Effects of climate changes on distribution of Eremanthus erythropappus and E. incanus (Asteraceae) in Brazil

Abstract

Phylogeographic patterns of endemic species are critical keys to understand its adaptation to future climate change. Herein, based on chloroplast DNA, we analyzed the genetic diversity of two endemic and endangered tree species from the Brazilian savanna and Atlantic forest (Eremanthus erythropappus and Eremanthus incanus). We also applied the climate-based ecological niche modeling (ENM) to evaluate the impact of the Quaternary climate (last glacial maximum ~ 21 kyr BP (thousand years before present) and Mid-Holocene ~ 6 kyr BP) on the current haplotype distribution. Moreover, we modeled the potential effect of future climate change on the species distribution in 2070 for the most optimistic and pessimistic scenarios. One primer/enzyme combination (SFM/HinfI) revealed polymorphism with very low haplotype diversity, showing only three different haplotypes. The haplotype 1 has very low frequency and it was classified as the oldest, diverging from six mutations from the haplotypes 2 and 3. The E. erythropappus populations are structured and differ genetically according to the areas of occurrence. In general, the populations located in the north region are genetically different from those located in the center-south. No genetic structuring was observed for E. incanus. The ENM revealed a large distribution during the past and a severe decrease in geographic distribution of E. erythropappus and E. incanus from the LGM until present and predicts a drastic decline in suitable areas in the future. This reduction may homogenize the genetic diversity and compromise a relevant role of these species on infiltration of groundwater.

Keywords

Ecological niche modeling / Genetic diversity / Climate change / Chloroplast DNA

References

[1] Abbott RJ, Brochmann C. History and evolution of the arctic flora: in the footsteps of Eric Hulten. Mol Ecol, 2003, 12: 299-313.

[2] Abbott RJ, Comes HP. Evolution in the Arctic: a phylogeographic analysis of the circumarctic plant, Saxifraga oppositifolia (Purple saxifrage). New Phytol, 2004, 161: 211-224.

[3] Araújo LC (1944) Vanillosmopsis erythropappa (DC.) Sch. Bip: sua exploração florestal. Dissertation, Escola Nacional de Agronomia, Seropédica

[4] Avise JC. Molecular markers, natural history, and evolution, 1994, New York: Chapman & Hall

[5] Avise J, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Evol Syst, 1987, 18: 489-522.

[6] Barberi M, Salgado-Labouriau ML, Suguio K. Paleovegetation and paleoclimate of “Vereda de Águas Emendadas”, DF, Central Brazil. J South Am Earth Sci, 2000, 13: 241-254.

[7] Barreira S, Sebbenn AM, Scolforo JRS, Kageyama PY. Diversidade genética e sistema de reprodução em população nativa de Eremanthus erythropappus (DC.) MacLeish sob exploração. Sci For, 2006, 71: 119-130.

[8] Beck J. Predicting climate change effects on agriculture from ecological niche modeling: who profits, who loses?. Clim Change, 2013, 116: 177-189.

[9] Behling H. Late Quaternary environmental changes in the Lagoa da Curuça region (eastern Amazonia, Brazil) and evidence of Podocarpus in the Amazon lowland. Veg Hist Archaeobot, 2001, 10: 175-183.

[10] Behling H, Hooghiemstra H (2001) Neotropical savanna environments in space and time: late Quaternary interhemispheric comparisons. In: Interhemispheric climate linkages. Boulder, Colorado, pp 307–323

[11] Birky CW, Walsh JB. Effects of linkage on rates of molecular evolution. Proc Natl Acad Sci, 1988, 85: 6414-6418.

[12] Camolesi JF (2007) Volumetria e teor alfa-bisabolol para candeia Eremanthus erythropappus. Dissertation, Universidade Federal de Lavras

[13] Carvalho CS, Ballesteros-Mejia L, Ribeiro MC, Côrtes MC, Santos AS, Collevatti RG. Climatic stability and contemporary human impacts affect the genetic diversity and conservation status of a tropical palm in the Atlantic Forest of Brazil. Conserv Genet, 2017, 18: 467-478.

