Skip to main content

Advertisement

SpringerLink
Log in

Diversification of Caiophora (Loasaceae subfam. Loasoideae) during the uplift of the Central Andes

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

An Erratum to this article was published on 17 January 2017

Abstract

Andean orogeny and the ecological changes that followed promoted diversification in plant and animal lineages since the Early Miocene. The angiosperm genus Caiophora (Loasaceae, subfam. Loasoideae) comprises around 50 species that are endemic to South America. These are distributed from southern Ecuador to Central Chile and Argentina. Bee pollination and distribution at low-intermediate elevations probably represent the ancestral condition in the lineage that includes Caiophora and its allied genera. The majority of Caiophora species grow at high elevations in the Andes, where some depend on vertebrate pollination. Previous studies did not resolve phylogenetic relationships within Caiophora, which precluded the dating of the origin and divergence of this group. We used markers of one nuclear (ITS) and one plastid region (trnSGCU-trnGUUC) to solve phylogenetic relationships among 19 Caiophora species (including different accessions). We also included 10 species of the allied genera Blumenbachia and Loasa. Aosa rostrata and Xylopodia klaprothioides were used as outgroups. Phylogenetic reconstruction strongly supports the monophyly of Caiophora, and although several clades within this genus are poorly supported, our study yielded a better infra-generic resolution than previous studies. The origin of Caiophora is dated to the Early-Middle Miocene and can be related to the uplift of the Cordilleras Frontal and Principal and to Pacific marine transgressions. According to our estimations, Caiophora began to diversify during the Middle-Late Miocene and this unfolding proceeded eastwards during the Pliocene and the Pleistocene, in parallel to the uplift of different Andean mountain ranges.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ackermann, M. (2012). Studies on systematics, morphology and taxonomy of Caiophora and reproductive biology of Loasaceae and Mimulus (Phrymaceae). PhD Thesis. Free University of Berlin, Germany.

  • Ackermann, M., & Weigend, M. (2006). Nectar, floral morphology and pollination syndrome in Loasaceae subfam. Loasoideae (Cornales). Annals of Botany, 98, 503–514.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ackermann, M., Achatz, M., & Weigend, M. (2008). Hybridization and crossability in Caiophora (Loasaceae, subfam. Loasoideae): are interfertile species and inbred populations results of a recent radiation? American Journal of Botany, 95, 1109–1121.

    Article  PubMed  Google Scholar 

  • Altshuler, D. L., Dudley, R., & McGuire, J. A. (2004). Resolution of a paradox: hummingbird flight at high elevation does not come without a cost. Proceedings of the National Academy of Sciences of the United States of America, 101, 17731–17736.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Antonelli, A., & Sanmartín, I. (2011). Why are there so many plant species in the Neotropics? Taxon, 60, 403–414.

    Google Scholar 

  • Antonelli, A., Nylander, J. A., Persson, C., & Sanmartín, I. (2009). Tracing the impact of the Andean uplift on Neotropical plant evolution. Proceedings of the National Academy of Sciences, 106, 9749–9754.

    Article  CAS  Google Scholar 

  • Armijo, R., Lacassin, R., Coudurier-Curveur, A., & Carrizo, D. (2015). Coupled tectonic evolution of Andean orogeny and global climate. Earth-Science Reviews, 143, 1–35.

    Article  Google Scholar 

  • Arroyo, M. T. K., Primack, R., & Armesto, J. J. (1985). Community studies in pollination ecology in the high temperate Andes of Central Chile. I. Pollination mechanism and altitudinal variation. American Journal of Botany, 69, 82–97.

  • Baranzelli, M. C., Johnson, L. J., Cosacov, A., & Sérsic, A. N. (2014). Historical and ecological divergence among populations of Monttea chilensis (Plantaginaceae), an endemic endangered shrub bordering the Atacama Desert, Chile. Evolutionary Ecology, 28, 751–774.

