65. Yang SL, Meerow AW (1996) The Cycas pectinata (Cycadaceae) complex: genetic structure and gene flow. Int J Plant Sci 157:468–483CrossRefGoogle Scholar
  66. Yang Y, Li Y, Li LF, Ge XJ, Gong X (2008) Isolation and characterization of microsatellite markers for Cycas debaoensis YC Zhong et CJ Chen (Cycadaceae). Mol Ecol Resour 8:913–915CrossRefPubMedGoogle Scholar
  67. Zhan QQ, Wang JF, Gong X, Peng H (2011) Patterns of chloroplast DNA variation in Cycas debaoensis (Cycadaceae): conservation implications. Conserv Genet 12:959–970CrossRefGoogle Scholar
  68. Zhang FM, Su T, Yang Y, Zhai YH, Ji YH, Chen ST (2010) Development of seven novel EST–SSR markers from Cycas panzhihuaensis (Cycadaceae). Am J Bot 97:e159–e161CrossRefPubMedGoogle Scholar
  69. Zhang M, Wang ZF, Jian SG, Ye WH, Cao HL, Zhu P, Li L (2009) Isolation and characterization of microsatellite markers for Cycas hainanensis CJ Chen (Cycadaceae). Conserv Genet 10:1175–1176CrossRefGoogle Scholar
  70. Zhang W, Yang XJ, Fu XP, Zheng SL, Wang YD (2012) A polyxylic cycad trunk from the Middle Jurassic of western Liaoning, China, and its evolutionary implications. Rev Palaeobot Palynol 183:50–60CrossRefGoogle Scholar
  71. Zhong ZR, Li N, Qian D, Jin JH, Chen T (2011) Maternal inheritance of plastids and mitochondria in Cycas L. (Cycadaceae). Mol Genet Genomics 286:411–416CrossRefPubMedGoogle Scholar
  72. Zonneveld B (2012) Genome sizes for all genera of Cycadales. Plant Biol 14:253–256CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of BotanyChinese Academy of SciencesKunmingChina

Personalised recommendations

Cite article

Buy options