[Palaeontology, Vol. 58, Part 6, 2015, pp. 937–952]

FRONTIERS IN PALAEONTOLOGY

EARLY PHYLOGENY OF CRINOIDS WITHIN THE PELMATOZOAN CLADE by WILLIAM I. AUSICH1, THOMAS W. KAMMER2, ELIZABETH C. RHENBERG3 and DAVID F. WRIGHT1 1School of Earth Sciences, The Ohio State University, 155 South Oval Mall, Columbus, OH 43210, USA; e-mails: [email protected], [email protected] 2Department of Geology and Geography, West Virginia University, Morgantown, WV 26506, USA; e-mail: [email protected] 3Department of Geology, Earlham College, 801 National Road West, Richmond, IN 47374-4095, USA; e-mail: [email protected]

Typescript received 2 June 2015; accepted in revised form 24 August 2015

Abstract: Phylogenetic relationships among early crinoids phyletic), hybocrinids and disparids. The Protocrinoida are evaluated by maximizing parsimonious-informative should be maintained, but the Aethocrinida should be placed characters that are unordered and unweighted. Primarily within the Cladida. The results of this study identify phylo- Tremadocian–Darriwilian (Early–Middle Ordovician) taxa genetic structure amongst the major early crinoid lineages are analysed. Stratigraphic congruence metrics support the and delineate the relative positions of crinoid higher taxa best phylogenetic hypothesis derived using parsimony meth- along a tree. Each valid higher taxon discussed herein ods. This study confirms the traditionally recognized lineages requires a comprehensive treatment to delimit within-lineage of Palaeozoic crinoids and provides new information on the phylogenetic relationships. branching order of evolving lineages. Camerates are basal crinoids with progressively more tipward groups (from an Key words: Echinodermata, Ordovician, phylogenetic Ordovician perspective) being protocrinoids, cladids (para- methods, stratigraphic congruence.

C RINOIDS are regarded as the most primitive of the five derm evolution? In this contribution, we adopt results living echinoderm classes (asteroids, crinoids, echinoids, from echinoderm universal elemental homology studies holothurians and ophiuroids), but the phylogenetic posi- that have demonstrated that crinoids are nested within tion of crinoids amongst Palaeozoic echinoderms has clades of other stalked echinoderms (Sumrall 2008, been widely debated. The oldest known crinoids are from 2010; Sumrall and Waters 2012; Kammer et al. 2013; the early Tremadocian (Ordovician) (Guensburg and Sumrall 2014). With stalked echinoderms, including cri- Sprinkle 2001, 2003, 2009; Guensburg 2010); and as part noids, recognized as a clade (the Pelmatozoa Leuckart, of the Great Ordovician Biodiversification Event (GOBE), 1848), phylogenetic relationships of early crinoid evolu- they diversified to become the dominant stalked echino- tion are examined. derm clade by the early Late Ordovician (Sandbian). Cri- Various hypotheses for the origin and early evolution noids became progressively more dominant amongst of crinoids have relied on the supposition that specific stalked echinoderms in most marine settings through the characters had special significance in identifying ancestor– remainder of the Palaeozoic and were instrumental in descendant relationships (e.g. ambulacral floor plates or establishment of the structure of Palaeozoic epifaunal lintels), that a priori interpretations of morphological suspension-feeding communities (Ausich and Bottjer trends (such as the reduction in the number of plates) 1982; Bottjer and Ausich 1987). dictated evolutionary vectors or that specific taxa must However, a consensus has been difficult to reach represent the outgroup. These studies and the arguments concerning the phylogenetic position of crinoids therein are in Sprinkle (1973, 1976), Ausich (1996, 1998a, amongst Ordovician clades and the early diversification b, c), Guensburg and Sprinkle (2003, 2007, 2009), Guens- of the Crinoidea. At the heart of this issue is a funda- burg et al. (2010) and Guensburg (2012) and do not need mental question of echinoderm phylogeny as a whole. to be repeated here. Rather, as discussed herein, computa- Are stalked echinoderms a clade or a grade of echino- tional phylogenetic methods have been used to determine

