Bryan T. DREW, Cara TARULLO, Jeffrey P. ROSE, Kenneth J. SYTSMA

Using a supermatrix approach to explore phylogenetic relationships, divergence times, and historical biogeography of Saxifragales

The Saxifragales is a morphologically and ecologically diverse clade of flowering plants with a cosmopolitan distribution. Although families and genera within the order exhibit classic biogeographical disjunctions, no studies to date have rigorously examined and described its historical biogeography. Here, we analyze the historical biogeography of Saxifragales by first generating a new chronogram for the order using a supermatrix approach, based on 61 loci from 251 representative members of Saxifragales. Our results suggest that Saxifragales originated in the early Albian approximately 107 Ma and diversified rapidly in the next 15 Ma, with all stem lineages of extant families present by the Campanian at approximately 75 Ma. The ancestral geographic range of the order is unclear, but ancestral range reconstructions point to an East Asian origin as the most tenable hypothesis. Ancestral ranges of the Haloragaceae/Crassulaceae clade suggest a strong signal for an Australasia origin for all families, and Saxifragaceae shows strong signal for bidirectional movement across the Asian-Alaskan land bridge during the Upper Cretaceous. Disjunct distributions are best explained by long-distance dispersal rather than vicariance, but we demonstrate that timing and directionality within particular disjunctions are similar within Saxifragales and consistent with results from distantly related angiosperm clades.

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Angiosperm Phylogeny Group (APG) IV (2016). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society. 181: 1-20.
Barker NP, Weston PH, Rutschmann F, Sauquet H (2007). Molecular dating of the ‘Gondwanan’plant family Proteaceae is only partially congruent with the timing of the break-up of Gondwana. Journal of Biogeography. 34: 2012-2027.
Bellot S, Cusimano N, Luo S, Sun G, Zarre S et al. (2016). Assembled plastid and mitochondrial genomes, as well as nuclear genes, place the parasite family Cynomoriaceae in the Saxifragales. Genome Biology and Evolution. 8: 2214-2230.
Berger BA, Kriebel R, Spalink D, Sytsma KJ (2016). Divergence times, historical biogeography, and shifts in speciation rates of Myrtales. Molecular Phylogenetics and Evolution. 95: 116- 136.
Brockington SF, Alexandre R, Ramdial J, Moore MJ, Crawley et al. (2009). Phylogeny of the Caryophyllales sensu lato: Revisiting hypotheses on pollination biology and perianth differentiation in the core Caryophyllales. International Journal of Plant Sciences. 170: 627-643.
Buerki, S, Forest, F, Alvarez N, Nylander JAA, Arrigo N et al. (2011). An evaluation of new parsimony-based versus parametric inference methods in biogeography: a case study using the globally distributed plant family Sapindaceae Journal of Biogeography. 38: 531-550.
Cardinal-McTeague WM, Sytsma KJ, Hall JC (2016). Biogeography and diversification of Brassicales: a 103 million year chronicle. Molecular Phylogenetics and Evolution. 99: 204-224.
Carrillo-Reyes P, Sosa V, Mort ME (2009). Molecular phylogeny of the Acre clade (Crassulaceae): Dealing with the lack of definitions for Echeveria and Sedum. Molecular Phylogenetics and Evolution. 53: 267-276.
Chen LY, Zhao SY, Mao KS, Les DH, Wang QF et al. (2014). Historical biogeography of Haloragaceae: An out-of-Australia hypothesis with multiple intercontinental dispersals. Molecular Phylogenetics and Evolution. 78: 87-95.
Clayton JW, Soltis PS, Soltis DE (2009). Recent long-distance dispersal overshadows ancient biogeographical patterns in a pantropical angiosperm family (Simaroubaceae, Sapindales). Systematic Biology. 58: 395-410.
Cohen KM, Harper DA, Gibbard PL, Fan JX. (2019). ICS international Chronostratigraphic chart 2019/05.
Cuénoud P, Savolainen V, Chatrou LW, Powell M, Grayer RJ et al. (2002). Molecular phylogenetics of Caryophyllales based on nuclear 18S rDNA and plastid rbcL, atpB, and matK DNA sequences. American Journal of Botany. 89: 132-144.
Darriba D, Taboada, GL, Doallo, R, Posada D (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods. 9: 772-772.
Darwin CR (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray, London, England.
Davis CC, Chase MW (2004). Elatinaceae are sister to Malpighiaceae; Peridiscaceae belong to Saxifragales. American Journal of Botany. 91: 262-273.
