Abstract
The comparison of inter-population quantitative variation and neutral variation based on molecular markers (QST − FST) has been extensively used to infer the influence of different selection forces on potentially adaptive traits. Only recently have studies focused on two levels of inter-population genetic structuring: among regions (or groups) and among subpopulations within groups. This work aimed to compare quantitative and molecular variation within these two hierarchical levels for Hancornia speciosa Gomes, a fruit tree species that is native to the Brazilian Cerrado. Six quantitative traits related to initial plant growth were evaluated in a common garden environment using samples from 57 maternal families (treatments) derived from 29 subpopulations within four botanical varieties. The quantitative divergence among the botanical varieties (QGT) and among the subpopulations within varieties (QSG) for each trait were compared with the corresponding neutral variation (FGT and FSG) obtained based on six microsatellite loci using a parametric bootstrap procedure. The molecular results revealed a low degree of divergence among the botanical varieties and significant structuring among the subpopulations within varieties. The estimates of the quantitative divergence among the varieties (QGT) tended to be greater than the divergence among the subpopulations within varieties (QSG) for five out of the six quantitative traits. The comparison between the quantitative and molecular parameters suggests that divergent selection shaped the genetic structure among the botanical varieties for some traits, while the variation among the subpopulations within varieties was influenced by genetic drift and uniform selection.
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References
Almeida GQ, Vieira MC, Ganga RMD, Chaves LJ (2019) Agronomic evaluation of a Hancornia speciosa Gomes germplasm collection from the Brazilian Cerrado. Crop Breed Appl Biotechnology:19 (In press)
Boaventura-Novaes CRD, Novaes E, Mota EES, Telles MPC, Coelho ASG, Chaves LJ (2018) Genetic drift and uniform selection shape evolution of most traits in Eugenia dysenterica DC. (Myrtaceae). Tree Genet Genomes 14:76. https://doi.org/10.1007/s11295-018-1289-2
Bonnin I, Prosperi J, Olivierit I (1996) Genetic markers and quantitative genetic variation in Medicago truncutula (Leguminosae): a comparative analysis of population structure. Genetics 143:1795–1805
Collevatti RG, Olivatti AM, Telles MPC, Chaves LJ (2016) Gene flow among Hancornia speciosa (Apocynaceae) varieties and hybrid fitness. Tree Genet Genomes 12:74–85. https://doi.org/10.1007/s11295-016-1031-x
Collevatti RG, Rodrigues EE, Vitorino LC, Lima-Ribeiro MS, Chaves LJ, Telles MPC (2018) Unravelling the genetic differentiation among varieties of the Neotropical savanna tree Hancornia speciosa Gomes. Ann Bot 122:973–984. https://doi.org/10.1093/aob/mcy060
Costa CF, Collevatti RG, Chaves LJ, Lima JS, Soares TN, Telles MPC (2017) Genetic diversity and fine-scale genetic structure in Hancornia speciosa Gomes (Apocynaceae). Biochem Syst Ecol 72:63–67. https://doi.org/10.1016/j.bse.2017.03.001
Creste S, Tulmann-Neto A, Figueira A (2001) Detection of single sequence repeat polymorphism in denaturing polyacrylamide sequencing gels by silver staining. Plant Mol Biol Rep 19:299–306
Cubry P, Scotti I, Oddou-Muratorio S, Lefevre F (2017) Generalization of the QST framework in hierarchically structured populations: impacts of inbreeding and dominance. Mol Ecol Resour 17:76–83. https://doi.org/10.1111/1755-0998.12693
Darrault RO, Schlindwein C (2005) Limited fruit production in Hancornia speciosa (Apocynaceae) and pollination by nocturnal and diurnal insects. Biotropica 37:381–388. https://doi.org/10.1111/j.1744-7429.2005.00050.x
Diniz-Filho JAF, Barbosa ACOF, Chaves LJ, Souza KS, Dobrovolski R, Rattis L, Terribile LC, Lima-Ribeiro MS, Oliveira G, Brum FT, Loyola R, Telles MPC (2018) Overcoming the worst of both worlds: integrating climate change and habitat loss into spatial conservation planning of genetic diversity in the Brazilian Cerrado. Biodivers Conserv 29:1–16. https://doi.org/10.1007/s10531-018-1667-y
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15
Earl DA, VonHold BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/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. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Flores IS, Silva AK, Furquim LC, Castro CFS, Chaves LJ, Collevatti RG, Lião LM (2018) HR-MAS NMR Allied to chemometric on Hancornia speciosa varieties differentiation. J Braz Chem Soc 29:708–714. https://doi.org/10.21577/0103-5053.20170191
Ganga RMD, Chaves LJ, Naves RV (2009) Parâmetros genéticos em progênies de Hancornia speciosa Gomes do Cerrado. Sci For 37:395–404
Ganga RMD, Ferreira GA, Chaves LJ, Naves RV, Nascimento JL (2010) Caracterização de frutos e árvores de populações naturais de Hancornia speciosa Gomes do cerrado. Rev Bras Frutic 32:101–113. https://doi.org/10.1590/S0100-29452010005000019
