Complex phylogeographic patterns indicate Central American origin of two widespread Mesoamerican Quercus (Fagaceae) species

  • Hernando Rodríguez-Correa
  • Ken Oyama
  • Mauricio Quesada
  • Eric J. Fuchs
  • Maura Quezada
  • Lilian Ferrufino
  • Susana Valencia-Ávalos
  • Alfredo Cascante-Marín
  • Antonio González-Rodríguez
Original Article
Part of the following topical collections:
  1. Taxonomy

Abstract

The northern Neotropical region is characterized by a heterogeneous geological and climatic history. Recent studies have shown contrasting patterns regarding the role of geographic elements as barriers that could have determined phylogeographic structure in various species. Recently, the phylogeography and biogeography of Quercus species have been studied intensively, and the patterns observed so far suggest contrasting evolutionary histories for Neotropical species in comparison with their Holarctic relatives. The goal of this study was to describe the phylogeographic structure of two Neotropical oak species (Quercus insignis and Quercus sapotifolia) in the context of the geological and palaeoclimatic history of the northern Neotropics. Populations through the distribution range of both species were collected and characterized using nine chloroplast DNA microsatellite loci. Both oak species showed high levels of genetic diversity and strong phylogeographic structure. The distribution of genetic variation in Q. insignis suggested an influence of two major barriers, the Isthmus of Tehuantepec and the Nicaraguan Depression, while Q. sapotifolia exhibited a genetic structure defined by the heterogeneity of the Chortis highlands. The haplotype networks of both species indicated complex histories, suggesting that colonization from the Sierra Madre de Chiapas to central Mexico and from the north of the Nicaraguan Depression to the Costa Rican mountains may have occurred during different stages, and apparently more than one time. In conclusion, the phylogeographic structure of Neotropical oak species seems to be defined by a combination of geological and climatic events.

Keywords

Neotropical trees Middle America Palaeodistribution Phylogeography Historical demography 

Notes

Acknowledgements

The authors thank Jorge Lobo for laboratory access at the Universidad de Costa Rica (UCR) and Jesus Llanderal, German Sandoval, Wilson Zúñiga, Carlos Funes, Carlos O’Reilly, Iliam Rivera, and Katya Romero for support during the field stage. Paul C. Standley (EAP) and Cyril Hardy Nelson Sutherland (TEFH) herbariums provided logistic assistance in Honduras. The comments by Eduardo Ruiz-Sánchez to a previous version of the manuscript are gratefully acknowledged. H. Rodríguez-Correa specially thanks the Programa de Becas Posdoctorales (DGAPA, UNAM) for providing funding to develop postdoctoral studies at UNAM. HRC also thanks the financial support received by the Red Latinoamericana de Botánica-Andrew W. Mellon Foundation Grant 2010-2011, and all authors acknowledge support from PAPIIT IV201015 and CONACYT 240136 grants.

Data archiving statement

Genotypic data for the studied species will be submitted to the Dryad Digital Repository (datadryad.org/) following its data management policy, the accession numbers will be supplied once available. Meanwhile, data is provided as a supplementary file.

Supplementary material

11295_2017_1147_MOESM1_ESM.xlsx (23 kb)
ESM 1 (XLSX 22 kb)