    Article  Google Scholar 

  • Barnes, J. B., & Ehlers, T. A. (2009). End member models for Andean Plateau uplift. Earth-Science Reviews, 97, 105–132.

    Article  Google Scholar 

  • Bechis, F., Encinas, A., Concheyro, A., Litvak, V. D., Aguirre-Urreta, B., & Ramos, V. A. (2014). New age constraints for the Cenozoic marine transgressions of northwestern Patagonia, Argentina (41°-43° S): paleogeographic and tectonic implications. Journal of South American Earth Sciences, 52, 72–93.

    Article  CAS  Google Scholar 

  • Bryson Jr., R. W., García-Vázquez, U. O., & Riddle, B. R. (2012). Relative roles of Neogene vicariance and Quaternary climate change on the historical diversification of bunchgrass lizards (Sceloporus scalaris group) in Mexico. Molecular Phylogenetics and Evolution, 62, 447–457.

    Article  PubMed  Google Scholar 

  • Cavides-Vidal, E., Bozinovic, F., & Rosenmann, M. (1987). Thermal freedom of Graomys griseoflavus in a seasonal environment. Comparative Biochemistry and Physiology Part A: Physiology, 87, 257–259.

    Article  Google Scholar 

  • Chaves, J. A., Weir, J. T., & Smith, T. B. (2011). Diversification in Adelomyia hummingbirds follows Andean uplift. Molecular Ecology, 20, 4564–4576.

    Article  PubMed  Google Scholar 

  • Clapperton, C. H. (1983). The glaciation of the Andes. Quaternary Science Reviews, 2, 83–155.

    Article  Google Scholar 

  • Cocucci, A. A., & Sérsic, A. N. (1998). Evidence of rodent pollination in Cajophora coronata (Loasaceae). Plant Systematics and Evolution, 211, 113–128.

    Article  Google Scholar 

  • Cosacov, A., Sérsic, A. N., & Sosa, V. (2010). Multiple periglacial refugia in the Patagonian steppe and post-glacial colonization of the Andes: the phylogeography of Calceolaria polyrhiza. Journal of Biogeography, 37, 1463–1477.

    Google Scholar 

  • Cruden, R. W. (1972). Pollinators in high-elevation ecosystems: relative effectiveness of birds and bees. Science, 176, 1439–1440.

    Article  CAS  PubMed  Google Scholar 

  • Donato, M., Posadas, P., Miranda-Esquivel, D. R., Jaureguizar, E. O., & Cladera, G. (2003). Historical biogeography of the Andean region: evidence from Listroderina (Coleoptera: Curculionidae: Rhytirrhinini) in the context of the South American geobiotic scenario. Biological Journal of the Linnean Society, 80, 339–352.

    Article  Google Scholar 

  • Drummond, C. S., Eastwood, R. J., Miotto, S. T. S., & Hughes, C. E. (2012a). Multiple continental radiations and correlates of diversification in Lupinus (Leguminosae): testing for key innovations with incomplete taxon sampling. Systematic Biology, 61, 443–460.

    Article  PubMed  PubMed Central  Google Scholar 

  • Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012b). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Echavarria, L., Hernndez, R., Allmendinger, R., & Reynolds, J. (2003). Subandean thrust and fold belt of northwestern Argentina: geometry and timing of the Andean evolution. AAPG Bulletin, 87, 965–985.

    Article  Google Scholar 

  • Felsenstein, J. (1984). Distance methods for inferring phylogenies: a justification. Evolution, 38, 16–24.

    Article  Google Scholar 

  • Fenster, C. B., Armbruster, W. S., Wilson, P., Dudash, M. R., & Thomson, J. D. (2004). Pollination syndrome and floral specialization. Annual Review of Ecology, Evolution and Systematics, 25, 375–403.

