Biogeography and Evolution of the Atacama Desert Flora
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Biogeography and Evolution of the Atacama Desert Flora Tim Böhnert 1 , Felix F. Merklinger 1 , Sonja Böker 1 , Dörte Harpke 2 , Alexandra Stoll 3 , Frank Blaner 2,4 , Maximilian Weigend 1 , Dietmar Quandt 1 , Federico Luebert 1,5, * 1 Nees Instute for Biodiversity of Plants, University of Bonn, Bonn, Germany. 2 Leibniz Instute of Plant Genecs and Crop Plant Research (IPK), Gatersleben, Germany. 3 Centro de Estudios Avanzados en Zonas Aridas, CEAZA, La Serena Chile. 4 German Centre for Integrave Biodiversity Research (iDiv) Halle-Jena-Leipzig, Germany. 5 Departamento de Silvicultura y Conservación de la Naturaleza, Universidad de Chile, Sanago, Chile. *fl[email protected] Context The Atacama Desert, located on the western side of the Andes in northern Chile, harbors a range of endemic species adapted to hyper- arid habitats. Vegetaon is largely restricted to coastal fog oases and the Andean foothills, which are separated by a largely vegetaon-free zone. In the context of a large-scale project on landscape and bioc evoluon of hyperarid environments, we invesgate the origin and diversificaon of three plant groups as well as gene-flow between populaons of four widely distributed plant taxa in the Atacama Desert. Diversificaons have been shown to be surpri- singly recent in some Atacama clades, which is at odds with the high age assumed for this desert. Here, we report the results of a mole- cular dang analysis of the Atacama endemic Cristaria (Malvaceae) based on three plasd markers. Furthermore, we present preliminary data on gene-flow among populaons of four species of Ophryosporus (Asteraceae) using Ge- notyping-By-Sequencing (GBS) data. References Areces-Berazain & Ackerman 2016. Phylogenecs, delimit- aon and historical biogeography of the pantropical tree genus Thespesia (Malvaceae, Gossypieae). Bot. J. Linn. Soc. 181, 171–198. Areces-Berazain & Ackerman 2017. Diversificaon and fruit evoluon in eumalvoids (Malvaceae). Bot. J. Linn. Soc. 184, 401–417. Carvalho et al. 2011. Paleocene Malvaceae from northern South America and their biogeographical implicaons. Am. J. Bot. 98: 1337–1355. Germeraad JH et al. 1968. Palynology of Terary sediments from tropical areas. Rev. Palaebot. Palyno. 6: 189–348. Heath et al. 2014. The fossilized birth-death process for co- herent calibraon of divergence-me esmates. PNAS 111, E2957-66. Kräusel 1939. Ergebnisse der Forschungsreisen Prof. E. Stro- mers in den Wüusten Ägyptens, IV. Die fossilen Floren Ägyptens. Abh. Bay. Akad. der Wis. 47: 1–140. MacPhail & Truswell 1989. Palynostragraphy of the central west Murray Basin. BMR J. Aust. Geol. Geop. 11: 301– 331. Funding This study was financed by the German Research Founda- on (DFG) in the framework of the Collaborave Research Centre 1211 – Evoluon at the dry limit (hp://s1211. uni-koeln.de/). Ophryosporus (Asteraceae) [F.F. Merklinger] Methods: Monophyly and realaonships of species of Ophryosporus from the Atacama Desert, with respect to Andean and E South Ame- rican taxa of the genus, were evaluated prior to the populaon genec analyses. A phylogenec analysis based on ITS sequence data was carri- ed out using a Bayesian approach in MrBayes. GBS data were generated on a Illumina HiSeq Sequencer at populaon level for four Atacama species and a phylogenec analysis of a conca- tenated SNP matrix was conducted. Cristaria (Malvaceae) [T. Böhnert] Methods: We used the molecular data set of Areces-Berzein and Ackermann (2017; ndhF, trnK/matK and rpl16), complemented with se- quences from 50 samples of Malveae from our own