From micro- to macroevolution: insights from a Neotropical bromeliad with high population genetic structure adapted to rock outcrops

A Correction to this article was published on 27 August 2020

This article has been updated

Abstract

Geographic isolation and reduced population sizes can lead to local extinction, low efficacy of selection and decreased speciation. However, population differentiation is an essential step of biological diversification. In allopatric speciation, geographically isolated populations differentiate and persist until the evolution of reproductive isolation and ecological divergence completes the speciation process. Pitcairnia flammea allows us to study the evolutionary consequences of habitat fragmentation on naturally disjoint rock-outcrop species from the Brazilian Atlantic Rainforest (BAF). Our main results showed low-to-moderate genetic diversity within populations, and deep population structuring caused by limited gene flow, low connectivity, genetic drift and inbreeding of long-term isolation and persistence of rock-outcrop populations throughout Quaternary climatic oscillations. Bayesian phylogenetic and model-based clustering analyses found no clear northern and southern phylogeographic structure commonly reported for many BAF organisms. Although we found two main lineages diverging by ~2 Mya during the early Pleistocene, species’ delimitation analysis assigned most of the populations as independent evolving entities, suggesting an important role of disjoint rock outcrops in promoting high endemism in this rich biome. Lastly, we detected limited gene flow in sympatric populations although some hybridization and introgression were observed, suggesting a continuous speciation process in this species complex. Our data not only inform us about the extensive differentiation and limited gene flow found among Pitcairnia flammea species complex, but they also contain information about the mechanisms that shape the genetic architecture of small and fragmented populations of isolated rock outcrop of recently radiated plants.

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Fig. 1: Geographic distribution of cpDNA haplotypes of Pitcairnia flammea species complex.
Fig. 2: Median-joining network of cpDNA haplotypes of Pitcairnia flammea complex.
Fig. 3: Clustering analyses of genomic variation across the range of Pitcairnia flammea populations.
Fig. 4: FST values for pairwise comparison between populations of Pitcairnia flammea.
Fig. 5: Species tree resulting from the BEAST analysis of plastid DNA regions of Pitcairnia flammea species complex.
Fig. 6: Bayesian phylogenetic tree of plastid DNA haplotypes of Pitcairnia flammea species complex with posterior probabilities (>0.9) shown below the branches, and ages indicated for selected nodes (bars indicate 95% HPD).

Data availability

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.4tmpg4f73.

Change history

  • 27 August 2020

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

References

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

    CAS  PubMed  Google Scholar 

  2. Aguiar-Melo C, Zanella CM, Goetze M et al. (2019) Ecological niche modeling and a lack of phylogeographic structure in Vriesea incurvata suggest historically stable areas in the southern Atlantic Forest. Am J Bot 106:971–983

    PubMed  Google Scholar 

  3. Allmon WD (1992) A causal analysis of stages in allopatric speciation. Oxf Surv Evol Biol 8:219–257

    Google Scholar 

  4. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    CAS  PubMed  Google Scholar 

  5. Barbará T, Martinelli G, Fay MF, Mayo SJ, Lexer C (2007) Population differentiation and species cohesion in two closely related plants adapted to Neotropical high-altitude ‘inselbergs’, Alcantarea imperialis and Alcantarea geniculata (Bromeliaceae). Mol Ecol 16:1981–1992

    PubMed  Google Scholar 

  6. Barres L, Batalha-Filho H, Schnadelbach AS, Roque N (2019) Pleistocene climatic changes drove dispersal and isolation of Richterago discoidea (Asteraceae), an endemic plant of campos rupestres in the central and eastern Brazilian sky islands. Bot J Linn Soc 189:132–152

    Google Scholar 

  7. Batalha-Filho H, Miyaki CY (2016) Late Pleistocene divergence and postglacial expansion in the Brazilian Atlantic Forest: multilocus phylogeography of Rhopias gularis (Aves: Passeriformes). J Zool Syst Evol Res 54:137–147

    Google Scholar 

  8. Benites VM, Schaefer CEGR, Simas FNB, Santos HG (2007) Soils associated with rock outcrops in the Brazilian mountain ranges Mantiqueira and Espinhaço. Rev Bras Bot 30:569–577

