Biogeography and Evolution of the Atacama Desert Flora Tim Böhnert1, Felix F. Merklinger1, Sonja Böker1, Dörte Harpke2, Alexandra Stoll3, Frank Blattner2,4, Maximilian Weigend1, Dietmar Quandt1, Federico Luebert1,5,*

1Nees Institute for Biodiversity of , University of Bonn, Bonn, Germany. 2Leibniz Institute of Genetics and Crop Plant Research (IPK), Gatersleben, Germany. 3Centro de Estudios Avanzados en Zonas Aridas, CEAZA, La Serena Chile. 4German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Germany. 5Departamento de Silvicultura y Conservación de la Naturaleza, Universidad de Chile, Santiago, Chile. *[email protected]

Context Ophryosporus (Asteraceae) [F.F. Merklinger] The Atacama Desert, located on the western distributed plant taxa in the Atacama Desert. Methods: Monophyly and realationships of side of the Andes in northern Chile, harbors a Diversifications have been shown to be surpri- species of Ophryosporus from the Atacama range of endemic species adapted to hyper- singly recent in some Atacama clades, which Desert, with respect to Andean and E South Ame- arid habitats. Vegetation is largely restricted is at odds with the high age assumed for this rican taxa of the , were evaluated prior to to coastal fog oases and the Andean foothills, desert. Here, we report the results of a mole- the population genetic analyses. A phylogenetic which are separated by a largely vegetation-free cular dating analysis of the Atacama endemic analysis based on ITS sequence data was carri- zone. In the context of a large-scale project on () based on three plastid ed out using a Bayesian approach in MrBayes. landscape and biotic evolution of hyperarid markers. Furthermore, we present preliminary GBS data were generated on a Illumina HiSeq environments, we investigate the origin and data on gene-flow among populations of four Sequencer at population level for four Atacama diversification of three plant groups as well as species of Ophryosporus (Asteraceae) using Ge- species and a phylogenetic analysis of a conca- gene-flow between populations of four widely notyping-By-Sequencing (GBS) data. tenated SNP matrix was conducted.

Ophryosporus triangularis Cristaria (Malvaceae) [T. Böhnert] 100 Ophryosporus cumingii Ophryosporus piquerioides a b 72 100 100 Ophryosporus piquerioides Ophryosporus anomalus 100 65 74 30 20 10 0 Ophryosporus axilliflorus ecaophora chuutesis 99 2.83 Ophryosporus freyreisii ≥ 05 15°S ecaophora aehioi Ophryosporus heptanthus 08 – 05 ecaophora heterophylla Ophryosporus paradoxus Ophryosporus triangularis Cristaria laucophylla O. triangularis Ophryosporus triangularis ●● ●● 20.29 93 ●●● Cristaria laucophylla Ophryosporus triangularis ●●● 58 ●● Ophryosporus triangularis ●● Cristaria multiflora 20°S ● Ophryosporus triangularis Cristaria multifida Ophryosporus triangularis O. paradoxus Cristaria multifida Ophryosporus triangularis ● 7.42 ● O. triangularis ● 100 C aspera orosula Ophryosporus triangularis 100 O. floribundus ● Cristaria teuissia Ophryosporus triangularis O. johnstonii laiathus Ophryosporus johnstonii ● O. pinifolius ● 25°S ● Cristaria uetesiaa Ophryosporus johnstonii ● ● 82 ecaophora Cristaria oliae Ophryosporus johnstonii ● 99 5 4.21 ● Cristaria aryliiolia 100 99 Ophryosporus triangularis 100 O. johnstonii ● Ophryosporus triangularis ● Cristaria iteerria ●● Cristaria Ophryosporus paradoxus 21 Cristaria cocia 100 Ophryosporus paradoxus ● 30°S ● 75 Cristaria iriiluteola Ophryosporus paradoxus ●● 58 Cristaria caleraa Ophryosporus pinifolius 51 Ophryosporus pinifolius O. floribundus 64 Cristaria iaiaa Ophryosporus pinifolius 99 Cristaria iteerria Ophryosporus pinifolius N Cristaria aicola Ophryosporus pinifolius 35°S Ophryosporus pinifolius Cristaria c aspera 100 Ophryosporus pinifolius 90 0 100 200 300 km O. pinifolius Cristaria racilis Ophryosporus peruvianus Cristaria oliae Ophryosporus peruvianus 73 phaeralcea Ophryosporus peruvianus C iriiluteola piata 100 Aristeguietia salvia 40°S O. peruvianus Cristaria cocia Ageratina glechonophylla 76°W 72°W 68°W Cristaria iteerria Cristaria iteerria phaeralcea Maleae Cristaria leucatha a. Bayesian analysis based on ITS. Coastal Ata- b. Maximum Likelihood tree based on 70,000 1040 | 1 i Cristaria aicola cama species Ophryosporus paradoxus, O. tri- bp matrix. GBS data indicate that the Atacama Cristaria aeophora angularis and O. johnstonii (green) form a mo- species of Ophryosporus fall into two distinct alastru Cristaria aspera nophyletic group. E South American species are clades, separated by fixed allele compositions. Cristaria cyaea Cristaria racilis retrieved as monophylum and are sister to the Species form monophyletic groups, albeit with isootea C iteerria loulata coastal Atacama species. The Andean species O. weak support. However, our data also suggest ala Cristaria issecta pinifolius (blue) is sister to O. peruvianus from that gene flow among species of each clade has Cristaria oata Andean Peru. taken place. Cristaria oata