    Article  Google Scholar 

  • Gaiero, D. M., Simonella, L., Gassó, S., Gili, S., Stein, A. F., Sosa, P., Becchio, R., Arce, J., & Marelli, H. (2013). Ground/satellite observations and atmospheric modeling of dust storms originating in the high Puna-Altiplano deserts (South America): implications for the interpretation of paleo-climatic archives. Journal of Geophysical Research: Atmospheres, 118, 3817–3831.

    Google Scholar 

  • Gamble, T., Simons, A. M., Colli, G. R., & Vitt, L. J. (2008). Tertiary climate change and the diversification of the Amazonian gecko genus Gonatodes (Sphaerodactylidae, Squamata). Molecular Phylogenetics and Evolution, 46, 269–277.

    Article  PubMed  Google Scholar 

  • Garzione, C. N., Molnar, P., Libarkin, J. C., & MacFadden, B. J. (2006). Rapid late Miocene rise of the Bolivian Altiplano. Evidence from removal of mantle lithosphere. Earth and Planetary Science Letters, 241, 543–556.

    Article  CAS  Google Scholar 

  • Giambiagi, L. B., & Ramos, V. A. (2002). Structural evolution of the Andes in a transitional zone between flat and normal subduction (33°30′–33°45′S), Argentina and Chile. Journal of South American Earth Studies, 15, 101–116.

    Article  Google Scholar 

  • Graham, A., Gregory-Wodzicki, K. M., & Wright, K. L. (2001). Studies in Neotropical Paleobotany. XV. A Mio-Pliocene palynoflora from the Eastern Cordillera, Bolivia: implications for the uplift history of the Central Andes. American Journal of Botany, 88, 1545–1557.

    Article  CAS  PubMed  Google Scholar 

  • Hamilton, M. B. (1999). Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Molecular Ecology, 8, 521–523.

    CAS  PubMed  Google Scholar 

  • Hoiss, B., Krauss, J., Potts, S. G., Roberts, S., & Steffan-Dewenter, I. (2012). Altitude acts as an environmental filter on phylogenetic composition, traits and diversity in bee communities. Proceedings of the Royal Society B-Biological Sciences, 279, 4447–4456.

    Article  PubMed Central  Google Scholar 

  • Hoke, G. D., & Garzione, C. N. (2008). Paleosurfaces, paleoelevation, and the mechanisms for the late Miocene topographic development of the Altiplano plateau. Earth and Planetary Science Letters, 271, 192–201.

    Article  CAS  Google Scholar 

  • Hufford, L., McMahon, M. M., Sherwood, A. M., Reeves, G., & Chase, M. W. (2003). The major clades of Loasaceae: phylogenetic analysis using the plastid matK and trnL-trnF regions. American Journal of Botany, 90, 1215–1228.

    Article  CAS  PubMed  Google Scholar 

  • Hufford, L., McMahon, M. M., O’Quinn, R., & Poston, M. E. (2005). A phylogenetic analysis of Loasaceae, subfamily Loasoideae based on plastid DNA sequences. International Journal of Plant Sciences, 166, 289–300.

    Article  CAS  Google Scholar 

  • Hughes, C., & Eastwood, R. (2006). Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proceedings of the National Academy of Sciences of the United States of America, 103, 10334–10339.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jobb, G., Haeseler, A. V., & Strimmer, K. (2004). TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evolutionary Biology. doi:10.1186/1471-2148-4-18.

    PubMed  PubMed Central  Google Scholar 

  • Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamb, S., Hoke, L., Kennan, L., & Dewey, J. (1997). Cenozoic evolution of the Central Andes in Bolivia and northern Chile. Geological Society, London, Special Publications, 121, 237–264.

    Article  Google Scholar 

  • Levina, M., Horton, B. K., Fuentes, F., & Stockli, D. F. (2014). Cenozoic sedimentation and exhumation of the foreland basin system preserved in the Precordillera thrust belt (31–32°S), southern central Andes, Argentina. Tectonics, 33, 1659–1680.

