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Disentangling the effects of isolation-by-distance and isolation-by-environment on genetic differentiation among Rhododendron lineages in the subgenus Tsutsusi

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Abstract

Ecological speciation has long been noted as a central topic in the field of evolutionary biology, and investigation into the relative importance of ecological and geographical factors is becoming increasingly emphasized. We surveyed genetic variation of 277 samples from 25 populations of nine Rhododendron species within Tsutsusi subgenus in Taiwan using simple sequence repeats of expressed sequence tags. Bayesian clustering revealed four genetic lineages: (1) the Rhododendron simsii, Rhododendron kanehirai, and Rhododendron nakaharae lineage (lineage 1); (2) the Rhododendron longiperulatum, Rhododendron breviperulatum, and Rhododendron noriakianum lineage (lineage 2); (3) the Rhododendron rubropilosum lineage (lineage 3); and (4) the Rhododendron oldhamii lineage (lineage 4). Asymmetric introgressions were found from lineage 3 into lineages 1 and 2 (introgressed lineages). Genetic admixture of non-R. oldhamii species was also revealed by a neighbor-joining tree. Variation partitioning showed that environment explained much larger portions of genetic variation than geography between non-introgressed lineages (i.e., between R. oldhamii and other lineages). However, the Mantel and partial Mantel tests and the multiple matrix regression with randomization found that isolation-by-distance played a more important role than isolation-by-environment (IBE) in contributing to genetic variation in most between lineage comparisons. Nevertheless, strong IBE was found when compared between non-introgressed lineages of R. oldhamii and R. rubropilosum, suggesting post-speciation ecological divergence. Several environmental variables, including annual mean temperature, aspect, isothermality, seasonal precipitation, slope, and soil pH, could be important ecological drivers involved in reproductive isolation between R. oldhamii and non-R. oldhamii species within the Tsutsusi subgenus.

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References

  • Abbott R, Albach D, Ansell S et al (2013) Hybridization and speciation. J Evol Biol 26:229–246

    Article  CAS  PubMed  Google Scholar 

  • Abreu IA, Cabelli DE (2009) Superoxide dismutases—a review of the metal-associated mechanistic variations. Biochim Biophys Acta 1804:263–274

    Article  PubMed  CAS  Google Scholar 

  • Alberto FJ, Aitken SN, Alía R et al (2013) Potential for evolutionary responses to climate change—evidence from tree populations. Glob Chang Biol 19:1645–1661

    Article  PubMed  PubMed Central  Google Scholar 

  • Allen AP, Gillooly JF, Savage VM, Brown JH (2006) Kinetic effects of temperature on rates of genetic divergence and speciation. Proc Natl Acad Sci U S A 103:9130–9135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allendorf FW, Luikart GH, Aitken SN (2012) Conservation and the genetics of populations. Blackwell, West Sussex

    Google Scholar 

  • Ammal EKJ (1950) Polyploidy in the genus Rhododendron. Rhododendron Year Book 5:92–98

    Google Scholar 

  • Anacker BL, Strauss SY (2014) The geography and ecology of plant speciation: range overlap and niche divergence in sister species. Proc R Soc B 281:20132980

    Article  PubMed  PubMed Central  Google Scholar 

  • Arnold ML (2006) Evolution through genetic exchange. Oxford University Press, Oxford

    Google Scholar 

  • Arnold ML, Martin NH (2009) Adaptation by introgression. J Biol 8:82

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, Oxford, pp 3–30

    Google Scholar 

  • Barton NH (2001) The role of hybridization in evolution. Mol Ecol 10:551–568

    Article  CAS  PubMed  Google Scholar 

  • Batelli G, Verslues PE, Agius F et al (2007) SOS2 promotes salt tolerance in part by interacting with the vacuolar H+-ATPase and upregulating its transport activity. Mol Cell Biol 27:7781–7790

    Article  CAS  PubMed  PubMed Central  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 Lond B 263:1619–1626

    Article  Google Scholar 

  • Bekh-Ochir D, Shimada S, Yamagami A et al (2013) A novel mitochondrial DnaJ/Hsp40 family protein BIL2 promotes plant growth and resistance against environmental stress in brassinosteroid signaling. Planta 237:1509–1525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632