References

  1. Alexander L, Woeste K (2014) Pyrosequencing of the northern red oak (Quercus rubra L.) chloroplast genome reveals high quality polymorphisms for population management. Tree Genet Genomes 10:803–812CrossRefGoogle Scholar
  2. Arellano E, González-Cozátl FX, Rogers D (2005) Molecular systematics of Middle American harvest mice Reithrodontomys (Muridae), estimated from mitochondrial cytochrome b gene sequences. Mol Phylogenet Evol 37:529–540CrossRefPubMedGoogle Scholar
  3. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1637–48Google Scholar
  4. Braconnot P, Otto-Bliesner B, Harrison S, Joussaume S, Peterschmitt JY et al (2007) Results of PMIP2 coupled simulations of the Mid-Holocene and Last Glacial Maximum–part 2: feedbacks with emphasis on the location of the ITCZ and mid- and high latitudes heat budget. Clim Past 3:279–296CrossRefGoogle Scholar
  5. Castoe TA, Chippindale PT, Campbell JA, Ammerman LK, Parkinson CL (2003) Molecular systematic of the middle American jumping pitvipers (genus Atropoides) and phylogeography of the Atropoides nummifer Complex. Herpetologica 59:421–432CrossRefGoogle Scholar
  6. Cavender-Bares J, González-Rodríguez A, Pahlich A, Koehler K, Deacon N (2011) Phylogeography and climatic niche evolution in the live oaks (Quercus series Virentes) from the tropics to the temperate zone. J Biogeogr 38:962–981CrossRefGoogle Scholar
  7. Cavender-Bares J, González-Rodríguez A, Eaton D, Hipp A, Beulke A, Manos P (2015) Phylogeny and biogeography of the American live oaks (Quercus subsection Virentes): a genomic and population genetics approach. Mol Ecol 24:3668–3687Google Scholar
  8. Chen D, Zhang X, Kang H, Sun X, Yin S, Du H, Yamanaka N, Gapare W, Wu HX, Liu C (2012) Phylogeography of Quercus variabilis based on chloroplast DNA sequence in east Asia: multiple glacial refugia and mainland-migrated island population. PLoS One 7(10):e47268CrossRefPubMedPubMedCentralGoogle Scholar
  9. Collins WD, Blackmon M, Bitz C, Bonan G, Bretherton CS (2004) The community climate system model: CCSM3. J Clim 19:2122–2143CrossRefGoogle Scholar
  10. Cottrell JE, Munro RC, Tabbener HE, Gillies ACM, Forrest GI, Deans JD, Lowe AJ (2002) Distribution of chloroplast DNA variation in British oaks (Quercus robur and Quercus petrae): the influence of postglacial colonization and human management. Forest Ecol Manag 156:191–195CrossRefGoogle Scholar
  11. Csaikl UM, Burg K, Fineschi S, Konig AO, Mátyás G, Petit RJ (2002) Chloroplast DNA variation in the alpine region. Forest Ecol Manag 156:131–145CrossRefGoogle Scholar
  12. DaCosta JM, Klicka J (2008) The Great American Interchange in birds: a phylogenetic perspective with the genus Trogon. Mol Ecol 17:1328–1343CrossRefPubMedGoogle Scholar
  13. Daza JM, Castoe TA, Parkinson CL (2010) Using regional comparative phylogeographic data from snake lineages to infer historical processes in Middle America. Ecography 33:343–354Google Scholar
  14. de Nascimento L, Willis KJ, Fernández-Palacios JM, Criado C, Whittaker RJ (2009) The long-term ecology of the lost forests of La Laguna, Tenerife (Canary Islands). J Biogeogr 36:499–514Google Scholar
  15. Dumolin-Lapègue S, Demesure B, Fineschi S, Le Corre V, Petit RJ (1997) Phylogeographic structure of white oaks throughout the European continent. Genetics 146:1475–1487PubMedPubMedCentralGoogle Scholar
  16. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581CrossRefPubMedGoogle Scholar
  17. Eizirik E, Bonatto SL, Johnson WE, Crawshaw PG Jr, Vié JC, Brousset DM, O’Brien SJ, Salzano FM (1998) Phylogeographic patterns and evolution of the mitochondrial DNA control region in two Neotropical cats (Mammalia, Felidae). J Mol Evol 47:613–624CrossRefPubMedGoogle Scholar
  18. Eizirik E, Kim J-H, Menotti-Raymond M, Crawshaw PG Jr, O’Brien SJ, Jhonson WE (2001) Phylogeography, population history and conservation genetics of jaguars (Panthera onca, Mammalia, Felidae). Mol Ecol 10:65–79CrossRefPubMedGoogle Scholar
  19. Excoffier L, Laval G, Schneider S (2005) Arlequin ver 3.5. An integrated software package for population genetics data analysis. Evol Bioinforma 1:47–60Google Scholar