    Article  Google Scholar 

  • Luebert, F., & Weigend, M. (2014). Phylogenetic insights into Andean plant diversification. Frontiers in Ecology and Evolution. doi:10.3389/fevo.2014.00027.

    Google Scholar 

  • Martinez, J. J., Ferro, L. I., Mollerach, L. I., & Barquez, R. M. (2012). The phylogenetic relationships of the Andean swamp rat genus Neotomys (Rodentia, Cricetidae, Sigmodontinae) based on mitochondrial and nuclear markers. Acta Theriologica, 57, 277–287.

    Article  Google Scholar 

  • Martini, M.A., Strelin, J.A., Kaplan, M.R., & Schaefer, J.M. (2012). Glacial and periglacial geomorphology and chronology around the Nevado de Chañi (Cordillera Oriental of Jujuy): implication for past climate in NW Argentina. Resource document. AGU Fall Meeting Abstracts. http://adsabs.harvard.edu/abs/2012AGUFMEP53C1053M. Accessed 13 Oct 2016.

  • McGuire, J. A., Witt, C. C., Remsen Jr., J. V., Corl, A., Daniel, L., Rabosky, D. L., Altshuler, D. L., & Dudley, R. (2014). Molecular phylogenetics and the diversification of hummingbirds. Current Biology, 24, 910–916.

    Article  CAS  PubMed  Google Scholar 

  • Meng, H. H., & Zhang, M. L. (2013). Diversification of plant species in arid Northwest China: species-level phylogeographical history of Lagochilus Bunge ex Bentham (Lamiaceae). Molecular Phylogenetics and Evolution, 68, 398–409.

    Article  PubMed  Google Scholar 

  • Mercer, J. H., & Sutter, J. (1982). Late Miocene—earliest Pliocene glaciation in Southern Argentina: implications for global ice-sheet history. Palaeogeography, Palaeoclimatology, Palaeoecology, 38, 185–206.

    Article  Google Scholar 

  • Minelli, A., & Fusco, G. (2012). On the evolutionary developmental biology of speciation. Evolutionary Biology, 39, 242–254.

    Article  Google Scholar 

  • Moré, M., Cocucci, A. A., & Sérsic, A. N. (2015). Phylogeny and floral trait evolution in Jaborosa (Solanaceae). Taxon, 64, 523–534.

    Article  Google Scholar 

  • Muschick, M., Indermaur, A., & Salzburger, W. (2012). Convergent evolution within an adaptive radiation of cichlid fishes. Current Biology, 22, 2362–2368.

    Article  CAS  PubMed  Google Scholar 

  • Mutke, J., Jacobs, R., Meyers, K., Henning, T., & Weigend, M. (2014). Diversity patterns of selected Andean plant groups correspond to topography and habitat dynamics, not orogeny. Frontiers in Genetics. doi:10.3389/fgene.2014.00351.

    PubMed  PubMed Central  Google Scholar 

  • Müller, J., Müller, K., Quandt, D., & Neinhuis, C. (2010). PhyDe-Phylogenetic Data Editor. Program distributed by the author. Available at: http://www.phyde.de/index.html.

  • Nespolo, R. F., Opazo, J. C., & Rosenmann, F. B. (1999). Thermal acclimation, maximum metabolic rate, and nonshivering thermogenesis of Phyllotis xanthopygus (Rodentia) in the Andes Mountains. Journal of Mammalogy, 80, 742–748.

    Article  Google Scholar 

  • Nielsen, R. (2002). Mapping mutations on phylogenies. Systematic Biology, 51, 729–739.

    Article  PubMed  Google Scholar 

  • Nylin, S., Slove, J., & Janz, N. (2014). Host plant utilization, host range oscillations and diversification in Nymphalid butterflies: a phylogenetic investigation. Evolution, 68, 105–124.

    Article  PubMed  Google Scholar 

  • Palazzesi, L., Gottschling, M., Barreda, V., & Weigend, M. (2012). First Miocene fossils of Vivianiaceae shed new light on the phylogeny, divergence times, and historical biogeography of Geraniales. Botanical Journal of the Linnean Society, 107, 67–85.