field collecons, including nearly all spe- cies of Cristaria from the Atacama Desert. We ran two dang analyses in beast2, first with the fossilized-birth-death (FBD) process model and 18 fossil calibraons (Heath et al. 2014, Areces-Berzein & Ackermann 2016, 2017) and a classic node calibraon approach with four fos- sils (see table 1). Results & Discussion: Phylogenec analysis with 333 samples across Malvoideae confirms the monophyly of Cristaria and the sister rela- on to Lecanophora. The FBD approach reveals very weak posterior propabilies for fossil place- ments and therefore unreliable age constraints. The analysis with four fossils gave good support and more relaible age esmates. The split bet- ween Cristaria and Lecanophora probably took place during the early Miocene, while the radia- on of Cristaria took place within the last 2 Mio. years. Conclusion & Outlook Divergence mes of Cristaria suggest that the split from Lacanophora predates the major phase of the Central Andean upliſt, but do not discard an East-West vicariant scenario. Diver- sificaon of Cristaria in the Atacama desert ap- pears to coincide with the onset of hyperaridity during the late Miocene and early Pliocene. The results in Ophryosporus suggest high genec connecvity among coastal species and among Andean species, but low connecvity between coastal and Andean species. The northern An- dean Atacama species appears to be more clo- sely related to the Central Andean species from Peru than to the other coastal Atacama species. In the context of this project, we are conducng addional phylogenec and dang analyses in the species-rich genera Atriplex (Amarantha- ceae) and Cryptantha (Boraginaceae), making use of Sanger and NGS sequencing approaches. Further populaon genec analyses are also being carried out in Eulychnia spp. (Cactaceae), Huidobria frucosa (Loasaceae), and Tillandsia landbeckii (Bromeliaceae), both with GBS and microsatellite data. 30 20 10 0 Quat. Oligocene Miocene Plioc. Mya Lecanophora ameghinoi Cristaria viridiluteola Cristaria dissecta Cristaria aspera Cristaria glaucophylla Cristaria ovata Cristaria cf. concinna Cristaria argyliifolia Cristaria gracilis Cristaria molinae C. viridiluteola var. pinnata Cristaria andicola C. aspera var. formosula Cristaria cyanea Cristaria gracilis Cristaria cf. aspera Cristaria calderana C. integerrima var. lobulata Cristaria mulfida Cristaria integerrima Cristaria cf. tenuissima Cristaria integerrima Cristaria integerrima Cristaria leucantha Cristaria concinna Cristaria integerrima Cristaria ovata Cristaria mulflora Lecanophora chubutensis Cristaria mulfida Cristaria diaziana Cristaria adenophora Cristaria andicola Cristaria molinae Cristaria glaucophylla Lecanophora heterophylla Cristaria cf. fuentesiana PP ≥ 0.95 PP 0.8 – 0.95 2.83 20.29 4.21 7.42 Gossypieae ca. 126 spp. | 65 Malveae ca. 1040 spp. | 165 ca. 639 spp. | 92 Hibisceae Eumalvoideae Core Malvoideae Plagianthus Lecanophora Cristaria Sidalcea Malvastrum Sphaeralcea Sphaeralcea Anisodontea Malva 21 spp. 5-6 spp. Abulon alliance alliance alliance I alliance II alliance alliance alliance alliance Fossil taxon Age [Mya] Clade Reference Hibiscoxylon nylocum 88 – 66 Core Malvoideae Kräusel (1939) Malvaciphyllum macondicus 60 – 58 Eumalvoideae Carvalho et al. (2011) Malvacearumpollis sp. 37 – 30 Malveae MacPhail & Truswell (1989) Echiperiporites estelae 45 – 34 Hibisceae Germeraad et al. (1968) 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 Malvoideae. 