Genetic patterns in Neotropical Magnolias (Magnoliaceae) using de novo developed microsatellite markers.
Journal
Heredity
ISSN: 1365-2540
Titre abrégé: Heredity (Edinb)
Pays: England
ID NLM: 0373007
Informations de publication
Date de publication:
04 2019
04 2019
Historique:
received:
27
03
2018
accepted:
05
09
2018
revised:
01
09
2018
pubmed:
29
10
2018
medline:
10
6
2020
entrez:
29
10
2018
Statut:
ppublish
Résumé
Conserving tree populations safeguards forests since they represent key elements of the ecosystem. The genetic characteristics underlying the evolutionary success of the tree growth form: high genetic diversity, extensive gene flow and strong species integrity, contribute to their survival in terms of adaptability. However, different biological and landscape contexts challenge these characteristics. This study employs 63 de novo developed microsatellite or SSR (Single Sequence Repeat) markers in different datasets of nine Neotropical Magnolia species. The genetic patterns of these protogynous, insect-pollinated tree species occurring in fragmented, highly-disturbed landscapes were investigated. Datasets containing a total of 340 individuals were tested for their genetic structure and degree of inbreeding. Analyses for genetic structure depicted structuring between species, i.e. strong species integrity. Within the species, all but one population pair were considered moderate to highly differentiated, i.e. no indication of extensive gene flow between populations. No overall correlation was observed between genetic and geographic distance of the pairwise species' populations. In contrast to the pronounced genetic structure, there was no evidence of inbreeding within the populations, suggesting mechanisms favouring cross pollination and/or selection for more genetically diverse, heterozygous offspring. In conclusion, the data illustrate that the Neotropical Magnolias in the context of a fragmented landscape still have ample gene flow within populations, yet little gene flow between populations.
Identifiants
pubmed: 30368529
doi: 10.1038/s41437-018-0151-5
pii: 10.1038/s41437-018-0151-5
pmc: PMC6460770
doi:
Substances chimiques
DNA, Plant
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
485-500Subventions
Organisme : Fonds Wetenschappelijk Onderzoek (Research Foundation Flanders)
ID : K210116N
Pays : International
Organisme : Fonds Wetenschappelijk Onderzoek (Research Foundation Flanders)
ID : V431816N
Pays : International
Organisme : Fonds Wetenschappelijk Onderzoek (Research Foundation Flanders)
ID : V445315N
Pays : International
Organisme : Bijzonder Onderzoeksfonds (Special Research Fund)
ID : BOF.DOC.2014.0062.01
Pays : International
Références
Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S (2008) Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol Appl 1(1):95–111
pubmed: 25567494
pmcid: 3352395
doi: 10.1111/j.1752-4571.2007.00013.x
Aparicio A, Hampe A, Fernández-Carrillo L, Albaladejo RG (2012) Fragmentation and comparative genetic structure of four mediterranean woody species: complex interactions between life history traits and the landscape context. Divers Distrib 18(3):226–235
doi: 10.1111/j.1472-4642.2011.00823.x
Austerlitz F, Mariette S, Machon N, Gouyon PH, Godelle B (2000) Effects of colonization processes on genetic diversity: differences between annual plants and tree species. Genetics 154(3):1309–1321
pubmed: 10757772
pmcid: 1461003
doi: 10.1093/genetics/154.3.1309
Bousquet J, Strauss SH, Doerksen AH, Price RA (1992) Extensive variation in evolutionary rate of rbcL gene sequences among seed plants. Proc Natl Acad Sci USA 89(16):7844–7848
pubmed: 1502205
doi: 10.1073/pnas.89.16.7844
pmcid: 49808
Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by Taq DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 20(6):1004–1006. 1008–1010
pubmed: 8780871
doi: 10.2144/96206st01
Calonje M, Martín-Bravo S, Dobeš C, Gong W, Jordon-Thaden I, Kiefer C et al. (2009) Non-coding nuclear DNA markers in phylogenetic reconstruction. Plant Syst Evol 282(3):257–280
doi: 10.1007/s00606-008-0031-1
Cires E, De Smet Y, Cuesta C, Goetghebeur P, Sharrock S, Gibbs D et al. (2013) Gap analyses to support ex situ conservation of genetic diversity in Magnolia, a flagship group. Biodivers Conserv 22(3):567–590
doi: 10.1007/s10531-013-0450-3
de Queiroz K (1998) The general lineage concept of species, species criteria, and the process of speciation. A conceptual unification and terminological recommendations. In: Howard DJ, Berlocher SH (eds) Endless forms. Species and speciation. Oxford University Press, New York, NY, p 57–75