Deng JB, Drew BT, Mavrodiev EV, Gitzendanner MA, Soltis PS et al. (2015). Phylogeny, divergence times and historical biogeography of the angiosperm family Saxifragaceae. Molecular Phylogenetics and Evolution. 83: 86-98.
Donoghue MJ, Smith SA (2004). Patterns in the assembly of temperate forests around the Northern Hemisphere. Proceedings of the Royal Society of London. Series B: Biological Sciences. 359: 1633-644.
Drew BT, Liu S, Bonifacino JM, Sytsma KJ (2017). Amphitropical disjunctions in New World Menthinae: Three Pliocene dispersals to South America following late Miocene dispersal to North America from the Old World. American Journal of Botany. 104: 1695-1707.
Drummond AJ, Rambaut A (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology. 7: 214.
Drummond AJ, Suchard MA, Xie D Rambaut A (2012). Bayesian phylogenetics with BEAUti and the BEAST 17. Molecular Biology and Evolution. 29: 1969-1973.
Dupin J, Matzke NJ, Särkinen T, Knapp S, Olmstead RG et al. (2017). Bayesian estimation of the global biogeographical history of the Solanaceae. Journal of Biogeography. 44: 887-899.
Fishbein M, Hibsch-Jetter C, Soltis DE, Hufford L (2001). Phylogeny of Saxifragales (angiosperm, eudicots): Analysis of a rapid, ancient radiation. Systematic Biology. 50: 814-847.
Fishbein M, Soltis DE (2004). Further resolution of the rapid radiation of Saxifragales (angiosperm, eudicots) supported by mixed model Bayesian analysis. Systematic Botany. 29: 883- 891.
Folk RA, Stubbs RL, Mort ME, Cellinese N, Allen JM et al. (2019). Rates of niche and phenotype evolution lag behind diversification in a temperate radiation. Proceedings of the National Academy of Sciences USA. 116: 10874-10882.
Folk RA, Stubbs RL, Engle-Wrye NJ, Soltis DE, Okuyama Y (2021). Biogeography and habitat evolution of Saxifragaceae, with a revision of generic limits and a new tribal system. Taxon. 70: 263-85.
Givnish TJ, Millam KC, Evans TM, Hall JC, Pires JC et al. (2004). Ancient vicariance or recent long-distance dispersal? Inferences about phylogeny and South American-African disjunctions in Rapateaceae and Bromeliaceae based on ndhF sequence data. International Journal of Plant Sciences. 165: 35-54.
Graham A (2011). The age and diversification of terrestrial New World ecosystems through Cretaceous and Cenozoic time. American Journal of Botany. 98: 336-351.
Hermsen EJ, Gandolfo MA, Nixon KC, Crepet WL (2006). The impact of extinct taxa on understanding the early evolution of angiosperm clades: an example incorporating fossil reproductive structures of Saxifragales. Plant Systematics and Evolution. 260: 141-169.
Hermsen EJ (2013). A review of the fossil record of the genus Itea (Iteaceae, Saxifragales) with comments on its historical biogeography. The Botanical Review. 79: 1-47.
Hoot SB, Magallon S, Crane PR (1999). Phylogeny of basal eudicots based on three molecular data sets: atpB, rbcL, and 18S nuclear ribosomal DNA sequences. Annals of the Missouri Botanical Garden. 86: 1-32.
Ickert-Bond SM, Wen J (2006). Phylogeny and biogeography of Altingiaceae: evidence from combined analysis of five noncoding chloroplast regions. Molecular Phylogenetics and Evolution. 39: 512-528.
Jian S, Soltis PS, Gitzendanner MA, Moore MJ, Li R et al. (2008). Resolving an ancient, rapid radiation in Saxifragales. Systematic Biology. 57: 38-57.
Klaus KV, Matzke NJ (2019). Statistical comparison of traitdependent biogeographical models indicates that Podocarpaceae dispersal is influenced by both seed cone traits and geographical distance. Systematic Biology. 69: 61-75.
Liu XQ, Ickert-Bond SM, Chen LQ, Wen J (2013). Molecular phylogeny of Cissus L of Vitaceae (the grape family) and evolution of its pantropical intercontinental disjunctions. Molecular Phylogenetics and Evolution. 66, 43- 53
Maddison WP, Maddison DR (2019). Mesquite: a modular system for evolutionary analysis Version 3.61 http:// wwwmesquiteprojectorg
Magallón S, Crane PR, Herendeen PS (1999). Phylogenetic pattern, diversity and diversification of eudicots. Annals of the Missouri Botanical Garden. 86: 297-372.