© The Palaeontological Association doi: 10.1111/pala.12204 937 938 PALAEONTOLOGY, VOLUME 58 both the outgroup taxa using universal elemental homol- glyptocystitoids, blastoids and coronoids and formally ogy (Sumrall 2014) and, herein, are used to test compet- recognized this homology scheme as universal elemental ing hypotheses for early crinoid phylogeny using the homology. They recognized the following characters as maximum number of phylogenetically informative equally homologous across clades: oral plates, primary peristomial weighted characters with no a priori assumptions of cover plates, ambulacral cover plates, ambulacral symme- ordering. try around the mouth, major body openings, and plating arrangements that follow Loven’s Law (Sumrall and Waters 2012). Finally, Kammer et al. (2013) extended the UNIVERSAL ELEMENTAL HOMOLOGY universal elemental homology scheme to include many radiate echinoderm clades, including the edrioasteroids, Historically, the morphological terminology for each pel- stromatocystitids, isorophids, various ‘eocrinoids’ (includ- matozoan group was largely derived independently of ing gogiids), edrioblastoids, glyptocystitoids, eumorpho- other groups. This created a confusing system where, for cystitoids, paracrinoids, coronoids and crinoids. Using example, a radial plate in one group may or may not be universal elemental homology and other characteristics, homologous to a radial plate in another group (Sumrall Sumrall (2014, 2015) demonstrated that the Pelmatozoa 2008; Sumrall and Waters 2012). This inability to separate is a clade and crinoids are nested within the Blastozoa homology from homoplasy based on existing character Sprinkle, 1973. Because the Blastozoa were defined as terms, coupled with the high morphological disparity separate from the Crinozoa (Sprinkle 1973, 1976), the within the Pelmatozoa, made any phylogenetic analysis of Pelmatozoa should now be restored to contain blasto- stalked echinoderms nearly intractable. zoans and crinoids. The solution to this problem is universal elemental homology. Sumrall (2008, 2010) recognized that the plat- ing of the ambulacral system (axial skeleton of Mooi and MATERIALS AND METHODS David 1998, 2008), particularly around the mouth, was morphologically conserved among echinoderms. Within a As part of the ‘Assembling the Echinoderm Tree of Life’ heterochronic framework, Sumrall (2008) identified project (www.echintol.org), crinoids have been coded homologies between Lepadocystis (glyptocystitoid) and using a rubric of 132 characters with a total of 568 poten- Hemicosmites (hemicosmitoid), considering only oral tial character states (Ausich et al. 2015, appendix 1). For plates and ambulacral floor plates. Sumrall and Waters the present study, all Tremadocian–Darriwilian (Early– (2012) developed this concept further by considering Middle Ordovician) crinoids and some Sandbian and

FIG. 1. Examples of the major lineages of Ordovician crinoids. A, protocrinoid, Glenocrinus globularis Guensburg and Sprinkle, 2003, FMNH PE 52733, Tremadocian (from Guensburg and Sprinkle (2003); reproduced with permission from the Paleontological Research Institution, Ithaca, NY). B, cyathocrinid, Porocrinus elegans Kesling and Paul, 1968, USNM 42196b, Sandbian. C, camerate, Diabolocri- nus arbucklensis Kolata, 1982, OU 8880, Sandbian. D, cladid, Fresnedacrinus ibericus Ausich et al., 2002, MNCN-I-35379, Darriwilian. E, disparid, Tetragonocrinus pygmaeus (Eichwald, 1860), PIN RAS 3038/101, Darriwilian. F, hybocrinid, Hybocrinus conicus Billings, 1857, USNM S2054, Sandbian. All scale bars represent 5 mm. AUSICH ET AL.: EARLY CRINOID PHYLOGENY 939