100 93 99 100 100 100 Ophryosporus cumingii Ophryosporus piquerioides 100 Ophryosporus piquerioides Ophryosporus anomalus Ophryosporus axilliflorus Ophryosporus freyreisii Ophryosporus heptanthus 100 Ophryosporus paradoxus Ophryosporus triangularis Ophryosporus triangularis Ophryosporus triangularis Ophryosporus triangularis Ophryosporus triangularis Ophryosporus triangularis Ophryosporus triangularis Ophryosporus triangularis Ophryosporus triangularis Ophryosporus johnstonii Ophryosporus johnstonii Ophryosporus johnstonii 99 Ophryosporus triangularis Ophryosporus triangularis 100 Ophryosporus paradoxus Ophryosporus paradoxus Ophryosporus paradoxus 100 99 Ophryosporus pinifolius Ophryosporus pinifolius Ophryosporus pinifolius Ophryosporus pinifolius Ophryosporus pinifolius Ophryosporus pinifolius Ophryosporus pinifolius Ophryosporus peruvianus Ophryosporus peruvianus Ophryosporus peruvianus Aristeguietia salvia Ageratina glechonophylla 100 58 65 72 74 100 99 82 64 51 58 75 73 90 100 O. peruvianus O. pinifolius O. floribundus O. johnstonii O. triangularis a. Bayesian analysis based on ITS. Coastal Ata- cama species Ophryosporus paradoxus, O. tri- angularis and O. johnstonii (green) form a mo- nophylec group. E South American species are retrieved as monophylum and are sister to the coastal Atacama species. The Andean species O. pinifolius (blue) is sister to O. peruvianus from Andean Peru. b. Maximum Likelihood tree based on 70,000 bp matrix. GBS data indicate that the Atacama species of Ophryosporus fall into two disnct clades, separated by fixed allele composions. Species form monophylec groups, albeit with weak support. However, our data also suggest that gene flow among species of each clade has taken place. Ophryosporus triangularis Cristaria leucantha Cristaria integerrima Cristaria dissecta Earth – Evolution at the dry limit ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● 15°S 20°S 25°S 30°S 35°S 40°S 76°W 72°W 68°W N 0 100 200 300 km ● ● O. paradoxus O. triangularis O. floribundus O. johnstonii O. pinifolius a b
Transcript of Biogeography and Evolution of the Atacama Desert Flora
Biogeography and Evolution of the Atacama Desert FloraTim 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 Plants, University of Bonn, Bonn, Germany. 2Leibniz Institute of Plant 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]
ContextThe Atacama Desert, located on the western side of the Andes in northern Chile, harbors a range of endemic species adapted to hyper- arid habitats. Vegetation is largely restricted to coastal fog oases and the Andean foothills, which are separated by a largely vegetation-free zone. In the context of a large-scale project on landscape and biotic evolution of hyperarid environments, we investigate the origin and diversification of three plant groups as well as gene-flow between populations of four widely
distributed plant taxa in the Atacama Desert. Diversifications have been shown to be surpri-singly recent in some Atacama clades, which is at odds with the high age assumed for this desert. Here, we report the results of a mole-cular dating analysis of the Atacama endemic Cristaria (Malvaceae) based on three plastid markers. Furthermore, we present preliminary data on gene-flow among populations of four species of Ophryosporus (Asteraceae) using Ge-notyping-By-Sequencing (GBS) data.
ReferencesAreces-Berazain & Ackerman 2016. Phylogenetics, delimit-
ation and historical biogeography of the pantropical tree genus Thespesia (Malvaceae, Gossypieae). Bot. J. Linn. Soc. 181, 171–198.
Areces-Berazain & Ackerman 2017. Diversification and fruit evolution in eumalvoids (Malvaceae). Bot. J. Linn. Soc. 184, 401–417.
Carvalho et al. 2011. Paleocene Malvaceae from northern South America and their biogeographical implications. Am. J. Bot. 98: 1337–1355.