Dick CW, Hardy OJ, Jones FA, Petit RJ (2008) Spatial scales of pollen and seed-mediated gene flow in tropical rain forest trees. Trop Plant Biol 1(1):20–33
doi: 10.1007/s12042-007-9006-6
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361
doi: 10.1007/s12686-011-9548-7
Ellstrand NC, Whitkus R, Rieseberg LH (1996) Distribution of spontaneous plant hybrids. Proc Natl Acad Sci USA 93(10):5090–5093
pubmed: 11607681
doi: 10.1073/pnas.93.10.5090
pmcid: 39411
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620
pubmed: 15969739
doi: 10.1111/j.1365-294X.2005.02553.x
Figlar RB, Nooteboom HP (2004) Notes on Magnoliaceae IV. Blumea 49(1):87–100
doi: 10.3767/000651904X486214
Frankham R, Ballou JD, Briscoe DA (2010) Introduction to Conservation Genetics, 2nd edn. Cambridge University Press, Cambridge
doi: 10.1017/CBO9780511809002
García-Morales LJ, Iamonico D, García Jiménez J (2017) Nomenclatural remarks on Magnolia sect. Macrophylla (Magnoliaceae), with description of a new species from North America (Tamaulipas, Mexico). Phytotaxa 309(3):238–244
doi: 10.11646/phytotaxa.309.3.4
Gibbs PE, Semir J, da Cruz ND (1977) Floral biology of Talauma ovata St. Hil. (Magnoliaceae). Cienc Cult 29:1436–1441
González Torres LR, Palmarola A, González Oliva L, Bécquer ER, Testé E, Barrios D (2016) Lista roja de la flora de Cuba. Bissea 10(número especial1):1–352
Gottsberger G (1977) Some aspects of beetle pollination in the evolution of flowering plants. Plant Syst Evol Suppl 1:211–226
Graignic N, Tremblay F, Bergeron Y (2016) Genetic consequences of selection cutting on sugar maple (Acer saccharum Marshall). Evol Appl 9(6):777–790
pubmed: 27330554
pmcid: 4908464
doi: 10.1111/eva.12384
Guichoux E, Lagache L, Wagner S, Chaumeil P, Léger P, Lepais O et al. (2011) Current trends in microsatellite genotyping. Mol Ecol Resour 11(4):591–611
pubmed: 21565126
doi: 10.1111/j.1755-0998.2011.03014.x
Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48(2):361–372
pubmed: 1637966
doi: 10.2307/2532296
Hamrick JL (2004) Response of forest trees to global environmental changes. Ecol Manag 197(1–3):323–335
doi: 10.1016/j.foreco.2004.05.023
Hamrick JL, Godt MJW, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plant species. New (Dordr) 6(1–4):95–124
Hartl DL, Clark AG (1997) Principles of Population Genetics, 3rd edn. Sinauer Associates, Inc, Sunderland, MA
Hoban S, Gaggiotti O, ConGRESS Consortium, Bertorelle G (2013) Sample Planning Optimization Tool for conservation and population Genetics (SPOTG): a software for choosing the appropriate number of markers and samples. Methods Ecol Evol 4(3):299–303
doi: 10.1111/2041-210x.12025
Hodel RG, Segovia-Salcedo MC, Landis JB, Crowl AA, Sun M, Liu X et al. (2016) The report of my death was an exaggeration: A review for researchers using microsatellites in the 21st century. Appl Plant Sci 4(6):1600025
doi: 10.3732/apps.1600025
Holleley CE, Geerts PG (2009) Multiplex Manager 1.0: a cross-platform computer program that plans and optimizes multiplex PCR. Biotechniques 46(7):511–517
pubmed: 19594450
doi: 10.2144/000113156
Holm S (1979) A simple sequentially rejective multiple test procedure. Scand Stat Theory Appl 6(2):65–70
Howard RA (1948) The morphology and systematics of the West Indian Magnoliaceae. Bull Torre Bot Club 75(4):335–357
doi: 10.2307/2560339
Ishida K, Yoshimaru H, Itô H (2003) Effects of geitonogamy on the seed set of Magnolia obovata Thunb. (Magnoliaceae). Int J Plant Sci 164(5):729–735
doi: 10.1086/376812
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24(11):1403–1405
pubmed: 18397895
doi: 10.1093/bioinformatics/btn129
Kalia RK, Rai MK, Kalia S, Singh R, Dhawan AK (2011) Microsatellite markers: an overview of the recent progress in plants. Euphytica 177(3):309–334
doi: 10.1007/s10681-010-0286-9
Kalinowski ST, Taper ML (2006) Maximum likelihood estimation of the frequency of null alleles at microsatellite loci. Conserv Genet 7(6):991–995
doi: 10.1007/s10592-006-9134-9
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S et al. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649
pubmed: 22543367
pmcid: 3371832
doi: 10.1093/bioinformatics/bts199
Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) diveRsity: An R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4(8):782–788
doi: 10.1111/2041-210X.12067
Kikuchi S, Isagi Y (2002) Microsatellite genetic variation in small and isolated populations of Magnolia sieboldii ssp. japonica. Hered (Edinb) 88(4):313–321