Katian (Late Ordovician) crinoids were considered additional criterion for evaluating equally most-parsimo- (Fig. 1). The character matrix appropriate for analysis of nious trees was set: topologies recovering protocrinoids the taxa considered here includes as many as 104 (Titanocrinus and Glenocrinus; Guensburg and Sprinkle parsimony-informative characters with as many as 445 2003, 2010) as sister taxa were preferred over topologies character states, depending on the exact analysis (data favouring a polyphyletic Protocrinoida. This preference matrix available in Morphobank, project P2182; http:// is based on their stratigraphic position and unique www.morphobank.org). mode of calyx growth among crinoids. In the end, 12 All analyses were conducted in PAUP 4.0a142 (Swof- Tremadocian–Darriwilian taxa were eliminated from ford 2015) using the criterion of maximum parsimony. most parsimony analyses (Table 1). All characters were initially treated as equally weighted The temporal stepwise phylogenetic approach of Ausich and unordered. Each analysis was a heuristic search with (1998a, b) recognizes that the branching at the base of a random addition that was repeated 1000 times. Branch clade has historical consequences for the entire clade. swapping was performed using the tree-bisection recon- However, the opposite may not be true; that is, the evolu- nection (TBR) algorithm. Both the strict consensus and tion in younger portions of a clade may not necessarily 50% majority-rule trees were evaluated, and Adams be used to constrain the phylogeny of earlier portions of consensus trees were evaluated where appropriate. The a clade. In the stepwise approach, only the oldest subset consistency index (CI), retention index (RI) and rescaled- of taxa are considered first. Then, progressively younger consistency index (RC) are presented for each tree. Boot- taxa are included in analyses. Ideally, this stepwise strap values and Bremer support were also calculated in approach will yield similar results at each step. Accord- PAUP 4.0a142. ingly, analyses are presented for Tremadocian–Dapingian Initial analyses using all taxa coded for this project crinoids, Tremadocian–Darriwilian taxa and Tremado- identified 38 724 most-parsimonious trees. The resultant cian–Darriwilian with a few Sandbian and Katian taxa. strict consensus (Ausich et al. 2015, fig. 1) is highly Homology among crinoid calyx plates is a matter that unresolved yet recovered several small clades including has received much discussion (Ubaghs 1978a; Simms some camerates, a monophyletic Hybocrinida, two TABLE 1. Rationale for not including certain Tremadocian– cyathocrine sister taxa, two disparid sister taxa and Darriwilian taxa in many analyses. three other disparids; however, no relationships among major crinoid groups are delineated. Further, if only Genus Explanation Tremadocian–Darriwilian crinoids are analysed, 2350 Adelphicrinus* Resultant analysis yielded 409 most-parsimonious trees are found. The resultant strict most-parsimonious trees with Adelphicrinus on consensus tree (Ausich et al. 2015, fig. 2A) is again lar- a polytomy with protocrinoids and basal gely one broad polytomy. Although poorly resolved, the cladids corresponding 50% majority-rule tree groups all dis- Cnemecrinus* Resultant analysis yielded 1042 most- parids together (with a few other taxa) and all post- parsimonious trees with protocrinoids split: Tremadocian camerates together. However, the pro- Cnemecrinus on a polytomy with Glenocrinus tocrinoids were not recovered as sister taxa, and Tre- and basal cladids madocian camerates are variously grouped with Delgadocrinus* Fewer than 50% of characters could be coded protocrinoids and cladids (Ausich et al. 2015, fig. 2B). Eknomocrinus Resultant analysis yielded 374 most- Three primary strategies, not mutually exclusive, were parsimonious trees with protocrinoids split: Eknomocrinus groups with Glenocrinus employed to increase topological resolution and to Isotomocrinus Plots as a disparid, but introduces polytomies make it possible to test competing hypotheses of phylo- and the base of and within the disparids – genetic relationships among early crinoid lineages. Each no changes to arrangement of major groups of these methods leads to a different subset of taxa for Maennilicrinus* Fewer than 50% of characters could be coded analysis. These strategies include the following: (1) Merocrinus Issues surrounding position of Merocrinus removal of problematic taxa (those contributing to discussed in the text character conflict) from analysis; (2) a posterior Othneiocrinus Fewer than 50% of characters could be coded reweighting of characters based on their rescaled-consis- Pandoracrinus* Plots as a disparid, but introduces a basal tency indices (sensu Kroh and Smith 2010); and (3) the polytomy and for all disparids – no changes stepwise stratigraphic sampling approach of Ausich to arrangement of major groups (1998a, b). A taxon was a candidate for elimination if Perittocrinus* Fewer than 50% of characters could be coded Putilovocrinus* Fewer than 50% of characters could be coded fewer than 50% of characters were coded and/or a Revalocrinus Fewer than 50% of characters could be coded taxon was identified as a ‘wildcard’ (Wiley and Lieber- man 2011) in an Adams consensus tree of all coded *Wildcard taxon from Adams consensus tree of all coded taxa taxa (Ausich et al. 2015, appendix 2). Also note an (Ausich et al. 2015, appendix 2). 940 PALAEONTOLOGY, VOLUME 58

