The northeastern symposium on evolutionary divergence time: fossil and molecular dating: molecular and fossil dating: a compatible match?
What is Fossil Dating?
Traditionally, the timing of insect divergences was estimated using the fossil record. Palaeoentomologists would identify insect fossil taxa (e.g., Hennig, 1981; Carpenter, 1992; Rasnitsyn and Quick, 2002), dating the ages of the strata that the fossils were preserved in, or the fossil itself, using methods such as isotope estimation or geomagnetic polarity timescales (see Grimaldi and Engel, 2005 for review). In some cases, fossils from a particular deposit may be used to suggest an older origin of an insect group; if a taxon's first appearance is already diverse and abundant in the fossil record, but it is not represented in earlier strata, it may be possible to infer that the taxon diverged earlier than the fossils suggest. The insect fossil record is widespread across every continent, and diverse in the methods and levels of preservation (Grimaldi and Engel, 2005). Fossils can be compression or impression fossils, i.e., material that is found on or in rock, or amber fossils, i.e., material Suspended in fossilized plant resin. While compression or impression fossils may retain structural pigments, wing venation, and general body characteristics, amber deposits often yield additional external body morphological characters, as well as eggs, fecal matter, etc. (e.g., Grimaldi et al., 2000; Wichard et al., 2009; Rust et al., 2010). With increased access to CT-scanning technology, we may soon have new insights into the internal anatomy of amber-preserved insects (e.g., Lak et al., 2008, 2009). But while the fossil record is good for many insect groups (such as Odonata: Bechly, 1996; or Dictyoptera: Grimaldi, 1997), it can be quite poor or non-existent for others (such as Lepidoptera, Phthiraptera). In these cases, trace fossils such as frass, burrows or larval cases may be useful (Grimaldi and Engel, 2005). In general, fossil dating provides reliable, albeit potentially conservative, estimates for the ages of insect taxa.
[FIGURE 1 OMITTED]
A New Method of Insect Dating
The advent of "molecular dating" has enabled organismal entomologists and molecular evolutionary biologists to use DNA sequence data to obtain molecular dates for insect divergences. For a group as speciose as Insecta, the potential of such a method to confirm or contradict fossil-based estimates of the origins of herbivory, mutualism, flight, parasitism and other remarkable insect behaviors is intriguing. Indeed, the number of insect-focused studies using molecular dating methods has been increasing exponentially since the beginning of computer based methods (see Figure 1, adapted from Ware and Grimaldi, in press). Molecular dating may have some advantages over fossil dating, in that it provides a method to obtain temporal information for species with little or no fossil record, and for which trace fossils are also scarce (e.g., Phthiraptera). It can also be used in conjunction with fossil dating to address gaps in the fossil record, provide support for or reject hypotheses based on geological data, or to generate new hypotheses altogether (Sarich and Wilson, 1967). However, it also has disadvantages. Molecular dating requires sequence data and can therefore only be carried out on extant (or recently extinct) taxa, and this excludes much of the evolutionary insect biota. Furthermore, methods of molecular dating must be able to model DNA sequence evolution well; if the model is not a good fit to the data, then the dates obtained may not be accurate.
What is Molecular Dating?
The discovery of a "molecular clock" by Zuckerkandl & Pauling in the 1960s--the observation that the amount of sequence divergence between two taxa depends on the time since the two species diverged (rather than the amount of morphological evolution that has occurred)immediately opened up the possibilities of using DNA sequences to "molecular date" species divergences (Zuckerkandl and Pauling, 1965). In phylogenies produced from molecular data, phylogenetic branch lengths (measured in nucleotide substitutions per site) are a product of both substitution rate and time: a large number of changes on a branch can be due to old dates or fast rates. Molecular dating consists of "calibrating" the molecular clock - using dated fossils to calculate the substitution rates in one part of the tree, so that these known rates can then be extrapolated across the phylogeny to estimate divergence dates of taxa in another area.