    Article  Google Scholar 

  • Perez, F., Arroyo, M. T. K., Medel, R., & Hershkovitz, M. A. (2006). Ancestral reconstruction of flower morphology and pollination systems in Schizanthus (Solanaceae). American Journal of Botany, 93, 1029–1038.

    Article  PubMed  Google Scholar 

  • Ramos, V. A., Cristallini, E. O., & Pérez, D. J. (2002). The Pampean flat-slab of the Central Andes. Journal of South American Earth Studies, 15, 59–78.

    Article  Google Scholar 

  • Revell, L. J. (2012). Phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217–223.

    Article  Google Scholar 

  • Revell, L. J. (2014). Graphical methods for visualizing comparative data on phylogenies. In L. Z. Garamszegi (Ed.), Modern phylogenetic comparative methods and their application in evolutionary biology (pp. 77–103). Berlin, Heidelberg: Springer.

    Google Scholar 

  • Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

    Article  CAS  PubMed  Google Scholar 

  • Rubioldo, D., Seggiaro, R., Gallardo, E., Disalvo, A., Sanchez, M., Turel, A., Ramallo, E., Sandruss, A., & Godeas, M. (2001). Hoja Geológica 2366-II / 2166-IV, La Quiaca. Geología y Provincias de Jujuy y Salta. Instituto de Recursos Minerales, Servicio Geológico Minero Argentino. Boletín 246, p. Buenos Aires.

  • Rutschmann, F. (2006). Molecular dating of phylogenetic trees: a brief review of current methods that estimate divergence times. Diversity and Distributions, 12, 35–48.

    Article  Google Scholar 

  • Sanderson, M. J. (1997). A nonparametric approach to estimating divergence times in the absence of rate constancy. Molecular Biology and Evolution, 14, 1218–1231.

    Article  CAS  Google Scholar 

  • Schenk, J. J., & Hufford, L. (2010). Effects of substitution models on divergence time estimates: simulations and an empirical study of model uncertainty using Cornales. Systematic Botany, 35, 578–592.

    Article  Google Scholar 

  • Sérsic, A., Cosacov, A., Cocucci, A. A., Johnson, L. A., Pozner, R., Avila, L. J., Sites Jr., J. W., & Morando, M. (2011). Emerging phylogeographical patterns of plants and terrestial vertebrates from Patagonia. Biological Journal of the Linnean Society, 103, 475–494.

    Article  Google Scholar 

  • Smith, S. D., & Baum, D. A. (2006). Phylogenetics of the florally diverse Andean clade Iochrominae (Solanaceae). American Journal of Botany, 93, 1140–1153.

    Article  PubMed  Google Scholar 

  • Smith, S. D., Ané, C., & Baum, D. A. (2008). The role of pollinator shifts in the floral diversification of Iochroma (Solanaceae). Evolution, 62, 793–806.

    Article  PubMed  Google Scholar 

  • Solà, E., Sluys, R., Gritzalis, K., & Riutort, M. (2013). Fluvial basin history in the northeastern Mediterranean region underlies dispersal and speciation patterns in the genus Dugesia (Platyhelminthes, Tricladida, Dugesiidae). Molecular Phylogenetics and Evolution, 66, 887–888.

    Article  Google Scholar 

  • Starck, D., & Anzótegui, L. M. (2001). The late Miocene climatic change—persistence of a climatic signal through the orogenic stratigraphic record in northwestern Argentina. Journal of South American Earth Sciences, 14, 763–774.

    Article  Google Scholar 

  • Stech, M., Veldman, S., & Larraín, J. (2013). Molecular species delimitation in the Racomitrium canescens Complex (Grimmiaceae) and implications for DNA barcoding of species complexes in mosses. PloS One. doi:10.1371/journal.pone.0053134.