[14] CESM (2017) Community earth system model. http://www.cesm.ucar.edu/models/ccsm4.0/. Accessed 12 Apr 2017

[15] Chen JM, Zhao SY, Liao YY, Gichira AW, Gituru RW, Wang QF. Chloroplast DNA phylogeographic analysis reveals significant spatial genetic structure of the relictual tree Davidia involucrata (Davidiaceae). Conserv Genet, 2015, 16: 583-593.

[16] Cloutier D, Povoa JS, Procopio LC, Leao NV, Wadt LD, Ciampi AY, Schoen DJ. Chloroplast DNA variation of Carapa guianensis in the Amazon basin. Silvae Genet, 2005, 54(1–6): 270-274.

[17] Collevatti RG, Terribile LC, Lima-Ribeiro MS, Nabout JC, Oliveira G, Rangel TF, Rabelo SG, Diniz-Filho JA. A coupled phylogeographical and species distribution modelling approach recovers the demographical history of a neotropical seasonally dry forest tree species. Mol Ecol, 2012, 21: 5845-5863.

[18] Collevatti RG, Terribile LC, Oliveira G, Lima-Ribeiro MS, Nabout JC, Rangel TF, DinizFilho JA. Drawbacks to palaeodistribution modelling: the case of South American seasonally dry forests. J Biogeogr, 2013, 40: 345-358.

[19] Collevatti RG, Terribile LC, Rabelo SG, Lima-Ribeiro MS. Relaxed random walk model coupled with ecological niche modelling unravel the dispersal dynamics of a neotropical savannah tree species in the deeper Quaternary. Front Plant Sci, 2015, 6: 653.

[20] Comes HP, Kadereit JW. The effect of Quaternary climatic changes on plant distribution and evolution. Trends Plant Sci, 1998, 11: 432-438.

[21] De-Granville JJ. Phytogeographical characteristics of the Guianan forests. Taxon, 1988, 1: 578-594.

[22] Demesure B, Sodzi N, Petit RJ. A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol, 1995, 4: 129-134.

[23] Dumolin-Lapegue S, Pemonge MH, Petit RJ. An enlarged set of consensus primers for the study of organelle DNA in plants. Mol Ecol, 1997, 6: 393-397.

[24] Elith J, Graham CH, Anderson RP, Dudík M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, Li J. Novel methods improve prediction of species’ distributions from occurrence data. Ecography, 2006, 1: 129-151.

[25] Estopa RA, Souza AD, Moura MC, Botrel MC, Mendonça EG, Carvalho D. Diversidade genética em populações naturais de candeia (Eremanthus erythropappus (DC.) MacLeish). Sci For, 2006, 70: 97-106.

[26] Excoffier L, Smouse PE. Using allele frequencies and geographic subdivision to reconstruct gene trees within a species: molecular variance parsimony. Genetics, 1994, 136: 343-359.

[27] Excoffier L, Laval G, Schineider SL. Arlequin versión 3.11: a sofware for population genetic data analysis, 2007, Geneva: University of Geneva.

[28] Fielding AH, Bell JF. A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv, 1997, 24: 38-49.

[29] GBIF (2018) Global biodiversity information facility: Free and open access to biodiversity data. https://www.gbif.org. Accessed 22 Aug 2018

[30] Gent PR. The community climate system model version 4. J Clim, 2011, 24: 4973-4991.

[31] Gries R, Louzada J, Almeida S, Macedo R, Barlow J. Evaluating the impacts and conservation value of exotic and native tree afforestation in Cerrado grasslands using dung beetles. Insect Conserv Diver, 2012, 5: 175-185.

[32] Hamilton MB. Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol, 1999, 8: 513-525.

[33] Hernandez PA, Graham CH, Master LL, Albert DL. The effect of sample size and species characteristics on performance of different species distribution modeling methods. Ecography, 2006, 29: 773-785.

[34] Hewitt G. The genetic legacy of the quaternary ice ages. Nature, 2000, 405: 907.

