Abstract
Analyzing the roles of ecology and geography on speciation and lineage diversification can shed light on the processes that generate and maintain biodiversity. Additionally, lineages rapidly diversifying across unstable habitats provide substantial challenges for resolving evolutionary histories and delimiting species. Physaria is represented in South American by six species distributed from southern Bolivia to northern central Argentina and growing in highlands of the southern-central Andes, but also along the hills and lowlands of central-eastern Argentina. This biogeographical variability, not common among other South American crucifers (Brassicaceae), prompted us to conduct different climatic niche and geographical range comparisons to study the potential roles of ecology and geography through the diversification of the group. However, the remarkable similarity between these species, coupled with the continuous variability of the diagnostic morphological characters, blurs the species boundaries. Therefore, in order to identify independent evolving lineages, we first employed species delimitation methods together with the general lineage concept of species, and used molecular sequences from nuclear ribosomal and chloroplast loci. Secondly, and in the light of the lineages obtained, we explored the roles of geography and ecology on the diversification of South American Physaria and tested for presence of phylogenetic niche-conservatism or niche-divergence patterns, as well as potential ecological speciation. Lineages identified by these delimitation methods were highly congruent with described species; nevertheless, some morphospecies were included under the same independent evolutionary lineage. Our results suggest that the climatic niche divergence along the heterogeneous landscape apparently was a major factor promoting diversification of the South American Physaria. Divergence was registered mainly on the temperature dimension, which promoted shifts between cold-temperate habitats associated with the highlands of the central-southern Andes and warm lowlands from central-eastern Argentina, i.e., the Monte and Dry Chaco ecoregions. In addition, some degree of niche divergence along the precipitation gradient was also secondarily recovered. Allopatry and dispersal capabilities also seem to be associated with the diversification of the group, presumably through the Late Pliocene-Pleistocene, and promoted by glacial cycles and climatic oscillations during the Quaternary. Results of these analyses are also discussed in a general context, which will contribute to the understanding of the evolutionary and ecological patterns of South American Brassicaceae.
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Data availability
Data generated or analyzed in this paper are included in the electronic supplementary material, the TreeBase repository (http://purl.org/phylo/treebase/phylows/study/TB2:S26615), and the Figshare repository (https://doi.org/10.6084/m9.figshare.12645218). New DNA sequences generated for this study are available in the GenBank repository (see corresponding GenBank numbers and vouchers in Appendix 1).
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Acknowledgements
Our deep gratitude goes to Dr. Ihsan A. Al-Shehbaz for the critical review of this work and his valuable support, guidance, and suggestions in the study of South American Brassicaceae over the years. We thank the directors, curators, and collection managers of the herbaria listed. Special thanks are to Lone Aagesen, Juan M. Acosta, and Ariel Lliully Aguilar for their help in the fieldtrips. We especially appreciate the help of editors and two anonymous reviewers who provided useful suggestions to improve the early version of this paper. Botanical collections associated to this project were conducted under the permits: APN No. 1103 and 1546 (Argentina) and VMABCC No. 026/09 (Bolivia).
Funding
This work was funded by ANPCyT (Agencia Nacional de Promoción Científica y Tecnológica) grant PICT-2016-0096, CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas) grant PIP-112-201301-00124CO, and the National Geographic Society grant #9841-16, for which we are profoundly grateful.