Germeraad JH et al. 1968. Palynology of Tertiary sediments from tropical areas. Rev. Palaebot. Palyno. 6: 189–348.
Heath et al. 2014. The fossilized birth-death process for co-herent calibration of divergence-time estimates. PNAS 111, E2957-66.
Kräusel 1939. Ergebnisse der Forschungsreisen Prof. E. Stro-mers in den Wüusten Ägyptens, IV. Die fossilen Floren Ägyptens. Abh. Bay. Akad. der Wis. 47: 1–140.
MacPhail & Truswell 1989. Palynostratigraphy of the central west Murray Basin. BMR J. Aust. Geol. Geop. 11: 301–331.
FundingThis study was financed by the German Research Founda-tion (DFG) in the framework of the Collaborative Research Centre 1211 – Evolution at the dry limit (http://sfb1211.uni-koeln.de/).
Ophryosporus (Asteraceae) [F.F. Merklinger]
Methods: Monophyly and realationships of species of Ophryosporus from the Atacama Desert, with respect to Andean and E South Ame-rican taxa of the genus, were evaluated prior to the population genetic analyses. A phylogenetic analysis based on ITS sequence data was carri-ed out using a Bayesian approach in MrBayes. GBS data were generated on a Illumina HiSeq Sequencer at population level for four Atacama species and a phylogenetic analysis of a conca-tenated SNP matrix was conducted.
Cristaria (Malvaceae) [T. Böhnert]
Methods: We used the molecular data set of Areces-Berzein and Ackermann (2017; ndhF, trnK/matK and rpl16), complemented with se-quences from 50 samples of Malveae from our own field collections, including nearly all spe-cies of Cristaria from the Atacama Desert. We ran two dating analyses in beast2, first with the fossilized-birth-death (FBD) process model and 18 fossil calibrations (Heath et al. 2014, Areces-Berzein & Ackermann 2016, 2017) and a classic node calibration approach with four fos-sils (see table 1).
Results & Discussion: Phylogenetic analysis with 333 samples across Malvoideae confirms the monophyly of Cristaria and the sister rela-tion to Lecanophora. The FBD approach reveals very weak posterior propabilities for fossil place-ments and therefore unreliable age constraints. The analysis with four fossils gave good support and more relaible age estimates. The split bet-ween Cristaria and Lecanophora probably took place during the early Miocene, while the radia-tion of Cristaria took place within the last 2 Mio. years.
Conclusion & OutlookDivergence times of Cristaria suggest that the split from Lacanophora predates the major phase of the Central Andean uplift, but do not discard an East-West vicariant scenario. Diver-sification of Cristaria in the Atacama desert ap-pears to coincide with the onset of hyperaridity during the late Miocene and early Pliocene. The results in Ophryosporus suggest high genetic connectivity among coastal species and among Andean species, but low connectivity between coastal and Andean species. The northern An-dean Atacama species appears to be more clo-
sely related to the Central Andean species from Peru than to the other coastal Atacama species.In the context of this project, we are conducting additional phylogenetic and dating analyses in the species-rich genera Atriplex (Amarantha-ceae) and Cryptantha (Boraginaceae), making use of Sanger and NGS sequencing approaches. Further population genetic analyses are also being carried out in Eulychnia spp. (Cactaceae), Huidobria fruticosa (Loasaceae), and Tillandsia landbeckii (Bromeliaceae), both with GBS and microsatellite data.
30 20 10 0
Quat.Oligocene Miocene Plioc.
