Past climatic fluctuations are associated with morphological differentiation in the cloud forest endemic tree Ocotea psychotrioides (Lauraceae)
Abstract
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.
Keywords
Climatic stability Clinal variation Ecological niche models Leaf size Pleistocene glacial cyclesNotes
Acknowledgements
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
References
- 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. https://doi.org/10.1111/j.1365-2664.2006.01214.x CrossRefGoogle Scholar
- Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070 Google Scholar
- 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. https://doi.org/10.1016/j.mambio.2011.09.008 CrossRefGoogle Scholar
- 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. https://doi.org/10.1111/bij.12362 CrossRefGoogle Scholar
- 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. https://doi.org/10.1126/science.1166955 CrossRefPubMedGoogle Scholar
- 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. https://doi.org/10.1111/mec.13269 CrossRefGoogle Scholar
- 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. https://doi.org/10.2307/2666133 CrossRefGoogle Scholar
- Colautti RI, Barrett SCH (2013) Rapid adaptation to climate facilitates range expansion of an invasive plant. Science 342:364–366. https://doi.org/10.1126/science.1242121 CrossRefPubMedGoogle Scholar
- 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. https://doi.org/10.1175/JCLI3761.1 CrossRefGoogle Scholar
- Comes HP, Kadereit JW (1998) The effect of Quaternary climatic changes on plant distribution and evolution. Trends Pl Sci 3:432–438. https://doi.org/10.1016/S1360-1385(98)01327-2 CrossRefGoogle Scholar
- Davis MB, Shaw RG (2001) Range shifts and adaptive responses to Quaternary climate change. Science 292:673–679. https://doi.org/10.1126/science.292.5517.673 CrossRefPubMedGoogle Scholar
- de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886. https://doi.org/10.1080/10635150701701083 CrossRefPubMedGoogle Scholar
- 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. https://doi.org/10.1080/14772000.2016.1251504 CrossRefGoogle Scholar
- 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. https://doi.org/10.1046/j.1365-2699.2003.00834.x CrossRefGoogle Scholar
- Fielding AH, Bell JF (1997) Review of methods for the assessment of prediction errors in conservation presence/absence models. Environm Conservation 24:38–49. https://doi.org/10.1017/S0376892997000088 CrossRefGoogle Scholar
- 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
- 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. https://doi.org/10.1186/1471-2148-11-38 CrossRefPubMedPubMedCentralGoogle Scholar
- Grant V (1989) Especiación Vegetal. Limusa, MexicoGoogle Scholar
- 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. https://doi.org/10.1016/j.ympev.2011.08.023 CrossRefGoogle Scholar
- 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
- Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software package for education and data analysis. Paleontol Electronica 4:4. http://palaeo-electronica.org/2001_1/past/issue1_01.htm
- 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
- Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans Ser B 359:183–195. https://doi.org/10.1098/rstb.2003.1388 CrossRefGoogle Scholar
- 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. https://doi.org/10.1002/joc.1276 CrossRefGoogle Scholar
- Holman JE, Hughes JM, Fensham RJ (2003) A morphological cline in Eucalyptus: a genetic perspective. Molec Ecol 12:3013–3025. https://doi.org/10.1046/j.1365-294X.2003.01970.x CrossRefGoogle Scholar
- Johnson HB (1975) Plant pubescence: an ecological perspective. Bot Rev (Lancaster) 41:233–258CrossRefGoogle Scholar
- Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174. https://doi.org/10.2307/2529310 CrossRefPubMedGoogle Scholar
- 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. https://doi.org/10.1073/pnas.0906380106 CrossRefPubMedPubMedCentralGoogle Scholar
- Liu C, White M, Newell G (2013) Selecting thresholds for the prediction of species occurrence with presence-only data. J Biogeogr 40:778–789. https://doi.org/10.1111/jbi.12058 CrossRefGoogle Scholar
- 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. https://doi.org/10.1600/036364415X690085 CrossRefGoogle Scholar
- 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