    Google Scholar 

  9. Boisselier-Dubayle MC, Leblois R, Samadi S, Lambourdie’re J, Sarthou C (2010) Genetic structure of the xerophilous bromeliad Pitcairnia geyskesii on inselbergs in French guiana—a test of the forest refuge hypothesis. Ecography (Cop) 33:175–184

    Google Scholar 

  10. Bonatelli IAS, Perez MF, Peterson AT et al. (2014) Interglacial microrefugia and diversification of a cactus species complex: phylogeography and palaeodistributional reconstructions for Pilosocereus aurisetus and allies. Mol Ecol 23:3044–3063

    CAS  PubMed  Google Scholar 

  11. Boneh L, Kuperus P, Van Tienderen PH (2003) Microsatellites in the bromeliads Tillandsia fasciculata and Guzmania monostachya. Mol Ecol Notes 3:302–303

    CAS  Google Scholar 

  12. Byrne M, Krauss SL, Millar MA et al. (2019) Persistence and stochasticity are key determinants of genetic diversity in plants associated with banded iron formation inselbergs Biol Rev 94:753–772

    PubMed  Google Scholar 

  13. Cabanne GS, Santos FR, Miyaki CY (2007) Phylogeography of Xiphorhynchus fuscus (Passeriformes, Dendrocolaptidae): Vicariance and recent demographic expansion in southern Atlantic forest. Biol J Linn Soc 91:73–84

    Google Scholar 

  14. Cabanne GS, Sari EHR, Meyer D, Santos FR, Miyaki CY (2013) Matrilineal evidence for demographic expansion, low diversity and lack of phylogeographic structure in the Atlantic forest endemic Greenish Schiffornis Schiffornis virescens (Aves: Tityridae). J Ornithol 154:371–384

    Google Scholar 

  15. Cardoso DC, Cristiano MP, Tavares MG, Schubart CD, Heinze J (2015) Phylogeography of the sand dune ant Mycetophylax simplex along the Brazilian Atlantic Forest coast: Remarkably low mtDNA diversity and shallow population structure. BMC Evol Biol 15:1–13

    CAS  Google Scholar 

  16. Carnaval AC, Moritz C (2008) Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest. J Biogeogr 35:1187–1201

    Google Scholar 

  17. Carnaval AC, Waltari E, Rodrigues MT et al. (2014) Prediction of phylogeographic endemism in an environmentally complex biome. Proc R Soc B Biol Sci 281:20141461

    Google Scholar 

  18. Colombi VH, Lopes SR, Fagundes V (2010) Testing the Rio Doce as a riverine barrier in shaping the atlantic rainforest population divergence in the rodent Akodon cursor. Genet Mol Biol 33:785–789

    PubMed  PubMed Central  Google Scholar 

  19. Corander J, Cheng L, Marttinen P, Tang J (2013) BAPS: bayesian analysis of population structure. Manual v 6:0

    Google Scholar 

  20. Costa LP (2003) The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals. J Biogeogr 30:71–86

    Google Scholar 

  21. Couvet D (2002) Deleterious effects of restricted gene flow in fragmented populations. Conserv Biol 16:369–376

    Google Scholar 

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

    Google Scholar 

  23. Darriba D, Taboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    CAS  PubMed  PubMed Central  Google Scholar 

  24. de Paula LF, Leal BS, Rexroth J, Porembski S, Palma-Silva C (2017) Transferability of microsatellite loci to Vellozia plicata (Velloziaceae), a widespread species on Brazilian inselbergs. Rev Bras Bot 40:1071–1075

    Google Scholar 

  25. Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169

    CAS  Google Scholar 

  26. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    PubMed  PubMed Central  Google Scholar 

  27. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Google Scholar 

  29. Ennos R (1994) Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72:250–259

    Google Scholar 

  30. 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

    CAS  PubMed  Google Scholar 

  31. 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

    PubMed  Google Scholar 

  32. Franco FF, Jojima CL, Perez MF, Zappi DC, Taylor N, Moraes EM (2017) The xeric side of the Brazilian Atlantic Forest: the forces shaping phylogeographic structure of cacti. Ecol Evol 7:9281–9293

