Gene flow between vicariant tree species: insights into savanna-forest evolutionary relationships
Tóm tắt
Studying the genetic structure of vicariant species (i.e., closely related species that occupy ecologically distinct yet adjacent habitats) can shed light on the evolution and divergence of species with different ecological requirements. A previous phylogeographic study identified chloroplast DNA haplotype sharing between two vicariant tree species, one from forest (Hymenaea courbaril) and one from savanna (H. stigonocarpa) habitats. These species co-occur in the Brazilian Cerrado, a biome that encompasses forest patches and riverine forests within a savanna matrix. In order to investigate the evolutionary processes involved in the genetic divergence of these trees, we used nuclear microsatellite markers, statistical methods including approximate Bayesian computation (ABC), and leaf morphology to analyze neighboring and distant populations. Bayesian analysis revealed admixture between the species. ABC analysis supported the scenarios with the occurrence of gene flow between species during the Last Glacial Maximum or from the Holocene to the present, when compared to alternative scenarios of no gene flow or constant gene flow since divergence. However, putative hybrids did not exhibit intermediate leaflet morphology, which could be related to distinct selective pressures maintaining species integrity even in the face of gene flow. Our results suggest that despite morphological differences between savanna and forest species, interspecific barriers to gene flow might not be fully developed between vicariant tree species and that interspecific hybridization in trees from Cerrado biome may be an underdiagnosed process.
Tài liệu tham khảo
Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, Boughman JW, Brelsford A, Buerkle CA, Buggs R, Butlin RK, Dieckmann U, Eroukhmanoff F, Grill A, Cahan SH, Hermansen JS, Hewitt G, Hudson AG, Jiggins C, Jones J, Keller B, Marczewski T, Mallet J, Martinez-Rodriguez P, Most M, Mullen S, Nichols R, Nolte AW, Parisod C, Pfennig K, Rice AM, Ritchie MG, Seifert B, Smadja CM, Stelkens R, Szymura JM, Vainola R, Wolf JBW, Zinner D (2013) Hybridization and speciation. J Evol Biol 26:229–246
Ackerly DD, Dudley SA, Sultan SE, Schmitt J, Coleman JS, Linder CR, Sandquist DR, Geber MA, Evans AS, Dawson TE, Lachowicz MJ (2000) The evolution of plant ecophysiological traits: recent advances and future directions. Bioscience 50:979–995
Archibald S, Bond WJ (2003) Growing tall vs growing wide: tree architecture and allometry of Acacia karroo in forest, savanna, and arid environments. Oikos 102:3–14
Asquith NM, Terborgh J, Arnold AE, Riveros CM (1999) The fruits the agouti ate: Hymenaea courbaril seed fate when its disperser is absent. J Trop Ecol 15:229–235
Barros FV, Goulart MF, Telles SBS, Lovato MB, Valladares F, Lemos-Filho JP (2012) Phenotypic plasticity to light of two congeneric trees from contrasting habitats: Brazilian Atlantic forest versus Cerrado (savanna). Plant Biol 14:208–215
Bawa KS (1974) Breeding systems of tree species of a lowland tropical community. Evolution 28:85–92
Beaumont MA (2008) Joint determination of topology, divergence time, and immigration in population trees. In:Matsumura S, Forster P, Renfrew C (eds) simulations, genetics, and human prehistory. McDonald Institute for Archaeological Research, Cambridge, pp 135–154
Beaumont MA, Zhang WY, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035
Behling H, Lichte M (1997) Evidence of dry and cold climatic conditions at glacial times in tropical southeastern Brazil. Quat Res 48:348–358
Behling H, Negrelle RRB (2001) Tropical rain forest and climate dynamics of the Atlantic lowland, southern Brazil, during the late quaternary. Quat Res 56:383–389
Bittencourt NS Jr, Moraes CIG (2010) Self-fertility and polyembryony in South American yellow trumpet trees (Handroanthus chrysotrichus and H. ochraceus, Bignoniaceae): a histological study of postpollination events. Plant Syst Evol 288:59–76
Caddah MK, Campos T, Zucchi MI, Souza AP, Bittrich V, Amaral MCE (2013) Species boundaries inferred from microsatellite markers in the Kielmeyera coriacea complex (Calophyllaceae) and evidence of asymmetric hybridization. Plant Syst Evol 299:731–741