    Google Scholar 

  • Strelin, M. M., Benitez-Vieyra, S., Ackermann, M., & Cocucci, A. (2016a). Flower reshaping in the transition to hummingbird pollination in Loasaceae, subfam. Loasoideae despite absence of corolla tubes or spurs. Evolutionary Ecology, 30, 401–407.

    Article  Google Scholar 

  • Strelin, M. M., Benitez-Vieyra, S., Fornoni, J., Klingenberg, C. P., & Cocucci, A. A. (2016b). Exploring the ontogenetic scaling hypothesis during the diversification of pollination syndromes in Caiophora (Loasaceae, subfam. Loasoideae). Annals of Botany, 117, 937–947.

    Article  PubMed  Google Scholar 

  • Swofford, D.L. (2003). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Särkinen, T., Pennington, R. T., Lavin, M., Simons, M. F., & Hughes, C. E. (2012). Evolutionary islands in the Andes: persistence and isolation explain high endemism in Andean dry tropical forests. Journal of Biogeography, 39, 884–900.

    Article  Google Scholar 

  • Weigend, M., & Gottschling, M. (2006). Evolution of funnel-revolver flowers and ornithophily in Nasa (Loasaceae). Plant Biology, 8, 120–142.

    Article  CAS  PubMed  Google Scholar 

  • Weigend, M., Gottschling, M., Hoot, S., & Ackermann, M. (2004). A preliminary phylogeny of Loasaceae subfam. Loasoideae (Angiospermae: Cornales) based on trnL(UAA) sequence data, with consequences for systematics and historical biogeography. Organisms Diversity & Evolution, 4, 73–90.

    Article  Google Scholar 

  • Weigend, M., Gröger, A., & Ackermann, M. (2005). The seeds of Loasaceae subfam. Loasoideae (Cornales) II: seed morphology of “South Andean Loasas” (Loasa, Caiophora, Scyphanthus and Blumenbachia). Flora-Morphology, Distribution, Functional Ecology of Plants, 200, 569–591.

    Article  Google Scholar 

  • Weigend, M., Ackermann, M., & Henning, T. (2010). Reloading the revolver- male fitness as a simple explanation for complex reward partitioning in Nasa macrothyrsa (Loasaceae, Cornales). Biological Journal of the Linnean Society, 100, 124–131.

    Article  Google Scholar 

  • Wen, J., & Zimmer, E. (1996). Phylogeny and biogeography of Panax L (the ginseng genus, Araliaceae): inferences from ITS sequences of nuclear ribosomal RNA. Molecular Phylogenetics and Evolution, 6, 167–177.

    Article  CAS  PubMed  Google Scholar 

  • West-Eberhard, M. J. (2005). Developmental plasticity and the origin of species differences. Proceedings of the National Academy of Sciences, 102, 6543–6549.

    Article  CAS  Google Scholar 

  • Xia, X., & Xie, Z. (2001). DAMBE: software package for data analysis in molecular biology and evolution. Journal of Heredity, 92, 371–373.

    Article  CAS  PubMed  Google Scholar 

  • Xia, X., Xie, Z., Salemi, M., Chen, L., & Wang, Y. (2003). An index of substitution saturation and its application. Molecular Phylogenetics and Evolution, 26, 1–7.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Z., & Rannala, B. (2012). Molecular phylogenetics: principles and practice. Nature Reviews Genetics, 13, 303–314.

    Article  CAS  PubMed  Google Scholar 

  • Zech, J., Zech, R., Kubik, P. W., & Veit, H. (2009). Glacier and climate reconstruction at Tres Lagunas, NW Argentina, based on 10 Be surface exposure dating and lake sediment analyses. Palaeogeography, Palaeoclimatology, Palaeoecology, 284, 180–190.

    Article  Google Scholar 

  • Zuloaga, F.O., Morrone, O., Belgrano, M.J., Marticorena, C., & Marchesi, E. (2008). Catálogo de las plantas vasculares del Cono Sur. Monogr. Syst. Bot. Missouri Bot. Gard, 107(1–3), i–xcvi, 1–3348.

