Plant Systematics and Evolution

, Volume 304, Issue 5, pp 607–617 | Cite as

Past climatic fluctuations are associated with morphological differentiation in the cloud forest endemic tree Ocotea psychotrioides (Lauraceae)

  • Andrés Ernesto Ortiz-Rodríguez
  • Santiago Ramírez-Barahona
  • Dolores González Hernández
  • Francisco Lorea-Hernández
Original Article


Pleistocene glacial periods have had a major influence on the geographical patterns of genetic structure of species in tropical montane regions. However, their effect on morphological differentiation among populations of cloud forest plants remains virtually unexplored. Here, we address this question by testing whether geographical patterns of morphological variation in Ocotea psychotrioides can be explained by the intensity of climate change occurring during 130,000 years. For this, we measured vegetative and reproductive traits for 96 individuals from 36 localities registered across the species’ distribution range. Species distribution models and multivariate statistics were used to investigate geographical patterns of morphological variation and test their association with current and past climatic conditions. Leaf size and pubescence in O. psychotrioides showed a latitudinal pattern of clinal variation that does not fit the geographical gradient of increasing leaf size towards lower latitudes observed globally among plants. Instead, the observed clinal variation conforms to a pattern of increasing leaf size towards higher latitudes. However, our analyses showed weak to non-significant association between morphology and current climate. Interestingly, our analyses showed that predicted shifts in the distribution range of O. psychotrioides during the last 130,000 years were accompanied by significant changes in climatic conditions, particularly temperature seasonality and precipitation. Accordingly, climatic instability showed a better fit to the observed patterns of leaf size and pubescence variation than current climate conditions. These results suggest that climatic instability during the Pleistocene glacial periods might play a key role in promoting morphological differentiation among populations of cloud forest plants.


Climatic stability Clinal variation Ecological niche models Leaf size Pleistocene glacial cycles 



We thank Carlos Durán, Sergio Avendaño and Manuel Escamilla for field and laboratory support. During the development of this work Eduardo Ruiz Sánchez, Teresa Terrazas and Yuyini Licona Vera made valuable criticisms and suggestions. We also thank the directors and curators of the following herbaria for making specimens of O. psychotrioides available for this study: ENCB, F, IEB, INB, K, MEXU, MICH, MO, NY, HUAP and XAL. This study was supported by the master scholarship CONACyT-294119 of the first author.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Supplementary material 1 (PDF 86 kb)
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Supplementary material 6 (PDF 194 kb)