[35] Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol, 2005, 25: 1965-1978.

[36] Iganci JR, Heiden G, Miotto ST, Pennington RT. Campos de Cima da Serra: the Brazilian subtropical highland grasslands show an unexpected level of plant endemism. Bot J Linn Soc, 2011, 167: 378-393.

[37] Kremer A, Ronce O, Robledo-Arnuncio JJ, Guillaume F, Bohrer G, Nathan R, Bridle JR, Gomulkiewicz R, Klein EK, Ritland K, Kuparinen A. Long distance gene flow and adaptation of forest trees to rapid climate change. Ecol Lett, 2012, 15: 378-392.

[38] Ledru MP. Late quaternary environmental and climatic changes in central Brazil. Quat Res, 1993, 39: 90-98.

[39] Lexer A, Widmer C. Glacial refugia: sanctuaries for allelic richness, but not for gene diversity. Trends Ecol Evol, 2001, 16: 267-268.

[40] Lima JS, Ballesteros-Mejia L, Lima-Ribeiro MS, Collevatti RG. Climatic changes can drive the loss of genetic diversity in a Neotropical savanna tree species. Global Change Biol, 2017, 23: 4639-4650.

[41] Loeuille B, Lopes JC, Pirani JR. Taxonomic novelties in Eremanthus (Compositae: vernonieae) from Brazil. Kew Bull, 2012, 67: 1-9.

[42] Lorenzi H. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil, 1992, Nova Odessa: Plantarum.

[43] MacLeish ANFF. Revision of Eremanthus (Compositae: vernonieae). Ann Missouri Bot Gard, 1987, 74: 265-290.

[44] Mayle FE, Burn MJ, Power M, Urrego DH. Vimeux F, Sylvestre F, Khodri M. Vegetation and fire at the last glacial maximum in tropical South America. Past climate variability from the last glacial maximum to the holocene in South America and surrounding regions, 2009, Berlin: Springer 89 112

[45] Miranda NA, Titon M, Pereira IM, Fernandes JSC, Gonçalves JF, Rocha FM. Culture medium, growth regulators and ways of sealing test tubes on in vitro multiplication of candeia (Eremanthus incanus (Less.) Less). Sci Flor, 2016, 44: 1009-1018.

[46] Moura MCO (2005) Distribuição da variabilidade genética em populações naturais de Eremanthus erythropappus (DC.) MacLeish por isoenzimas e RAPD. D. Phil. Thesis. Universidade Federal de Lavras

[47] Murphy PG, Lugo AE. Bullock SH, Mooney HA, Medina E. Dry forests of central America and the Caribbean. Seasonally dry tropical forests, 1995, Cambridge: Cambridge University Press 9 34

[48] Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J. Biodiversity hotspots for conservation priorities. Nature, 2000, 403: 853-858.

[49] Nabout JC, Magalhães MR, de Amorim Gomes MA, Da Cunha HF. The impact of global climate change on the geographic distribution and sustainable harvest of Hancornia speciosa (Apocynaceae) in Brazil. Environ Manag, 2016, 57: 814-821.

[50] Nei M, Maruyama T, Chakraborty R. The bottleneck effect and genetic variability in populations. Evolution, 1975, 29: 1-10.

[51] Newton AC, Allnutt TR, Gillies AC, Lowe AJ, Ennos RA. Molecular phylogeography, intraspecific variation and the conservation of tree species. Trends Ecol Evol, 1999, 14: 140-145.

[52] Pádua JA, Brandão MM, de Carvalho D. Spatial genetic structure in natural populations of the overexploited tree Eremanthus erythropappus (DC.) macleish (Asteraceae). Biochem Syst Ecol, 2016, 66: 307-311.

[53] Pennington TR, Prado DE, Pendry CA. Neotropical seasonally dry forests and Quaternary vegetation changes. J Biogeogr, 2000, 27: 261-273.

[54] Peterson AT. Ecological niche conservatism: a time-structured review of evidence. J Biogeogr, 2011, 38: 817-827.

