Skip to main content
Log in

Demography of the upward-shifting temperate woody species of the Rhododendron pseudochrysanthum complex and ecologically relevant adaptive divergence in its trailing edge populations

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Trailing edge populations of upward migrating species induced by postglacial climatic warming can be evolutionarily significant in the face of global warming. We tested for population size changes between lower- and higher-elevation populations located in the same mountainous regions of the upward-shifting temperate woody species of the Rhododendron pseudochrysanthum complex in Taiwan. We also tested whether natural selection evoked adaptive divergence in trailing edge populations of this species complex. We genotyped 26 expressed sequence tag-simple sequence repeat (EST-SSR) loci of 185 individuals from nine populations of the R. pseudochrysanthum complex including Rhododendron rubropunctatum, Rhododendron hyperythrum, Rhododendron morii, and R. pseudochrysanthum. R. rubropunctatum populations in the R. pseudochrysanthum complex possessed the lowest estimates of genetic diversity and effective population size. Higher-elevation R. pseudochrysanthum populations had lower effective population sizes than lower-elevation R. morii populations in Hohuanshan and Tahsueshan, as revealed by estimates using both MIGRATE-N and approximate Bayesian computation (ABC). R. rubropunctatum populations diverged significantly from populations of other members of the R. pseudochrysanthum complex. An outlier potentially under positive selection specific to R. rubropunctatum populations was identified and strongly associated with ecologically relevant environmental variables. Postglacial climatic warming has a significant influence on population isolation in the R. pseudochrysanthum complex. The results indicate adaptive evolution in the trailing edge populations, i.e., R. rubropunctatum populations of the upward shifting R. pseudochrysanthum complex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abdo Z, Crandall KA, Joyce P (2004) Evaluating the performance of likelihood methods for detecting population structure and migration. Mol Ecol 13:837–851

    Article  PubMed  Google Scholar 

  • Ackerly DD (2003) Community assembly, niche conservatism, and adaptive evolution in changing environments. Int J Plant Sci 164:S165–S184

    Article  Google Scholar 

  • Beaumont MA, Balding DJ (2004) Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol 13:969–980

    Article  CAS  PubMed  Google Scholar 

  • Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lon Ser B Biol Sci 263:1619–1626

    Article  Google Scholar 

  • Beaumont MA, Zhang W, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035

    PubMed  Google Scholar 

  • Bolte S, Schiene K, Dietz KJ (2000) Characterization of a small GTP-binding protein of the rab 5 family in Mesembryanthemum crystallinum with increased level of expression during early salt stress. Plant Mol Biol 42:923–36

    Article  CAS  PubMed  Google Scholar 

  • Booy G, Hendriks RJJ, Smulders MJM, Van Groenendael M, Vosman B (2000) Genetic diversity and the survival of populations. Plant Biol 2:379–395

    Article  Google Scholar 

  • Carrera-Hernández JJ, Gaskin SJ (2007) Spatio temporal analysis of daily precipitation and temperature in the basin of Mexico. J Hydrol 336:231–249

    Article  Google Scholar 

  • Chung J-D, Lin T-P, Chen Y-L, Cheng Y-B, Hwang S-Y (2007) Phylogeographic study reveals the origin and evolutionary history of a Rhododendron species complex in Taiwan. Mol Phylogent Evol 42:14–24

    Article  CAS  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  Google Scholar 

  • Cornuet J-M, Santos F, Beaumont MA, Robert CP, Marin J-M, Balding DJ, Guillemaud T, Estoup A (2008) Inferring population history with DIYABC: a user-friendly approach to approximate Bayesian computations. Bioinformatics 24:2713–2719

    Article  CAS  PubMed  Google Scholar 

  • Cornuet J-M, Ravigné V, Estoup A (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinforma 11:401

    Article  Google Scholar 

  • Cross JR (1975) Biological flora of the British Isles: Rhododendron ponticum L. J Ecol 63:345–364

    Article  Google Scholar 

  • Dieringer D, Schlötterer C (2003) Microsatellite Analyser: a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169

    Article  CAS  Google Scholar 

  • Dirnböck T, Essl F, Rabitsch W (2011) Disproportional risk for habitat loss of high-altitude endemic species under climate change. Global Change Biol 17:990–996

    Article  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf material. Phytochem Bull 19:11–15

    Google Scholar 

  • Ebine K, Fujimoto M, Okatani Y, Nishiyama T, Goh T, Ito E, Dainobu T, Nishitani A, Uemura T, Sato MH, Thordal-Christensen H, Tsutsumi N, Nakano A, Ueda T (2011) A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat Cell Biol 13:853–859

