Exploring the Impact of Fossil Constraints on the Divergence Time Estimates of Derived Liverworts

CORE Metadata, citation and similar papers at core.ac.uk Provided by Springer - Publisher Connector Plant Syst Evol (2013) 299:585–601 DOI 10.1007/s00606-012-0745-y ORIGINAL ARTICLE Exploring the impact of fossil constraints on the divergence time estimates of derived liverworts Kathrin Feldberg • Jochen Heinrichs • Alexander R. Schmidt • Jirˇ´ı Vańˇa • Harald Schneider Received: 16 October 2012 / Accepted: 17 December 2012 / Published online: 12 January 2013 Ó The Author(s) 2013. This article is published with open access at Springerlink.com Abstract In this study, we evaluate the impact of fossil Jurassic. Our results provide a note of caution regarding the assignments and different models of calibration on diver- interpretation of chronograms derived from DNA sequence gence time estimates carried out as Bayesian analyses. variation of extant species based on a single calibration Estimated ages from preceding studies and liverwort point and/or low accuracy of the assignment of fossils to inclusions from Baltic amber are used as constraints on a nodes in the phylogeny. molecular phylogeny of Cephaloziineae (Jungermanniops- ida) obtained from sequences of two chloroplast coding Keywords Amber fossils Á BEAST Á Cephaloziineae Á regions: rbcL and psbA. In total, the comparison of 12 Divergence time estimates Á Jungermanniopsida different analyses demonstrates that an increased reliability of the chronograms is linked to the number of fossils assigned and to the accuracy of their assignments. Inclu- Introduction sion of fossil constraints leads to older ages of most crown groups, but has no influence on lineage through time plots DNA-sequence-based divergence time estimates are now suggesting a nearly constant accumulation of diversity widely employed to study the evolution of various lineages since the origin of Cephaloziineae in the early to Middle of animals, fungi and plants. The application of these methods resulted in a dramatic improvement of our understanding of evolutionary events and processes, espe- K. Feldberg Á J. Heinrichs (&) cially in lineages with a poor and patchy fossil record Abteilung Systematische Botanik, Albrecht-von-Haller-Institut (Hedges and Kumar 2009). However, these results are fu¨r Pflanzenwissenschaften, Georg-August-Universita¨t often controversial, especially when comparisons with the Go¨ttingen, Untere Karspu¨le 2, 37073 Go¨ttingen, Germany fossil record can be drawn (e.g. Donoghue and Benton e-mail: [email protected] 2007; Kenrick et al. 2012; Parham et al. 2012). These A. R. Schmidt controversies are partly caused by confusion about the Georg-August-Universita¨tGo¨ttingen, Courant Research Centre accuracy of the information obtained by DNA sequence- Geobiology, Goldschmidtstraße 3, 37077 Go¨ttingen, Germany based or fossil-based reconstruction of lineage histories and J. Vańˇa ages (Kenrick et al. 2012). Department of Botany, Charles University, Bena´tska´ 2, Arguably, one of the most important sources of inac- 128 01 Praha 2, Prague, Czech Republic curacy in molecular-based divergence time estimates is the need to calibrate the molecular clocks using fossil evidence H. Schneider Institute of Botany, the Chinese Academy of Sciences, (Donoghue and Benton 2007; Hedges and Kumar 2009; State Key Laboratory of Systematic and Evolutionary Botany, Parham et al. 2012). Other approaches, such as estimates of 100093 Beijing, China geological events have been considered as alternatives to fossil-based calibrations, but their usage is restricted to H. Schneider Department of Botany, The Natural History Museum London, certain cases and could result in misleading estimates London SW7 5BD, UK (Renner 2005). Early methods of molecular clock dating 123 586 K. Feldberg et al. used single calibration points despite the fact that the age The high quality of the preservation of amber fossils of a fossil is nearly always documented as a time interval. allows for a description of many morphological characters Improvement has been achieved by the introduction of that are phylogenetically or taxonomically informative. methods that employ minimum and maximum age con- The exquisite preservation enables the application of roles straints beside one or several calibration points (Ho 2007; to the assignment proposed as best practice (Parham et al. Benton et al. 2009; Inoue et al. 2010; Magallon 2010; 2012) despite some uncertainties concerning the taxonomic Heled and Drummond 2012; Lukoschek et al. 2012; Sau- interpretation and age of the fossils. Several studies quet et al. 2012). The most recent innovations allow us to focused on the relationships of amber inclusions of liver- integrate the information given by fossil evidence in form worts to extant taxa (Grolle 1983, 1985, 1993; Gradstein