- Lowry DB (2012) Ecotypes and the controversy over stages in the formation of new species. Biol J Linn Soc 106:241–257. https://doi.org/10.1111/j.1095-8312.2012.01867.x CrossRefGoogle Scholar
- 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. https://doi.org/10.1046/j.1365-2699.1999.00361.x CrossRefGoogle Scholar
- Moritz C, Patton JL, Schneider CJ, Smith TB (2000) Diversification of rainforest faunas: an integrated molecular approach. Annual Rev Ecol Syst 31:533–563. https://doi.org/10.1146/annurev.ecolsys.31.1.533 CrossRefGoogle Scholar
- 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. https://doi.org/10.1016/j.actao.2011.07.001 CrossRefGoogle Scholar
- Niering WA, Whittaker RH, Lowe CH (1963) The saguaro: a population in relation to environment. Science 142:15–23. https://doi.org/10.1126/science.142.3588.15 CrossRefPubMedGoogle Scholar
- 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. https://doi.org/10.1186/1471-2148-14-60 CrossRefPubMedPubMedCentralGoogle Scholar
- 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. https://doi.org/10.1111/mec.12841 CrossRefGoogle Scholar
- 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. https://doi.org/10.1093/jhered/esu113 CrossRefGoogle Scholar
- 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. https://doi.org/10.1111/j.1365-2699.2010.02372.x CrossRefGoogle Scholar
- 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. https://doi.org/10.1371/journal.pone.0056283 CrossRefPubMedPubMedCentralGoogle Scholar
- 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. https://doi.org/10.1186/s12862-016-0648-6 CrossRefPubMedPubMedCentralGoogle Scholar
- 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. https://doi.org/10.1126/science.1120808 CrossRefPubMedGoogle Scholar
- 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. https://doi.org/10.1080/17550874.2012.713403 CrossRefGoogle Scholar
- Parkhurst DF (1976) Effects of Verbascum thapsus leaf hairs on heat and mass transfer: a reassessment. New Phytol 76:453–457CrossRefGoogle Scholar
- Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Modelling 190:231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026 CrossRefGoogle Scholar
- 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. https://doi.org/10.1600/036364411X553153 CrossRefGoogle Scholar
- R Core Team (2016) R: a language and environment for statistical computing. R Foundation for statistical computing. Vienna, Austria. Available at http://www.R-project.org
- 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. https://doi.org/10.1002/ece3.483 CrossRefPubMedPubMedCentralGoogle Scholar
- 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. https://doi.org/10.1111/jbi.12396 CrossRefGoogle Scholar
- 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. https://doi.org/10.2307/2997468 CrossRefGoogle Scholar
- 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. https://doi.org/10.1002/ece3.938 CrossRefPubMedPubMedCentralGoogle Scholar
- Rzedowski J (1996) Análisis preliminar de la flora vascular de los bosques mesófilos de montaña de México. Acta Bot Mex 35:25–44CrossRefGoogle Scholar
- Solís Neffa VG (2010) Geographic patterns of morphological variation in Turnera sidoides subsp. pinnatifida (Turneraceae). Pl Syst Evol 284:231–253. https://doi.org/10.1007/s00606-009-0249-6 CrossRefGoogle Scholar
- 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. https://doi.org/10.1098/rspb.2009.1272 CrossRefGoogle Scholar
- Twyford AD, Kidner CA, Ennos RA (2014) Genetic differentiation and species cohesion in two widespread Central American Begonia species. Heredity 112:382–390. https://doi.org/10.1038/hdy.2013.116 CrossRefPubMedGoogle Scholar
- 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. https://doi.org/10.1016/j.foreco.2008.08.002 CrossRefGoogle Scholar
- van der Werff H (2002) A synopsis of Ocotea (Lauraceae) in Central America and southern Mexico. Ann Missouri Bot Gard 89:429–451. https://doi.org/10.2307/3298602 CrossRefGoogle Scholar
- 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
- 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
- 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
- Werger MJA, Ellenbroek GA (1978) Leaf size and leaf consistence of a riverine forest formation along a climatic gradient. Oecologia 34:297–308. https://doi.org/10.1007/BF00344908 CrossRefPubMedGoogle Scholar
- 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. https://doi.org/10.1126/science.aal4760 CrossRefPubMedGoogle Scholar