    Article  CAS  PubMed  Google Scholar 

  • Ebine K, Miyakawa N, Fujimoto M, Uemura Y, Nakano A, Ueda T (2012) Endosomal trafficking pathway regulated by ARA6, a RAB5 GTPase unique to plants. Small GTPases 3:23–27

    Article  PubMed Central  PubMed  Google Scholar 

  • Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol 17:1170–1188

    Article  CAS  PubMed  Google Scholar 

  • Ellis JR, Burke JM (2007) EST-SSRs as a resource for population genetic analyses. Heredity 99:125–132

    Article  CAS  PubMed  Google Scholar 

  • Escaravage N, Pornon A, Doche B, Till-Bottaraud I (1997) Breeding system in an alpine species Rhododendron ferrugineum L. (Ericaceae) in the French northern Alps. Can J Bot 75:736–743

    Article  Google Scholar 

  • Estoup A, Jarne P, Cornuet J-M (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Excoffier L, Hofer T, Foll M (2009) Detecting loci under selection in a hierarchically structured population. Heredity 103:285–298

    Article  CAS  PubMed  Google Scholar 

  • Fagundes NJR, Ray N, Beaumont MA (2007) Statistical evaluation of alternative models of human evolution. Proc Natl Acad Sci U S A 104:17614–17619

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Frankham R (1995) Inbreeding and extinction - a threshold effect. Conser Biol 9:792–799

    Article  Google Scholar 

  • Garcia-Ramos G, Kirkpatrick M (1997) Genetic models of adaptation and gene flow in peripheral populations. Evolution 51:21–28

    Article  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  CAS  PubMed  Google Scholar 

  • Gavrilets S, Vose A (2007) Case studies and mathematical models of ecological speciation. 2. Palms on an oceanic island. Mol Ecol 16:2910–2921

    Article  PubMed  Google Scholar 

  • Girod C, Vitalis R, Leblois R, Fréville H (2011) Inferring population decline and expansion from microsatellite data: a simulation-based evaluation of the Msvar method. Genetics 188:165–179

    Article  PubMed  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices. Version 2.9.3. http://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 11 March 2013

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  CAS  PubMed  Google Scholar 

  • Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467

    Article  PubMed  Google Scholar 

  • Hardy EA, Spaeth PA, Li C (2009) Niche conservatism above the species level. Proc Natl Acad Sci U S A 106:19707–19714

    Article  Google Scholar 

  • Herrera C, Bazaga P (2008) Adding a third dimension to the edge of a species’ range: altitude and genetic structuring in mountainous landscapes. Heredity 100:275–285

    Article  CAS  PubMed  Google Scholar 

  • Hirao AS (2010) Kinship between parents reduces offspring fitness in a natural population of Rhododendron brachycarpum. Ann Bot 105:637–646

    Article  PubMed  Google Scholar 

  • Holderegger R, Herrmann D, Poncet B, Gugerli F, Thuiller W, Taberlet P, Gielly L, Rioux D, Brodbeck S, Aubert S, Manel S (2008) Land ahead: using genome scans to identify molecular markers of adaptive divergence. Plant Ecol Divers 1:273–283

    Article  Google Scholar 

  • Holliday JA, Suren H, Aitken SN (2012) Divergent selection and heterogeneous migration rates across the range of Sitka spruce (Picea sitchensis). Proc R Soc B 279:1675–1683

    Article  PubMed  Google Scholar 

  • Huang C-C, Hung K-H, Hwang C-C, Huang J-C, Lin H-D, Wang W-K, Wu P-Y, Hsu T-W, Chiang T-Y (2011) Genetic population structure of the alpine species Rhododendron pseudochrysanthum sensu lato (Ericaceae) inferred from chloroplast and nuclear DNA. BMC Evol Biol 11:108

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hurlbert SH (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586

    Article  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Joost S, Bonin A, Bruford MW, Després L, Conord C, Erhardt G, Taberlet P (2007) A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation. Mol Ecol 16:3955–3969

    Article  CAS  PubMed  Google Scholar 

  • Joost S, Kalbermatten M, Bonin A (2008) Spatial analysis method (SAM): a software tool combining molecular and environmental data to identify candidate loci for selection. Mol Ecol Res 8:957–960