Magallón S, Gómez-Acevedo S, Sánchez-Reyes LL, HernándezHernández T (2015). A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist. 207: 437-453.
Maldonado C, Molina CI, Zizka A, Persson C, Taylor CM et al. (2015). Estimating species diversity and distribution in the era of Big Data: to what extent can we trust public databases? Global Ecology and Biogeography. 24: 973-984.
Manchester, SR, Kapgate, DK and Wen, J (2013). Oldest fruits of the grape family (Vitaceae) from the Late Cretaceous Deccan Cherts of India. American Journal of Botany. 100: 1849-1859.
Matasci, N, Hung, LH, Yan, Z, Carpenter, EJ, Wickett, NJ, Mirarab, S, Nguyen, N, Warnow, T, Ayyampalayam, S, Barker, M, Burleigh, JG, 2014 Data access for the 1,000 Plants (1KP) project. Gigascience. 3: 2047-217X.
Matzke NJ (2012). Founder-event speciation in BioGeoBEARS package dramatically improves likelihoods and alters parameter inference in Dispersal-Extinction-Cladogenesis (DEC) analyses. Frontiers of Biogeography. 4: 210.
Miller MA, Pfeiffer W, Schwartz T (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees, in: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA, pp 1-8.
Moody ML, Les DH (2007). Phylogenetic systematics and character evolution in the angiosperm family Haloragaceae. American Journal of Botany. 94, 2005-2025.
Moore MJ, Bell CD, Soltis PS, Soltis DE (2007). Using plastid genomic-scale data to resolve enigmatic relationships among basal angiosperms. Proceedings of the National Academy of Sciences USA. 104: 19363-19368.
Moore MJ, Hassan N, Gitzendanner MA, Bruenn RA, Croley M, et al. (2011). Phylogenetic analysis of the plastid inverted repeat for 244 species: insights into deeper-level angiosperm relationships from a long, slowly evolving sequence region. International Journal of Plant Sciences. 172: 541-558
Moore MJ, Soltis PS, Bell CD, Burleigh JG, Soltis DE (2010). Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots. Proceedings of the National Academy of Sciences USA. 107: 4623-4628.
Morgan DR, Soltis DE (1993). Phylogenetic relationships among members of the Saxifragaceae sensu lato based on rbcL sequence data. Annals of the Missouri Botanical Garden. 80: 631-660.
Mort ME, Soltis DE, Soltis, PS Francisco-Ortega, J Santos-Guerra A (2001). Phylogenetic relationships and evolution of Crassulaceae inferred from matK sequence data. American Journal of Botany. 88: 76-91.
Nickrent DL, Joshua PD, Frank EA (2005). Discovery of the photosynthetic relative of the Maltese mushroom Cynomorium. BMC Evolutionary Biology. 5: 38.
Nie ZL, Sun H, Manchester SR, Meng Y, Luke, Q, et al. (2012). Evolution of the intercontinental disjunctions in six continents in the Ampelopsis clade of the grape family (Vitaceae). BMC Evolutionary Biology. 12: 17.
Omland KE (1999). The assumptions and challenges of ancestral state reconstructions. Systematic biology 48: 604-611.
Olmstead RG, de Pamphilis C W, Wolfe AD, Young ND, Elisens WJ et al. (2001). Disintegration of the Scrophulariaceae. American Journal of Botany. 88: 348-361
de Queiroz A (2005). The resurrection of oceanic dispersal in historical biogeography. Trends in Ecology and Evolution. 20: 68-73.
Rambaut A, Drummond AJ, Suchard M (2014). Tracer v1 6 http:// beastbioedacuk /software/tracer/
Raven PH (1963). Amphitropical relationships in the floras of North and South America. The Quarterly Review of Biology. 38: 151- 177.
Raven PH (1972). Plant species disjunctions: a summary. Annals of the Missouri Botanical Garden. 59: 234-246.
Ree RH, Sanmartín I (2018). Conceptual and statistical problems with the DEC+ J model of founder-event speciation and its comparison with DEC via model selection. Journal of Biogeography. 45: 741-749.
Ree RH, Smith SA (2008). Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology. 57: 4-14.
Refulio-Rodriguez NF, Olmstead RG (2014). Phylogeny of Lamiidae. American Journal of Botany. 101: 287-299.
Renner S (2004). Plant dispersal across the tropical Atlantic by wind and sea currents. International Journal of Plant Sciences. 165: S23-S33.
Rose JP, Kleist TJ, Löfstrand SD, Drew BT, Schönenberger J et al. (2018). Phylogeny, historical biogeography, and diversification of angiosperm order Ericales suggest ancient Neotropical and East Asian connections. Molecular Phylogenetics and Evolution. 122: 59-79.
