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Phylogenetics, Divergence Times and Diversification from Three Genomic bs_bs_banner Botanical Journal of the Linnean Society, 2015, 178, 375–393. With 6 figures Phylogenetics, divergence times and diversification from three genomic partitions in monocots KATE L. HERTWECK1,2*, MICHAEL S. KINNEY3, STEPHANIE A. STUART4, OLIVIER MAURIN5, SARAH MATHEWS6, MARK W. CHASE7, MARIA A. GANDOLFO8 and J. CHRIS PIRES3 1National Evolutionary Synthesis Center (NESCent), 2024 West Main Street Suite A200, Durham, NC 27705, USA 2Division of Biological Sciences, 311 Bond Life Sciences Center, University of Missouri, 1201 Rollins Street, Columbia, MO 65211, USA 3Biology Department, University of La Verne, 1950 Third Street, La Verne, CA 91750, USA 4Department of Biological Sciences, Faculty of Science, Macquarie University, Sydney, NSW 2109, Australia 5Molecular Systematics Laboratory, African Centre for DNA barcoding (ACDB), Department of Botany and Plant Biotechnology, University of Johannesburg, APK Campus, PO Box 524, Auckland Park, 2006, South Africa 6Harvard University Herbaria, 22 Divinity Avenue, Cambridge, MA 02138, USA 7Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK 8LH Bailey Hortorium, Plant Biology, School of Integrative Plant Science, Cornell University, 410 Mann Library Building, Ithaca, NY 14853, USA Received 14 February 2014; revised 6 June 2014; accepted for publication 6 January 2015 Resolution of evolutionary relationships among some monocot orders remains problematic despite the application of various taxon and molecular locus sampling strategies. In this study we sequenced and analysed a fragment of the low-copy, nuclear phytochrome C (PHYC) gene and combined these data with a previous multigene data set (four plastid, one mitochondrial, two nuclear ribosomal loci) to determine if adding this marker improved resolution and support of relationships among major lineages of monocots. Our results indicate the addition of PHYC to the multigene dataset increases support along the backbone of the monocot tree, although relationships among orders of commelinids remain elusive. We also estimated divergence times in monocots by applying newly evaluated fossil calibrations to our resolved phylogenetic tree. Inclusion of early-diverging angiosperm lineages confirmed the origin of extant monocots c. 131 Mya and strengthened the hypothesis of recent divergence times for some lineages, although current divergence time estimation methods may inadequately model rate heterogeneity in monocots. We note significant shifts in diversification in at least two monocot orders, Poales and Asparagales. We describe patterns of diversification in the context of radiation of other relevant plant and animal lineages. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 178, 375–393. ADDITIONAL KEYWORDS: divergence time estimation – fossil calibration – molecular phylogenetics – monocotyledoneous plants. *Corresponding author. Current address: University of Texas at Tyler, 3900 University Blvd, Tyler, TX 75799, USA. E-mail: [email protected] © 2015 The Authors. Botanical Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of 375 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 178, 375–393 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 376 K. L. HERTWECK ET AL. INTRODUCTION Age estimates for nodes in the monocot phyloge- netic tree are characterized by wide confidence inter- Molecular phylogenetics has greatly improved our vals, due to variation in parameters used to date understanding of the evolution of monocotyledoneous lineages and/or differences in the datasets (taxa and plants. Nearly all studies have found support for data; Sanderson & Doyle, 2001). In the case of mono- monocots as a monophyletic group (e.g. Chase et al., cots, major sources of variation include: limited taxon, 1993), and one found them well supported as sister to molecular locus and fossil sampling; uncertainty sur- Ceratophyllum L. and eudicots (Saarela et al., 2007). rounding fossil calibration points; and variability in APG III (2009) recognized 77 monocot families in 11 methods used to infer divergence times. Use of com- orders; Dasypogonaceae remains unplaced to order plete plastome data from limited taxonomic sampling level. The two most recent and comprehensive molecu- from across angiosperms placed the date of the origin lar phylogenetic studies improved resolution and of monocots between 140 and 150 Mya (Chaw et al., support for major lineages by pursuing different sam- 2004; Leebens-Mack et al., 2005). Estimates of the pling strategies. Graham et al. (2006) used relatively age of extant monocots based