    Article  PubMed  Google Scholar 

  • Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbor matrices. Ecol Model 153:51–68

    Article  Google Scholar 

  • Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73:1045–1055

    Article  Google Scholar 

  • Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New York

    Book  Google Scholar 

  • Burgess KS, Morgan M, Deverno L, Husband BC (2005) Asymmetrical introgression between two Morus species (M. alba, M. rubra) that differ in abundance. Mol Ecol 14:3471–3483

    Article  CAS  PubMed  Google Scholar 

  • Caballero A, Rodriguez-Ramilo S (2010) A new method for the partition of allelic diversity within and between subpopulations. Conserv Genet 11:2219–2229

    Article  Google Scholar 

  • Caballero A, Rodriguez-Ramilo S, Avila V, Fernandez J (2010) Management of genetic diversity of subdivided populations in conservation programmes. Conserv Genet 11:409–419

    Article  Google Scholar 

  • Chang CT, Lin TC, Lin NH (2009) Estimating the critical load and the environmental and economic impact of acid deposition in Taiwan. J Geogr Sci 56:39–58 (In Chinese)

    Google Scholar 

  • Chang CT, Wang SF, Vadeboncoeur MA, Lin TC (2014) Relating vegetation dynamics to temperature and precipitation at monthly and annual timescales in Taiwan using MODIS vegetation indices. Int J Remote Sens 35:598–620

    Article  Google Scholar 

  • Chen C-Y, Liang B-K, Chung J-D, Chang C-T, Hsieh Y-C, Lin T-C, Hwang S-Y (2014) Demography of the upward-shifting temperate woody species of the Rhododendron pseudochrysanthum complex and ecologically relevant adaptive divergence in its trailing edge populations. Tree Genet Genomes 10:111–126

    Article  CAS  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland

    Google Scholar 

  • D’Aman M, Zimmermann NE, Pearman PB (2013) Conservation of phylogeographic lineages under climate change. Glob Ecol Biogeogr 22:93–104

    Article  Google Scholar 

  • De Schepper S, Leus L, Mertens M, Van Bockstaele E, De Loose M (2001) Flow cytometric analysis of ploidy in Rhododendron (subgenus Tsutsusi). HortSci 36:125–127

    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 

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

    Google Scholar 

  • Dray S (2013) packfor: forward selection with permutation (Canoco p.46), R package version 0.0-8. Available at: http://r-forge.r-project.org/R/?group_id=195. Accessed 25 Oct 2013

  • Eeckhaut T, Samyn G, Van Bockstaele E (2003) Interspecific breeding in the Rhododendron genus involving R. simsii hybrids. Acta Hortic 612:165–172

    Article  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 

  • Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242

    Article  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 Resour 10:564–567

    Article  PubMed  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 

  • Fernández J, Toro MA, Caballero A (2004) Managing individuals’ contributions to maximize the allelic diversity maintained in small, conserved populations. Conserv Biol 18:1–10

    Article  Google Scholar 

  • Foll M, Gaggiotti O (2008) A genome scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993

    Article  PubMed  PubMed Central  Google Scholar 

  • Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion. Accessed 8 Mar 2016

  • Fraser LG, Harvey CF, Crowhurst RN, De Silva HN (2004) EST-derived microsatellites from Actinidia species and their potential for mapping. Theor Appl Genet 108:1010–1016

    Article  CAS  PubMed  Google Scholar 

  • Funk DJ, Nosil P, Etges WJ (2006) Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proc Natl Acad Sci U S A 103:3209–3213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gangappa SN, Botto JF (2014) The BBX family of plant transcription factors. Trends Plant Sci 19:460–470

    Article  CAS  PubMed  Google Scholar 

  • Georgian E, Fang Z, Emshwiller E, Pidgeon A (2015) The pollination ecology of Rhododendron floccigerum Franchet (Ericaceae) in Weixi, Yunnan Province, China. J Pollination Ecol 16:72–81

    Google Scholar 

  • Gevaudant F, Duby von Stedingk E et al (2007) Expression of a constitutively activated plasma membrane H+-ATPase alters plant development and increases salt tolerance. Plant Physiol 144:1763–1776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Givnish TJ (2010) Ecology of plant speciation. Taxon 59:1326–1366

    Google Scholar 

  • 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 

  • Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc Lond B 351:1291–1298

    Article  Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Article  Google Scholar 

