REVIEW ARTICLE published: 13 July 2012 doi: 10.3389/fgene.2012.00130 Recent progress in paleontological methods for dating theTree of Life Michel Laurin* UMR 7207, CNRS/MNHN/UPMC, Earth History Department, Muséum National d’Histoire Naturelle, Paris, France Edited by: Dating the Tree of Life (TOL) has become a major goal of biological research. Beyond the Alex Pyron, The George Washington intrinsic interest of reconstructing the history of taxonomic diversification, time-calibrated University, USA trees (timetrees for short, as used throughout below) are required in many types of com- Reviewed by: parative analyses, where branch lengths are used to assess the conservation importance Michael S. Lee, South Australian Museum, Australia of lineages, correlation between characters, or to assess phylogenetic niche conservatism, Alex Pyron, The George Washington among other uses. Improvements in dating the TOL would thus benefit large segments of University, USA the biological community, ranging from conservation biology and ecology through func- Chris Organ, Harvard University, USA tional biology and paleontology. Recently, progress has been made on several fronts: *Correspondence: in compiling databases and supertrees incorporating paleontological data, in computing Michel Laurin, UMR 7207, CNRS/MNHN/UPMC, Earth History confidence intervals on the true stratigraphic range of taxa, and in using birth-and-death Department, Muséum National processes to assess the probability distribution of the time of origin of specified taxa. d’Histoire Naturelle, 43 rue Buffon, Combined paleontological and molecular dating has also progressed through the inser- CP 48, 75005 Paris, France. e-mail: [email protected] tion of extinct taxa into data matrices, which allows incorporation of their phylogenetic uncertainty into the dating analysis. Keywords: phylogenetics, molecular dating, molecular clock, paleontological dating, stratigraphic range, fossil record, confidence intervals INTRODUCTION much biodiversity as possible), but all these approaches are prob- WHY DATE THE TREE OF LIFE? lematic to various extents. There is no universally accepted species Some of the most basic questions about the evolution of life con- concept, despite repeated attempts to unify species concepts (e.g., cern the chronology of events. When did a given taxon appear? de Queiroz, 1998). As such, the entities that we call “species” and When did it diversify? Was its diversification slow and gradual, or that are registered into various databases are not ontologically did it occur in bursts (evolutionary radiations), and if so, when comparable; some are clades, some are reproductive communities, were these bursts, and what caused them? Answering such ques- some are evolutionary lineages, others are phenetic clusters, and tions is important not only to satisfy our intellectual curiosity yet others belong to two or more of these categories. This problem about the history of life, but also to allow sophisticated analyses in has far-reaching consequences for conservation biology (Bertrand other fields. et al., 2006), and it has hampered developments of a new, phylo- Dating the Tree of Life (TOL) has become a major goal of bio- genetic code of biological nomenclature for species (Laurin and logical research, as shown by various well-funded initiatives (at Cantino, 2007). Taxa belonging to higher categories are even more least in the USA), such as the Assembling the Tree of Life program problematic in conservation biology because, like species, they of the National Science Foundation (http://www.nsf.gov/funding/ share no objective properties, and they often differ rather strongly pgm_summ.jsp?pims_id=5129), which has distributed over US $ in many important aspects, such as geological age of origin, num- 57 000 000 since 2006. Dating the TOL has also been the exclu- ber of included species, or phenotypic variability (Laurin, 2005, sive subject of a large, recent edited book (Hedges and Kumar, 2008; Bertrand et al., 2006). The most objective solution that has 2009a), and some molecular systematics laboratories now special- been advocated (and widely applied) to circumvent all these prob- ize in this task. This interest in dating the TOL is not surprising lems is to use phylogenetic diversity (the sum of branch lengths because beyond the intrinsic goal of reconstructing the history of expressed as time), as this captures the sum of the unique his- taxonomic diversification, timetrees are required in many types of tory of a given clade, or of a given fauna or flora of a region comparative analyses. In fact, time data are so useful that Avise and (Faith, 1992). Liu (2011) have suggested to systematically add this information In comparative biology, timetrees have become essential