Camargo A, Morando M, Avila LJ, Sites JW (2012) Species delimitation with ABC and other coalescent-based methods: a test of accuracy with simulations and an empirical example with lizards of the Liolaemus darwinii complex (Squamata: Liolaemidae). Evolution 66:2834–2849
Cavallari MM, Gimenes MA, Billit C, Torres RB, Zucchi MI, Cavalheiro AJ, Bouvet JM (2010) Population genetic relationships between Casearia sylvestris (Salicaceae) varieties occurring sympatrically and allopatrically in different ecosystems in south-east Brazil. Ann Bot-London 106:627–636
Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis models and estimation procedures. Am J Hum Genet 19:233–257
Ciampi AY, Azevedo VCR, Gaiotto FA, Ramos AC, Lovato MB (2008) Isolation and characterization of microsatellite loci for Hymenaea courbaril and transferability to Hymenaea stigonocarpa, two tropical timber species. Mol Ecol Resour 8:1074–1077
Collevatti RG, Leoi LCT, Leite SA, Gribel R (2009) Contrasting patterns of genetic structure in Caryocar (Caryocaraceae) congeners from flooded and upland Amazonian forests. Biol J Linn Soc 98:278–290
Costa WS, Souza AL, Souza PB (2011) Ecologia, manejo, silvicultura e tecnologia de espécies nativas da Mata Atlântica. Espécies Nativas da Mata Atlântica 2 http://www.sifloresta.ufv.br/bitstream/handle/123456789/11139/Jatoba_Ecologia,%20manejo,%20silvicultura%20e%20tecnologia%20de%20especies%20nativas%20da%20Mata%20atlantica%20.pdf?sequence=1&isAllowed=y. Accessed 10 November 2015
Currat M, Ruedi M, Petit RJ, Excoffier L (2008) The hidden side of invasions: massive introgression by local genes. Evolution 62:1908–1920
Dieringer D, Schlotterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169
Duarte MC, Esteves GL, Salatino MLF, Walsh KC, Baum DA (2011) Phylogenetic analyses of Eriotheca and related genera (Bombacoideae, Malvaceae). Syst Bot 36:690–701
Dunphy BK, Hamrick JL, Schwagerl J (2004) A comparison of direct and indirect measures of gene flow in the bat-pollinated tree Hymenaea courbaril in the dry forest life zone of southwestern Puerto Rico. Int J Plant Sci 165:427–436
Eiten G (1972) The Cerrado vegetation of Brazil. Bot Rev 38:201–341
Estoup A, Jarne P, Cornuet JM (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604
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
Excoffier L, Dupanloup I, Huerta-Sanchez E, Sousa VC, Foll M (2013) Robust demographic inference from genomic and SNP data. PLoS Genet 9:e1003905
Excoffier L, Estoup A, Cornuet JM (2005) Bayesian analysis of an admixture model with mutations and arbitrarily linked markers. Genet 169 (3):1727-1738
Excoffier L, Foll M (2011) Fastsimcoal: a continuous-time coalescent simulator of genomic diversity under arbitrarily complex evolutionary scenarios. Bioinformatics 27:1332–1334
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
Fiaschi P, Plunkett GM (2011) Monophyly and phylogenetic relationships of neotropical Schefflera (Araliaceae) based on plastid and nuclear markers. Syst Bot 36:806–817
Firetti-Leggieri F, Costa IR, Lohmann LG, Semir J, Forni-Martins ER (2011) Chromossome studies in Bignonieae (Bignoniaceae): the first record of polyploidy in Anemopaegma. Cytologia 76:185–191
Forni-Martins ER, Martins FR (2000) Chromosome studies on Brazilian cerrado plants. Genet Mol Biol 23:947–955
Forni-Martins ER, Pinto-Maglio CAF, Cruz ND (1995) Chromosome numbers in Brazilian cerrado plants. Rev Bras Genet 18:281–288
Fougère-Danezan M, Maumont S, Bruneau A (2007) Relationships among resin-producing Detarieae s.L. (Leguminosae) as inferred by molecular data. Syst Bot 32:748–761
Furley PA (1992) Edaphic changes at the forest savanna boundary with particular reference to the Neotropics. In: Furley P, Proctor J, Ratter J (eds) Nature and dynamics of forest-savanna boundaries. Chapman & Hall, London, pp 91–117
Garcia MG, Silva RS, Carniello MA, Veldman JW (2011) Molecular evidence of cryptic speciation, historical range expansion, and recent intraspecific hybridization in the neotropical seasonal forest tree Cedrela fissilis (Meliaceae). Mol Phylogenet Evol 61:639–649
Gibbs PE, Oliveira PE, Bianchi MB (1999) Postzygotic control of selfing in Hymenaea stigonocarpa (Leguminosae-Caesalpinioideae), a bat-pollinated tree of the Brazilian cerrados. Int J Plant Sci 160:72–78
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html. Acessed 30 Oct 2015