  • Hill WG, Rasbash J (1986) Models of long term artificial selection in finite populations. Genet Res 48:41–50

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485

    Article  CAS  PubMed  Google Scholar 

  • Hsieh Y-C, Chung J-D, Wang C-N, Chang C-T, Chen C-Y, Hwang S-Y (2013) Historical connectivity, contemporary isolation and local adaptation in a widespread but discontinuously distributed species endemic to Taiwan, Rhododendron oldhamii (Ericaceae). Heredity 111:147–156

    Article  PubMed  PubMed Central  Google Scholar 

  • Huete AR, Didan K, Miura T, Rodriguez EP, Gao X, Ferreira LG (2002) Overview of the radiometric and biophysical performance of the MODIS vegetation indices. Remote Sens Environ 83:195–213

    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 

  • Jeffreys H (1961) Theory of probability, 3rd edn. Oxford University Press, Oxford

    Google Scholar 

  • Jiggins CD, Mallet J (2000) Bimodal hybrid zones and speciation. Trends Ecol Evol 15:250–255

    Article  PubMed  Google Scholar 

  • Jones JR, Ranney TG, Lynch NP (2007) Ploidy levels and relative genome sizes of diverse species, hybrids, and cultivars of Rhododendron. J Am Rhododendron Soc 61:220–227

    Google Scholar 

  • Jump AS, Marchant R, Peñuelas J (2009) Environmental change and the option value of genetic diversity. Trends Plant Sci 14:51–58

    Article  CAS  PubMed  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 

  • Kamvar ZN, Grünwald NJ (2015) Algorithms and equations utilized in poppr version 2.1. 0. Available at: http://CRAN.R-project.org/package=poppr. Accessed 7 Mar 2016

  • Kaplan F, Guy CL (2004) β-Amylase induction and the protective role of maltose during temperature Shock. Plant Physiol 135:1674–1684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kay K (2006) Reproductive isolation between two closely related hummingbird-pollinated neotropical gingers. Evolution 60:538–552

    PubMed  Google Scholar 

  • Kim M, Cui M-L, Cubas P, Gillies A, Lee K, Chapman MA, Abbott RJ, Coen E (2008) Regulatory genes control a key morphological and ecological trait transferred between species. Science 322:1116–1119

    Article  CAS  PubMed  Google Scholar 

  • Kozak KH, Graham CH, Wiens JJ (2008) Integrating GIS-based environmental data into evolutionary biology. Trends Ecol Evol 23:141–148

    Article  PubMed  Google Scholar 

  • Kron KA, Powell EA (2009) Molecular systematics of Rhododendron subgenus Tsutsusi (Rhodoreae, Ericoideae, Ericaceae). Edinb J Bot 66:81–95

    Article  Google Scholar 

  • Kudo G (1993) Relationship between flowering time and fruit set of the entomophilous alpine shrub, Rhododendron aureum (Ericaceae), inhabiting snow patches. Am J Bot 80:1300–1304

    Article  Google Scholar 

  • Kuussaari M, Bommarco R, Heikkinen RK et al (2009) Extinction debt: a challenge for biodiversity conservation. Trends Ecol Evol 24:564–571

    Article  PubMed  Google Scholar 

  • Lavergne S, Evans MEK, Burfield IJ, Jiguet F, Thuiller W (2013) Are species’ responses to global change predicted by past niche evolution? Philos Trans R Soc B 368:1610

    Google Scholar 

  • Ledig FT (1992) Human impacts on genetic diversity in forest ecosystems. OIKOS 63:87–108

    Article  Google Scholar 

  • Leigh F, Lea V, Law J, Wolters P, Powell W, Donini P (2003) Assessment of EST- and genomic microsatellite markers for variety discrimination and genetic diversity studies in wheat. Euphytica 133:359–366

    Article  CAS  Google Scholar 

  • Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952

    Article  Google Scholar 

  • Lenormand T, Raymond M (2000) Analysis of clines with variable selection and variable migration. Am Nat 155:70–82

    Article  PubMed  Google Scholar 

  • Lepais O, Petit RJ, Guichox E, Lavabre JE, Alberto F (2009) Species relative abundance and direction of introgression in oaks. Mol Ecol 18:2228–2242