doi: 10.1038/sj.hdy.6800047
Kramer AT, Ison JL, Ashley MV, Howe HF (2008) The paradox of forest fragmentation genetics. Conserv Biol 22(4):878–885
pubmed: 18544089
doi: 10.1111/j.1523-1739.2008.00944.x
Kremer A, Le Corre V (2012) Decoupling of differentiation between traits and their underlying genes in response to divergent selection. Hered (Edinb) 108(4):375–385
doi: 10.1038/hdy.2011.81
Larridon I, Walter HE, Guerrero PC, Duarte M, Cisternas MA, Peña Hernández C et al. (2015) An integrative approach to understanding the evolution and diversity of Copiapoa (Cactaceae), a threatened endemic Chilean genus from the Atacama Desert. Am J Bot 102(9):1506–1520
pubmed: 26373974
doi: 10.3732/ajb.1500168
Lewontin RC, Kojima K (1960) The evolutionary dynamics of complex polymorphisms. Evolution 14(4):458–472
Louis EJ, Dempster ER (1987) An exact test for Hardy-Weinberg and multiple alleles. Biometrics 43(4):805–811
pubmed: 3427165
doi: 10.2307/2531534
Lugo AE, Schmidt R, Brown S (1981) Tropical forests in the Caribbean. Ambio 10(6):318–324
Neale DB, Kremer A (2011) Forest tree genomics: growing resources and applications. Nat Rev Genet 12(2):111–122
pubmed: 21245829
doi: 10.1038/nrg2931
Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. II. Gene Freq data J Mol Evol 19(2):153–170
doi: 10.1007/BF02300753
Palmarola A, Romanov MS, Bobrov AVFCh, González-Torres LR (2016) Las magnolias de Cuba: Talauma – taxonomía y nomenclatura. Rev Del Jardín Botánico Nac 37:1–10
Pautasso M (2009) Geographical genetics and the conservation of forest trees. Perspect Plant Ecol Syst 11(3):157–189
doi: 10.1016/j.ppees.2009.01.003
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295
doi: 10.1111/j.1471-8286.2005.01155.x
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28(19):2537–2539
pubmed: 22820204
pmcid: 3463245
doi: 10.1093/bioinformatics/bts460
Pérez ÁJ, Arroyo F, Neill DA, Vázquez-García JA (2016) Magnolia chiguila and M. mashpi (Magnoliaceae): two new species and a new subsection (Chocotalauma, sect. Talauma) from the Chocó biogeographic region of Colombia and Ecuador Phytotaxa 286:267–276
doi: 10.11646/phytotaxa.286.4.5
Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst 37:187–214
doi: 10.1146/annurev.ecolsys.37.091305.110215
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959
pubmed: 10835412
pmcid: 1461096
doi: 10.1093/genetics/155.2.945
R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, https://www.R–project.org/ URL
Rivers M, Beech E, Murphy L, Oldfield S (2016) The Red List of Magnoliaceae - revised and extended. BGCI, Richmond, UK
Roberge J, Angelstam P (2004) Usefulness of the umbrella species concept as a conservation tool. Conserv Biol 18(1):76–85
doi: 10.1111/j.1523-1739.2004.00450.x
Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4(1):137–138
doi: 10.1046/j.1471-8286.2003.00566.x
Rousset F (2008) GENEPOP'007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8(1):103–106
pubmed: 21585727
doi: 10.1111/j.1471-8286.2007.01931.x
Schlötterer C (2004) The evolution of molecular markers — just a matter of fashion? Nat Rev Genet 5(1):63–69
pubmed: 14666112
doi: 10.1038/nrg1249
Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9(5):615–629
pubmed: 16643306
doi: 10.1111/j.1461-0248.2006.00889.x
Setsuko S, Ishida K, Ueno S, Tsumura Y, Tomaru N (2007) Population differentiation and gene flow within a metapopulation of a threatened tree, Magnolia stellata (Magnoliaceae). Am J Bot 94(1):128–136
pubmed: 21642215
doi: 10.3732/ajb.94.1.128
Slatkin M (2008) Linkage disequilibrium — understanding the evolutionary past and mapping the medical future. Nat Rev Genet 9(6):477–485
pubmed: 18427557
pmcid: 5124487
doi: 10.1038/nrg2361
Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101(42):15261–15264
pubmed: 15477597
doi: 10.1073/pnas.0403809101
pmcid: 524053
Sun Y, Wen X, Huang H (2011) Genetic diversity and differentiation of Michelia maudiae (Magnoliaceae) revealed by nuclear and chloroplast microsatellite markers. Genetica 139(11-12):1439–1447
pubmed: 22399358
doi: 10.1007/s10709-012-9642-0
Tamaki I, Setsuko S, Tomaru N (2009) Estimation of outcrossing rates at hierarchical levels of fruits, individuals, populations and species in Magnolia stellata. Hered (Edinb) 102(4):381–388
doi: 10.1038/hdy.2008.128
Thien LB (1974) Floral Biology of Magnolia. Am J Bot 61(10):1037–1045
doi: 10.1002/j.1537-2197.1974.tb12321.x
Thiers, B. [continuously updated]. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. http://sweetgum.nybg.org/science/ih/ .