Goulart MF, Lovato MB, Barros FD, Valladares F, Lemos JP (2011) Which extent is plasticity to light involved in the ecotypic differentiation of a tree species from savanna and forest? Biotropica 43:695–703
Grant PR, Grant BR (2014) Evolutionary biology: speciation undone. Nature 507:178–179
Hamilton G, Currat M, Ray N, Heckel G, Beaumont M, Excoffier L (2005) Bayesian estimation of recent migration rates after a spatial expansion. Genetics 170:409–417
Heringer EP, Barroso GM, Rizzo JA, Rizzini CT (1976) A Flora do Cerrado. In: Ferri MG, coord. IV Simpósio sobre o Cerrado: bases para utilização agropecuária. São Paulo: USP. pp 211–231
Heuertz M, Carnevale S, Fineschi S, Sebastiani F, Hausman JF, Paule L, Vendramin GG (2006) Chloroplast DNA phylogeography of European ashes, Fraxinus sp (Oleaceae): roles of hybridization and life history traits. Mol Ecol 15:2131–2140
Hiscock SJ, Dickinson HG (1993) Unilateral incompatibility within the Brassicaceae: further evidence for the involvement of the self-incompatibility (S)-locus. Theor Appl Genet 86:744–753
Hoffmann WA, Franco AC (2003) Comparative growth analysis of tropical forest and savanna woody plants using phylogenetically independent contrasts. J Ecol 91:475–484
Hovenden MJ, Vander Schoor JK (2005) The response of leaf morphology to irradiance depends on altitude of origin in Nothofagus cunninghamii. New Phytol 169:291–297
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405
Lee YT, LAngenheim JH (1975) Systematics of the genus Hymenaea L. (Leguminosae, Caesalpinioidae, Detarieae). U Calif Publ Bot 69:1–109
Lacerda DR, Lemos Filho JP, Acedo MDP, Lovato MB (2002) Molecular differentiation of two vicariant neotropical tree species, Plathymenia foliolosa and P. reticulata (Mimosoideae), inferred using RAPD markers. Plant Syst Evol 235:67–77
Leonard JM, Bollmann SR, Hays JB (2003) Reduction of stability of Arabidopsis genomic and transgenic DNA-repeat sequences (microsatellites) by inactivation of AtMSH2 mismatch-repair function. Plant Physiol 133:328–338
Lexer C, Kremer A, Petit RJ (2006) Comment: shared alleles in sympatric oaks: recurrent gene flow is a more parsimonious explanation than ancestral polymorphism. Mol Ecol 15:2007–2012
Marino IAM, Benazzo A, Agostini C, Mezzavilla M, Hoban SM, Patarnello T, Zane L, Bertorelle G (2013) Evidence for past and present hybridization in three Antarctic icefish species provides new perspectives on an evolutionary radiation. Mol Ecol 22:5148–5161
Mittermeier RA, Gil PR, Hoffman M, Pilgrim J, Brooks T, Mittermeier CG, Lamoreux J, Fonseca GAB (2004) Hotspots revisited: Earth’s biologically richest and most threatened terrestrial ecoregions. CEMEX, Mexico City
Muir G, Schlotterer C (2005) Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridizing oaks (Quercus spp.). Mol Ecol 14:549–561
Neuenschwander S, Largiader CR, Ray N, Currat M, Vonlanthen P, Excoffier L (2008) Colonization history of the Swiss Rhine basin by the bullhead (Cottus gobio): inference under a Bayesian spatially explicit framework. Mol Ecol 17:757–772
Nielsen EE, Bach LA, Kotlicki P (2006) HYBRIDLAB (version 1.0): a program for generating simulated hybrids from population samples. Mol Ecol Notes 6:971–973
Oliveira PE, Gibbs PE (1994) Pollination and breeding systems of six Vochysia species (Vochysiaceae) in central Brazil. J Trop Ecol 10:509–522
Oliveira PE, Gibbs PE (2002) Pollination and reproductive biology in Cerrado plant communities. In: Oliveira PS, Marquis RJ (eds) The Cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 329–347
Oliveira-Filho AT, Ratter JA (2002) Vegetation physiognomies and woody flora of the Cerrado biome. In: Oliveira PS, Marquis RJ (eds) The Cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 91–120
Page RDM (1996) Tree view: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
Palma-Silva C, Wendt T, Pinheiro F, Barbara T, Fay MF, Cozzolino S, Lexer C (2011) Sympatric bromeliad species (Pitcairnia spp.) facilitate tests of mechanisms involved in species cohesion and reproductive isolation in neotropical inselbergs. Mol Ecol 20:3185–3201
Pennington RT, Richardson JE, Lavin M (2006) Insights into the historical construction of species-rich biomes from dated plant phylogenies, neutral ecological theory and phylogenetic community structure. New Phytol 172:605–616
Petit RJ, Excoffier L (2009) Gene flow and species delimitation. Trends Ecol Evol 24:386–393