  20. Fielding AH, Bell JF (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 24:38–49CrossRefGoogle Scholar
  21. Fineschi S, Taurchini D, Grossoni P, Petit RJ, Vendramin GG (2002) Chloroplast DNA variation in white oaks in Italy. Forest Ecol Manag 156:103–114CrossRefGoogle Scholar
  22. Fu YX (1997) Statistical tests of neutrality against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedPubMedCentralGoogle Scholar
  23. Goldstein DB, Ruiz-Linares A, Cavalli-Sforza LL, Feldman MW (1995) An evaluation of genetic distances for use with microsatellite loci. Genetics 139:463–471PubMedPubMedCentralGoogle Scholar
  24. González-Espinosa M, Meave JA, Lorea-Hernández FG, Ibarra-Manríquez G, Newton AC (2011) The red list of Mexican cloud forest trees. Fauna and Flora International (FFI), CambridgeGoogle Scholar
  25. González-Rodríguez A, Bain JF, Golden JL, Oyama K (2004) Chloroplast DNA variation in the Quercus affinis-Quercus laurina complex in Mexico: geographical structure and associations with nuclear and morphological variation. Mol Ecol 13:3467–3476CrossRefPubMedGoogle Scholar
  26. González-Rodríguez A, Arias DM, Oyama K (2005) Genetic variation of populations within the Quercus affinis-Quercus laurina (Fagaceae) complex analyzed with RAPD markers. Can J Bot 83:155–162CrossRefGoogle Scholar
  27. Grivet D, Deguilloux M, Petit RJ, Sork V (2006) Contrasting patterns of historical colonization in white oaks (Quercus spp.) in California and Europe. Mol Ecol 15:4085–4093CrossRefPubMedGoogle Scholar
  28. Gutiérrez-García T, Vázquez-Domínguez E (2013) Consensus between genes and stones in the biogeographic and evolutionary history of Central America. Quat Res 79:311–324CrossRefGoogle Scholar
  29. Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population level. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  30. Hasbún CR, Gómez A, Khöler GG, Lunt DH (2005) Mitochondrial DNA phylogeography of the Mesoamerican spiny-tailed lizards (Ctenosaura quinquecarinata complex): historical biogeography, species status and conservation. Mol Ecol 14:3095–3107CrossRefPubMedGoogle Scholar
  31. Hasumi H, Emori S (2004) K-1 coupled GCM (MIROC) description. Center for Climate System Research (CCSR), University of Tokyo; National Institute for Environmental Studies (NIES); Frontier Research Center for Global Change (FRCGC). http://ccsr.aori.u-tokyo.ac.jp/~hasumi/miroc_description.pdf. Accesed 20 July 2014
  32. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  33. Hooghiemstra H, van der Hammen T (2004) Quaternary Ice-Age dynamics in the Colombian Andes: developing an understanding of our legacy. Phil Trans R Soc Lond B 359:173–181Google Scholar
  34. Jardón-Barbolla L, Delgado-Valerio P, Geada-López G, Vázquez-Lobo A, Piñero D (2011) Phylogeography of Pinus subsection Australes in the Caribbean basin. Ann Bot-London 107:229–241CrossRefGoogle Scholar
  35. Jímenez P, López de Heredia U, Collada C, Lorenzo Z, Gil L (2004) High variability of chloroplast DNA in three Mediterranean evergreen oaks indicates complex evolutionary history. Heredity 93:510–515CrossRefPubMedGoogle Scholar
  36. Koehler K, Center A, Cavender-Bares J (2012) Evidence of a freezing tolerance-growth rate trade-off in the live oaks (Quercus series Virentes) across tropical-temperate divide. New Phytol 193:730–744CrossRefPubMedGoogle Scholar
  37. Liu H, Takeichi Y, Kamiya K, Harada K (2013) Phylogeography of Quercus phillyraeoides (Fagaceae) in Japan as revealed by chloroplast DNA variation. J Forest Res-JPN 18:361–370CrossRefGoogle Scholar
  38. López de Heredia U, Carrión JS, Jiménez P, Collada C, Gill L (2007) Molecular and palaeoecological evidence for multiple glacial refuia for evergreen oaks on the Iberian Peninsula. J Biogeogr 34:1505–1517CrossRefGoogle Scholar
  39. Lumaret R, Mir C, Michaud H, Raynal V (2002) Phylogeographic variation of chloroplast DNA in holm oak (Quercus ilex L.) Mol Ecol 11:2327–2336CrossRefPubMedGoogle Scholar
