Organisms Diversity & Evolution

, Volume 17, Issue 1, pp 29–41 | Cite as

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

  • Marina Micaela Strelin
  • José Ignacio Arroyo
  • Stella Fliesswasser
  • Markus Ackermann
Original Article


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 (trnS GCU -trnG UUC ) 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.


Diversification Caiophora Loasaceae, subfam. Loasoideae Diversification Central Andes Orogeny 



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).

Supplementary material

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Table S1 (XLS 28 kb)
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Table S2 (XLS 48 kb)
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Table S3 (DOC 95 kb)
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Appendix S1 (XML 89 kb)
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Table S4 (DOCX 15 kb)
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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)
13127_2016_312_MOESM7_ESM.pdf (26 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)
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Fig. S3. Phylogenetic trees based on ITS markers obtained with: a) MP; b) NJ; c) ML; d) BI methods. (PDF 27 kb)
13127_2016_312_MOESM9_ESM.pdf (25 kb)
Fig. S4. Phylogenetic trees based on trnSGCU-trnGUUC markers obtained with: a) MP; b) NJ; c) ML; d) BI methods. (PDF 25 kb)
13127_2016_312_MOESM10_ESM.pdf (35 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)


  1. 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.Google Scholar
  2. Ackermann, M., & Weigend, M. (2006). Nectar, floral morphology and pollination syndrome in Loasaceae subfam. Loasoideae (Cornales). Annals of Botany, 98, 503–514.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 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.CrossRefPubMedGoogle Scholar
  4. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Antonelli, A., & Sanmartín, I. (2011). Why are there so many plant species in the Neotropics? Taxon, 60, 403–414.Google Scholar
  6. 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.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.Google Scholar
  9. 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.CrossRefGoogle Scholar
  10. Barnes, J. B., & Ehlers, T. A. (2009). End member models for Andean Plateau uplift. Earth-Science Reviews, 97, 105–132.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. Chaves, J. A., Weir, J. T., & Smith, T. B. (2011). Diversification in Adelomyia hummingbirds follows Andean uplift. Molecular Ecology, 20, 4564–4576.CrossRefPubMedGoogle Scholar
  15. Clapperton, C. H. (1983). The glaciation of the Andes. Quaternary Science Reviews, 2, 83–155.CrossRefGoogle Scholar
  16. Cocucci, A. A., & Sérsic, A. N. (1998). Evidence of rodent pollination in Cajophora coronata (Loasaceae). Plant Systematics and Evolution, 211, 113–128.CrossRefGoogle Scholar
  17. 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
  18. Cruden, R. W. (1972). Pollinators in high-elevation ecosystems: relative effectiveness of birds and bees. Science, 176, 1439–1440.CrossRefPubMedGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. Felsenstein, J. (1984). Distance methods for inferring phylogenies: a justification. Evolution, 38, 16–24.CrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. 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
  26. 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.CrossRefPubMedGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. 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.CrossRefPubMedGoogle Scholar
  30. Hamilton, M. B. (1999). Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Molecular Ecology, 8, 521–523.PubMedGoogle Scholar
  31. 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.CrossRefPubMedCentralGoogle Scholar
  32. 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.CrossRefGoogle Scholar
  33. 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.CrossRefPubMedGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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.PubMedPubMedCentralGoogle Scholar
  37. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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.CrossRefGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. Luebert, F., & Weigend, M. (2014). Phylogenetic insights into Andean plant diversification. Frontiers in Ecology and Evolution. doi: 10.3389/fevo.2014.00027.Google Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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. Accessed 13 Oct 2016.
  43. 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.CrossRefPubMedGoogle Scholar
  44. 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.CrossRefPubMedGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. Minelli, A., & Fusco, G. (2012). On the evolutionary developmental biology of speciation. Evolutionary Biology, 39, 242–254.CrossRefGoogle Scholar