Tozaki T, Mashima S, Hirota K, Miura N, Choi-Miura N, Tomita M (2001) Characterization of equine microsatellites and microsatellite-linked repetitive elements (eMLREs) by efficient cloning and genotyping methods. DNA Res 8(1):33–45
pubmed: 11258798
doi: 10.1093/dnares/8.1.33
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4(3):535–538
doi: 10.1111/j.1471-8286.2004.00684.x
Vartia S, Collins PC, Cross TF, Fitzgerald RD, Gauthier DT, McGinnity P et al. (2014) Multiplexing with three-primer PCR for rapid and economical microsatellite validation. Hereditas 151(2–3):43–54
pubmed: 25041267
doi: 10.1111/hrd2.00044
Vavrek MJ (2011) fossil: Palaeoecological and palaeogeographic analysis tools. Palaeontol Electron 14(1):1–16
Vázquez-García JA, Véliz-Pérez ME, Tribouillier-Navas E, Muñiz-Castro MA (2013a) Magnolia quetzal and Magnolia mayae, a new species and a new record, respectively, for the flora of Guatemala. Phytotaxa 76(1):1–6
doi: 10.11646/phytotaxa.76.1.1
Vázquez-García JA, Pérez-Farrera MÁ, Martínez-Camilo R, Muñiz-Castro MÁ, Martínez-Meléndez N (2013b) Magnolia lacandonica (subsection Talauma, Magnoliaceae), a new rainforest species from Chiapas, Mexico Phytotaxa 79:30–36
doi: 10.11646/phytotaxa.79.1.2
Waples RS (2015) Testing for Hardy-Weinberg proportions: have we lost the plot? J Hered 106(1):1–19
pubmed: 25425676
doi: 10.1093/jhered/esu062
Ward SM, Jasieniuk M (2009) Sampling weedy and invasive plant populations for genetic diversity analysis. Weed Sci 57(6):593–602
doi: 10.1614/WS-09-082.1
Watanabe S, Kaneko Y, Maesako Y, Noma N (2017) Detecting the early genetic effects of habitat degradation in small size remnant populations of Machilus thunbergii Sieb. et Zucc. (Lauraceae). Int J For Res 2017:1–7
Weber JL (1990) Informativeness of human (dC-dA)
pubmed: 1974878
doi: 10.1016/0888-7543(90)90195-Z
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38(6):1358–1370
pubmed: 28563791
Wheeler GL, Dorman HE, Buchanan A, Challagundla L, Wallace LE (2014) A review of the prevalence, utility, and caveats of using chloroplast simple sequence repeats for studies of plant biology. Appl Plant Sci 2(12):1400059
doi: 10.3732/apps.1400059
Whittle CA, Johnston MO (2003) Broad-scale analysis contradicts the theory that generation time affects molecular evolutionary rates in plants. J Mol Evol 56(2):223–233
pubmed: 12574868
doi: 10.1007/s00239-002-2395-0
Xin Z, Chen J (2012). A high throughput DNA extraction method with high yield and quality. Plant Methods 8(26).
Zhao X, Ma Y, Sun W, Wen X, Milne R (2012) High genetic diversity and low differentiation of Michelia coriacea (Magnoliaceae), a Critically Endangered endemic in Southeast Yunnan, China. Int J Mol Sci 13(4):4396–4411
pubmed: 22605985
pmcid: 3344221
doi: 10.3390/ijms13044396