    Article  CAS  PubMed  Google Scholar 

  • Levin DA, Francisco-Ortega J, Jansen RK (1996) Hybridization and the extinction of rare plant species. Conserv Biol 10:10–16

    Article  Google Scholar 

  • Li H-L (1978) Ericaceae. In: Li HL et al (eds) Flora of Taiwan, 1st edn. National Taiwan University, Taipei, pp 15–46

    Google Scholar 

  • Li H-L, Lu S-Y, Yang Y-P Tseng YH (1998) Ericaceae. In: Huang T-C et al (eds) Flora of Taiwan, 2nd edn. National Taiwan University, Taipei, pp 17–39

    Google Scholar 

  • Liu J-Z, Whitham SA (2013) Overexpression of a soybean nuclear localized type–III DnaJ domain-containing HSP40 reveals its roles in cell death and disease resistance. Plant J 74:110–121

    Article  CAS  PubMed  Google Scholar 

  • Liu M, Shi J, Lu C (2013) Identification of stress-responsive genes in Ammopiptanthus mongolicus using ESTs generated from cold- and drought-stressed seedlings. BMC Plant Biol 13:88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin NH, Bouck AC, Arnold ML (2006) Detecting adaptive trait introgression between Iris fulva and I. brevicaulis in highly selective field conditions. Genetics 172:2481–2489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McLaughlin JF, Hellman JJ, Boggs CL, Ehrlich PR (2002) Climate change hastens population extinctions. Proc Natl Acad Sci U S A 99:6070–6074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milne RI, Abbott RJ (2008) Reproductive isolation among two interfertile Rhododendron species: low frequency of post-F1 hybrid genotypes in alpine hybrid zones. Mol Ecol 17:1108–1121

    Article  CAS  PubMed  Google Scholar 

  • Moran EV, Willis J, Clark JS (2012) Genetic evidence for hybridization in red oaks (Quercus sect. Lobatae, Fagaceae). Am J Bot 99:92–100

    Article  PubMed  Google Scholar 

  • Nakazato T, Bogonovich M, Moyle LC (2007) Environmental factors predict adaptive phenotypic differentiation within and between two wild Andean tomatoes. Evolution 62:774–792

    Article  CAS  Google Scholar 

  • Nakazato T, Warren DL, Moyle LC (2010) Ecological and geographic modes of species divergence in wild tomatoes. Am J Bot 97:680–693

    Article  PubMed  Google Scholar 

  • Nei M (1972) Genetic distances between populations. Am Nat 106:283–292

    Article  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 

  • Oksanen J, Blanchet FG, Kindt R et al (2011) Vegan: community ecology package. R package version 2.0-1. Available at: http://CRAN.R-project.org/package=vegan. Accessed 31 Dec 2013

  • 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 

  • Oubory NJ, Pertoldi C, Loeschcke V, Bijlsma R, Hedrick PW (2010) Conservation genetics in transition to conservation genomics. Trends Genet 26:177–187

    Article  CAS  Google Scholar 

  • Papadopulos AST, Kaye M, Devaux C et al (2014) Evaluation of genetic isolation within an island flora reveals unusually widespread local adaptation and supports sympatric speciation. Philos Trans R Soc B 369:20130342

    Article  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Pashley CH, Ellis JR, McCauley DE, Burke JM (2006) EST databases as a source for molecular markers: lessons from Helianthus. J Hered 97:381–388

    Article  CAS  PubMed  Google Scholar 

  • Pease JB, Haak DC, Hahn MW, Moyle LC (2016) Phylogenomics reveals three sources of adaptive variation during a rapid radiation. PLoS Biol 14:e1002379

    Article  PubMed  PubMed Central  Google Scholar 

  • Pembleton LW, Cogan NOI, Forster FW (2013) StAMPP: an R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Mol Ecol Resour 13:946–952

    Article  CAS  PubMed  Google Scholar 

  • Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87:2614–2625

    Article  PubMed  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Pilon M, Cohu CM, Ravet K, Abdel-Ghany SE, Gaymard F (2009) Essential transition metal homeostasis in plants. Curr Opion Plant Biol 12:347–357