Origins of the Rocks and Clocks Debate
Molecular dating has been heralded as one of the most useful tools to arise from the genetic revolution (e.g., Bromham and Penny, 2003). Unfortunately, the dates produced by many of the earliest dating studies proved controversial: several molecular estimates for events in the fossil record were considerably older than the palaeontological data suggested (for reviews of the rocks versus clocks debate see Smith and Peterson (2002), Sanderson, et al. (2004), Brown, et al. (2008)). For example, molecular dates for the Cambrian explosion, the sudden appearance of all major metazoan phyla in the fossil record -543 million years ago (mya), were between at least 100-650 million years earlier than the fossil appearances of these taxa (see Bromham et al., 2000). The fossil radiations of mammals, birds and angiosperms produced similarly inflated molecular dates (e.g., Kumar and Hedges, 1997; Cooper and Penny, 1998; Wikstrom et al., 2001 and refs therein), and the differences among these estimates have been used to suggest artifacts of preservation in the fossil record, and even to question long-standing ecological theories (such as the mammalian radiation after the extinction of the dinosaurs (Bromham et al., 2000)).
While gaps in the fossil record or the "lag" time from initial mutation to substantial phenotypic difference (Brown et al., 2008) may have been partly the cause of differences between molecular and fossil dates, a large proportion of blame was leveled at the molecular methods. This is because it had become increasingly apparent that the assumption of a "strict" molecular clock was not universally valid. Instead, there was evidence that variation in DNA substitution rates was widespread across taxonomic groups. Crucially, this variation was not only stochastic (the clock "ticks" sporadically, following a Poisson process) but could also differ systematically among species (Laird et al., 1969; Kohne, 1970). If substitution rates vary between closely related lineages, dates obtained by traditional methods of molecular dating will be seriously affected, as the assumption of a constant rate of evolution between taxa will be violated. Dates will tend to be overestimated if rate variation is not accounted for, even if only "clock-like" DNA sequences are used for dating analyses; the "clock tests" used to detect rate variation were unfortunately shown to lack power (Bromham et al., 2000).
Early Insect Dating
So how does this affect the molecular dating of insects? Critically, there is much evidence to suggest that lineage-specific substitution rate variation is a much greater problem in insects than vertebrates (e.g., Zoraptera, Phthiraptera, Diptera). This arises from relatively deeper divergences and much greater taxonomic diversity among extant lineages, as well as the seemingly high evolutionary lability of factors that affect substitution rates between even closely related species (e.g., generation time, population size, sociality, parasitism, longevity (Thomas et al., 2010; Woolfit and Bromham, 2005; Bromham and Leys, 2006; Hassanin, 2006). Such factors are likely to seriously bias insect divergence dates obtained using traditional dating methods. It is perhaps fortunate then that very few insect molecular dating studies were published before the end of the twentieth century (notable exceptions include: Russo et al., 1995; Pellmyr and Leebens-Mack, 1999; Emerson et al., 2000a; Emerson et al., 2000b). Whether this was due to scarcity of fossils or a lack of suitably "clock-like" sequences (Gaunt and Miles, 2000), or even the fact that insect molecular systematics was still a relatively young field (only more recently increasing dramatically in scope and breadth), it meant that insect molecular dating studies managed to avoid many of the problems associated with strictclock dating analyses. With the advent of new dating methods, the burgeoning field of insect molecular systematics was ready to take off.
The Relaxed Clock and Dating with Confidence
The recent development of "relaxed-clock" molecular dating methods has once again raised hope that accurate divergence dates might be obtained from molecular data (e.g., r8s: Sanderson (2003), multidivtime: Thorne and Kishino (2002), BEAST: Drummond and Rambaut (2007). These methods are able to incorporate substitution rate variation into date estimation by assuming that rates can change across the tree, but that temporal information (e.g., from fossil
data) can be used to inform how rates evolve. Such relaxed clock methods can be classified into a number of different types, based on the assumptions they make underlying how rates evolve across the tree (for review see Welch and Bromham, 2005). For example, some approaches use local molecular clocks, which assume that different parts of the phylogeny are characterized by a few different rates (e.g., Yoder and Yang, 2000). Other more commonly used "rate-smoothing" methods assume that substitution rates evolve across the tree, with changes in rate approximating statistical distributions, e.g., lognormal or Poisson. Methods can also differ in their assumptions about whether evolutionary rates are correlated among closely related lineages, usually referred to as "autocorrelation" (Sanderson, 1997; Thorne et al., 1998), or whether rates are "uncorrelated" across the phylogeny (Huelsenbeck et al., 2000; Drummond et al., 2006). Finally, different relaxed clock methods can use different statistical frameworks to estimate divergence times, for example, penalized likelihood (Sanderson et al., 2003) or Bayesian estimation (Huelsenbeck et al., 2000; Thorne and Koshino, 2002; Drummond and Rambaut, 2007).