    PubMed  PubMed Central  Google Scholar 

  33. Frankham R, Ballou JD, Dudash MR et al. (2012) Implications of different species concepts for conserving biodiversity. Biol Conserv 153:25–31

    Google Scholar 

  34. Folk RA, Freudenstein JV (2015) ‘Sky islands’ in the eastern U.S.A.?—Strong phylogenetic structure in the Heuchera parviflora group (Saxifragaceae). Taxon 64:254–271

    Google Scholar 

  35. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    CAS  PubMed  Google Scholar 

  36. Givnish TJ, Barfuss MHJ, Van EeB et al. (2014) Adaptive radiation, correlated and contingent evolution, and net species diversification in Bromeliaceae. Mol Phylogenet Evol 71:55–78

    PubMed  Google Scholar 

  37. Givnish TJ, Millam KC, Evans TM et al. (2004) Ancient vicariance or recent long-distance dispersal? inferences about phylogeny and South American–African disjunctions in Rapateaceae and Bromeliaceae based on ndh F sequence data. Int J Plant Sci 165:S35–S54

    CAS  Google Scholar 

  38. Gonçalves-Oliveira RC, Wöhrmann T, Benko-Iseppon AM et al. (2017) Population genetic structure of the rock outcrop species Encholirium spectabile (Bromeliaceae): the role of pollination vs. seed dispersal and evolutionary implications. Am J Bot 104:868–878

    PubMed  Google Scholar 

  39. Grazziotin FG, Monzel M, Echeverrigaray S, Bonatto SL (2006) Phylogeography of the Bothrops jararaca complex (Serpentes: Viperidae): past fragmentation and island colonization in the Brazilian Atlantic Forest. Mol Ecol 15:3969–3982

    CAS  PubMed  Google Scholar 

  40. Harvey MG, Seeholzer GF, Smith BT, Rabosky DL, Cuervo AM, Brumfield RT (2017) Positive association between population genetic differentiation and speciation rates in New World birds. Proc Natl Acad Sci USA 114:6328–6333

    CAS  PubMed  Google Scholar 

  41. He K, Jiang X (2014) Sky islands of southwest China. I: an overview of phylogeographic patterns. Chin Sci Bull 59:585–597

    Google Scholar 

  42. Hedin M, Carlson D, Coyle F (2015) Sky island diversification meets the multispecies coalescent—Divergence in the spruce-fir moss spider (Microhexura montivaga, Araneae, Mygalomorphae) on the highest peaks of southern Appalachia. Mol Ecol 24:3467–3484

    PubMed  Google Scholar 

  43. Hirsch LD, Zanella CM, Aguiar-Melo C, Costa LM, Bered F (2020) Interspecific gene flow and an intermediate molecular profile of Dyckiajulianae (Bromeliaceae), an endemic species from southern Brazil. Bot J Linn Soc 192:675–690

    Google Scholar 

  44. Hmeljevski KV, Nazareno AG, Leandro Bueno M, dos Reis MS, Forzza RC (2017) Do plant populations on distinct inselbergs talk to each other? A case study of genetic connectivity of a bromeliad species in an Ocbil landscape. Ecol Evol 7:4704–4716

    PubMed  PubMed Central  Google Scholar 

  45. Honnay O, Jacquemyn H (2007) Susceptibility of common and rare plant species to the genetic consequences of habitat fragmentation. Conserv Biol 21:823–831

    PubMed  Google Scholar 

  46. Kearse M, Moir R, Wilson A et al. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    PubMed  PubMed Central  Google Scholar 

  47. Kessler M, Abrahamczyk S, Krömer T (2020) The role of hummingbirds in the evolution and diversification of Bromeliaceae: unsupported claims and untested hypotheses. Bot J Linn Soc 192:592–608