1994; Ausich 1996, 1998a, b; Guensburg and Sprinkle Institute, Russian Academy of Sciences; USNM S, Springer 2003; Wright in press; and others). The calyx plate Collection, National Museum of Natural History, Smithsonian homology scheme used here is taken basically from Institution. Ubaghs (1978a), the traditional homology scheme, because this scheme is supported by what is known about OUTGROUP TAXA early development in both living and Palaeozoic crinoids. Modifications to the Ubaghs (1978a) scheme used in this study include the recognition of lintels (in only tricyclic Previous phylogenetic analyses of radiate echinoderms crinoids), and coding the C-ray aboral cup plates in some using universal elemental homology characters supported disparids as infer- and super-radial plates rather than the monophyly of the Pelmatozoa (Sumrall 2014, 2015). radial and anibrachials or brachianals (see Ausich 1996, Crinoids are nested within blastozoan clades, including 1998a). In addition, gap plates (Guensburg and Sprinkle ‘eocrinoids’, diploporoids and glyptocystitoids (Sumrall 2003) are coded. 2014). Thus, representatives for these clades were used as Alternative calyx plate homology schemes were also outgroups for analyses presented here, including the considered to test among competing hypotheses. For ‘eocrinoid’ Rhopalocystis, the diploporoids Echi- example, analyses were performed using disparids coded nosphaerites, Eumorphocystis and Protocrinites, and the with the homologies of Ausich (1996, 1998a, b), that is glyptocystitoids Cheirocystis and Glyptocystella. These taxa assuming the basal circlet was absent in all disparids. In are used to represent typical morphologies in these major some analyses, glyptocystitoid thecal plate circlets were clades and are not necessarily meant to suggest specific coded as if they were homologous to crinoid plate ancestors of the Crinoidea. circlets. In other analyses, specific crinoids were coded in In all cases, these six taxa have oral region plating simi- accordance with alternative homologies proposed by other lar or equivalent to that of early crinoids (Kammer et al. authors. However, as discussed below, none of the clado- 2013). Although all six of these taxa have characters that grams derived using alternative homologies yielded more clearly distinguish them from the Crinoidea and place compelling overall results than the basic aboral cup them within their respective clades, Eumorphocystis and homology scheme for crinoids (Ubaghs, 1978a, with Rhopalocystis share some non-oral-region characters with modifications noted above). In addition, the hypothesis crinoids. Eumorphocystis has erect exothecal feeding that Merocrinus is a pseudodicyclic crinoid (Guensburg appendages, and a large opening exits from these appen- 2012; Sprinkle and Guensburg 2013) was tested. dages into the theca. In addition, these exothecal appen- The R package strap (Bell and Lloyd 2015) was used dages are supported by a distinct radially positioned plate to plot a time-scaled phylogeny to geological time and to in the theca. However, note that these appendages differ calculate four stratigraphic congruence measures, includ- from crinoids by bearing brachioles. ing the Stratigraphic Consistency Index (SCI; Huelesbeck Rhopalocystis Ubaghs, 1963 is an unusual stalked echin- 1994), Relative Completeness Index (RCI; Benton and oderm. It has brachiolar appendages and epispires, so it Storrs 1994), Manhattan Stratigraphic Measure (MSM*; was placed in the ‘eocrinoids’, which is now understood Siddel 1998; Pol and Norell 2001) and Gap Excess Ratio to be a polyphyletic group (Ubaghs 1968; Sprinkle 1973; (GER; Willis 1999; see discussion in Bell and Lloyd Smith 1984; Paul 1988; Sumrall 1997; David et al. 2000; 2015). The calculated value for each measure is compared Zamora et al. 2013). However, the theca of Rhopalocystis to a null model generated through Monte Carlo simula- is organized like a crinoid. There are four plate circlets, tion resulting in a distribution of 1000 tree topologies, coded here as lintels, infrabasals, basals and radials. The thus allowing calculation of p-values for the observed lintel circlet is one fused plate, there are four infrabasals, metrics. Trees were time-scaled using the very conserva- and other circlets are comprised of five plates. Theca plate tive ‘basic’ approach where nodes are constrained to be circlets are basically offset from one another by 36 de- as old as their oldest descendant, commonly resulting in grees. The radial plates are radial in orientation, and fixed trees with many zero-length branches (Norell 1992; plates above the radial plates (‘fixed brachials’) lead Smith 1994). directly to the ambulacra. Between the ‘fixed brachials’, Analyses were performed on genera represented by there are interradial plates, and more plates are present in exemplar species. A listing of exemplar species is in the CD interray than in other interrays. Despite the lack Ausich et al. (2015, appendix 3). of arms and the presence of epispires, the calyx plating of Rhopalocystis is basically the same as that of crinoids, and Institutional abbreviations. FMNH, Field Museum of Natural coding used here reflects this. History; MNCN, Museo Nacional de Ciencias Naturales, Madrid, All six taxa were used and designated as outgroups for Spain; OU, Sam Noble Oklahoma Museum of Natural History, rooting purposes. However, various subsets of these six University of Oklahoma; PIN RAS, Borissiak Paleontological taxa were also considered in alternative analyses. AUSICH ET AL.: EARLY CRINOID PHYLOGENY 941