  40. Magri D, Fineschi S, Bellarosa R, Buonamici A, Sebastiani F, Schirone B, Simeone MC, Vendramin GG (2007) The distribution of Quercus suber chloroplast haplotypes matches the paleogeographical history of the western Mediterranean. Mol Ecol 16:5259–5266Google Scholar
  41. Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by “Monmonier’s algorithm”. Hum Biol 76:173–190CrossRefPubMedGoogle Scholar
  42. Marshall JS (2007) Geomorphology and physiographic provinces. In: Bundschuc J, Alvarado GE (eds) Central America: geology, resources, hazards, vol 1. Taylor & Francis, London, pp 75–122Google Scholar
  43. Marsico TD, Hellman JJ, Romero-Severson J (2009) Patterns of seed dispersal and pollen flow in Quercus garryana (Fagaceae) following post-glacial climatic changes. J Biogeogr 36:929–941CrossRefGoogle Scholar
  44. Montes-Hernández B, López-Herrera (2013) Seedling establishment of Quercus insignis: a critically endangered oak tree species in southern Mexico. Forest Ecol Manag 310:927–934CrossRefGoogle Scholar
  45. Morales JF (2010) Fagaceae. In: Hammel BE, Grayum MH, Herrera C, Zamora N (eds) Manual de plantas de Costa Rica, Dicotiledóneas (Clusiaceae-Gunneraceae), vol 5. Missouri Botanical Garden, St. Louis, pp 777–781Google Scholar
  46. Mulcahy DG, Morrill BH, Mendelson JR III (2006) Historical biogeography of low-land species of toads (Bufo) across the Trans-Mexican Neovolcanic Belt and the Isthmus of Tehuantepec. J Biogeogr 33:1889–1904CrossRefGoogle Scholar
  47. Navascués M, Hardy OJ, Burgarella C (2009) Characterization of demographic expansions from pairwise comparisons of linked microsatellite haplotypes. Genetics 181:1013–1019CrossRefPubMedPubMedCentralGoogle Scholar
  48. Nixon KC (1985) A biosystematics study of Quercus series Virentes (the live oaks) with phylogenetic analyses of Fagales, Fagaceae and Quercus. PhD Thesis, University of Texas, Austin, TxGoogle Scholar
  49. Novick RR, Dick CW, Lemes MR, Navarro C, Caccone S, Bermingham E (2003) Genetic structure of a Mesoamerican population of big-leaf mahogany (Swietenia macrophylla) inferred from microsatellite analysis. Mol Ecol 12:2885–2893CrossRefPubMedGoogle Scholar
  50. Olalde M, Herrán A, Espinel S, Goicochea PG (2002) White oaks phylogeography in the Iberian Penninsula. Forest Ecol Manag 156:89–102CrossRefGoogle Scholar
  51. Ordóñez-Garza N, Matson JO, Strauss RE, Bradley RD, Salazar-Bravo J (2010) Patterns of phenotypic and genetic variation in three species of endemic Mesoamerican Peromyscus (Rodentia: Cricetidae). J Mammal 91:848–859CrossRefGoogle Scholar
  52. Ornelas JF, Sosa V, Soltis DE, Daza JM, Gonzalez C, Soltis PS, Gutíerrez-rodríguez C, Espinosa de los Monteros A, Castoe TA, Bell C, Ruiz-Sáncez E (2013) Complex evolutionary history of threatened cloud forest of northern Mesoamerica. PLoS One 8:e56283CrossRefPubMedPubMedCentralGoogle Scholar
  53. Otto-Bliesner BL, Marshall SJ, Overpeck JT, Miller GH, Hu A (2006) Simulating Arctic climate warmth and icefield retreat in the Last Interglaciation. Science 311:1751–1753CrossRefPubMedGoogle Scholar
  54. Peñaloza-Ramírez JM (2011) Filogeografía e hibridación en cuatro especies del género Quercus (Fagaceae) en México. PhD Thesis, Universidad Nacional Autónoma de México, MexicoGoogle Scholar
  55. Petit RJ, Brewer S, Bordács S, Burg K, Cheddadi R, Coart E, Cottrel J, Csaikl M, van Dam B, Deans JD, Espinel S, Fineschi S, Finkeldey R, Glaz I, Goicochea PG, Jensen JS, Konig AO, Lowe AJ, Madsen SF, Mátyás G, Munro RC, Popescu F, Slade D, Tabbener H, de Vries SGM, Ziegenhagen B, de Beaulieu J, Kremer A (2002a) Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. Forest Ecol Manag 156:49–74CrossRefGoogle Scholar
  56. Petit RJ, Csaikl UM, Bordács S, Burg K, Coart E, Cottrel J, van Dam B, Deans JD, Dumolin-Lapègue S, Fineschi S, Finkeldey R, Gillies A, Glaz I, Goicochea PG, Jensen JS, Konig AO, Lowe AJ, Madsen SF, Mátyás G, Munro RC, Olalde M, Pemonge M, Popescu F, Slade D, Tabbener H, Taurchini D, de Vries SGM, Ziegenhagen B, Kremer A (2002b) Chloroplast DNA variation in European oaks phylogeography and patterns of diversity based on data from over 2600 populations. Forest Ecol and Manag 156:5–26CrossRefGoogle Scholar