    Google Scholar 

  48. Khan G, Godoy MO, Franco FF, Perez MF, Taylor NP, Zappi DC, Machado MC, Moraes EM (2018) Extreme population subdivision or cryptic speciation in the cactus Pilosocereus jauruensis? A taxonomic challenge posed by a naturally fragmented system. Syst Biodivers 16:188–199

    Google Scholar 

  49. Lavor P, van den Berg C, Jacobi CM, Carmo FF, Versieux LM (2014) Population genetics of the endemic and endangered Vriesea minarum (Bromeliaceae) in the Iron Quadrangle, Espinhaço Range, Brazil. Am J Bot 101:1167–1175

    PubMed  Google Scholar 

  50. Leal BSS, Graciano VA, Chaves CJN, Huacre LAP, Heuertz M, Palma-Silva C (2019) Dispersal and local persistence shape the genetic structure of a widespread Neotropical plant species with a patchy distribution. Ann Bot 124:499–512

    CAS  PubMed  Google Scholar 

  51. Leal BSS, Palma da Silva C, Pinheiro F (2016) Phylogeographic studies depict the role of space and time scales of plant speciation in a highly diverse Neotropical region. CRC Crit Rev Plant Sci 35:215–230

    Google Scholar 

  52. 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

    Google Scholar 

  53. Leite YLR, Costa LP, Loss AC et al. (2016) Neotropical forest expansion during the last glacial period challenges refuge hypothesis. Proc Natl Acad Sci 113:1008–1013

    CAS  PubMed  Google Scholar 

  54. Lexer C, Marthaler F, Humbert S et al. (2016) Gene flow and diversification in a species complex of Alcantarea inselberg bromeliads. Bot J Linn Soc 181:505–520

    Google Scholar 

  55. Lousada JM, Lovato MB, Borba EL (2013) High genetic divergence and low genetic variability in disjunct populations of the endemic Vellozia compacta (Velloziaceae) occurring in two edaphic environments of Brazilian campos rupestres. Rev Bras Bot 36:45–53

    Google Scholar 

  56. Martinelli G (2007) Mountain biodiversity in Brazil. Rev Brasileira de Botanica 30:587–597

    Google Scholar 

  57. Martins F, de M (2011) Historical biogeography of the Brazilian Atlantic forest and the Carnaval-Moritz model of Pleistocene refugia: what do phylogeographical studies tell us? Biol J Linn Soc 104:499–509

    Google Scholar 

  58. Maswanganye KA, Cunningham MJ, Bennett NC, Chimimba CT, Bloomer P (2017) Life on the rocks: multilocus phylogeography of rock hyrax (Procavia capensis) from southern Africa. Mol Phylogenet Evol 114:49–62

    PubMed  Google Scholar 

  59. Meirelles ST, Pivello VR, Joly CA (1999) The vegetation of granite rock outcrops in Rio de Janeiro, Brazil, and the need for its protection. Environ Conserv 26:10–20

    Google Scholar 

  60. Menezes L, Canedo C, Batalha-Filho H, Garda AA, Gehara M, Napoli MF (2016) Multilocus phylogeography of the treefrog Scinax eurydice (Anura, Hylidae) reveals a plio-pleistocene diversification in the atlantic forest. PLoS ONE 11:e0154626

    PubMed  PubMed Central  Google Scholar 

  61. Millar MA, Coates DJ, Byrne M (2013) Genetic connectivity and diversity in inselberg populations of Acacia woodmaniorum, a rare endemic of the Yilgarn Craton banded iron formations. Heredity 111:437–444

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Mittermeier R, Gill P, Hoffmann M, Pilgrim J, Brooks J, Mittermeier C (2005) Hotspots revisited: earth’s biologically richest and most endangered terrestrial ecoregions. Chicago University: Cemex, Mexico City

  63. Monteiro RF, Forzza RC (2008) A Família Bromeliaceae no Parque Estadual do Initipoca, Minas Gerais, Brasil. Bol Botânica da Univ São Paulo 26.