While multidivtime and r8s have both become common in the literature since their introduction (Thome and Koshino, 2002; Sanderson, 2003), it is the program BEAST (Drummond and Rambaut, 2007) that has seen the largest expansion in usage for insect dating, particularly over the last few years (see figure 1). This probably arises from a number of factors. Firstly, like r8s and multidivtime, BEAST is freely available but has the added benefit of several associated programs (BEAUti, Tracer, LogCombiner, TreeAnnotator, Tree Stat and Fig Tree), which provide a user-friendly interface to run dating analyses and to analyze the generated trees. In addition, BEAST allows a wide range of nucleotide and protein models of sequence evolution to be implemented. Second, a major difference between the methods is that BEAST is able to take into account uncertainties in the phylogeny, jointly estimating molecular dates along with the topology and other evolutionary parameters, such as estimates of population size over time (Bayesian skyline or skyride plots). In multidivtime and r8s, the user first estimates the topology, then uses the branch lengths to date lineage divergences. Third, in BEAST, fossil calibrations can be inputted as probability distributions, rather than just as maximum/minimum dates or point estimates, allowing for uncertainties in the prior knowledge of fossil dates to be taken into account. Lastly, as in multidivtime, the Bayesian framework means that molecular date estimates are produced with a measure of the associated variance (reporting credibility intervals of dates).
The current state of insect dating
Relaxed clock methods have provided fascinating insights into the timing of divergences for insect taxa with limited or with no fossil record, for example, patterns of co-speciation between lice and primates (Reed et al., 2007; Light et al., 2009), or patterns of biogeographical speciation in stick-insects (Buckley et al., 2010). Entomological molecular dating can also yield insights into other areas of research, for example human evolution, particularly for species characteristics that may not fossilize, such as behavior or disease. Molecular dates have provided information about insect vector-borne diseases e.g., Yellow fever in mosquito (Bryant et al., 2007) as well as human behavior, such as when early humans began wearing clothes, from the divergence between human body and hair lice (Kittler et al., 2003).
There have been several hundred insect molecular dating studies since Gaunt and Miles's 2002 seminal paper, and these studies have provided dating estimates for 19 of the approximately 30 insect orders (Odonata, Plecoptera, Orthoptera, Phasmatodea, Isoptera, Blattaria, Mantodea, Grylloblattodea, Hemiptera, Phthiraptera, Thysanoptera, Coleoptera, Megaloptera, Neuroptera, Rhaphidioptera, Diptera, Hymenoptera, Lepidoptera and Trichoptera). The Northeastern Symposium on Evolutionary Divergence Time (NSEDT) highlighted the broad taxonomic focus of current insect molecular dating research. Papers examining 9 different insect orders were presented: Phthiraptera (lice: Jessica Light), Isoptera (termites: Jessica Ware and David Grimaldi), Mantodea (preying mantises: Gavin Svenson), Hymenoptera (ants and bees: Sean Brady and ants: Corrie Moreau; separate talks), Orthoptera (grasshoppers: Hojun Song), Hemiptera (cicadas: Christopher Owen), Palaeoptera (dragonflies and mayflies; Jessica Thomas), Odonata (dragonfies and damselflies: Seth Bybee), Lepidoptera (butterflies and moths: Akito Kawahara), Trichoptera (caddisflies: Christy Jo Geraci), as well as additional methodological talks (Frank Burbrink, Sergios-Orestis Kolokotronis, Alex Pyron, and Sara Ruane).
