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UC Merced Frontiers of Biogeography UC Merced Frontiers of Biogeography Title Historical assembly of Zygophyllaceae in the Atacama Desert Permalink https://escholarship.org/uc/item/2fs0w8dx Journal Frontiers of Biogeography, 0(0) Authors Böhnert, Tim Weigend, Maximilian Merklinger, Felix et al. Publication Date 2019 DOI 10.21425/F5FBG45197 Supplemental Material https://escholarship.org/uc/item/2fs0w8dx#supplemental License https://creativecommons.org/licenses/by/4.0/ 4.0 Peer reviewed eScholarship.org Powered by the California Digital Library University of California – Böhnert et al. | revised manuscript for Frontiers of Biogeography | Research Article 1 Journal 2 Frontiers of Biogeography - Original Research Paper 3 Publication year: 2020 4 Issue: 12.2 5 Article doi: doi:10.21425/F5FBG45197 6 Article number: e45197 7 Article format: Long (author names in front page + abstract + 6-10 keywords) 8 Article type: Research Article 9 Article series: Not applicable to this article 10 Title: Historical assembly of Zygophyllaceae in the Atacama Desert 11 Subtitle: n.a. 12 Author list: Tim Böhnert, Maximilian Weigend, Felix F. Merklinger, Dietmar Quandt, Federico Luebert 13 Tim Böhnert: https://orcid.org/0000-0003-1415-7896 14 Maximilian Weigend: https://orcid.org/0000-0003-0813-6650 15 Felix Merklinger: https://orcid.org/0000-0003-2197-0412 16 Dietmar Quandt: https://orcid.org/0000-0003-4304-6028 17 Federico Luebert: https://orcid.org/0000-0003-2251-4056 18 Strapline author: Böhnert et al. 19 Strapline running title: Historical assembly of Zygophyllaceae in the Atacama Desert 20 Supplementary Materials: Yes (2) 21 22 1 – Böhnert et al. | revised manuscript for Frontiers of Biogeography | Research Article 23 Historical assembly of Zygophyllaceae in the Atacama Desert 24 25 Tim Böhnert1 *, Maximilian Weigend1, Felix Merklinger1, Dietmar Quandt1 2, Federico Luebert1 3 26 27 1 Nees Institute for Biodiversity of Plants, University of Bonn, Bonn, Germany 28 2 Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), AG ETX, Gatersleben, Germany 29 3 Departamento de Silvicultura y Conservación de la Naturaleza, Universidad de Chile, Santiago, Chile 30 * corresponding author: [email protected], +49 (0) 228 73-7025, Meckenheimer Allee 170, 31 53115 Bonn, Germany 32 33 Tim Böhnert: https://orcid.org/0000-0003-1415-7896 34 Maximilian Weigend: https://orcid.org/0000-0003-0813-6650 35 Felix Merklinger: https://orcid.org/0000-0003-2197-0412 36 Dietmar Quandt: https://orcid.org/0000-0003-4304-6028 37 Federico Luebert: https://orcid.org/0000-0003-2251-4056 38 39 Abstract 40 The Atacama Desert harbors a unique arid-adapted flora with a high degree of endemism, the origin 41 of which is poorly understood. In the Atacama Desert, Zygophyllaceae is represented by five endemic 42 species: one member of Zygophylloideae: Fagonia chilensis; and four members of Larreoideae: 43 Bulnesia chilensis and Porlieria chilensis, the only representatives in the Atacama Desert of genera 44 with disjunct distributions between Argentina, Peru and Chile; and monotypic endemic genera 45 Metharme lanata and Pintoa chilensis. Zygophyllaceae are thus a particularly suitable group for 46 studying the historical assembly of the Atacama Desert flora as each of these species may represent 47 independent biogeographical events. We made use of published as well as original plastid DNA 48 sequences (rbcL, trnL-trnF & trnS-trnG) to reevaluate the phylogenetic relationships of the Atacama 49 Zygophyllaceae. Bayesian divergence time estimates as implemented in BEAST2 and ancestral area 50 reconstruction with the Dispersal Extinction Cladogenesis approach using BioGeoBEARS were applied 51 to infer ancestral ranges. We compiled the most complete data set of Larreoideae to date with 25 of 52 28 species. Bulnesia rivas-martinezii from Bolivia forms a clade with Pintoa chilensis from the 53 Atacama Desert, rendering the genus Bulnesia paraphyletic. Most representatives of Zygophyllaceae 54 colonized the Atacama Desert during the Miocene, and only Fagonia dispersed more recently. The 55 colonization history of the Atacama Desert in South America is reflected by three individual 56 distribution patterns or floristic elements. The presence of Bulnesia, Pintoa, and Metharme is best 57 explained by Andean vicariance, while the southern Atacama Desert representative, Porlieria 2 – Böhnert et al. | revised manuscript for Frontiers of Biogeography | Research Article 58 chilensis, has a continuous distribution into central Chile from where it probably dispersed further 59 north. The only South American Fagonia species (F. chilensis) likely colonized the Chilean-Peruvian 60 Coastal Desert via long distance dispersal from North America. 61 62 Keywords: Andes, arid environments, Bulnesia, Chile, Historical biogeography, Larreoideae, 63 Metharme, South America 64 65 Highlights: 66 • The most comprehensive phylogeny of Larreoideae (Zygophyllaceae) is here presented, 67 including all taxa native to the Atacama Desert and only three missing species. 