since to taxon names. we have realized that comparative data are not statistically inde- These advances in evolutionary biology, which require time- pendent from each other. This is because closely related taxa trees, have revolutionized modern science by allowing more tend to resemble each other more closely than distantly related rigorous analyses. For instance, conservation studies previously taxa. Thus, all modern comparative techniques for inter-specific used species counts (at best) or higher taxon count (of genera, fam- datasets incorporate phylogenetic information, ideally in the form ilies, or even orders) to assess the biodiversity of various regions of timetrees. The interest of this approach is demonstrated by the (hotspots or simply areas that could be protected to preserve as high number of ISI citations (1371) of the paper by Felsenstein www.frontiersin.org July 2012 | Volume 3 | Article 130 | 1 “fgene-03-00130” — 2012/7/12 — 15:10 — page1—#1 Laurin Recent Progress in paleontological dating (1985a) that presented the method of phylogenetically inde- and lissamphibians (Ruta and Coates, 2007; Anderson et al., 2008; pendent contrasts (ISI databanks consulted on March 4, 2011). Marjanovi´c and Laurin, 2009). Similarly, the related method called phylogenetic generalized least More recently, use of the fossil record has increasingly been squares (PGLS; Martins and Hansen, 1997; Pagel, 1997) is increas- complemented by molecular timetrees, a change allowed by the ingly used in such studies (e.g., Spoor et al., 2007; Organ et al., tremendous growth of molecular phylogenetics in the last two 2011a,b). Branch lengths are also needed to study phylogenetic decades (e.g., Sanderson, 2003; Hedges and Kumar, 2009a), even niche conservatism (Patterson and Givnish,2002; Desdevises et al., though the roots of molecular dating hark back to the 1960s 2003; Losos, 2008), evolutionary trends from paleontological data (Zuckerkandl and Pauling, 1962). The basic principle of molecular (Laurin, 2010a), or to determine ancestral conditions through dating rests on inferring how much molecular change has occurred methods such as squared-change parsimony (e.g., Laurin, 2004; on each branch of the reconstructed tree (or trees, when Bayesian Finarelli and Flynn, 2006), Maximum Likelihood (Pagel, 1999), or methods are used). This is not straightforward because multiple Bayesian inference (e.g., Organ et al., 2011a,b). changes can occur at a given nucleotide site, and given that there Various evolutionary problems, such as the search of a corre- are only four possible states (A, T, C, or G), a given site may revert lation between past climatic changes or geological events (i.e., the to its initial condition. Furthermore, all sites do not evolve at the break-up of Pangea) and taxonomic or phenotypic diversification, same speed; some genes evolve faster than others, mitochondrial require timetrees to be meaningfully studied (e.g., Paradis, 2004; genes tend to evolve faster than most nuclear genes, silent portions San Mauro et al., 2005). Thus, timetrees are at the core of several of the genome tend to evolve faster than functionally important biological fields, so any project that would significantly improve portions, and third codon positions evolve faster than first and sec- how they are built would benefit a large segment of the biological ond codon positions because many changes in the third position community. result in the same amino acid. Thus, molecular biologists have From an economic perspective, the applications of timetrees developed various evolutionary models that attempt to account in conservation biology (Faith, 1992), through better-informed for these factors, as well as sophisticated methods to select the choices in conservation priorities (of regions or taxa), are prob- best-supported model (e.g., Posada, 2008). ably the most important. Indeed, the twenty-first century faces The resulting tree is usually not ultrametric because each lin- a major biodiversity crisis and may well be the “century of eage evolves at its own rate; thus, the tips (extant terminal taxa) extinction” (Dubois, 2003), in addition to (and partly because are each at a slightly different patristic distance from the root of) facing climate change caused by greenhouse gas emissions. of the tree. The differences in height represent deviations from Biodiversity is important for the maintenance of ecosystems, the hypothesis of a molecular clock. The tree can be ultrametri- and the crucial role of “ecosystem services” (in maintaining a cized using various algorithms, which, in a best-case scenario, climate favorable to agriculture and human health, in absorb- results in a tree in which branch lengths are proportional to ing greenhouse gases, etc.) are