Ruhfel BR, Bove CP, Philbrick CT, Davis CC (2016). Dispersal largely explains the Gondwanan distribution of the ancient tropical clusioid plant clade. American Journal of Botany. 103: 1117- 1128.
Sang T, Crawford DJ, Stuessy TF (1997). Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). American Journal of Botany. 84: 1120-1136.
Schäferhoff B, Fleischmann A, Fischer E, Albach DC, Borsch T, et al. (2010). Towards resolving Lamiales relationships: insights from rapidly evolving chloroplast sequences. BMC Evolutionary Biology. 10: 352.
Schönenberger J, Anderberg AA, Sytsma KJ (2005). Molecular phylogenetics and patterns of floral evolution in the Ericales. International Journal of Plant Sciences. 166: 265-288.
Schultheis LM, Donoghue MJ (2004). Molecular phylogeny and biogeography of Ribes (Grossulariaceae), with an emphasis on gooseberries (subg Grossularia). Systematic Botany. 29: 77-96.
Shi S, Chang HT, Chen Y, Qu L, Wen J (1998). Phylogeny of the Hamamelidaceae based on the ITS sequences of nuclear ribosomal DNA. Biochemical Systematics and Ecology. 26: 55- 69.
Simpson MG, Johnson LA, Villaverde T, Guilliams CM (2017). American amphitropical disjuncts: Perspectives from vascular plant analyses and prospects for future research. American Journal of Botany. 104: 1600-1650.
Smith SA, Beaulieu J, Donoghue MJ (2010). An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proceedings of the National Academy of Sciences USA. 107: 5897-5902.
Soltis DE, Clayton JW, Davis CC, Gitzendanner MA, Cheek, M, et al. (2007). Monophyly and relationships of the enigmatic amphitropical family Peridiscaceae. Taxon. 56: 65-73.
Soltis DE, Mort ME, Latvis M, Mavrodiev EV, O’Meara BC, et al. (2013). Phylogenetic relationships and character evolution analysis of Saxifragales using a supermatrix approach. American Journal of Botany. 100: 916-929.
Soltis DE, Smith SA, Cellinese N, Wurdack KJ, Tank DC et al. (2011). Angiosperm phylogeny: 17 genes, 640 taxa American Journal of Botany. 98: 704-730.
Soltis DE, Soltis PS (1997). Phylogenetic relationships among Saxifragaceae sensu lato: a comparison of topologies based on 18s and rbcL sequences. American Journal of Botany. 84: 504- 522.
Soltis DE, Soltis PS, Chase MW, Mort ME, Albach AC (2000). Angiosperm phylogeny inferred from 18s rDNA, rbcL, and atpB sequences. Botanical Journal of the Linnean Society. 133: 381-461.
Soltis DE, Soltis PS, Clegg MT, Durbin M (1990). rbcL sequence divergence and phylogenetic relationships in Saxifragaceae sensu lato. Proceedings of the National Academy of Sciences USA. 87: 4640-4644.
Spalink D, Drew BT, Pace MC, Zaborsky JG, Li P et al. (2016a). Evolution of geographical place and niche space: patterns of diversification in the North American sedge (Cyperaceae) flora. Molecular Phylogenetics and Evolution. 95, 183-195
Spalink D, Drew BT, Pace MC, Zaborsky JG, Starr JR et al. (2016b). Biogeography of the cosmopolitan sedges (Cyperaceae) and the area-richness correlation in plants. Journal of Biogeography. 43: 1893-1904.
Stamatakis A (2014). RAxML Version 8: A tool for Phylogenetic Analysis and Post-Analysis of Large Phylogenies. Bioinformatics 9: 1312-1313.
Stubbs RL, Folk RA, Xiang CL, Chen S, Soltis DE, et al. (2020) A phylogenomic perspective on evolution and discordance in the alpine-arctic plant clade Micranthes (Saxifragaceae). Frontiers in Plant Science. 10: 1773.
Sun Y, Moore MJ, Zhang S, Soltis PS, Soltis DE et al. (2016). Phylogenomic and structural analyses of 18 complete plastomes across nearly all families of early-diverging eudicots, including an angiosperm-wide analysis of IR gene content evolution. Molecular Phylogenetics and Evolution. 96: 93-101.
Tank DC, Eastman JM, Pennell MW, Soltis PS, Soltis DE et al. (2015) Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications. New Phytologist. 207: 454-467.