THE IMPERATIVE FOR PHYLOGENETIC 1996). Also, the Treatise included Proexenocrinus as a ANALYSES monobathrid camerate (Strimple and McGinnis 1972; Ubaghs 1978c) rather than as a diplobathrid camerate as The Crinoidea have been recognized as a distinct group it is currently understood (Ausich 1986). However, since of echinoderms since their definition by Miller (1821). 1978, the number of Early Ordovician crinoids has However, their early diversification and relationship to increased from 3 to 16 (Table 2); and significantly, the other echinoderms has never been settled. This includes number of Tremadocian crinoids has increased from one the epic debates of F. A. Bather versus F. Springer and C. to seven (Guensburg and Sprinkle 2003, 2009; Guensburg Wachsmuth (Wachsmuth and Springer 1897; Bather 2010), with additional taxa yet to be described (Gahn, 1899, 1900) as well as more recently developed alternative 2015). Further, since 1978 Echmatocrinus Sprinkle 1973 hypotheses (e.g. Sprinkle 1973, 1976; Ausich 1996, 1998a, has become widely regarded as a cnidarian (Conway b; Guensburg and Sprinkle 2003; Guensburg 2012; also Morris 1993a, b; Ausich and Babcock 1998, 2000; but see see discussions in Ubaghs 1978b). One way in which to Sprinkle and Collins, 1998, 2011). Thus, its morphology categorize thinking on this topic is: (1) literature leading is not relevant for understanding crinoid phylogeny. up to and including the 1978 crinoid Treatise (Moore Unfortunately, the increased knowledge of Tremado- and Teichert 1978); and (2) post-1978 literature. As cian crinoids clarified neither the position of the Cri- clearly illustrated by Moore (1952, figs 18–27) and noidea within the Echinodermata nor early crinoid Ubaghs (1978b, fig. 207), higher taxa (i.e. subclasses and phylogenetic relationships. Predictably, Tremadocian cri- orders) were readily identified, but essentially nothing was noids possess many familiar but also many surprising understood regarding the evolutionary inter-relationships morphologies. For example, the protocrinoids (Glenocri- amongst early crinoids. This lack of understanding was nus and Titanocrinus) have a mode of calyx plate growth driven largely by a lack of Early Ordovician crinoids. in which multiple generations of plates are intercalated Aethocrinus, Proexenocrinus and Ramseyocrinus were the between presumable major plate circlets. This growth style only Early Ordovician crinoids included in the Treatise is similar to that of many diploporoids (Parsley 1982) (Moore and Teichert 1978). Further, the plate homologies and unlike that in any other crinoids. Furthermore, all of of Aethocrinus were equivocal (Ubaghs 1969; Philip and the Tremadocian forms have ‘extra’ plating, either among Strimple 1971) and have remained an issue (Ausich the plate circlets of the aboral cup, plates fixed above the

TABLE 2. Tremadocian–Dapingian crinoids considered for phylogenetic analyses.

