800


Journal of Paleontology 91(4):799–814


This revival of interest inmorphologic phylogenetics is good news for paleontologists because nearly all phylogenies of fossil species are inferred using only morphologic character data. Indeed, there has been an increasing number of studies employing probabilistic approaches to estimate phylogenies with morphologic data, especially in paleontology (e.g., Wagner, 1998, 1999; Snively et al., 2004; Pollitt et al., 2005; Clarke andMiddleton, 2008; Pyron, 2011;Ronquist et al., 2012; Slater, 2013, 2015;Wright and Stigall, 2013; Lee et al., 2014; Close et al., 2015; Bapst et al., 2016; Gorscak and O’Connor, 2016). Particularly promising for systematic paleontology is the


advent of tip-dating approaches for inferring phylogenies contain- ing non-contemporaneous taxa (Pyron, 2011; Ronquist et al., 2012; Gavryushkina et al., 2014). Bayesian total-evidence tip-dating combines molecular sequences, morphologic character data, and temporal information on fossil distributions to simultaneously estimate the best tree topologies, branch lengths, and divergence times among extinct and extant lineages (Ronquist et al., 2012; Lee and Palci, 2015). Tip-dating approaches operate on the simple assumption that evolution can be modeled as a function of time, with either a strict or relaxed clock-likemodel of character change. Although most tip-dating studies combine fossil and living species (e.g., Pyron, 2011; Ronquist et al., 2012; Slater, 2013), tip-dating approaches equally apply to character matrices containing only morphologic data (Slater, 2015) and/or with only fossil taxa (Lee et al., 2014; Bapst et al., 2016; Gorscak and O’Connor, 2016). Moreover, mathematical models originally developed for studying the spread of viruses in epidemiology have found applications in fossil tip-dating (Stadler et al., 2012; Stadler and Yang, 2013; Gavryushkina et al., 2014). The ‘fossilized birth–death’ process (Stadler, 2010; Heath et al., 2014) has recently been applied within a Bayesian context as a more realistic tree prior distribution that accounts for macroevolutionary and sampling processes (Gavryushkina et al., 2014). This paper presents the first application of Bayesian tip-


dating methods to a fossil-only data set of invertebrate animals. Here, I examine phylogenetic relationships among early to middle Paleozoic crinoids (Echinodermata). Crinoids are parti- cularly amenable for the purposes herein because: (1) they have a well-sampled fossil record (Foote and Raup, 1996); (2) their skeletal morphology is highly complex and character-rich (Ubaghs, 1978; Foote, 1994; Ausich et al., 2015); and (3) test- ing phylogenetic hypotheses among crinoid higher taxa requires sampling non-contemporaneous taxa over long timescales (>107 years), making them an ideal system for implementing a tip-dating approach (Ronquist et al., 2012). Because the approach taken herein is novel to the invertebrate fossil record, I provide a brief discussion on Bayesian tip-dating and the fossilized birth–death process tree prior to familiarize the reader with these emerging methods. Although this makes the paper necessarily technical in places, it is hoped those sections will provide a useful resource for other systematic paleontologists interested in probabilistic approaches to fossil phylogenetics.


Previous work on crinoid phylogeny


The Crinoidea form the sister group to all other extant echino- derm classes (Asteroidea, Echinoidea, Holothruoidea, and Ophiuroidea) and have an extensive geologic history spanning


the Lower Ordovician (ca. 480 Ma) to the present day. Ever since Bather (1899) published his seminal work A Phylogenetic Classification of the Pelmatozoa, crinoid systematists have sought a robust evolutionary template for understanding the phylogenetic distribution of fossil and living species (Ausich and Kammer, 2001). Other than a few isolated studies con- ducted at low taxonomic levels (e.g., Kammer, 2001; Gahn and Kammer, 2002), most phylogenetic research using computa- tional methods has focused on inferring relationships within two key time intervals: the Ordovician and the Recent (Ausich, 1998; Guensburg, 2012; Hemery et al., 2013; Rouse et al., 2013; Ausich et al., 2015; Summers et al., 2014; Cole, 2017). These intervals are significant because they bookend the evolutionary history of crinoids into their early diversification during the Ordovician Period and their present-day diversity in marine ecosystems.However, these intervals are separated by ~480million years, and phylogenetic research linking post-Ordovician stem taxa with the crown Crinoidea remains a largely unexplored area of research (Simms, 1988; Simms and Sevastopulo, 1993; Webster and Jell, 1999). Crinoids are traditionally divided into several higher taxa,


including the Camerata, Disparida, Hybocrinida, Cladida, Flexibilia, and the Articulata (Moore and Teichert, 1978). Except for articulate crinoids, these groups first appear in Ordovician rocks. Despite more than a century of controversy, phylogenetic relationships among Ordovician taxa are reaching a consensus. For example, all recent analyses of Ordovician crinoids strongly support an early divergence between camerate and non-camerate crinoids (Guensburg, 2012; Ausich et al., 2015; Cole, 2017). Thus, the Camerata is the sister clade to all non-camerate crinoids. Similarly, both Guensburg (2012) and Ausich et al. (2015) recovered a monophyletic Hybocrinida as the sister clade to a subset of cladid taxa. Ordovician analyses also recovered a monophyletic Disparida as sister to the clade of cyathocrine cladids and hybocrinids (Guensburg, 2012; Ausich et al., 2015). However, relationships among taxa placed currently within the Cladida, and their relationships to other higher taxa, have been a long-standing problem in crinoid systematics (McIntosh, 1986, 2001; Sevastopulo and Lane, 1988; Kammer and Ausich, 1992, 1996; Simms and Sevastopulo, 1993). In his review of echinoderm phylogeny and classification,


Smith (1984) lamented the cladid portion of the crinoid tree was one of the “outstanding areas of ignorance in echinoderm phylogeny” (Smith, 1984, p. 456). Indeed, the Cladida (sensu Moore and Laudon, 1943) have long been considered a para- phyletic group because some nominal cladids are hypothesized to be more closely related to flexible and/or articulate crinoids than other cladids (Springer, 1920; Simms and Sevastopulo, 1993; Brower, 1995;Ausich, 1998;Wright, 2015).Unfortunately, recent phylogenetic analyses not only confirm that Ordovician cladids are a paraphyletic assemblage (Guensburg, 2012; Ausich et al., 2015), but also that the validity of theCladida and their constituent higher taxa (i.e.,Dendrocrinida andCyathocrinida) cannot be fully remedied by simply adopting Simms and Sevastopulo’s(1993) recommendation to place the Flexibilia and Articulata within the Cladida. In addition, because the monophyletic status of a taxon requires a temporal reference frame (conventionally taken as the present day), it is unknown whether some recovered ‘clades’ in Ordovician analyses retain their monophyletic status when


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