    Article  Google Scholar 

  • Jump AS, Mátyás C, Peñuelas J (2009) The altitude-for-latitude disparity in range retractions of woody species. Trends Ecol Evol 24:694–701

    Article  PubMed  Google Scholar 

  • Jump AS, Huang T-J, Chou C-H (2012) Rapid altitudinal migration of mountain plants in Taiwan and its implications for high altitude biodiversity. Ecography 35:204–210

    Article  Google Scholar 

  • Kalinowski ST (2005) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Kameyama Y, Isagi Y, Nakagoshi N (2000) Microsatellite analysis of pollen flow in Rhododendron metternichii var. hondoense. Ecol Res 15:263–269

    Article  Google Scholar 

  • Kameyama Y, Isagi Y, Nakagoshi N (2001) Patterns and levels of gene flow in Rhododendron metternichii var. hondoense revealed by microsatellite analysis. Mol Ecol 10:205–216

    Article  CAS  PubMed  Google Scholar 

  • Kane NC, Rieseberg LH (2007) Selective sweeps reveal candidate genes for adaptation to drought and salt tolerance in common sunflower, Helianthus annuus. Genetics 175:1823–1824

    Article  CAS  PubMed  Google Scholar 

  • Kirkpatrick M, Barton NH (1997) Evolution of a species’ range. Am Nat 150:1–23

    Article  CAS  PubMed  Google Scholar 

  • Kondo T, Nakagishi N, Isagi Y (2009) Shaping of genetic structure along Pleistocene and modern river systems in the hydrochorous riparian azalea, Rhododendron ripense (Ericaceae). Am J Bot 96:1532–1543

    Article  PubMed  Google Scholar 

  • Körner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22:569–574

    Article  PubMed  Google Scholar 

  • Lee C-Y, Liew P-M (2009) Late Quaternary vegetation and climate changes inferred from a pollen record of Dongyuan lake in southern Taiwan. Palaeogeo Palaeoclim Palaeoecol 287:58–66

    Article  Google Scholar 

  • Lenoir J, Gégout JC, Marquet PA, de Ruffray P, Brisse H (2008) A significant upward shift in plant species optimum elevation during the 20th century. Science 320:1768–1771

    Article  CAS  PubMed  Google Scholar 

  • Levin DA (2012) Mating system shifts on the trailing edge. Ann Bot 109:613–620

    Article  PubMed  Google Scholar 

  • Li H-L, Lu S-Y, Yang Y-P, Tseng Y-H (1998) Ericaceae. In: Editorial Committee of the Flora of Taiwan (ed) Flora of Taiwan, vol 4, 2nd edn. Taipei, Taiwan, pp 17–39

  • Liew P-M, Chung N-J (2001) Vertical migration of forests during the last glacial period in subtropical Taiwan. West Pac Earth Sci 1:405–414

    Google Scholar 

  • Liew P-M, Kuo C-M, Huang S-Y (1998) Vegetation change and terrestrial carbon storage of eastern Asia during the last glacial maximum as indicated by new pollen records of northern Taiwan. Global Plant Change 16:85–94

    Article  Google Scholar 

  • Liew P-M, Huang S-Y, Kuo C-M (2006) Pollen stratigraphy, vegetation and environment of the last glacial and Holocene-A record from Toushe Basin, central Taiwan. Quat Internl 147:16–33

    Article  Google Scholar 

  • Mäkinen HS, Shikano T, Cano JM, Merilä J (2008) Hitchhiking mapping reveals a candidate genomic region for natural selection in three-spined Stickleback chromosome VIII. Genetics 178:453–465

    Article  PubMed  Google Scholar 

  • Marriage TN, Hudman S, Mort ME, Orive ME, Shaw RG, Kelly JK (2009) Direct estimation of the mutation rate at dinucleotide microsatellite loci in Arabidopsis thaliana (Brassicaceae). Heredity 103:310–317

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Marshall DL, Avritt JJ, Maliakal-Witt S, Medeiros JS, Shaner MGM (2010) The impact of plant and flower age on mating patterns. Ann Bot 105:7–22

    Article  PubMed  Google Scholar 

  • Nosil P, Egan SP, Funk DJ (2008) Heterogeneous genomic differentiation between walking-stick ecotypes: ‘isolation by adaptation’ and multiple roles for divergent selection. Evolution 62:316–336

    Article  PubMed  Google Scholar 

  • Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155

    Article  CAS  PubMed  Google Scholar 

  • Ohsawa T, Ide Y (2008) Global patterns of genetic variation in plant species along vertical and horizontal gradients on mountains. Global Ecol Biogeogr 17:152–163