  1. Allouche O, Tsoar A, Kadmon R (2006) Assessing the accuracy of species distribution models: prevalence, kappa, and the true skill statistic (TSS). J Appl Ecol 43:1223–1232. CrossRefGoogle Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. Google Scholar
  3. Ávila-Valle ZA, Castro-Campillo A, León-Paniagua L, Salgado-Ugalde IH, Navarro-Sigüenza AG, Hernández-Baños BE, Ramírez-Pulido J (2012) Geographic variation and molecular evidence of the Blackish Deer Mouse complex (Peromyscus furvus, Rodentia: Muridae). Mamm Biol 77:166–177. CrossRefGoogle Scholar
  4. Cabanne GS, Trujillo-Arias N, Calderón L, D’Horta FM, Miyak CY (2014) Phenotypic evolution of an Atlantic Forest passerine (Xiphorhynchus fuscus): biogeographic and systematic implications. Biol J Linn Soc 113:1047–1066. CrossRefGoogle Scholar
  5. Carnaval AC, Hickerson MJ, Haddad CFB, Rodrigues MT, Moritz C (2009) Stability predicts genetic diversity in the Brazilian Atlantic Forest hotspot. Science 323:785–789. CrossRefPubMedGoogle Scholar
  6. Cavender-Bares J, González-Rodríguez A, Eaton DA, Hipp AA, Beulke A, Manos PS (2015) Phylogeny and biogeography of the American live oaks (Quercus subsection Virentes): a genomic and population genetics approach. Molec Ecol 24:3668–3687. CrossRefGoogle Scholar
  7. Chanderbali AS, van der Werff H, Renner SS (2001) Phylogeny and historical biogeography of Lauraceae: evidence from the chloroplast and nuclear genomes. Ann Missouri Bot Gard 88:104–134. CrossRefGoogle Scholar
  8. Colautti RI, Barrett SCH (2013) Rapid adaptation to climate facilitates range expansion of an invasive plant. Science 342:364–366. CrossRefPubMedGoogle Scholar
  9. Collins WD, Bitz CM, Blackmon ML, Bonan GB, Bretherton CS, Carton JA, Chang P, Doney SC, Hack JJ, Henderson TB, Kiehl JT, Large WG, McKenna DS, Santer BD, Smith RD (2006) The Community Climate System Model version 3 (CCSM3). J Climate 19:2122–2143. CrossRefGoogle Scholar
  10. Comes HP, Kadereit JW (1998) The effect of Quaternary climatic changes on plant distribution and evolution. Trends Pl Sci 3:432–438. CrossRefGoogle Scholar
  11. Davis MB, Shaw RG (2001) Range shifts and adaptive responses to Quaternary climate change. Science 292:673–679. CrossRefPubMedGoogle Scholar
  12. de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886. CrossRefPubMedGoogle Scholar
  13. Donati D, Bianchi C, Pezzi G, Conte L, Hofer A, Chiarucci A (2017) Biogeography and ecology of the genus Turbinicarpus (Cactaceae): environmental controls of taxa richness and morphology. Syst Biodivers 15:361–371. CrossRefGoogle Scholar
  14. Drezner TD (2003) Revisiting Bergmann’s rule for saguaros (Carnegiea gigantea (Engelm.) Britt. and Rose): stem diameter patterns over space. J Biogeogr 30:353–359. CrossRefGoogle Scholar
  15. Fielding AH, Bell JF (1997) Review of methods for the assessment of prediction errors in conservation presence/absence models. Environm Conservation 24:38–49. CrossRefGoogle Scholar
  16. Givnish TJ (1987) Comparative studies of leaf form: assessing the relative roles of selective pressures and phylogenetic constraints. New Phytol 106(Supplement s1):131–160Google Scholar
  17. González C, Ornelas JF, Gutiérrez-Rodríguez C (2011) Selection and geographic isolation influence hummingbird speciation: genetic, acoustic and morphological divergence in the wedge-tailed sabrewing (Campylopterus curvipennis). BMC Evol Biol 11:38. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Grant V (1989) Especiación Vegetal. Limusa, MexicoGoogle Scholar
  19. Gutiérrez-Rodríguez C, Ornelas JF, Rodríguez-Gómez F (2011) Chloroplast DNA phylogeography of a distylous shrub (Palicourea padifolia, Rubiaceae) reveals past fragmentation and demographic expansion in Mexican cloud forests. Molec Phylogen Evol 61:603–615. CrossRefGoogle Scholar
  20. Haffer J, Prance G (2001) Climatic forcing of evolution in Amazonia during the Cenozoic: on the refuge theory of biotic differentiation. Amazoniana 16:579–607Google Scholar
  21. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software package for education and data analysis. Paleontol Electronica 4:4.
  22. Hernández-Verdugo S, Porras F, Pacheco-Olvera A, López-España RG, Villarreal-Romero M, Parra-Terraza S, Osuna T (2012) Caracterización y variación ecogeográfica de poblaciones de chile (Capsicum annuum var. glabriusculum) silvestre del noroeste de México. Polibotánica 33:175–191Google Scholar