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Fig. S1
Maximum likelihood tree generated with nrITS sequences and RAxML 8.2.10 showing the monophyly of South American Physaria. Values on branches correspond to Bootstrap support ≥ 50%. Units of branch length are proportional to nucleotide substitutions per site. (PDF 256 kb)
Fig. S2
Distribution map of South American Physaria and delimited area corresponding to the 50 km1423 buffered minimum convex polygon (study area) used in the niche analyses and geographic range comparisons. (PDF 1266 kb)
Fig. S3
Maximum likelihood trees generated with RAxML 8.2.10 showing the phylogenetic placement of sampled specimens of South American Physaria. a, nrITS dataset. b, cpDNA dataset (trnL-F/trnH-psbA/trnG intron/trnS-trnG). c, concatenated nrITS+cpDNA dataset. Values on branches correspond to Bootstrap support ≥ 50%. Units of branch length are proportional to nucleotide substitutions per site. Boxes to the rigth show delimited lineages. For tip labels: CRA, P. crassistigma, LAT, P. lateralis; MEN, P. mendocina; OKA, P. okanensis; PYG, P. pygmaea; URB: P. urbaniana. Image: Flower and fruit of P. mendocina (PDF 793 kb)
Fig. S4
Maximum clade credibility trees obtained from the analyses with MrBayes 3.2.6 showing the phylogenetic placement of sampled specimens of South American Physaria. a, nrITS dataset. b, cpDNA dataset (trnL-F/trnH-psbA/trnG intron/trnS-trnG). c, concatenated n rITS+cpDNA dataset. Circles on branches correspond to posterior probabilities (PP) ≥ 50%. Units of branch length are proportional to nucleotide substitutions per site. Boxes to the rigth show delimited lineages. For tip labels: CRA, P. crassistigma, LAT, P. lateralis; MEN, P. mendocina; OKA, P. okanensis; PYG, P. pygmaea; URB: P. urbaniana. Image: flower and fruit of P. crassistigma. (PDF 937 kb)
Fig. S5
Phylogenetic placement of sampled specimens of South American Physaria. a, Primary concordance tree from the BUCKy analyses using the 6002 trees from the nrITS and the cpDNA datasets obtained in the MrBayes analyses and under α = 1. Concordance factor values (CF) ≥ 0.5 are shown on branches. Units of branch length are proportional to the concordance factor. Results from concordance analyses varying the discordance prior (α) had no effect on topology or concordance. Stars on nodes indicate delimited lineages of South American Physaria. b, filtered supernetwork generated in SplitsTree 4.14.8 using 1000 Bayesian posterior trees per each nrITS and cpDNA dataset with the Z-closure algorithm, and filtering the splits to show only those present in a minimum of 30% input trees. Shades groups represent delimited lineages. (PDF 537 kb)
Fig. S6
Results from the climatic niche analyses in the environmental space obtained using the PCA env method. a–c, Correlation circles showing the contribution of environmental variables on the first three axes of the PCA-env and the percentage of inertia explained. a, PC1 vs PC2. b, PC1 vs PC3. c, PC2 vs PC3. d, Bar plot from the broken-stick analysis. PCA-env axes with larger percentages of accumulated inertia than the broken-stick variances are significant (three in this case). (PDF 31 kb)
Fig. S7
Univariate climatic niche comparisons in the environmental space among delimited lineages of South American Physaria. a, density plots computed for each independently evolving lineage using the PCenv1, PCenv2, PCenv3, elevation, annual mean temperature (BIO1), and annual mean precipitation (BIO12). b, p-values from Kruskal-Wallis test together with the Bonferroni correction for multiple comparisons to assess for differences between Physaria lineages for the three first PCs, elevation, BIO1, and BIO12. Values marked with an asterisk (red cells) are rejected at α=0.05. Labels: CRA, crassistigma lineage; NLA, northern lateralis lineage; SLA, southern lateralis lineage; MEN, mendocina lineage; URB, urbaniana lineage; YUN, yungas lineage. (PDF 645 kb)
Fig. S8
Geographic range overlap of delimited lineages of South American Physaria for the present time. Binary (presence/absence) distributions maps for delimited lineages derived from the species distribution modelling (SDM) in MaxEnt using the maximum training sensitivity plus specificity as threshold. Blue and green cells indicate presence of only one lineage, while red cells indicate presence of both species (sympatric cells). (PDF 1635 kb)
Fig. S9
Geographic range overlap of delimited lineages of South American Physaria for the Last Glacial Maximum (LGM) (~ 21 kya). Binary (presence/absence) distributions maps for delimited lineages derived from the species distribution modelling (SDM) in MaxEnt using the maximum training sensitivity plus specificity as threshold. Blue and green cells indicate presence of only one lineage, while red cells indicate presence of both species (sympatric cells). (PDF 2255 kb)
Table S1
(DOCX 13 kb)
Table S2
(DOCX 5 kb)
Table S3
(DOCX 10 kb)
Table S4
(DOCX 11 kb)
ESM 14
ITS alignment for the South American Physaria dataset used for phylogenetic analyses in this study. (NEX 32 kb)
ESM 15
trnL-F alignment for the South American Physaria dataset used for phylogenetic analyses in this study. (NEX 39 kb)
ESM 16
trnH-psbA alignment for the South American Physaria dataset used for phylogenetic analyses in this study. (NEX 15 kb)
ESM 17
trnG intron alignment for the South American Physaria dataset used for phylogenetic analyses in this study. (NEX 31 kb)
ESM 18
trnS-trnG alignment for the South American Physaria dataset used for phylogenetic analyses in this study. (NEX 26 kb)
Appendix 1
Appendix 1
Taxa and GenBank accession numbers for the ITS, trnH-psbA , trnL-F, trnG intron, and trnS-trnG sequences used in the molecular analyses.