    Article  Google Scholar 

  • Ono A, Dohzono I, Sugawara T (2008) Bumblebee pollination and reproductive biology of Rhododendron semibarbatum (Ericaceae). J Plant Res 121:319–327

    Article  PubMed  Google Scholar 

  • Parisod C, Joost S (2010) Divergent selection in trailing- versus leading-edge populations of Biscutella laevigata. Ann Bot 105:655–660

    Article  CAS  PubMed  Google Scholar 

  • Pascual M, Chapuis MP, Mestres F, Balanyá J, Huey RB, Gilchrist GW, Serra L, Estoup A (2007) Introduction history of Drosophila subobscura in the New World: a microsatellite based survey using ABC methods. Mol Ecol 16:3069–3083

    Article  CAS  PubMed  Google Scholar 

  • Pearson G, Lago-Leston A, Mota C (2009) Frayed at the edges: selective pressure and adaptive response to abiotic stressors are mismatched in low diversity edge populations. J Ecol 97:450–462

    Article  Google Scholar 

  • Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Bëer E, Robinson S, Vásquez-Carrillo C, Pauli JN, Palsbøll PJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418

    Article  PubMed  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

  • Quiroga MP, Premoli AC (2007) Genetic patterns in Podocarpus parlatorei reveal the long-term persistence of cold-tolerant elements in the southern Yungas. J Biogeogr 34:447–455

    Article  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci U S A 94:9197–9201

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) Genepop (version 1.2): Population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Savolainen O, Kujala ST, Sokol C, Pyhäjärvi T, Avia K, Knürr T, Kärkkäinen K, Hicks S (2011) Adaptive potential of northernmost tree populations to climate change, with emphasis on Scots pine (Pinus sylvestris L.). J Hered 102:526–536

    Article  PubMed  Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford

    Google Scholar 

  • Thuiller E, Albert C, Araujo M, Berry P, Cabeza M, Guisan A, Hickler T, Midgley G, Paterson J, Schurr F (2008) Predicting global change impacts on plant species’ distributions: Future challenges. Pers Plant Ecol Evol System 9:137–152

    Article  Google Scholar 

  • Tsukada M (1966) Late Pleistocene vegetation and climate in Taiwan (Formosa). Proc Natl Acad Sci U S A 55:543–548

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Peter S (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Vernoud V, Horton AC, Yang ZB, Nielsen E (2003) Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol 131:1191–1208

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vitalis R, Dawson K, Boursot P (2001) Interpretation of variation across marker loci as evidence of selection. Genetics 158:1811–1823

    CAS  PubMed  Google Scholar 

  • Vitalis R, Dawson K, Boursot P, Belkhir K (2003) DetSel 1.0: A computer program to detect markers responding to selection. J Hered 94:429–431

    Article  CAS  PubMed  Google Scholar 

  • Wiens J, Graham C (2005) Niche conservatism: Integrating evolution, ecology, and conservation biology. Annu Rev Ecol Evol Syst 36:519–539

    Article  Google Scholar 

  • Woollard AD, Moore I (2008) The functions of Rab GTPases in plant membrane traffic. Curr Opin Plant Biol 11:1–10

    Article  Google Scholar 

  • Zhang L, Tian LH, Zhao JF, Song Y, Zhang CJ, Guo Y (2009) Identification of an apoplastic protein involved in the initial phase of salt stress response in rice root by two-dimensional electrophoresis. Plant Physiol 149:916–928

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Council, Executive Yuan, Taiwan (grant number NSC97-2313-B-003-002-MY3) to SYH. The authors are grateful to Yushan National Park for allowing them to collect plant materials. Funding for a graduate studentship to BKL and YCH and a postdoctoral associateship to CYC and CTC by the National Science Council is also acknowledged.

Data Archiving Statement

EST-SSR genotyping data of this study were deposited at Dryad: http://doi.org/10.5061/dryad.m33cb.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shih-Ying Hwang.

Additional information

Communicated by P. Ingvarsson

Chen and Liang contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 245 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, CY., Liang, BK., Chung, JD. et al. Demography of the upward-shifting temperate woody species of the Rhododendron pseudochrysanthum complex and ecologically relevant adaptive divergence in its trailing edge populations. Tree Genetics & Genomes 10, 111–126 (2014). https://doi.org/10.1007/s11295-013-0669-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-013-0669-x

Keywords

Navigation