Protocrinids Camerates Cladids Disparids Aethocrinids* Hybocrinids

Darriwilian Cefnocrinus Brechmocrinus Caleidocrinus (Huxleyocrinus) Perittocrinus Hoplocrinus Neoarchaeocrinus Fresnedacrinus Coralcrinus Revalocrinus Trichinocrinus Merocrinus Delgadocrinus Tripatocrinus Morenacrinus Heviacrinus Iocrinus Isotomocrinus Maennilicrinus Margoiocrinus Pandoracrinus Putilovocrinus Schaldichocrinus Tetragonocrinus Vosekocrinus Dapingian Ibexocrinus Othneiocrinus Floian Adelphicrinus Archaetaxocrinus Inyocrinus Celtocrinus Compagicrinus Pogonipocrinus Proexenocrinus Elpasocrinus Ramseyocrinus Tremadocian Glenocrinus Cnemecrinus Apektocrinus Alphacrinus Aethocrinus Titanocrinus Eknomocrinus

Note that Alphacrinus, Aptektocrinus, Eknomocrinus, Glenocrinus and Titanocrinus are from the early Tremadocian; and Aethocrinus and Cnemocrinus are from the late Tremadocian. *Note that the present analyses do not support the Aethocrinida. 942 PALAEONTOLOGY, VOLUME 58 aboral cup (i.e. fixed brachials and/or fixed interradial characterized taxa (Table 1), analysis of the remaining 30 plates) or odd extra plating (i.e. in the AB interray of Tremadocian–Darriwilian crinoids yielded a compelling Aethocrinus). Also, surprisingly, representatives from four consensus of two most-parsimonious trees (Fig. 2B). This major clades (protocrinoids, camerates, cladids and dis- result has the same basic tree topology from analyses of parids) occur in rocks of early Tremadocian age from Tremadocian–Dapingian taxa (Fig. 2A). Camerates were Laurentia, indicating that crinoids likely originated during once again recovered as sister to the clade comprised of the Cambrian, on a palaeocontinent other than Laurentia, all other crinoids. Protocrinoids are tipward of camerates or both. In any event, the co-occurrence of morphologi- and sister to other crinoids. The paraphyletic cladids are cally distinct higher taxa in the oldest crinoid faunas basically pectinate (Aethocrinus and Fresnedacrinus are means that each of these groups are equally likely to grouped), with the first four cladids (Apektocrinus, represent the ancestral morphology. Fresnedacrinus, Aethocrinus and Archaetaxocrinus) having one to several fixed brachials and interradial plates. Again, Aethocrinus is nested within the cladids. Tipward cladids PHYLOGENETIC ANALYSIS RESULTS lack fixed brachials and interradial plates, but Compagicri- nus and Elpasocrinus have a compound radianal. The two Tremadocian–Dapingian taxa hybocrinids (Hoplocrinus and Tripatocrinus) branch within the paraphyletic Cladida. Finally, disparids form a Analysis of all 17 Tremadocian–Dapingian crinoids clade in the most tipward position (Fig. 2B). resulted in nine most-parsimonious trees (Ausich et al. Experimentation with variations of included taxa or 2015, fig. 3). The strict consensus of these trees identified character codings either radically degrades the resolution the Disparida as a clade, but all other taxa form a broad of the tree or makes no difference. For example, inclusion polytomy. In the corresponding 50% majority-rule tree, of the three Tremadocian–Dapingian camerates (Adelphi- camerates and cladids are intermingled, and protocrinoids crinus, Cnemecrinus and Eknomocrinus), which were are positioned as a derived group. excluded in the analyses that yielded Figure 2, yielded an However, a single well-resolved tree results from the unfavourable tree (Ausich et al. 2015, fig. 5) with 514 elimination of Adelphicrinus, Cnemecrinus and Eknomocri- most-parsimonious trees and protocrinoids variously nus, which were identified as potentially problematic taxa positioned. (Table 1). The resultant cladogram and phylogram In addition to calculated tree metrics, the stability of (Fig. 2A; Ausich et al. 2015, fig. 4) have camerates basal the tree in Figure 2B is evaluated in several ways. For to all other crinoids, and other clades and paraclades example, analyses were run in which taxa were added to emerging tipward in the following order: protocrinoids, those used in Figure 2B. In each case, analyses were per- cladids, Aethocrinus, and disparids. With this topology, formed adding a few well-understood Sandbian and the monobathrid camerate (Celtocrinus) is more basal Katian taxa that possessed characteristic morphology of than the diplobathrid (Proexenocrinus). Cladids with both their clades (Table 3). These include analyses with cladids fixed brachials and fixed interray plates (Apektocrinus and and hybocrinids added to the taxa evaluated in Figure 2B. Archaetaxocrinus) are more primitive than those with the If eight additional cladids and hybocrinids are evaluated calyx comprised of only aboral cup plates (infrabasals, along with the taxa used in Figure 2B, a single most-par- basals and radials). simonious tree is obtained (Fig. 3A; Ausich et al. 2015, fig. 6) with the branching order of major clades at the base of the tree remaining basically the same. In addition, Tremadocian–Darriwilian taxa cyathocrine cladids, hybocrinids and disparids each form monophyletic groups; and cyathocrinids and hybocrinids Similar results are obtained with the analysis of all are sister groups. Heviacrinus is the most plesiomorphic Tremadocian–Darriwilian crinoids. Analysis of all 41 Tre- disparid. This result (Fig. 3A) is regarded as our best phy- madocian–Darriwilian crinoids (Table 2) resulted in a logenetic hypothesis because in addition to the topology very poorly resolved tree (Ausich et al. 2015, fig. 2). of Figure 2B, this tree recognizes structure within the However, after elimination of ‘wildcard’ and poorly broadly paraphyletic cladids (e.g. hybocrinids and cyatho-