Download references

Acknowledgements

We thank Marcela Moré and Cristina Acosta (IMBIV, CONICET, Universidad Nacional de Córdoba, Argentina); Romina Vidal-Russel (INIBIOMA, CONICET, Universidad Nacional del Comahue); Jorge Strelin, Mateo Martini and Diego Gaiero (CICTERRA, Universidad Nacional de Córdoba, Instituto Antártico Argentino); Matías Ghiglione (Instituto de Estudios Andinos, CONICET, Universidad Nacional de Buenos Aires, Argentina); and the two anonymous reviewers for contributing with their comments and suggestions to the quality of this manuscript. We thank Laura Gatica for editing the English of this manuscript and Maximilian Weigend (Nees Institut für Biodiversität der Pflanzen, Rheinische Friedrich-Wilhelms-Universität, Bonn, Germany) for providing material, funds and data for this study. M.S. has a scholarship from the National Scientific and Technical Research Council (CONICET).

Author information

Authors and Affiliations

  1. Laboratorio Ecotono, INIBIOMA (Universidad Nacional del Comahue-CONICET), Pasaje Gutierrez 1125, 8400, Bariloche, Rio Negro, Argentina

    Marina Micaela Strelin

  2. Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile

    José Ignacio Arroyo

  3. Instituto de Ecología & Biodiversidad (IEB-Chile), Casilla 653, Santiago, Chile

    José Ignacio Arroyo

  4. Nees Institut für Biodiversität der Pflanzen, Rheinische Friedrich-Wilhelms-Universität, Meckenheimer Allee 170, 53115, Bonn, Germany

    Markus Ackermann

  5. Institut für Integrierte Naturwissenschaften – Biologie, Universität Koblenz-Landau, Universitätsstr. 1, 56070, Koblenz, Germany

    Stella Fliesswasser & Markus Ackermann

Authors
  1. Marina Micaela Strelin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José Ignacio Arroyo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stella Fliesswasser
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Markus Ackermann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marina Micaela Strelin.

Additional information

An erratum to this article is available at http://dx.doi.org/10.1007/s13127-016-0318-y.

Electronic supplementary material

Table S1

(XLS 28 kb)

Table S2

(XLS 48 kb)

Table S3

(DOC 95 kb)

Appendix S1

(XML 89 kb)

Table S4

(DOCX 15 kb)

Fig. S1.

Substitution saturation plot. Relationship between observed (uncorrected) and estimated (corrected) genetic distances for a F84 model of nucleotide substitution. S: transitions and V: transversions. Linear relationship indicates no saturation. (JPEG 52 kb)

Fig. S2.

Phylogenetic trees based on concatenated ITS/ trnSGCU-trnGUUC markers obtained with: a) MP; b) NJ; c) ML; d) BI methods. (PDF 26 kb)

Fig. S3.

Phylogenetic trees based on ITS markers obtained with: a) MP; b) NJ; c) ML; d) BI methods. (PDF 27 kb)

Fig. S4.

Phylogenetic trees based on trnSGCU-trnGUUC markers obtained with: a) MP; b) NJ; c) ML; d) BI methods. (PDF 25 kb)

Fig. S5.

Consensus phylogenetic trees for: a) ITS; b) trnSGCU-trnGUUC; c) ITS/ trnSGCU-trnGUUC for the four reconstruction methods: maximum parsimony (MP), neighbour joining (NJ), maximum likelihood (ML), and bayesian inference (BI). (PDF 34 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Strelin, M.M., Arroyo, J.I., Fliesswasser, S. et al. Diversification of Caiophora (Loasaceae subfam. Loasoideae) during the uplift of the Central Andes. Org Divers Evol 17, 29–41 (2017). https://doi.org/10.1007/s13127-016-0312-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-016-0312-4

Keywords

Search

Navigation