68 • The five endemic Atacama Zygophyllaceae species are the result of individual colonization 69 events rather than a single one followed by in-situ diversification. 70 • The colonization of the Atacama Desert by Fagonia is likely the result of long-distance 71 dispersal from North America. 72 • The colonization of Bulnesia, Pintoa, and Porlieria is probably the results of individual 73 vicariance events and can be linked to the Andean uplift. 74 • In contrast to several species rich Atacama plant groups, which are mostly annuals, short- 75 lived perennials or shrubs, woody taxa like Zygophyllaceae failed to diversify in the Atacama 76 Desert. This is in contrast to the recent diversification of old world Zygophyllaceae, indicating 77 a low carrying capacity as well as an increased extinction rate for such life forms in this 78 hyperarid environment. 79 80 Introduction 81 Located in northern Chile, the Atacama Desert ranges from 18° S at the border region to Peru and 30° 82 S around La Serena, while it is restricted in the east by the Andean mountain range and the Pacific 83 Ocean to the west. Relative to its area, the Atacama Desert is surprisingly species-rich, harboring 84 about 550 species, of which 60 % are endemic (Dillon and Hoffmann 1997). However, diversity is not 85 equally distributed in the Atacama Desert. In its northern portion (approx. 18° to 26° S), most species 86 can be found along the coastal range as well as along the Andean foothills, while only few species can 87 survive the harsh conditions of the inner core of the Atacama Desert. Further south, the vegetation is 88 more broadly distributed: whereas the conditions are still predominantly arid, Andean and coastal 89 ranges are not separated by a barren zone (Villagrán et al. 1983, Rundel et al. 1991, Luebert and 90 Pliscoff 2017). 91 3 – Böhnert et al. | revised manuscript for Frontiers of Biogeography | Research Article 92 The historical assembly of the Atacama Desert flora has been linked to the timing of the major 93 factors controlling its aridity (Rundel et al. 1991). Recent evidence suggests that the age of aridity can 94 be dated back to the Miocene or even Oligocene (Dunai et al. 2005). However, we still lack a detailed 95 knowledge of the process, since an understanding of the timing of the onset of aridity remains 96 elusive (Ritter et al. 2018), and only few studies have addressed the timing of diversifications of 97 Atacama Desert plant groups (e.g., Luebert and Wen 2008, Dillon et al. 2009, Heibl and Renner 2012, 98 Böhnert et al. 2019). 99 100 Zygophyllaceae are key elements of world desert and semi-desert ecosystems, and their 101 diversification is thought to be linked with increased aridity during the Oligocene-Miocene transition, 102 especially in Zygophylloideae (Bellstedt et al. 2012, Wu et al. 2015, 2018). The family has a worldwide 103 distribution, but it is largely restricted to hot and dry regions. Five native genera of Zygophyllaceae 104 are documented for the Atacama Desert, making it one of the Atacama groups with the highest 105 phylogenetic diversity, although each genus is only represented by a single species. The genera 106 Bulnesia Gay, Metharme Phil. ex Engler, Pintoa Gay, and Porlieria Ruiz & Pav. belong to the New 107 World endemic Larreoideae, only Fagonia chilensis Hook. & Arn. belongs to the sub-cosmopolitan 108 Zygophylloideae. Bulnesia and Porlieria comprise four species each (Palacios and Hunziker 1984, 109 Godoy-Bürki et al. 2018), while Metharme and Pintoa are monotypic (Beier et al. 2003). 110 111 Understanding the historical assembly of a flora requires evidence for the spatial and temporal origin 112 of its component plant lineages. Based on a review of the distribution and phylogenetic relationships 113 of 53 plant taxa in the Atacama Desert and their closely related species, Luebert (2011) recognized 114 four distribution patterns or floristic elements: (1) tropical Andean, (2) central Chilean, (3) trans- 115 Andean disjunct, and (4) amphitropical disjunct. The two first elements represent species with closely 116 related taxa distributed immediately north or south of the Atacama Desert, pointing to direct floristic 117 exchanges between the Atacama Desert and its neighboring regions. Disjunct trans-Andean 118 elements, with species distributed on both sides of the Andes, are likely the result of vicariance due 119 to Andean uplift or of trans-Andean dispersal. American amphitropical disjunctions are explained as 120 the result of long-distance dispersal (LDD) events between North and South America (Simpson et al. 121 2017). 122 123 All four floristic elements appear to be present among the five representatives of Zygophyllaceae in 124 the Atacama Desert. Bulnesia chilensis Gay, Pintoa chilensis Gay, and Porlieria chilensis I.M. Johnst. 125 are found in the southern portion of the Atacama Desert, with Porlieria chilensis ranging into central 126 Chile. Metharme lanata Phil. ex Engl. in turn is found at the dry limit in the northern part of the 4 – Böhnert et al. | revised manuscript for Frontiers of Biogeography | Research Article 127 Atacama Desert. According to Lia et al. (2001) and Godoy-Bürki et al.
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