Physaria fendleri (A. Gray) O'Kane & Al-Shehbaz (outgroup) (AF055198, -, AF055266, -). Physaria crassistigma O'Kane & Al-Shehbaz. ARGENTINA. Mendoza. Las Heras: Above Villavicencio on road to Paramillo de Uspallata, roadside, open areas among shrubs, ca. 44 km before Uspallata, Al-Shehbaz et al. 808 (SI) (CRA6) (MW366047, MW366135, MW366090, MW366180, MW366223). Luján de Cuyo: Centro de Ski Vallecitos, ladera derecha de cerros subiendo por la pista de ski, Salariato et al. 252 (SI) (CRA3) (MW366023, MW366110, MW366068, MW366157, MW366201). Tunuyán: RP94, Camino al Portillo Argentino, 0.5 km de las Llaretas desde el puesto de gendarmeria hacia el portillo, Salariato et al. 207 (SI) (CRA1) (MW366021, MW366108, MW366066, MW366155, MW366199); camino del Portillo Argentino, desde Las Llaretas hacia el hotel abandonado, ca. 3 km del desvío a Valle de Manantiales, Salariato et al. 233 (SI) (CRA2) (MW366022, MW366109, MW366067, MW366156, MW366200); Ruta Provincial 94 de Manzano Histórico a Portillo Argentino, Zuloaga et al. 5292 (SI) (CRA5) (MW366040, MW366128, MW366083, MW366173, MW366216). Tupungato: Ruta provincial n° 94: entre Los Manantiales y Real de Piedras Coloradas, Cocucci & Sérsic 2253 (CORD, SI) (CRA4) (MW366037, MW366125, MW366080, MW366170, MW366214). Physaria lateralis O'Kane & Al-Shehbaz. ARGENTINA. Mendoza. Las Heras: Ruta Provincial 13, alrededor de Monolito, Giussani et al. 602 (SI) (LAT8) (MW366048, MW366137, MW366092, MW366182, MW366225). Malargüe: Base del Cerro Nevado por Ruta Prov. 180, Prina et al. 2630 (SI) (LAT6) (MW366038, MW366126, MW366081, MW366171, -). San Carlos: Refugio militar Gral. Alvarado, entrada a la Reserva Laguna del Diamante, Al-Shehbaz et al. 813 (SI) (LAT10) (MW366050, MW366139, -, MW366184, MW366226). San Rafael: Cerro Nevado, Prina, et al. 2917 (SRFA, SI) (LAT5) (MW366036, MW366124, MW366079, MW366169, -); de Termas del Sosneado a Laguna El Sosneado, Zuloaga et al. 12408 (SI) (LAT9) (MW366049, MW366138, MW366093, MW366183, -); Ruta Nacional 144, cuesta de los Terneros hacia 25 de Mayo, Zuloaga et al. 15277 (SI) (LAT11) (MW366042, MW366130, MW366085, MW366175, MW366218). San Luis. Coronel Pringles: Ruta Provincial 9, entre Trapiche y La Carolina, Aagensen 26 (SI) (LAT1) (MW366015, MW366102, MW366060, MW366149, MW366193); Ruta provincial 9, Monumento y Museo Lafinur, pasando La Carolina, Biganzoli 2034 (SI) (LAT7) (MW366039, MW366127, MW366082, MW366172, MW366215); Alrededores de la Gruta de Intihuasi, Cerana 1266 (CORD) (LAT4) (MW366033, MW366121, MW366076, MW366166, MW366211); Camino a San Francisco 10-15 km de La Carolina, Cerana 1330 (CORD) (LAT3) (MW366028, MW366115, -, -, -); Cañada Honda, Cerana 1360 (CORD) (LAT2) (MW366027, MW366114, -, MW366161, MW366205). Physaria mendocina (Phil.) O'Kane & Al-Shehbaz. ARGENTINA. Córdoba. Calamuchita: San Agustin (Cerro La Cruz), Cantero 6107 (CORD) (MEN4) (MW366020, MW366107, MW366065, MW366154, MW366198). Colón: Candonga, Cantero 5897 (CORD) (MEN8) (MW366029, MW366116, MW366072, MW366162, MW366206). Punilla: Quilpo (Canteras), Cantero 5928 (CORD) (MEN7) (MW366026, MW366113, MW366071, MW366160, MW366204); Valle Hermoso, Cantero 6039 (CORD) (MEN6) (MW366025, MW366112, MW366070, MW366159, MW366203). Rio Cuarto: Alta Gracia, Cantero 5834 (CORD) (MEN9) (MW366030, MW366117, MW366073, MW366163, MW366207); Achiras (Monte Guazú), Cantero 6291 (CORD) (MEN3) (MW366019, MW366106, MW366064, MW366153, MW366197); Cuchi Yaco (Cerca Salsacate), Cantero 5656 (CORD) (MEN10) (MW366031, MW366118, MW366074, MW366164, MW366208); El Saucesito, Cantero 5565 (CORD) (MEN11) (MW366032, MW366119, MW366075, MW366165, MW366209); Iguazu, Cantero 5550 (CORD) (MEN2) (MW366018, MW366105, MW366063, MW366152, MW366196); Mesa de la Argentina, Cantero 5636 (CORD) (MEN5) (MW366024, MW366111, MW366069, MW366158, MW366202). La Pampa. Lihué Calel: Parque Nacional Lihue Calel, camino interior hacia cerros más bajos y pinturas rupestres, Zuloaga & Salariato 16073 (SI) (MEN1) (MW366016, MW366103, MW366061, MW366150, MW366194). Mendoza. Las Heras: de la RN 14 hacia los Berros, RN 153, Zuloaga et al. 15741 (SI) (MEN14) (-, MW366136, MW366091, MW366181, MW366224). Tunuyán: Manzano Histórico, Deginani et al. 2173 (SI) (MEN16) (MW366043, MW366131, MW366086, MW366176, MW366219). Tupungato: Bajando del Cerro Cristo Rey, Deginani et al. 2295 (SI) (MEN15) (MW366052, MW366141, MW366095, MW366186, MW366228). Río Negro. Valcheta: En km 50, cerros basálticos, Kiesling 9923 (SI) (MEN13) (MW366035, MW366123, MW366078, MW366168, MW366213). San Juan. Angaco: Pie de Palo, Kiesling et al. 9384 (SI) (MEN12) (MW366034, MW366122, MW366077, MW366167, MW366212). Physaria okanensis Al-Shehbaz & Prina. ARGENTINA. Catamarca. Ambato: al norte de cumbres de cerro el manchao, Halloy 809 (LIL) (OKA2) (-, MW366120, -, -, MW366210); subiendo hacia el manchao desde el rodeo, en el sitio Falda del Momo, Cantero et al. 7254 (CORD) (OKA1) (MW366017, MW366104, MW366062, MW366151, MW366195). Physaria pygmaea O'Kane & Al-Shehbaz. ARGENTINA. Catamarca. Andalgalá: Capillitas, alrededores del globo meteorológico, Acosta & von Mering 624 (SI) (PYG1) (MW366055, MW366144, MW366098, MW366189, MW366231); cerca de Mina Capillitas. subida al globo meteorológico, Salomón et al. 234 (SI) (PYG3) (MW366044, MW366132, MW366087, MW366177, MW366220). Jujuy. Humahuaca: Mina Aguilar, Espinazo del Diablo, Zuloaga et al. 13572 (SI) (PYG4) (MW366046, MW366134, MW366089, MW366179, MW366222). La Rioja. Famatina: Pampa de Tambería, Barboza et al. 3359 (CORD) (PYG2) (MW366058, MW366147, -, MW366191, MW366234). Physaria urbaniana (Muschl.) O'Kane & Al-Shehbaz. ARGENTINA. La Rioja. Famatina: Entre la bifurcación hacia Tres Piedras y Los Tambitos, Barboza et al. 2875 (CORD) (URB4) (MW366057, MW366146, MW366100, MW366190, MW366233); Pampa de Achavil, pasando el Río Achavil rumbo a Tres Piedras, en la pampa del "Ajenjo", Barboza et al. 2854 (CORD) (URB3) (MW366056, MW366145, MW366099, -, MW366232). Salta. Cachi: Cuesta de obispo, 200 mts pasando piedra del Molino, Zuloaga et al. 12956 (SI) (URB6) (MW366041, MW366129, MW366084, MW366174, MW366217). Cachi: Parque Nacional Los Cardones, pasando el Cerro Negro o Malacanta. en curso de agua, Zanotti et al. 787 (SI) (URB2) (MW366053, MW366142, MW366096, MW366187, MW366229); RP 33, Cuesta del Obispo, Zanotti et al. 800 (SI) (URB1) (MW366051, MW366140, MW366094, MW366185, MW366227); RP 33, Cuesta del Obispo, Piedra del Molino, Acosta & von Mering 607 (SI) (URB7) (MW366054, MW366143, MW366097, MW366188, MW366230). Tucumán. Tafí: RP 307, Abra el Infiernillo, Zanotti et al. 860 (SI) (URB8) (MW366045, MW366133, MW366088, MW366178, MW366221). BOLIVIA. Tarija. Yunchara: al S. de Copacabana, Beck et al. 23756 (LPB) (URB5) (MW366059, MW366148, MW366101, MW366192, MW366235).
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Salariato, D.L., Zuloaga, F.O. Ecological and spatial patterns associated with diversification of South American Physaria (Brassicaceae) through the general concept of species. Org Divers Evol 21, 161–188 (2021). https://doi.org/10.1007/s13127-021-00486-z
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DOI: https://doi.org/10.1007/s13127-021-00486-z