exclusively on fossil few taxa with more loci from only the plastid genome, evidence tend to be younger, c. 90 Mya (Crepet, Nixon whereas Chase et al. (2006) utilized more comprehen- & Gandolfo, 2004), although the ancestors of mono- sive taxon sampling with fewer loci from plastid, cots were present from the Early Cretaceous (Smith, mitochondrial and nuclear genomes. Both analyses 2013). Reconciliation of variation in age estimates is provided strong support for monophyly of all monocot confounded by the contentious nature of the monocot lineages as defined by APG III (2009). Some relation- fossil record and a paucity of specimens compared ships among monocot orders are well supported; with other angiosperm lineages (Crepet & Gandolfo, however, several higher relationships are resolved 2008; Friis, Crane & Pedersen, 2011). Inadequacy of with only low to moderate support (Fig. 1). In particu- this fossil record is generally attributed to the poor lar, relationships among orders of commelinids preservation of herbaceous material and a lack of (Poales, Commelinales, Zingiberales, Arecales, Dasy- synapomorphies in many specimens (Crepet et al., pogonaceae) have proven difficult to elucidate (Givnish 2004). et al., 1999; Davis et al., 2004; Chase et al., 2006; Variation in methods similarly affects estimation of Graham et al., 2006; Barrett et al., 2013). divergence times for lineages in the monocots (Table 1). The first comprehensive evaluation of monocot divergence times utilized extensive taxo- 100/100 Commelinales 100/100 nomic sampling (878 taxa) of a single plastid locus 100/100 (rbcL), eight fossil calibrations and non-parametric commelinids Zingiberales 100/100 rate smoothing (NPRS) to date divergence of all major 100/100 Poales 58/- monocot lineages to the Early Cretaceous (Janssen & 100/100 Bremer, 2004). Anderson & Janssen (2009) reana- Dasypogonaceae 79/76 lysed this dataset with five additional fossil calibra- 100/- Arecales tions and the application of two new dating methods 77/70 [penalized likelihood (PL) and PATHd8]. PATHd8 95/94 Asparagales returned much younger divergence times for several monocot lineages, similar to other studies comparing 95/99 -/100 Liliales divergence times resulting from these programs 99/100 Dioscoreales (Brown et al., 2008). Magallón & Castillo (2009) 100/100 87/63 100/100 evaluated divergence times and diversification across Pandanales angiosperms using a stricter set of criteria for fossil 100/100 100/- calibrations and implementation of a Bayesian Petrosaviales relaxed molecular clock approach using BEAST; dates 89/84 100/100 Alismatales from this analysis were intermediate to the NPRS/PL and PATHd8 analyses. Bell, Soltis & Soltis (2010) 100/- Acorales conducted a similar analysis across angiosperms using BEAST and obtained substantially younger Figure 1. Summary of previously hypothesized relation- estimates for the emergence of crown groups in mono- ships among monocots (Chase et al., 2006; Graham et al., cots (Table 1). 2006). Numbers by nodes correspond to bootstrap values Progress to date in circumscribing relationships from Chase et al. (2006) and Graham et al. (2006), respec- among monocot orders and in estimating divergence tively. Open circles indicate fossil calibrations utilized by times of major lineages has relied largely on unipa- Anderson & Janssen (2009). rentally inherited organellar DNA (plastid and © 2015 The Authors. Botanical Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 178, 375–393 The Linnean Society of© London, 2015 The Authors. Botanical Journal of theTable Linnean Society published by John Wiley & Sons1. Ltd on behalf of Divergence times for the SL and CG of major monocot lineages Bell et al., 2010 Janssen & Anderson & Magallón & exponential, Lineage Bremer, 2004 Janssen, 2009 Castillo, 2009 lognormal This study Data utilized One gene One gene Five genes Three genes Eight genes (plastid, (plastid (plastid (plastid and (plastid mitochondrial, DNA) DNA) nrDNA) and nrDNA) nrDNA, PHYC) Dating method NPRS (r8s) PL (r8s) Relaxed clock Relaxed clock PL (r8s) Relaxed clock (program) (BEAST) (BEAST) root 160 (multidivtime) Botanical Journal of the Linnean Society (140–180) mean (95% CI) Monocots CG 134* 134* 127 130,146 131 (126–142) 138 (132–143) SL N/A N/A N/A 136,156 136 (130–147) 147 (142–152) Commelinids CG 120 120 115 96,103 118 (113–127) 110 (104–115) SL 122 122 119 101,107 121 (116–130) 115 (110–121) Acorales CG N/A N/A N/A N/A 9 (9–10) 30 (15–50)^ SL 134* 134* 127 130,146 131 (126–142) 138 (132–143) Alismatales CG 128 128 127 107,122 120 (115–129) 125 (119–131) SL 131 131 126 118,136 128 (123–139) 132
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