FIG. 2. Phylogenies for Tremadocian–Darriwilian crinoids. All results from PAUP 4.0a142; all analyses resulted from heuristic search with random addition and 1000 repetitions. A, Tremadocian–Dapingian crinoids, single most-parsimonious tree, tree length 232, CI = 0.612, RI = 0.612, RC = 0.375; bootstrap values above Bremer support values, as appropriate; B, Tremadocian–Darriwilian crinoids, strict consensus of two most-parsimonious trees, tree length 409, CI = 0.491, RI = 0.579, RC = 0.285; bootstrap values above Bremer support values, as appropriate. AUSICH ET AL.: EARLY CRINOID PHYLOGENY 943 944 PALAEONTOLOGY, VOLUME 58

TABLE 3. Sandbian and Katian crinoids considered in some analyses.

Camerates Cladids Disparids Hybocrinids

Anthracocrinus Carabocrinus Acolocrinus Hybocrinus Cotylacrinna Eoparisocrinus Cincinnaticrinus Hybocystites Diabolocrinus Illemocrinus Doliocrinus Gaurocrinus Palaeocrinus Glyptocrinus Porocrinus Paradiabolocrinus Triboloporus Pararchaeocrinus Triboloporus crinids are sister groups).With seven Sandbian camerates an evaluation of the tree topology versus the temporal added into an analysis, a more poorly resolved tree with position of genera on the tree. Figure 6 presents the cal- four most-parsimonious trees is generated (Fig. 3B). The culated stratigraphic congruence measures (dashed lines) major groups still persist. Camerates and protocrinoids of the observed tree against a null distribution of random form clades, but the camerates, protocrinoids and cladids tree topologies having the associated age data of the (including derivative taxa) are collapsed onto a polytomy. observed tree. For all metrics, the tree topology of All disparids form a single tipward clade (Fig. 3B). With Figures 3A and 5 fits the temporal distribution of genera three additional disparids added (Ausich et al. 2015, fig. significantly better than random (Table 4). 7), relationships amongst groups remain basically the Analyses were also run recoding calyx plate characters same with the topology of Figure 2B, with the exception following Ausich (1996, 1998a, b). This included glypto- that in the strict consensus a broad polytomy is present cystitoids (Glyptocystella and Cheirocystis) that were coded above Heviacrinus, the basal disparid. with lintels, infrabasals, basals and radials as the four All of these analyses recovered the Camerata, Pro- major plate circlets (proximal to distal). The cladogram tocrinoida, Hybocrinida and Disparida as distinct clades. that resulted from this analysis has more steps (Ausich All except one (which had a basal polytomy with camer- et al. 2015, fig. 8B); but otherwise, it is similar to the tree ates, protocrinoids, and all more tipward crinoids, in Figures 2B, 3A. However, note that disparids, hybocri- Fig. 3B) placed camerates as basal. Within the para- nids, some cladids and cyathocrines form a polytomy. phyletic cladids, cyathocrines were identified as a clade Additional analyses were run to consider the proposal and sister to the hybocrinids in Figure 3A. (Guensburg 2012; Sprinkle and Guensburg 2013) that Phylogenetic relationships were also evaluated with a Merocrinus is a pseudodicyclic crinoid. These analyses posterior weighting of characters (Kroh and Smith 2010). were executed with Merocrinus