Tarullo C, Folk R, Soltis PS, Soltis DE, Drew BT (2016). A supermatrix approach to solving relationships in Saxifragales. Poster presented at the Botanical Society of America conference in Savannah, Georgia.
Thomas DC, Chatrou LW, Stull GW, Johnson DM, Harris DJ, et al. (2015). The historical origins of palaeotropical intercontinental disjunctions in the pantropical flowering plant family Annonaceae. Perspectives in Plant Ecology, Evolution and Systematics. 17: 1-16.
Tiffney BH (1985). The Eocene North Atlantic land bridge: its importance in Tertiary and modern phytogeography of the Northern Hemisphere. Journal of the Arnold Arboretum. 66: 243-273.
Tiffney BH (2000). Geographic and climatic influences on the Cretaceous and Tertiary history of Euramerican floristic similarity. Acta Universitatis Carolinae, Geologica. 44: 5-16.
Tiffney BH, Manchester SR (2001). The use of geological and paleontological evidence in evaluating plant phylogeographic hypotheses in the Northern Hemisphere Tertiary. International Journal of Plant Sciences. 162: 3-17.
Walker JF, Yang Y, Feng T, Timoneda A, Mikenas J et al. (2018). From cacti to carnivores: Improved phylotranscriptomic sampling and hierarchical homology inference provide further insight into the evolution of Caryophyllales. American Journal of Botany. 105: 446-462
Wallace AR (1880). Island life McMillan and Co, London, England.
Wang H, Moore MJ, Soltis PS, Bell CD, Brockington SF et al. (2009). Rosid diversification and the rapid rise of angiospermdominated forests. Proceedings of the National Academy of Sciences USA. 106: 3853-3858.
Wen J (1999). Evolution of eastern Asian and eastern North American disjunct distributions in flowering plants. Annual Review of Ecology, Evolution, and Systematics. 30: 421-455.
Wen J (2001). Evolution of eastern Asian-eastern North American biogeographic disjunctions: few additional issues. International Journal of Plant Sciences. 162: 117-122.
Wen J, Ickert-Bond SM (2009). Evolution of the Madrean-Tethyan disjunctions and the North and South American amphitropical disjunctions in plants. Journal of Systematics and Evolution. 47: 331-348.
Wen, J, Ickert-Bond, SM, Nie, ZL, Li, R (2010). Timing and modes of evolution of eastern Asian-North American biogeographic disjunctions in seed plants. In: Darwin’s Heritage Today: Proceedings of the Darwin 200 Beijing International Conference. 252-269.
Wen J, Nie Z-L, Ickert-Bond SM (2016). Intercontinental disjunctions between eastern Asia and western North America in vascular plants highlight the biogeographic importance of the Bering land bridge from late Cretaceous to Neogene. Journal of Systematics and Evolution. 54: 469-490.
Wikström N, Savolainen V, Chase MW (2001). Evolution of the angiosperms: calibrating the family tree. Proceedings of the Royal Society of London. Series B: Biological Sciences. 268: 2211-2220.
Wurdack KJ, Davis CC (2009). Malpighiales phylogenetics: gaining ground on one of the most recalcitrant clades in the angiosperm tree of life. American Journal of Botany. 96, 1551-1570
Xi Z, Ruhfel BR, Schaefer H, Amorim AM, Sugumaran M, Wurdack KJ et al. (2012). Phylogenomics and a posteriori data partitioning resolve the Cretaceous angiosperm radiation Malpighiales. Proceedings of the National Academy of Sciences USA. 109: 17519-17524.
Xiang CL, Gitzendanner MA, Soltis DE, Peng H, Lei LG (2012). Phylogenetic placement of the enigmatic and critically endangered genus Saniculiphyllum (Saxifragaceae) inferred from combined analysis of plastid and nuclear DNA sequences. Molecular Phylogenetics and Evolution. 64: 357- 367.
Xiang QY, Soltis DE, Soltis PS (1998). The eastern Asian and eastern and western North American floristic disjunction: congruent phylogenetic patterns in seven diverse genera. Molecular Phylogenetics and Evolution. 10: 178-190.
Xie L, Yi TS, Li R, Li DZ, Wen J (2010). Evolution and biogeographic diversification of the witch-hazel genus (Hamamelis L, Hamamelidaceae) in the Northern Hemisphere. Molecular Phylogenetics and Evolution. 56: 675-689.
Zhang SD, Soltis DE, Yang Y, Li DZ, Yi TS (2011). Multi-gene analysis provides a well-supported phylogeny of Rosales. Molecular Phylogenetics and Evolution. 60: 21-28.