[55] Petit RJ, El Mousadik A, Pons O. Identifying populations for conservation on the basis of genetic markers. Conserv Biol, 1998, 24: 844-855.

[56] Phillips SJ (2017) A brief tutorial on maxent. http://biodiversityinformatics.amnh.org/open_source/maxent/. Accessed 13 Mar 2017

[57] Phillips SJ, Dudík M. Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography, 2008, 31: 161-175.

[58] Pons O, Petit RJ. Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics, 1996, 144: 1237-1245.

[59] Prado DE, Gibbs PE. Patterns of species distributions in the dry seasonal forests of South America. Ann Missouri Bot Gard, 1993, 1: 902-927.

[60] Prance GT. Phytogeographic support to the theory of Pleistocene forest refuges in the Amazon Basin, based on evidence from distribution patterns in Caryocaraceae, Chrysobalanaceae, Dichapetalaceae and Lecythidaceae. Acta Amaz, 1973, 3: 5-26.

[61] Prance GT. Biological diversification in the tropics, 1982, New York: Columbia University.

[62] Provan J, Soranzo N, Wilson NJ, Goldstein DB, Powell W. A low mutation rate for chloroplast microsatellites. Genetics, 1999, 153: 943-947.

[63] Ravenscroft CH, Whitlock R, Fridley JD. Rapid genetic divergence in response to 15 years of simulated climate change. Global Change Biol, 2015, 21: 4165-4176.

[64] Rawat A, Barthwal S, Ginwal HS. Comparative assessment of SSR, ISSR and AFLP markers for characterization of selected genotypes of Himalayan Chir pine (Pinus roxburghii Sarg.) based on resin yield. Silvae Genet, 2014, 63: 94-108.

[65] Schlögl PS, Souza AP, Nodari RO. PCR-RFLP analysis of non-coding regions of cpDNA in Araucaria angustifolia (Bert.) O. Kuntze. Genet Mol Biol, 2007, 30: 423-427.

[66] Scolforo JRS, Oliveira AD, Davide AC. O manejo sustentável da candeia: o caminhar de uma nova experiência florestal em Minas Gerais, 2012, Lavras: Editora UFLA.

[67] Silva AC, Rosado SCS, Vieira CT, Carvalho D. Variação genética entre e dentro de populações de candeia (Eremanthus erythropappus (DC.) MacLeish). Ci. Fl., 2007, 17: 271-277.

[68] Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM. IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change, Cambridge University Press. Cambridge

[69] Taberlet P, Gielly L, Pautou G, Bouvet J. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol, 1991, 17: 1105-1109.

[70] Tse-ring, K, Sharma, E, Chettri, N, Shrestha, AB (2010). Climate change vulnerability of mountain ecosystems in the Eastern Himalayas. International centre for integrated mountain development (ICIMOD). http://lib.riskreductionafrica.org/bitstream/handle/123456789/485/climate%20change%20vulnerability%20of%20mountain%20ecosystems%20in%20the%20Eastern%20Himalayas.pdf?sequence=1. Accessed 15 Apr 2017

[71] Vieira FDA, Fajardo CG, Carvalho D. Biologia floral de candeia (Eremanthus erythropappus, Asteraceae). Pesqui Florest Bras, 2012, 32: 477.

[72] Vieira FDA, Novaes RML, Fajardo CG, Santos RMD, Almeida HDS, Carvalho D, Lovat MB. Holocene southward expansion in seasonally dry tropical forests in South America: phylogeography of Ficus bonijesulapensis (Moraceae). Bot J Linn Soc, 2015, 177: 189-201.

[73] Wisz MS, Hijmans RJ, Li J, Peterson AT, Graham CH, Guisan A. Effects of sample size on the performance of species distribution models. Divers Distrib, 2008, 14: 763-773.

[74] Zuber SM, Villamil MB. Meta-analysis approach to assess effect of tillage on microbial biomass and enzyme activities. Soil Biol Biochem, 2016, 30: 176-187.