  23. Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans Ser B 359:183–195. CrossRefGoogle Scholar
  24. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. CrossRefGoogle Scholar
  25. Holman JE, Hughes JM, Fensham RJ (2003) A morphological cline in Eucalyptus: a genetic perspective. Molec Ecol 12:3013–3025. CrossRefGoogle Scholar
  26. Johnson HB (1975) Plant pubescence: an ecological perspective. Bot Rev (Lancaster) 41:233–258CrossRefGoogle Scholar
  27. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174. CrossRefPubMedGoogle Scholar
  28. Leaché AD, Koo MS, Spencer CL, Papenfuss TJ, Fisher RN, McGuire JA (2009) Quantifying ecological, morphological, and genetic variation to delimit species in the coast horned lizard species complex (Phrynosoma). Proc Natl Acad Sci USA 106:12418–12423. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Liu C, White M, Newell G (2013) Selecting thresholds for the prediction of species occurrence with presence-only data. J Biogeogr 40:778–789. CrossRefGoogle Scholar
  30. Lopez Laphitz RM, Ezcurra C, Vidal-Russell R (2015) Morphological variation in Quinchamalium (Schoepfiaceae) is associated with climatic patterns along its Andean distribution. Syst Bot 40:1045–1052. CrossRefGoogle Scholar
  31. Lorea-Hernández FG (2002) La familia Lauraceae en el sur de México: diversidad, distribución y estado de conservación. Bol Soc Bot México 71:59–70Google Scholar
  32. Lowry DB (2012) Ecotypes and the controversy over stages in the formation of new species. Biol J Linn Soc 106:241–257. CrossRefGoogle Scholar
  33. Luna-Vega I, Alcántara O, Espinosa D, Morrone JJ (1999) Historical relationships of the Mexican cloud forest: a preliminary vicariance model applying parsimony analysis of endemicity to vascular plant taxa. J Biogeogr 26:1299–1305. CrossRefGoogle Scholar
  34. Moritz C, Patton JL, Schneider CJ, Smith TB (2000) Diversification of rainforest faunas: an integrated molecular approach. Annual Rev Ecol Syst 31:533–563. CrossRefGoogle Scholar
  35. Nattero J, Sérsic AN, Cocucci AA (2011) Geographic variation of floral traits in Nicotiana glauca: relationships with biotic and abiotic factors. Acta Oecol 37:503–511. CrossRefGoogle Scholar
  36. Niering WA, Whittaker RH, Lowe CH (1963) The saguaro: a population in relation to environment. Science 142:15–23. CrossRefPubMedGoogle Scholar
  37. Odendaal LJ, Jacobs DS, Bishop JM (2014) Sensory trait variation in an echolocating bat suggests roles for both selection and plasticity. BMC Evol Biol 14:60. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Ornelas JF, González C (2014) Interglacial genetic diversification of Moussonia deppeana (Gesneriaceae), a hummingbird-pollinated, cloud forest shrub in northern Mesoamerica. Molec Ecol 23:4119–4136. CrossRefGoogle Scholar
  39. Ornelas JF, Rodríguez-Gómez F (2015) Influence of Pleistocene glacial/interglacial cycles on the genetic structure of the mistletoe cactus Rhipsalis baccifera (Cactaceae) in Mesoamerica. J Heredity 106:196–210. CrossRefGoogle Scholar
  40. Ornelas JF, Ruíz-Sánchez E, Sosa V (2010) Phylogeography of Podocarpus matudae (Podocarpaceae): pre-Quaternary relicts in northern Mesoamerican cloud forests. J Biogeogr 37:2384–2396. CrossRefGoogle Scholar
  41. Ornelas JF, Sosa V, Soltis DE, Daza JM, González C, Soltis PS, Gutiérrez-Rodríguez C, Espinosa de los Monteros A, Castoe TA, Bell C, Ruiz-Sánchez E (2013) Comparative phylogeographic analyses illustrate the complex evolutionary history of threatened cloud forests of northern Mesoamerica. PLoS ONE 8:e56283. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Ornelas JF, Gándara E, Vásquez-Aguilar AA, Ramírez-Barahona S, Ortiz-Rodriguez AE, González C, Mejía SMT, Ruiz-Sanchez E (2016) A mistletoe tale: postglacial invasion of Psittacanthus schiedeanus (Loranthaceae) to Mesoamerican cloud forests revealed by molecular data and species distribution modeling. BMC Evol Biol 16:78. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Otto-Bliesner BL, Marshall SJ, Overpeck JT, Miller GH, Hu A (2006) Simulating arctic climate warmth and icefield retreat in the last interglaciation. Science 311:1751–1753. CrossRefPubMedGoogle Scholar
  44. Paiaro V, Oliva G, Cocucci AA, Sérsic AN (2012) Geographic patterns and environmental drivers of flowers and leaf variation in an endemic legume of Southern Patagonia. Pl Ecol Divers 5:13–25. CrossRefGoogle Scholar