  64. Mota MR, Pinheiro F, Leal BSS, Wendt T, Palma-Silva C (2019) The role of hybridization and introgression in maintaining species integrity and cohesion in naturally isolated inselberg bromeliad populations. Plant Biol 21:122–132

    CAS  PubMed  Google Scholar 

  65. Myers N, Mittermeler RA, Mittermeler CG, Da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    CAS  Google Scholar 

  66. Nosil P (2012) Ecological speciation. Oxford University Press, Oxford; New York

    Google Scholar 

  67. Oliveira-Filho AT, Fontes MAL (2000) Patterns of floristic differentiation among Atlantic Forests in Southeastern Brazil and the influence of climate1. Biotropica 32:793–810

    Google Scholar 

  68. Paggi GM, Palma-Silva C, Bered F et al. (2008) Isolation and characterization of microsatellite loci in Pitcairnia albiflos (Bromeliaceae), an endemic bromeliad from the Atlantic Rainforest, and cross-amplification in other species. Mol Ecol Resour 8:980–982

    CAS  PubMed  Google Scholar 

  69. Palma-Silva C, Fay MF (2020) Bromeliaceae as a model group in understanding the evolution of Neotropical biota. Bot J Linn Soc 569–586

  70. Palma-Silva C, Cavallari MM, Barbará T et al. (2007) A set of polymorphic microsatellite loci for Vriesea gigantea and Alcantarea imperialis (Bromeliaceae) and cross-amplification in other bromeliad species. Mol Ecol Notes 7:654–657

    CAS  Google Scholar 

  71. Palma-Silva C, Cozzolino S, Paggi GM, Lexer C, Wendt T (2015) Mating system variation and assortative mating of sympatric bromeliads (Pitcairnia spp.) endemic to Neotropical inselbergs. Am J Bot 102:758–764

    PubMed  Google Scholar 

  72. Palma-Silva C, Leal BS, Chaves CJ, Fay MF (2016) Advances in and perspectives on evolution in Bromeliaceae. Bot J Linn Soc 181:305–322

    Google Scholar 

  73. Palma-Silva C, Lexer C, Paggi GM, Barbará T, Bered F, Bodanese-Zanettini MH (2009) Range-wide patterns of nuclear and chloroplast DNA diversity in Vriesea gigantea (Bromeliaceae), a Neotropical forest species. Heredity 103:503–512

    CAS  PubMed  Google Scholar 

  74. Palma-Silva C, Wendt T, Pinheiro F et al. (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

    CAS  PubMed  Google Scholar 

  75. Paz A, Spanos Z, Brown JL et al. (2019) Phylogeography of Atlantic Forest glassfrogs (Vitreorana): when geography, climate dynamics and rivers matter. Heredity 122:545–557

    CAS  PubMed  Google Scholar 

  76. Pennington RT, Lavin M, Prado DE, Pendry CA, Pell SK, Butterworth CA (2004) Historical climate change and speciation: Neotropical seasonally dry forest plants show patterns of both tertiary and quaternary diversification. Trans R Soc Lond B 359:515–537

    Google Scholar 

  77. Peres EA, Benedetti AR, Hiruma ST, Sobral-Souza T, Pinto-da-Rocha R (2019) Phylogeography of Sodreaninae harvestmen (Arachnida: Opiliones: Gonyleptidae): Insights into the biogeography of the southern Brazilian Atlantic Forest. Mol Phylogenet Evol 138:1–16

    PubMed  Google Scholar 

  78. Pinangé DSB, Krapp F, Zizka G et al. (2017) Molecular phylogenetics, historical biogeography andcharacter evolution in Dyckia (Bromeliaceae, Pitcairnioideae). Bot J Linn Soc 183:39–56

  79. Pinheiro F, Cozzolino S (2013) Epidendrum (Orchidaceae) as a model system for ecological and evolutionary studies in the Neotropics. Taxon 62:77–88

    Google Scholar 

  80. Pinheiro F, Cozzolino S, Draper D et al. (2014) Rock outcrop orchids reveal the genetic connectivity and diversity of inselbergs of northeastern Brazil. BMC Evol Biol 14:49

  81. Pinheiro F, Dantas-Queiroz MV, Palma-Silva C (2018) Plant species complexes as models to understand speciation and evolution: a review of South American studies. CRC Crit Rev Plant Sci 37:54–80