    Article  CAS  Google Scholar 

  • Prasch CM, Ott KV, Bauer H, Ache P, Herich R, Sonnewald U (2015) ß-amylase1 mutant Arabidopsis plants show improved drought tolerance due to reduced starch breakdown in guard cells. J Exp Bot 66:6059–6067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing, version 3.0.0. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org/

  • Ramsey J, Bradshaw HD, Schemske DW (2003) Components of reproductive isolation between the monkey flowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57:1520–1534

    Article  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 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ruiz-Sanchez E, Specht CD (2014) Ecological speciation in Nolina parviflora (Asparagaceae): lacking spatial connectivity along of the Trans-Mexican volcanic belt. PLoS ONE 9:e98754

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rungis D, Bérubé Y, Zhang J et al (2004) Robust simple sequence repeat markers for spruce (Picea spp.) from expressed sequence tags. Theor Appl Genet 109:1283–1294

    Article  CAS  PubMed  Google Scholar 

  • Schlüter D (2009) Evidence for ecological speciation and its alternative. Science 323:737–741

    Article  PubMed  CAS  Google Scholar 

  • Schlüter D, Conte GL (2009) Genetics and ecological speciation. Proc Natl Acad Sci U S A 106:9955–9962

    Article  PubMed  PubMed Central  Google Scholar 

  • Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207

    Article  PubMed  Google Scholar 

  • Seehausen O, Takimoto G, Roy D, Jokela J (2008) Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol Ecol 17:30–44

    Article  PubMed  Google Scholar 

  • Sexton JP, Hangartner SB, Hoffmann AA (2014) Genetic isolation by environment or distance: which pattern of gene flow is most common? Evolution 68:1–15

    Article  CAS  PubMed  Google Scholar 

  • Shafer ABA, Wolf JBW (2013) Widespread evidence for incipient ecological speciation: a meta-analysis of isolation-by-ecology. Ecol Lett 16:940–950

    Article  PubMed  Google Scholar 

  • Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279

    Article  Google Scholar 

  • Sobel JM (2014) Ecogeographic isolation and speciation in the genus Mimulus. Am Nat 184:565–579

    Article  PubMed  Google Scholar 

  • Sobel JM, Chen GF, Watt LR, Schemske DW (2010) The biology of speciation. Evolution 64:295–315

    Article  PubMed  Google Scholar 

  • Strasburg JL, Sherman NA, Wright KM, Moyle LC, Willis JH, Rieseberg LH (2012) What can patterns of differentiation across plant genomes tell us about adaptation and speciation? Philos Trans R Soc B 367:364–373

    Article  Google Scholar 

  • Stucki S, Orozco-terWengel P, Bruford MW et al, NEXTGEN Consortium (2014) High performance computation of landscape genomic models integrating local indices of spatial association. Available at arXiv:1405.7658v1 [q-bio.PE]. Accessed 7 Mar 2016

  • Su Z, Chai M-F, Lu P-L, An R, Chen J, Wang X-C (2007) AtMTM1, a novel mitochondrial protein, may be involved in activation of the manganese-containing superoxide dismutase in Arabidopsis. Planta 226:1031–1039

    Article  CAS  PubMed  Google Scholar 

  • Svensson EI (2012) Non-ecological speciation, niche conservatism and thermal adaptation: how are they are connected? Org Divers Evol 12:229–240

    Article  Google Scholar 

  • Tagane S, Hiramatsu M, Okubo H (2008) Hybridization and asymmetric introgression between Rhododendron eriocarpum and R. indicum on Yakushima Island, southwest Japan. J Plant Res 121:387–395

    Article  CAS  PubMed  Google Scholar 

  • Tamaki I, Okada M (2014) Genetic admixing of two evergreen oaks, Ouercus acuta and Q. sessilifolia (subgenus Cyclobalanopsis), is the result of interspecific introgressive hybridization. Tree Genet Genomes 10:989–999

    Article  Google Scholar 

  • Thompson SL, Lamothe M, Meirmans PG, Périnet P, Isabel N (2010) Repeated unidirectional introgression towards Populus balsamifera in contact zones of exotic and native poplars. Mol Ecol 19:132–145

    Article  CAS  PubMed  Google Scholar 

  • Thornthwaite CW (1948) An approach toward a rational classification of climate. Geogr Rev 38:55–94

    Article  Google Scholar 

  • Tiffin P, Olson MS, Moyle LC (2000) Asymmetric crossing barriers in angiosperms. Proc R Soc Lond B 268:861–867