of probability distributions. This kind of calibration is 1993; Grolle and Schmidt 2001; Grolle and Meister 2004a, usually part of relaxed molecular clock methods that esti- b; Heinrichs and Schmidt 2010; Heinrichs et al. 2011, mate divergence times based on the DNA sequence data 2012b). Thus, these fossils can be potentially assigned to using one or several genomic regions either as a single or particular nodes in the phylogeny of the studied lineage of several partitions. They allow the integration of several liverworts and some studies reconstructed the diversifica- fossil constraints in a single analysis, but require to study tion of selected liverwort lineages using either a DNA the impact of fossil assignments on the sister lineages of clock only approach or a DNA plus amber fossil approach the calibrated clades in the tree very careful (Benton et al. (Hartmann et al. 2006, 2007, 2009b; Wilson et al. 2007; 2009; Inoue et al. 2010; Magallon 2010; Parham et al. Devos and Vanderpoorten 2009). Amber inclusions are, 2012). however, not the only source of liverwort fossils (Krassilov Most authors agree on the importance of the calibration and Schuster 1984). Some liverworts fossils have been and constraining of molecular clocks with the fossil recorded with different taphonomic background such as record (Benton et al. 2009; Hedman 2010; Inoue et al. Sinolejeunea from the Middle Jurassic Yima Formation 2010; Magallon 2010; Pyron 2010; Wilkinson et al. 2011; (Yang and Wu 2010) or anatomical preserved remnants of Lukoschek et al. 2012; Sauquet et al. 2012) and various leafy liverworts from the Eocene of Canada (Steenbock methods have been made available to integrate this et al. 2011). information (Ho 2007; McCormack et al. 2010; Heled and Molecular phylogenetic studies indicate that the liver- Drummond 2012). So far, relatively few studies explored worts (Marchantiophyta) have separated from other lin- the impact of these parameters on the estimates obtained eages in the earliest diversification of plants on land (Qiu from these analyses (e.g., Jacques et al. 2007; Sauquet et al. 2006). Heinrichs et al. (2007) estimated the age of the et al. 2012). However, such studies are required to edu- leafy liverworts (Jungermanniidae) to the late Carbonifer- cate us about the limitations of the currently available ous (308.7 ± 7.8 Ma), but slightly older ages may need to methods and to develop guidelines of the employment of be considered given the uncertainty of divergence time parameter models and fossil information (Near and San- estimates of the oldest splits of liverworts (Clarke et al. derson 2004; Hedman 2010; Inoue et al. 2010; Lukoschek 2011; Kenrick et al. 2012). et al. 2012). In this study, we explore the integration of the amber Here, we use a main clade of leafy liverworts (Junger- fossil record in studies focusing on the diversification of a manniidae), the Cephaloziineae, as a model to study the derived lineage of liverworts, the Jungermannialean line- impact of fossil constraints. Generally, liverworts have a age Cephaloziineae (Crandall-Stotler et al. 2009), which rather limited fossil record (Krassilov and Schuster 1984; comprises the families Cephaloziaceae, Cephaloziellaceae, Taylor et al. 2009), but they are often found as amber Hygrobiellaceae, Adelanthaceae s. l. and Scapaniaceae s. l. inclusions with a very high quality in character preserva- We are particularly interested in the impact of alternative tion (Grolle and Meister 2004a). Unfortunately, amber assignments that reflect uncertainties in the interpretation occurs discontinuously in space and time (Grimaldi 1996). of the fossils’ relationships (see also Sauquet et al. 2012). This preservation bias in form of gaps in the record over This study will also provide us with empirical evidence time has to be taken into consideration when using amber about the performance of recently established methods to fossils to infer the diversification of organisms (Smith estimate divergence times in the context of phylogenetic 2001; Pyron 2010; Dornberg et al. 2011; Lloyd et al. 2012). uncertainty concerning the relationships of the taxa pre- DNA sequence-based divergence time estimates are served in the fossil record (Drummond et al. 2006). All potentially capable to overcome this shortcoming by inte- analyses were carried out using BEAST, a Bayesian grating the discontinuous amber fossil record into the MCMC method capable to obtain time-measured phylog- framework provided by either an already dated phylogeny enies with confidence intervals using relaxed molecular or preferably into simultaneously inferred divergence time clocks and various parameters to integrate information estimates. about the evolutionary processes and the fossil record 123 Exploring the impact of fossil

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