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Phylogenetic Stability, Tree Shape, and Character Compatibility: a Case Study Using Early Tetrapods

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Phylogenetic Stability, Tree Shape, and Character Compatibility: a Case Study Using Early Tetrapods Syst. Biol. 65(5):737–758, 2016 © The Author(s) 2016. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For Permissions, please email: [email protected] DOI:10.1093/sysbio/syw049 Advance Access publication June 10, 2016 Phylogenetic Stability, Tree Shape, and Character Compatibility: A Case Study Using Early Tetrapods , ,∗ MASSIMO BERNARDI1 2 ,KENNETH D. ANGIELCZYK3,JONATHAN S. MITCHELL4, AND MARCELLO RUTA5 1MUSE—Museo delle Scienze, Corso del Lavoro e della Scienza, 3, 38122 Trento, Italy; 2School of Earth Sciences, University of Bristol, Wills Memorial Building, Queens Road, Bristol BS8 1RJ, UK; 3Integrative Research Center, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL 60605-2496, USA; 4Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48103, USA; and 5School of Life Sciences, Joseph Banks Laboratories, University of Lincoln, Green Lane, Lincoln LN6 7DL, UK ∗ Correspondence to be sent to: Massimo Bernardi, MuSe—Museo delle Scienze, Corso del Lavoro e della Scienza, 3, 38122 Trento, Italy; Email: [email protected] Received 25 October 2014; reviews returned 31 March 2016; accepted 19 May 2016 Associate Editor: Benoit Dayrat Downloaded from Abstract.—Phylogenetic tree shape varies as the evolutionary processes affecting a clade change over time. In this study, we examined an empirical phylogeny of fossil tetrapods during several time intervals, and studied how temporal constraints manifested in patterns of tree imbalance and character change. The results indicate that the impact of temporal constraints on tree shape is minimal and highlights the stability through time of the reference tetrapod phylogeny. Unexpected values of imbalance for Mississippian and Pennsylvanian time slices strongly support the hypothesis that the Carboniferous http://sysbio.oxfordjournals.org/ was a period of explosive tetrapod radiation. Several significant diversification shifts take place in the Mississippian and underpin increased terrestrialization among the earliest limbed vertebrates. Character incompatibility is relatively high at the beginning of tetrapod history, but quickly decreases to a relatively stable lower level, relative to a null distribution based on constant rates of character change. This implies that basal tetrapods had high, but declining, rates of homoplasy early in their evolutionary history, although the origin of Lissamphibia is an exception to this trend. The time slice approach is a powerful method of phylogenetic analysis and a useful tool for assessing the impact of combining extinct and extant taxa in phylogenetic analyses of large and speciose clades. [Character compatibility; diversification shifts; Mesozoic; Paleozoic; tetrapod terrestrialization; tree balance; tree distance.] Phylogeny reconstruction is a cardinal component they included both “contemporaneous” taxa and “fossil” of modern evolutionary biology because it provides taxa from an earlier interval (e.g., the Devonian)? What at University of Michigan on September 27, 2016 the fundamental framework for investigating the would a phylogeny look like from the standpoint of a dynamics of evolutionary processes, including tempo systematist living in the Permian, in terms of accuracy and mode of change and models of group diversification. and stability? The significance of these questions goes Tree shape may be substantially altered by different beyond the specific arrangement of taxa on the tree, and regimes of character and taxon inclusion/exclusion, factors such as the rate of character state changes and the and by different character coding, ordering and potential of later-evolving characters to erode the signal weighting schemes. As a result, much interest surrounds of earlier-evolving characters should be considered. phylogenetic stability, namely “the tendency for clades Beginning with the work of the “Woods Hole Group” that are resolved by an analysis to continue to be of paleontologists (Raup et al. 1973; Gould et al. 1977; resolved when either the data or the analytical method Schopf 1979; see summaries by Slowinski and Guyer is altered” (Davis 1993, p. 188). Numerous methods 1989; Mooers and Heard 1997; Huss 2009), tree shape are now available for measuring cladistic stability has been used to analyze the tempo and mode of (e.g., Felsenstein 1985; Bremer 1988; Goloboff 1991; cladogenetic events (e.g., Savage 1983; Heard 1992; Guyer Kållersïo et al. 1992; Davis 1993; Faith and Ballard 1994; and Slowinski 1993; Mooers and Heard 1997; Chan and Farris et al. 1996; Gatesy 2000), that is the amount of Moore 2002; Good-Avila et al. 2006; Heath et al. 