    Google Scholar 

  82. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Google Scholar 

  83. Porembski S (2007) Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Rev Bras Botânica 30:579–586

    Google Scholar 

  84. 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 

  85. Raymond M, Rousset F (2006) An exact test for population differentiation. Evolution 49:1280–1283

    Google Scholar 

  86. Ribeiro RA, Lemos-Filho JP, Ramos ACS, Lovato MB (2011) Phylogeography of the endangered rosewood (Fabaceae): Insights into the evolutionary history and conservation of the Brazilian Atlantic Forest. Heredity 106:46–57

    CAS  PubMed  Google Scholar 

  87. Rivera D, Prates I, Rodrigues MT, Carnaval AC (2020) Effects of climate and geography on spatial patterns of genetic structure in tropical skinks. Mol Phylogenet Evol 143:106661

    PubMed  Google Scholar 

  88. Rozas J, Ferrer-Mata A, Sánchez-DelBarrio J. et al. (2017) DnaSP v6: DNA sequence polymorphism analysis of large datasets. Mol Biol Evol 34:3299–3302

    CAS  Google Scholar 

  89. Ruas RDB, Paggi GM, Melo CA, Hirsch LD, Bered F (2020) Strong genetic structure in Dyckia excelsa (Bromeliaceae), an endangered species found on ironstone outcrops in Pantanal, Brazil. Bot J Linn Soc 192:691–705

    Google Scholar 

  90. Saraiva DP, Mantovani A, Campostrini Forzza R (2015) Insights into the evolution of Pitcairnia (Pitcairnioideae-Bromeliaceae), Based on Morphological Evidence. Syst Bot 40:726–736

    Google Scholar 

  91. Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rainforest. Ann Bot 90:517–524

    PubMed  PubMed Central  Google Scholar 

  92. Scarano FR (2009) Plant communities at the periphery of the Atlantic rain forest: rare-species bias and its risks for conservation. Biol Conserv 142:1201–1208

    Google Scholar 

  93. Schubert K (2017) Systematik und Evolution der Gattung Pitcairnia L’Heritier (Bromeliaceae). Universität Kassel: Germany

  94. Schütz N, Krapp F, Wagner N, Weising K (2016) Phylogenetics of Pitcairnioideae s.s. (Bromeliaceae): evidence from nuclear and plastid DNA sequence data. Bot J Linn Soc 181:323–342

    Google Scholar 

  95. Silva GAR, Antonelli A, Lendel A, Moraes E, de M, Manfrin MH (2018) The impact of early quaternary climate change on the diversification and population dynamics of a South American cactus species. J Biogeogr 45:76–88

    Google Scholar 

  96. Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogeneticstudies in angiosperms: the tortoise and the hare III. Am J Bot 94:275–288

    CAS  PubMed  Google Scholar 

  97. Smith LB, Downs RJ (1974) Flora Neotropica, Vol. 14, No. 1, Pitcairnioideae (Bromeliaceae). Hafner Press: New York, USA

  98. Speziale KL, Ezcurra C (2012) The role of outcrops in the diversity of Patagonian vegetation: relicts of glacial palaeofloras? Flora Morphol Distrib Funct Ecol. Plants 207:141–149

    Google Scholar 

  99. Sukumaran J, Knowles LL (2017) Multispecies coalescent delimits structure, not species. Proc Natl Acad Sci 114:1607–1612

    CAS  PubMed  Google Scholar 

  100. Tapper SL, Byrne M, Yates CJ et al. (2014) Prolonged isolation and persistence of a common endemic on granite outcrops in both mesic and semi-arid environments in south-western Australia. J Biogeogr 41:2032–2044

    Google Scholar 

  101. Tchaicka L, Eizirik E, De Oliveira TG, Cândido JF, Freitas TRO (2007) Phylogeography and population history of the crab-eating fox (Cerdocyon thous). Mol Ecol 16:819–838

    CAS  PubMed  Google Scholar 

  102. Thomé MTC, Zamudio KR, Giovanelli JGR, Haddad CFB, Baldissera FA, Alexandrino J (2010) Phylogeography of endemic toads and post-Pliocene persistence of the Brazilian Atlantic Forest. Mol Phylogenet Evol 55:1018–1031