  45. Parkhurst DF (1976) Effects of Verbascum thapsus leaf hairs on heat and mass transfer: a reassessment. New Phytol 76:453–457CrossRefGoogle Scholar
  46. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Modelling 190:231–259. CrossRefGoogle Scholar
  47. Piedra-Malagón EM, Sosa V, Ibarra-Manríquez G (2011) Clinal variation and species boundaries in the Ficus petiolaris complex (Moraceae). Syst Bot 36:80–87. CrossRefGoogle Scholar
  48. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for statistical computing. Vienna, Austria. Available at
  49. Ramírez-Barahona S, Eguiarte LE (2013) The role of glacial cycles in promoting genetic diversity in the Neotropics: the case of cloud forests during the Last Glacial Maximum. Ecol Evol 3:725–738. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Ramírez-Barahona S, Eguiarte LE (2014) Changes in the distribution of cloud forests during the last glacial predict the patterns of genetic diversity and demographic history of the tree fern Alsophila firma (Cyatheaceae). J Biogeogr 41:2396–2407. CrossRefGoogle Scholar
  51. Rico-Gray V, Palacios-Rios M (1996) Leaf area variation in Rhizophora mangle L. (Rhizophoraceae) along a latitudinal gradient in Mexico. Global Ecol Biogeogr Lett 5:30–35. CrossRefGoogle Scholar
  52. Ruiz-Sánchez E, Ornelas JF (2014) Phylogeography of Liquidambar styraciflua (Altingiaceae) in Mesoamerica: survivors of a Neogene widespread temperate forest (or cloud forest) in North America? Ecol Evol 4:311–328. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Rzedowski J (1996) Análisis preliminar de la flora vascular de los bosques mesófilos de montaña de México. Acta Bot Mex 35:25–44CrossRefGoogle Scholar
  54. Solís Neffa VG (2010) Geographic patterns of morphological variation in Turnera sidoides subsp. pinnatifida (Turneraceae). Pl Syst Evol 284:231–253. CrossRefGoogle Scholar
  55. Stewart JR, Lister AM, Barnes I, Dalén L (2010) Refugia revisited: individualistic responses of species in space and time. Proc Roy Soc Biol Sci Ser B 277:661–671. CrossRefGoogle Scholar
  56. Twyford AD, Kidner CA, Ennos RA (2014) Genetic differentiation and species cohesion in two widespread Central American Begonia species. Heredity 112:382–390. CrossRefPubMedGoogle Scholar
  57. Uribe-Salas D, Sáenz-Romero C, González-Rodríguez A, Téllez-Valdéz O, Oyama K (2008) Foliar morphological variation in the white oak Quercus rugosa Née (Fagaceae) along a latitudinal gradient in Mexico: potential implications for management and conservation. Forest Ecol Managem 256:2121–2126. CrossRefGoogle Scholar
  58. van der Werff H (2002) A synopsis of Ocotea (Lauraceae) in Central America and southern Mexico. Ann Missouri Bot Gard 89:429–451. CrossRefGoogle Scholar
  59. van der Werff H, Lorea-Hernández FG (1997) Familia Lauraceae. In: Rzedowski J, Calderón G (eds) Flora del Bajío y de regiones adyacentes. Instituto de Ecología, A.C., Centro Regional del Bajío, Pátzcuano, pp 1–58Google Scholar
  60. Villaseñor JL (2010) El Bosque húmedo de montaña en México y sus plantas vasculares: Catálogo florístico-taxonómico. Comisión Nacional para el Conocimiento y uso de la Biodiversidad-Universidad Nacional Autónoma de México, Ciudad de MéxicoGoogle Scholar
  61. Wendt T (1993) Composition, floristic affinities, and origins of the canopy tree flora of the Mexican Atlantic slope rain forests. In: Ramamoorthy TP, Bye R, Lot A, Fa J (eds) Biological diversity of Mexico, origins and distribution. Oxford University Press, New York, pp 595–680Google Scholar
  62. Werger MJA, Ellenbroek GA (1978) Leaf size and leaf consistence of a riverine forest formation along a climatic gradient. Oecologia 34:297–308. CrossRefPubMedGoogle Scholar
  63. Wright IJ, Dong N, Maire V, Prentice IC, Westoby M, Díaz S, Gallagher RV, Jacobs BF, Kooyman R, Law EA, Leishman MR, Niinemets Ü, Reich PB, Sack L, Villar R, Wang H, Wilf P (2017) Global climatic drivers of leaf size. Science 357:917–921. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Andrés Ernesto Ortiz-Rodríguez
    • 1
  • Santiago Ramírez-Barahona
    • 2
  • Dolores González Hernández
    • 3
  • Francisco Lorea-Hernández
    • 3
  1. 1.Departamento de Biología EvolutivaInstituto de Ecología, A.C.XalapaMexico
  2. 2.Departamento BotánicaInstituto de BiologíaCiudad de MéxicoMexico
  3. 3.Departamento de Biodiversidad y SistemáticaInstituto de Ecología, A.C.XalapaMexico

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