However, despite the widespread and increasing popularity of molecular dating, issues remain with both the real and perceived disparities between molecular and fossil estimates. A serious problem is the observation that, even when using relaxed clock dating methods, molecular dates tend to be earlier than fossil estimates. One place this is consistently observed is for molecular estimates of rapid radiations (for example Wikstrom et al., 2001; Douzery et al., 2003). While the cause of this overestimation is not yet fully understood, it has been hypothesized that it may arise from an exceptional evolutionary process, for example concerted evolution in rates across all taxa (Bromham and Hendy, 2000). Dealing with these kinds of special processes will be particularly difficult. However, in addition, there is evidence that errors in divergence time estimation can still arise from branch length errors in phylogenetic analysis (e.g., Brown et al., 2008; Phillips, 2009), whether due to calibration points (e.g., Brochu, 2004), incongruence among genes (e.g., Springer et al., 2003) or model selection (e.g., Ware et al., 2008). Differences in date estimates arising from these sorts of error can be addressed, and it is important to reduce overall phylogenetic error, in order to reduce the error in dates.
Recently, Ware & Grimaldi (in press) reviewed insect dating studies to compare fossil based estimates with molecular based divergence times. For many taxa the rocks and clocks "agreed," although how this is defined is of course subjective, and consensus has not yet been reached in how much difference is acceptable between molecular and fossil estimates. Ware & Grimaldi found that when error is taken into account for both fossil ages and molecular dates, more than half of the examined studies had molecular ages that differed by no more than 25% from the fossil based estimates. Perhaps not unexpectedly, there were few estimated molecular dates for insects that were younger than the age of known crown group fossils (Ware and Grimaldi, in press). It is also clear, however, that certain methodologies, for example supertrees, may result in seriously overestimated molecular dates. It is essential to understand what causes these overestimations, in order to avoid them.
The papers here, by Duane McKenna, Corrie Moreau and Conrad Labandiera, highlight best practice in order to reduce error in molecular date estimations. First, it is important to consider the effects of topology and gene choice on dating estimates. The sensible use of genes may greatly improve the molecular dating estimates for many insect taxa; in his review of beetle dating, McKenna (this issue) highlights how gene and taxon choice can affect tree topology and, subsequently, molecular dating. Multiple molecular markers, recent accurate fossil information and robust dating methodology will, the authors suggest, greatly influence future beetle dating studies for the better. Second, one must make sure that fossils used in calibration of molecular dating studies are correctly assigned to lineages; Labandiera (this issue) discusses the extensive fossil record of Holometabola and how fossil taxa can be used to inform paleoecology. The four holometabolous taxa he evaluates suggest an earlier age for complete metamorphosis than estimated by either molecular or prior fossil dating. Labandiera underscores how vital a good understanding of morphology and the fossil record are for assigning fossil taxonomic positions, and reveals how different taxonomic assignment greatly affects node ages.
Last, but not least, one must ensure that the specific fossils used to calibrate molecular studies do not have undue influence on the tree topology and subsequent date estimates, as discussed in this issue by Moreau and Bell. Comparing the 43 fossils used in Moreau, et al. (2006), they find that five fossils are inconsistent, in disagreement with each other, yet the removal of these fossils did not significantly affect their dating results. Their method of evaluating a dataset with and without inconsistent fossils should be considered common practice, yet rarely are the fossils chosen for molecular dating analyses placed under such scrutiny.
For a group as diverse as insects, with such a remarkable array of behavior and ecology, we are only just beginning to understand the timing of their evolution. Molecular dating will shed light on some of the most interesting events in their diverse and enigmatic past.
JW acknowledges NSF Postdoctoral Research Fellowship 0804424. We would like to thank Rutgers University's Office of the Executive Dean, Department of Ecology and Evolution, Department of Entomology, and Office for the Advancement of Women in Science, Math and Engineering for funding the NSEDT symposium. Many thanks also go to the attendees of the symposium and to all of the speakers. Finally, thanks to Simon Ho and Meg Woofit for helpful comments on this manuscript.
Received 22 December 2010; accepted 11 March 2011.
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JESSICA A. THOMAS (1) AND JESSICA L. WARE (2,3)
(1) School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK
(2) Department of Biological Sciences, Rutgers University, 206 Boyden Hall, 195 University Avenue, Newark, NJ 07102, USA
(3) Email address for correspondence: jware42@andromeda. rutgers.edu
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