ossieae 126 Conclusion & Outlook Divergence times of Cristaria suggest that the sely related to the Central Andean species from split from Lacanophora predates the major Peru than to the other coastal Atacama species. phase of the Central Andean uplift, but do not In the context of this project, we are conducting discard an East-West vicariant scenario. Diver- additional phylogenetic and dating analyses in Cristaria leucantha Cristaria integerrima Cristaria dissecta ibisceae sification of Cristaria in the Atacama desert ap- the species-rich genera Atriplex (Amarantha- 63 Tab. 1 | List of crwon fossils used for the beast2 analysis. Placing of the fossils is indicated by green dots in the backbone phylogeny of the . pears to coincide with the onset of hyperaridity ceae) and Cryptantha (Boraginaceae), making Fossil taxon Age [Mya] Clade Reference during the late Miocene and early Pliocene. The use of Sanger and NGS sequencing approaches. Hibiscoxylon nyloticum 88 – 66 Core Malvoideae Kräusel (1939) results in Ophryosporus suggest high genetic Further population genetic analyses are also umaloideae Malvaciphyllum macondicus 60 – 58 Eumalvoideae Carvalho et al. (2011) connectivity among coastal species and among being carried out in Eulychnia spp. (Cactaceae),

Core Maloideae Core Malvacearumpollis sp. 37 – 30 MacPhail & Truswell (1989) Andean species, but low connectivity between Huidobria fruticosa (Loasaceae), and Tillandsia Echiperiporites estelae 45 – 34 Germeraad et al. (1968) coastal and Andean species. The northern An- landbeckii (Bromeliaceae), both with GBS and dean Atacama species appears to be more clo- microsatellite data. Methods: We used the molecular data set of Results & Discussion: Phylogenetic analysis Areces-Berzein and Ackermann (2017; ndhF, with 333 samples across Malvoideae confirms trnK/matK and rpl16), complemented with se- the monophyly of Cristaria and the sister rela- References quences from 50 samples of Malveae from our tion to Lecanophora. The FBD approach reveals Areces-Berazain & Ackerman 2016. Phylogenetics, delimit- Germeraad JH et al. 1968. Palynology of Tertiary sediments ation and historical biogeography of the pantropical tree from tropical areas. Rev. Palaebot. Palyno. 6: 189–348. own field collections, including nearly all- spe very weak posterior propabilities for fossil place- genus (Malvaceae, ). Bot. J. Linn. Heath et al. 2014. The fossilized birth-death process for co- cies of Cristaria from the Atacama Desert. We ments and therefore unreliable age constraints. Soc. 181, 171–198. herent calibration of divergence-time estimates. PNAS ran two dating analyses in beast2, first with The analysis with four fossils gave good support Areces-Berazain & Ackerman 2017. Diversification and fruit 111, E2957-66. the fossilized-birth-death (FBD) process model and more relaible age estimates. The split bet- evolution in eumalvoids (Malvaceae). Bot. J. Linn. Soc. Kräusel 1939. Ergebnisse der Forschungsreisen Prof. E. Stro- and 18 fossil calibrations (Heath et al. 2014, ween Cristaria and Lecanophora probably took 184, 401–417. mers in den Wüusten Ägyptens, IV. Die fossilen Floren Areces-Berzein & Ackermann 2016, 2017) and a place during the early Miocene, while the radia- Carvalho et al. 2011. Paleocene Malvaceae from northern Ägyptens. Abh. Bay. Akad. der Wis. 47: 1–140. South America and their biogeographical implications. MacPhail & Truswell 1989. Palynostratigraphy of the central classic node calibration approach with four fos- tion ofCristaria took place within the last 2 Mio. Am. J. Bot. 98: 1337–1355. west Murray Basin. BMR J. Aust. Geol. Geop. 11: 301– sils (see table 1). years. 331. Funding This study was financed by the German Research Founda- tion (DFG) in the framework of the Collaborative Research Earth – Evolution Centre 1211 – Evolution at the dry limit (http://sfb1211. at the dry limit uni-koeln.de/).