    Article  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  CAS  Google Scholar 

  • Via S (2009) Natural selection in action during speciation. Proc Natl Acad Sci U S A 106:9939–9946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang IJ (2013) Examining the full effects of landscape heterogeneity on spatial genetic variation: a multiple matrix regression approach for quantifying geographic and ecological isolation. Evolution 67:3403–3411

    Article  PubMed  Google Scholar 

  • Wang IJ, Glor RE, Losos JB (2013) Quantifying the roles of ecology and geography in spatial genetic divergence. Ecol Lett 16:175–182

    Article  PubMed  Google Scholar 

  • Wang C-Q, Guthrie C, Sarmast MK, Dehesh K (2014) BBX19 interacts with CONSTANS to repress FLOWERING LOCUS T transcription, defining a flowering time checkpoint in Arabidopsis. Plant Cell 26:3589–3602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitney KD, Randell RA, Rieseberg LH (2006) Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus. Am Nat 167:794–807

    Article  PubMed  Google Scholar 

  • Wolf JBW, Lindell J, Backström N (2010) Speciation genetics: current status and evolving approaches. Philos Trans R Soc B 365:1717–1733

    Article  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Ma C, Xu Y et al (2014) A zinc finger protein regulates flowering time and abiotic stress tolerance in Chrysanthemum by modulating gibberellin biosynthesis. Plant Cell 26:2038–2054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yatabe Y, Kane NC, Scotti-Saintagne C, Rieseberg LH (2007) Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 175:1883–1893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoichi W, Tomaru N (2014) Patterns of geographic distribution have a considerable influence on population genetic structure in one common and two rare species of Rhododendron (Ericaceae). Tree Genet Genomes 10:827–837

    Article  Google Scholar 

  • Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418

    Article  CAS  PubMed  Google Scholar 

  • Zanella M, Borghi GL, Pirone C et al (2016) β-amylase 1 (BAM1) degrades transitory starch to sustain proline biosynthesis during drought stress. J Exp Bot 67:1819–1826

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors are grateful for the technical assistance of Ting-Hsuan Chen and Yi-Chiang Hsieh in genotyping. We are also thankful for the assistance with sample collection from Ji-Shen Wu, Division of Silviculture, Taiwan Forest Research Institute. This study was financially supported by the Ministry of Science and Technology (grant no. NSC97-2313-B-003-002-MY3), Taiwan.

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Authors and Affiliations

  1. Laboratory of Molecular Phylogenetics, Department of Biology, National Museum of Natural Science, 1 Guanchien Road, Taichung, 40453, Taiwan

    Chun-Lin Huang

  2. Department of Life Science, National Taiwan Normal University, 88 Tingchow Road, Section 4, Taipei, 11677, Taiwan

    Jui-Hung Chen, Pei-Chun Liao, Jenn-Che Wang & Shih-Ying Hwang

  3. Department of Geography, National Taiwan University, 1 Roosevelt Road, Section 4, Taipei, 10617, Taiwan

    Chung-Te Chang

  4. Division of Silviculture, Taiwan Forestry Research Institute, 53 Nanhai Road, Taipei, 10066, Taiwan

    Jeng-Der Chung

Authors
  1. Chun-Lin Huang
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  2. Jui-Hung Chen
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  3. Chung-Te Chang
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  4. Jeng-Der Chung
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  5. Pei-Chun Liao
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  6. Jenn-Che Wang
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  7. Shih-Ying Hwang
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Corresponding author

Correspondence to Shih-Ying Hwang.

Ethics declarations

The authors declare that all plant materials collected comply with the law of government regulation. The funder provided support for research, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflict of interest

The authors declare that they have no competing interest.

Data archiving statement

Genetic data used in this study are available in Supplemental File 3.

Additional information

Communicated by P. Ingvarsson

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Huang, CL., Chen, JH., Chang, CT. et al. Disentangling the effects of isolation-by-distance and isolation-by-environment on genetic differentiation among Rhododendron lineages in the subgenus Tsutsusi . Tree Genetics & Genomes 12, 53 (2016). https://doi.org/10.1007/s11295-016-1010-2

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  • DOI: https://doi.org/10.1007/s11295-016-1010-2

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