2008). statistical support for tree nodes. However, a particularly Despite the important initial role of paleontologists, relevant aspect of stability in a paleontological context some subsequent work has focused on phylogenies of is the impact of taxa from different time intervals extant taxa only (although see Harcourt-Brown et al. on phylogenetic resolution. Because of such factors as 2001; Harcourt-Brown 2002). This “neontological bias” genetic saturation (e.g., Felsenstein 1978; Huelsenbeck is reflected by the fact that some recent applications and Hillis 1993) and morphological exhaustion (Wagner of diversification shift analyses to paleontological trees 2000a), later-evolving taxa might “erode” phylogenetic (e.g., Ruta et al. 2007; Lloyd et al. 2008; Botha-Brink signal among early-evolving taxa. Thus, it is important and Angielczyk 2010) required modifications of available to investigate whether phylogenetic stability (as defined methods to better fit the nature of fossil data (see also above) remains constant with the addition of later- Tarver and Donoghue 2011; Brocklehurst et al. 2015), evolving taxa, or whether it changes over clade even though the importance of fossil data has become history. As a metaphor (Wagner P.J. 2014, personal widely recognized (e.g., time-calibrating trees: Stadler communication), imagine a systematist living in the 2010; Parham et al. 2011; Didier et al. 2012). Harcourt- Pennsylvanian. How accurately could they reconstruct Brown (2002) suggested that analysis of tree balance the phylogeny of tetrapods using just the taxa in that at different time intervals in a group’s history could time period? Would the accuracy of their tree improve if provide insight into diversification patterns, but there 737 738 SYSTEMATIC BIOLOGY VOL. 65 has been little additional work on this topic. Here, we TABLE 1. The five time slices, their ages, and the number of taxa build on Harcourt-Brown’s (2002) study by examining which have their range in those slices changes in tree shape imparted by taxon addition during Time bin Age (Ma) Number of taxa successive time intervals, and discuss the implications of those changes. We focus on three complementary Devonian 419.2–358.9 6 aspects of tree shape: (1) stability, that is, the retrieval Mississippian 358.9–323.2 17 of identical mutual relationships among taxa when new Pennsylvanian 323.2–298.9 34 Permian 298.9–252.2 39 taxa are added to an existing data matrix; (2) balance, Mesozoic 252.2–66.0 7 that is, a measure of how symmetrical or asymmetrical a tree is; and (3) distribution of diversification shifts, Notes: The number of taxa considered in this study is 102: five taxa cross that is, occurrences of significant changes in rates of the boundary between two time slices, and have been considered as lineage splitting through time. In addition, we use belonging to both the time slices (ages from Cohen et al. 2013). character compatibility (e.g., Camin and Sokal 1965; Le Quesne 1969, 1982; Estabrook et al. 1976a, 1976b; presented here in light of future, more encompassing Downloaded from Meacham and Estabrook 1985) to examine how the studies. In that respect, our approach should be seen as structure of the data matrix yielding the trees of interest purely exploratory and the results from our investigation changes through successive time intervals. Empirical ought to be considered exclusively in light of the original work has shown that addition of fossils may alter findings in Ruta and Coates’ (2007). In summary, we hypotheses of relationships based on extant taxa only chose Ruta and Coates’ (2007) because the taxon sample http://sysbio.oxfordjournals.org/ (e.g., Gauthier et al. 1988; Cobbett et al. 2007), and in that study is large enough to allow us to investigate simulation studies have revealed that such altered clade stability over a relatively long time interval. We relationships may improve phylogenetic estimates (e.g., are aware that the study in question is neither the Huelsenbeck 1991; Wagner 2000b; Wagner and Sidor sole hypothesis of tetrapod interrelationships nor an 2000), a conclusion that has been backed up by real exhaustive treatment of taxa. We also note that the case studies (e.g., Cunningham et al. 1998). To build on lissamphibian radiation appears to be conspicuous only the metaphor of systematists living at different times in the Mesozoic, and remains modest at the beginning in the past (see above), strictly extant taxa are simply of that era (Marjanovi´cand Laurin 2014), so its impact is one particular case of “contemporaneous” taxa (i.e., taxa trivial for the case study presented here. from a single time slice). Fossil-based phylogenies allow at University of Michigan on September 27, 2016 us to look at different sets of “contemporaneous” taxa, and permit comparisons between “contemporaneous only”
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