Gilbert KJ, Whitlock MC (2015) QST - FST comparisons with unbalanced half-sib designs. Mol Ecol Resour 15:262–267. https://doi.org/10.1111/1755-0998.12303
Goudet J, Buchi L (2006) The effects of dominance, regular inbreeding and sampling design on QST, an estimator of population differentiation for quantitative traits. Genetics 172:1337–1347. https://doi.org/10.1534/genetics.105.050583
Jimenez HJ, Martins LSS, Montarroyos AVV, Silva-Junior JF, Alzate-Marin AL, Moraes-Filho RM (2015) Genetic diversity of the Neotropical tree Hancornia speciosa Gomes in natural populations in Northeastern Brazil. Genet Mol Res 14:17749–17757. https://doi.org/10.4238/2015.December.21.48
Leinonen T, McCairns RJS, O’Hara RB, Merilä J (2013) QST–FST comparisons: evolutionary and ecological insights from genomic heterogeneity. Nat Rev Genet 14:179–190. https://doi.org/10.1038/nrg3395
Leinonen T, O’Hara RB, Cano JM, Merilä J (2008) Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis. J Evol Biol 21:1–17. https://doi.org/10.1111/j.1420-9101.2007.01445.x
Lewis PO, Zaykin D (2001) Genetic data analysis: computer program for the analysis of allelic data (software). http://lewis.eeb.uconn.edu/lewishome/software.html. Accessed 16 march 2019
McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291. https://doi.org/10.1016/S0169-5347(02)02478-3
Mendonça RC, Felfili JM, Walter BMT, Silva-Junior MC, Rezende AV, Filgueiras TS, Nogueira PE, Fagg CW (2008) Flora vascular do bioma Cerrado: Checklist com 12.356 spécies. In: Sano SM, Almeida SP, Ribeiro JF (eds) Cerrado: ecologia e flora. Embrapa, Brasília, pp 421–442
Merilä J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903. https://doi.org/10.1046/j.1420-9101.2001.00348.x
Monachino J (1945) A revision of Hancornia (Apocynaceae). Lilloa, Tucumán 11:19–48
Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1111/j.1471-8286.2007.01758.x
Rodrigues AJL, Yamaguishi AT, Chaves LJ, Coelho ASG, Lima JS, Telles MPC (2015) Development of microsatellite markers for Hancornia speciosa Gomes (Apocynaceae). Genet Mol Res 14:7274–7278. https://doi.org/10.4238/2015.July.3.2
Rosa MEC, Naves RV, Oliveira-Junior JP (2005) Substrates for production and growth of mangaba (Hancornia speciosa Gomes) seedlings. Pesqui Agropecuária Trop 35:65–70
Santos PS, Freitas LS, Santana JGS, Muniz EM, Rabbani ARC, Silva AVC (2017) Genetic diversity and the quality of Mangabeira tree fruits (Hancornia speciosa Gomes—Apocynaceae), a native species from Brazil. Sci Hortic (Amsterdam) 226:372–378. https://doi.org/10.1016/j.scienta.2017.09.008
Searle SR, Fawcett RF (1970) Expected mean squares in variance components models having finite populations. Biometrics 26:243–254
Silva-Junior JF, Lédo AS (2006) Botânica. In: Silva-Junior JF, Lédo AS (eds) A cultura da Mangaba. Embrapa, Brasília, pp 26–33
Spitze K (1993) Population structure in Daphnia obtusa: quantitative genetic and allozymic variation. Genetics 135:367–374
Vencovsky R, Crossa J (2003) Measurements of representativeness used in genetic resources conservation and plant breeding. Crop Sci 43:1912–1921. https://doi.org/10.2135/cropsci2003.1912
Volis S, Yakubov B, Shulgina I, Ward D, Mendlinger S (2005) Distinguishing adaptive from nonadaptive genetic differentiation: comparison of QST and FST at two spatial scales. Heredity (Edinb) 95:466–475. https://doi.org/10.1038/sj.hdy.6800745
Weir BS (1996) Genetic data analysis II. Methods for discrete population genetic data. Sinauer, Sunderland
Whitlock MC (2008) Evolutionary inference from QST. Mol Ecol 17:1885–1896. https://doi.org/10.1111/j.1365-294X.2008.03712.x
Whitlock MC, Gilbert KJ (2012) QST in a hierarchically structured population. Mol Ecol Resour 12:481–483. https://doi.org/10.1111/j.1755-0998.2012.03122.x
Whitlock MC, Guillaume F (2009) Testing for spatially divergent selection: comparing QST to FST. Genetics 183:1055–1063. https://doi.org/10.1534/genetics.108.099812
Wright S (1951) The genetical structure of populations. Ann Eugenics 15:323–354
Wright S (1969) Evolution and the genetics of population. In: The theory of gene frequencies, vol 2. University of Chicago Press, Chicago
Acknowledgments
This paper is dedicated to Professor Roland Vencovsky (in memoriam) who inspired and encouraged us in quantitative and population genetic studies of wild plant species.
Our research has been supported by the project CERGEN (PRONEX/FAPEG/CNPq, Proc. 201210267000802). L.J. Chaves has been continuously supported by productivity grants from the National Council for Scientific and Technological Development, CNPq, Brazil.
We are very grateful to two anonymous reviewers who have greatly contributed to the improvement of this paper.
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Chaves, L.J., Ganga, R.M.D., Guimarães, R.A. et al. Quantitative and molecular genetic variation among botanical varieties and subpopulations of Hancornia speciosa Gomes (Apocynaceae). Tree Genetics & Genomes 16, 50 (2020). https://doi.org/10.1007/s11295-020-01444-0
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DOI: https://doi.org/10.1007/s11295-020-01444-0