Mya
Lecanophora ameghinoi
Cristaria viridiluteola
Cristaria dissecta
Cristaria aspera
Cristaria glaucophylla
Cristaria ovata
Cristaria cf. concinna
Cristaria argyliifolia
Cristaria gracilisCristaria molinaeC. viridiluteola var. pinnata
Cristaria andicola
C. aspera var. formosula
Cristaria cyaneaCristaria gracilis
Cristaria cf. aspera
Cristaria calderana
C. integerrima var. lobulata
Cristaria multifida
Cristaria integerrima
Cristaria cf. tenuissima
Cristaria integerrima
Cristaria integerrima
Cristaria leucantha
Cristaria concinna
Cristaria integerrima
Cristaria ovata
Cristaria multiflora
Lecanophora chubutensis
Cristaria multifida
Cristaria diaziana
Cristaria adenophora
Cristaria andicola
Cristaria molinae
Cristaria glaucophylla
Lecanophora heterophylla
Cristaria cf. fuentesiana
PP ≥ 0.95PP 0.8 – 0.95
2.83
20.29
4.21
7.42
Gossypieaeca. 126 spp. | 65
Malveaeca. 1040 spp. | 165
ca. 639 spp. | 92Hibisceae
Eum
alvo
idea
e
Core
Mal
void
eae
Plagianthus
Lecanophora
Cristaria
Sidalcea
Malvastrum
Sphaeralcea
Sphaeralcea
Anisodontea
Malva
21 spp.
5-6 spp.
Abutilon
alliance
alliance
alliance I
alliance II
alliance
alliance
alliance
alliance
Fossil taxon Age [Mya] Clade Reference
Hibiscoxylon nyloticum 88 – 66 Core Malvoideae Kräusel (1939)
Malvaciphyllum macondicus 60 – 58 Eumalvoideae Carvalho et al. (2011)
Malvacearumpollis sp. 37 – 30 Malveae MacPhail & Truswell (1989)
Echiperiporites estelae 45 – 34 Hibisceae Germeraad et al. (1968)
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 Malvoideae.
100
93
99100
100
100 Ophryosporus cumingiiOphryosporus piquerioides
100 Ophryosporus piquerioidesOphryosporus anomalusOphryosporus axilliflorusOphryosporus freyreisiiOphryosporus heptanthus
100
Ophryosporus paradoxusOphryosporus triangularisOphryosporus triangularisOphryosporus triangularisOphryosporus triangularisOphryosporus triangularisOphryosporus triangularisOphryosporus triangularisOphryosporus triangularisOphryosporus triangularisOphryosporus johnstoniiOphryosporus johnstoniiOphryosporus johnstonii
99 Ophryosporus triangularisOphryosporus triangularis
100Ophryosporus paradoxusOphryosporus paradoxusOphryosporus paradoxus
100
99
Ophryosporus pinifoliusOphryosporus pinifoliusOphryosporus pinifoliusOphryosporus pinifoliusOphryosporus pinifoliusOphryosporus pinifoliusOphryosporus pinifoliusOphryosporus peruvianusOphryosporus peruvianusOphryosporus peruvianusAristeguietia salviaAgeratina glechonophylla
100
58
65
7274
10099
82
6451
5875
73
90
100 O. peruvianus
O. pinifolius
O. floribundus
O. johnstonii
O. triangularis
a. Bayesian analysis based on ITS. Coastal Ata-cama species Ophryosporus paradoxus, O. tri-angularis and O. johnstonii (green) form a mo-nophyletic group. E South American species are retrieved as monophylum and are sister to the coastal Atacama species. The Andean species O. pinifolius (blue) is sister to O. peruvianus from Andean Peru.
b. Maximum Likelihood tree based on 70,000 bp matrix. GBS data indicate that the Atacama species of Ophryosporus fall into two distinct clades, separated by fixed allele compositions. Species form monophyletic groups, albeit with weak support. However, our data also suggest that gene flow among species of each clade has taken place.
Ophryosporus triangularis
Cristaria leucantha Cristaria integerrima Cristaria dissecta
Earth – Evolutiona t t h e d r y l i m i t
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15°S
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25°S
30°S
35°S
40°S76°W 72°W 68°W
N
0 100 200 300 km
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O. paradoxus O. triangularis O. floribundus O. johnstonii O. pinifolius
a b