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rambaut A, Drummond AJ (2009) Tracer Version:1.5 http://beast.bio.ed.ac.uk/Tracer. Accessed 5 October 2015
Ramos ACS, Lemos-Filho JP, Lovato MB (2009) Phylogeographical structure of the neotropical forest tree Hymenaea courbaril (Leguminosae: Caesalpinioideae) and its relationship with the vicariant Hymenaea stigonocarpa from Cerrado. J Hered 100:206–216
Ramos ACS, Lemos-Filho JP, Ribeiro RA, Santos FR, Lovato MB (2007) Phylogeography of the tree Hymenaea stigonocarpa (Fabaceae:Caesalpinioideae) and the influence of quaternary climate changes in the Brazilian cerrado. Ann Bot 100:1219–1228
Ratter JA, Bridgewater S, Ribeiro JF (2006) Biodiversity patterns of the woody vegetation of the Brazilian cerrado. In: Pennington RT, Ratter JA, Lewis GP (eds) Neotropical savannas and seasonally dry forests: plant diversity, biogeography and conservation. CRC⁄ Taylor & Francis, Boca Raton, pp 31–66
Ribeiro RD, Cardoso D, de Lima HC (2015) A new species of Hymenaea (Leguminosae: Caesalpinioideae) with a revised identification key to the genus in the Brazilian Atlantic forest. Syst Bot 40:151–156
Rieseberg LH, Ellstrand NC, Arnold M (1993) What can molecular and morphological markers tell us about plant hybridization? Crit Rev Plant Sci 12:213–241
Rizzini CT (1997) Tratado de fitogeografia do Brasil: aspectos ecológicos, sociológicos e florísticos. Âmbito Cultural, Rio de Janeiro
Sano SM, Fonseca CEL (2003) Taxa de Sobreviência e Frutificação de Espécies Nativas do Cerrado. Boletim de Pesquisa e Desenvolvimento. http://www.cpac.embrapa.br/baixar/91/t. Accessed 10 Nov 2015
Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380
Scliar MO, Gouveia MH, Benazzo A, Ghirotto S, Fagundes NJR, Leal TP, Magalhaes WCS, Pereira L, Rodrigues MR, Soares-Souza GB, Cabrera L, Berg DE, Gilman RH, Bertorelle G, Tarazona-Santos E (2014) Bayesian inferences suggest that Amazon Yunga natives diverged from Andeans less than 5000 ybp: implications for South American prehistory. BMC Evol Biol 14:174. doi:10.1186/s12862-014-0174-3
Silberbauer-Gottsberger L, Gottsberger G, Ehrendorfer F (1992) Hybrid speciation and radiation in the neotropical woody genus Tocoyena (Rubiaceae). Plant Syst Evol 181:143–169
Simon MF, Grether R, de Queiroz LP, Skema C, Pennington RT, Hughes CE (2009) Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire. Proc Natl Acad Sci U S A 106:20359–20364
Simon MF, Pennington T (2012) Evidence for adaptation to fire regimes in the tropical savannas of the Brazilian cerrado. Int J Plant Sci 173:711–723
Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462
Souza IM, Funch LS (2016) Synchronization of leafing and reproductive phenological events in Hymenaea L. species (Leguminosae, Caesalpinioideae): the role of photoperiod as the trigger. Braz J Bot. doi:10.1007/s40415-016-0314-7
Thuillet AC, Bru D, David J, Roumet P, Santomi S, Sourdille P, Bataillon T (2002) Direct estimation of mutation rate for 10 microsatellite loci in durum wheat, Triticum turgidum (L.) Thell. ssp. durum desf. Mol Biol Evol 19:122–125
Turchetto C, Fagundes NJR, Segatto ALA, Kuhlemeier C, Neffa VGS, Speranza PR, Bonatto SL, Freitas LB (2014) Diversification in the South American pampas: the genetic and morphological variation of the widespread Petunia axillaris complex (Solanaceae). Mol Ecol 23:374–389
Vähä JP, Primmer CR (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15:63–72
Vallejo-Marín M, Hiscock SJ (2016) Hybridization and hybrid speciation under global change. New Phytol 211:1170–1187
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 4:535–538
Vigouroux Y, Jaqueth JS, Matsuoka Y, Smith OS, Beavis WF, Smith JSC, Doebley J (2002) Rate and pattern of mutation at microsatellite loci in maize. Mol Biol Evol 19:1251–1260
Wang J, Abbott RJ, Peng YL, Du FK, Liu JQ (2011) Species delimitation and biogeography of two fir species (Abies) in central China: cytoplasmic DNA variation. Heredity 107:362–370
Warwick MC, Lewis GP (2003) Revision of Plathymenia (Leguminosae—Mimosoideae). Edinb J Bot 60:111–119
Wegmann D, Leuenberger C, Neuenschwander S, Excoffier L (2010) ABCToolBox: a versatile toolkit for approximate Bayesian computations. BMC Bioinformatics 11:116
Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci U S A 84:9054–9058