  47. Moré, M., Cocucci, A. A., & Sérsic, A. N. (2015). Phylogeny and floral trait evolution in Jaborosa (Solanaceae). Taxon, 64, 523–534.CrossRefGoogle Scholar
  48. Muschick, M., Indermaur, A., & Salzburger, W. (2012). Convergent evolution within an adaptive radiation of cichlid fishes. Current Biology, 22, 2362–2368.CrossRefPubMedGoogle Scholar
  49. 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.PubMedPubMedCentralGoogle Scholar
  50. Müller, J., Müller, K., Quandt, D., & Neinhuis, C. (2010). PhyDe-Phylogenetic Data Editor. Program distributed by the author. Available at:
  51. 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.CrossRefGoogle Scholar
  52. Nielsen, R. (2002). Mapping mutations on phylogenies. Systematic Biology, 51, 729–739.CrossRefPubMedGoogle Scholar
  53. 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.CrossRefPubMedGoogle Scholar
  54. 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.CrossRefGoogle Scholar
  55. 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.CrossRefPubMedGoogle Scholar
  56. 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.CrossRefGoogle Scholar
  57. Revell, L. J. (2012). Phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217–223.CrossRefGoogle Scholar
  58. 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
  59. Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.CrossRefPubMedGoogle Scholar
  60. 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.Google Scholar
  61. Rutschmann, F. (2006). Molecular dating of phylogenetic trees: a brief review of current methods that estimate divergence times. Diversity and Distributions, 12, 35–48.CrossRefGoogle Scholar
  62. Sanderson, M. J. (1997). A nonparametric approach to estimating divergence times in the absence of rate constancy. Molecular Biology and Evolution, 14, 1218–1231.CrossRefGoogle Scholar
  63. 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.CrossRefGoogle Scholar
  64. 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.CrossRefGoogle Scholar
  65. Smith, S. D., & Baum, D. A. (2006). Phylogenetics of the florally diverse Andean clade Iochrominae (Solanaceae). American Journal of Botany, 93, 1140–1153.CrossRefPubMedGoogle Scholar
  66. 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.CrossRefPubMedGoogle Scholar
  67. 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.CrossRefGoogle Scholar
  68. 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.CrossRefGoogle Scholar
  69. 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
  70. 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.CrossRefGoogle Scholar
  71. 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.CrossRefPubMedGoogle Scholar
  72. Swofford, D.L. (2003). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
  73. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 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.CrossRefGoogle Scholar
  75. Weigend, M., & Gottschling, M. (2006). Evolution of funnel-revolver flowers and ornithophily in Nasa (Loasaceae). Plant Biology, 8, 120–142.CrossRefPubMedGoogle Scholar
  76. 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.CrossRefGoogle Scholar
  77. 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.CrossRefGoogle Scholar
  78. 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.CrossRefGoogle Scholar
  79. 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.CrossRefPubMedGoogle Scholar
  80. West-Eberhard, M. J. (2005). Developmental plasticity and the origin of species differences. Proceedings of the National Academy of Sciences, 102, 6543–6549.CrossRefGoogle Scholar
  81. Xia, X., & Xie, Z. (2001). DAMBE: software package for data analysis in molecular biology and evolution. Journal of Heredity, 92, 371–373.CrossRefPubMedGoogle Scholar
  82. 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.CrossRefPubMedGoogle Scholar
  83. Yang, Z., & Rannala, B. (2012). Molecular phylogenetics: principles and practice. Nature Reviews Genetics, 13, 303–314.CrossRefPubMedGoogle Scholar
  84. 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.CrossRefGoogle Scholar
  85. 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.Google Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2016

Authors and Affiliations

  • Marina Micaela Strelin
    • 1
  • José Ignacio Arroyo
    • 2
    • 3
  • Stella Fliesswasser
    • 5
  • Markus Ackermann
    • 4
    • 5
  1. 1.Laboratorio EcotonoINIBIOMA (Universidad Nacional del Comahue-CONICET)Bariloche, Rio NegroArgentina
  2. 2.Departamento de Ecología, Facultad de Ciencias BiológicasPontificia Universidad Católica de ChileSantiagoChile
  3. 3.Instituto de Ecología & Biodiversidad (IEB-Chile)SantiagoChile
  4. 4.Nees Institut für Biodiversität der PflanzenRheinische Friedrich-Wilhelms-UniversitätBonnGermany
  5. 5.Institut für Integrierte Naturwissenschaften – BiologieUniversität Koblenz-LandauKoblenzGermany

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