    PubMed  Google Scholar 

  103. Turchetto-Zolet AC, Turchetto C, Cruz F et al. (2016) Phylogeography and ecological niche modelling in Eugenia uniflora (Myrtaceae) suggest distinct vegetational responses to climate change between the southern and the northern Atlantic Forest. Bot J Linn Soc 182:670–688

    Google Scholar 

  104. Vergara J, Acosta LE, González-Ittig RE, Vaschetto LM, Gardenal CN (2017) The disjunct pattern of the Neotropical harvestman Discocyrtus dilatatus (Gonyleptidae) explained by climate-driven range shifts in the Quaternary: paleodistributional and molecular evidence. PLoS ONE 12:1–32.

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  106. Wendt T, Canela MB, Gelli de Faria AP, Rios RI (2001) Reproductive biology and natural hybridization between two endemic species of Pitcairnia (Bromeliaceae). Am J Bot 88:1760–1767

    CAS  PubMed  Google Scholar 

  107. Wendt T, Canela MBF, Klein DE, Rios RI (2002) Selfing facilitates reproductive isolation among three sympatric species of Pitcairnia (Bromeliaceae). Plant Syst Evol 232:201–212

    Google Scholar 

  108. Wendt T, Canela MBF, Morrey-Jones JE, Henriques AB, Rios RI (2000) Recognition of Pitcairnia corcovadensis (Bromeliaceae) at the species Level. Syst Bot 25:389–398

    Google Scholar 

  109. Wiens JJ (2007) Species delimitation: new approaches for discovering diversity. Syst Biol 56:875–878

    PubMed  Google Scholar 

  110. Wiens JJ, Camacho A, Goldberg A et al. (2019) Climate change, extinction, and Sky Island biogeography in a montane lizard. Mol Ecol 28:2610–2624

    PubMed  Google Scholar 

  111. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed  PubMed Central  Google Scholar 

  112. Wöhrmann T, Michalak I, Zizka G, Weising K (2020) Strong genetic differentiation among populations of Fosterella rusbyi (Bromeliaceae) in Bolivia. Bot J Linn Soc 192:744–759

    Google Scholar 

  113. Wöhrmann T, Wagner N, Krapp F, Huettel B, Weising K (2012) Development of microsatellite markers in Fosterella rusbyi (bromeliaceae) using 454 pyrosequencing. Am J Bot 99:e160–e163

    PubMed  Google Scholar 

  114. Wöhrmann T, Weising K (2011) In silico mining for simple sequence repeat loci in a pineapple expressed sequence tag database and cross-species amplification of EST-SSR markers across Bromeliaceae. Theor Appl Genet 123:635–647

    PubMed  Google Scholar 

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We are thankful to Sérgio Luiz Nazareth for his assistance during fieldwork, to Juliana Ribeiro Martins Santin and Carolina Carvalho for their assistance in laboratory work. We also thank Karina Lucas da Silva-Brandão, Fabio Raposo do Amaral and Jordana Neri for comments in the early version of the paper. This study was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2009/52725-3, 2013/16440-0, 2013/12966-7, 2014/15588-6, 2014/02377-7, 2015/07685-4 and 2018/07596-0), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Edital Universal (475937/2013-9). We are thankful for the fellowship provided to CP (300819/2016-1) by Conselho Nacional de Desenvolvimento Científico e Tecnológico and to MMR by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). We also thank IAPT (International Association for Plant Taxonomy) for the IAPT research grants in plant systematics. The authors thank Espaço da Escrita – Pro-Reitoria de Pesquisa – UNICAMP – for the language services provided.

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Correspondence to Clarisse Palma-Silva.

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Mota, M.R., Pinheiro, F., Leal, B.S.d.S. et al. From micro- to macroevolution: insights from a Neotropical bromeliad with high population genetic structure adapted to rock outcrops. Heredity 125, 353–370 (2020). https://doi.org/10.1038/s41437-020-0342-8

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