  57. Phillips SJ, Anderson RP, Schapire PE (2006) Maximum entropy modelling of species geographic distributions. Ecol Model 190:231–259CrossRefGoogle Scholar
  58. Polzin T, Daneschmand SV (2003) On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 31:12–20CrossRefGoogle Scholar
  59. Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered allels. Genetics 144:1237–1245PubMedPubMedCentralGoogle Scholar
  60. Ramírez-Barahona S, Eguiarte L (2013) The role of glacial cycles in promoting genetic diversity in the Neotropics: the case of cloud forests during the Last Glacial Maximun. Ecol Evol 3:725–738CrossRefPubMedPubMedCentralGoogle Scholar
  61. Ramírez-Barahona S, Eguiarte L (2014) Changes in the distribution of cloud forest during the last glacial predict patterns of genetic diversity and demographic history of the tree fern alsophilla firma (Cyatheaceae). J Biogeogr 41:2396–2407CrossRefGoogle Scholar
  62. Ramírez-Barahona S, Luna-Vega I (2015) Geographic differentiation of tree ferns (Cyatheales) in tropical America. Am Fern J 105:73–85CrossRefGoogle Scholar
  63. Ramos-Ortiz S, Oyama K, Rodríguez-Correa H, González-Rodríguez A (2016) Geographic structure of genetic and phenotypic variation in the hybrid zone between Quercus affinis and Q. laurina in Mexico. Plant Spec Biol 31:219–232Google Scholar
  64. Rodríguez-Correa H (2015) Patrones de distribución y filogeografía de los encinos (quercus: fagaceae) en Mesoamérica y Los Andes. PhD Thesis. Universidad Nacional Autónoma de México, MexicoGoogle Scholar
  65. Rodríguez-Correa H, Oyama K, Mac Gregor-Fors I, González-Rodríguez A (2015) How are oaks distributed in the Neotropics? A perspective from species turnover, areas of endemism, and climatic niches. Int J Plant Sci 176:222–231CrossRefGoogle Scholar
  66. Rousset F (1996) Equilibrium values of measures of population subdivision for stepwise mutation processes. Genetics 142:1357–1362PubMedPubMedCentralGoogle Scholar
  67. Sebastiani F, Carnevale S, Vendramin GG (2004) A new set of mono- and dinucleotide chloroplast microsatellites in Fagaceae. Mol Ecol Notes 4:259–261CrossRefGoogle Scholar
  68. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedPubMedCentralGoogle Scholar
  69. Torres-Miranda A, Luna-Vega I, Oyama K (2013) New approaches to the biogeography and areas of endemism of red oaks (Quercus L., Section Lobatae). Syst Biol 62:555–573CrossRefPubMedGoogle Scholar
  70. Tovar-Sánchez E, Mussali-Galante P, Esteban-Jiménez R, Piñero D, Arias DM, Dorado O, Oyama K (2008) Chloroplast DNA polymorphism reveals geographic structure and introgression in the Quercus crassifolia x Quercus crassipes hybrid complex in Mexico. Botany 86:228–239CrossRefGoogle Scholar
  71. Valencia-A S (2004) Diversidad del género Quercus (Fagaceae) en México. B Soc Bot Mex 75:33–53Google Scholar
  72. Vázquez-Miranda H, Navarro-Sigüenza AG, Omland KE (2009) Phylogeography of the rufous-naped red (Camphylorhynchus rufinucha): speciation and hybridization in Mesoamerica. Auk 126:765–778CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Hernando Rodríguez-Correa
    • 1
  • Ken Oyama
    • 1
  • Mauricio Quesada
    • 1
  • Eric J. Fuchs
    • 2
  • Maura Quezada
    • 3
  • Lilian Ferrufino
    • 4
  • Susana Valencia-Ávalos
    • 5
  • Alfredo Cascante-Marín
    • 2
  • Antonio González-Rodríguez
    • 6
  1. 1.Escuela Nacional de Estudios Superiores Unidad MoreliaUniversidad Nacional Autónoma de MéxicoMoreliaMexico
  2. 2.Escuela de BiologíaUniversidad de Costa RicaSan JoséCosta Rica
  3. 3.Herbario de San Carlos de GuatemalaUniversidad San Carlos de GuatemalaGuatemalaGuatemala
  4. 4.Laboratorio de Histología Vegetal y EtnobotánicaUniversidad Nacional Autónoma de HondurasTegucigalpaHonduras
  5. 5.Herbario de la Facultad de Ciencias (FCME), Departamento de Biología ComparadaUniversidad Nacional Autónoma de MéxicoCoyoacánMexico
  6. 6.Laboratorio de Genética de la Conservación, Instituto de Investigaciones en Ecosistemas y SustentabilidadUniversidad Nacional Autónoma de MéxicoMoreliaMexico

Personalised recommendations