coded as a disparid and For this analysis, a heuristic search was performed on all with Merocrinus coded as a cladid (the lowest circlet crinoids used in the analyses in this study with coded as lintels). In both instances, numerous most-parsi- unweighted and unordered characters. An Adams consen- monious trees arose, and all taxa tipward of protocrinoids sus tree was used to identify and eliminate ‘wildcard’ are on a single broad polytomy (Ausich et al. 2015, figs taxa. The remaining taxa were analysed using posterior 9A, 10A). Results from the former place Merocrinus,as character weighting based on the rescaled-consistency well as Brechmocrinus and Morenacrinus, in the disparids index of each character in the pruned data set. This anal- (Ausich et al. 2015, fig. 9B). Alternatively, if Merocrinus is ysis resulted in one most-parsimonious tree (Fig. 4) with coded as a cladid, fewer most-parsimonious trees result similar topological relationships present on other analyses (Ausich et al. 2015, fig. 10B). Merocrinus is positioned on discussed above. However, note that Eknomocrinus plots the basal polytomy of disparids with Brechmocrinus and with cladids, and hybocrinids are nested within the Morenacrinus immediately basal. These results do not disparids. provide strong support for either hypothesis (Merocrinus The stratigraphic distribution of genera on the recov- is dicyclic versus pseudodicyclic). The structure of the ered tree topology is depicted in Figure 5, which is a Merocrinus aboral cup with a compound C radial and the time-scaled phylogeny of Figure 3A, our best phylogenetic C super-radial giving rise to both the C-ray arm and hypothesis. Stratigraphic congruence measures allow for the anal series are undoubtedly the characters aligning

FIG. 3. Phylogenies for Tremadocian–Darriwilian and some Sandbian crinoids. All results from PAUP 4.0a142; all analyses resulted from heuristic search with random addition and 1000 repetitions. A, tree in Figure 2B with six Sandbian cladids and two hybocrinids included, one most-parsimonious tree, tree length 497, CI = 0.433, RI = 0.571, RC = 0.247; B, tree in Figure 2B with seven Sandbian camerates included, strict consensus of four trees, tree length 546, CI = 0.458, RI = 0.585, RC = 0.268. H, Huxleyocrinus. AUSICH ET AL.: EARLY CRINOID PHYLOGENY 945 946 PALAEONTOLOGY, VOLUME 58

FIG. 4. Phylogeny for Tremadocian–Darriwilian and some Sandbian crinoids with ‘wildcard’ taxa eliminated and posterior weighting of characters, a single most-parsimonious tree, tree length 121.80, CI = 0.593, RI = 0.738, RC = 0.487. H, Huxleyocrinus.

Merocrinus with disparids. However, the fact that Merocri- the exclusion of the Inadunata and coronoids), includ- nus has a holomeric column argues against the suggestion ing, among others, Moore (1952), Ubaghs (1953), that this lowest circlet in Merocrinus represents stem Moore and Teichert (1978), Ausich (1996, 1998a, b), meres incorporated into the aboral cup (Guensburg 2012; Guensburg and Sprinkle (2003), and Guensburg (2012). Sprinkle and Guensburg 2013). The Cladida have long been recognized as paraphyletic because they contain the likely ancestors of the geologi- cally younger subclasses Flexibilia and Articulata DISCUSSION (Springer 1920; Simms and Sevastopulo 1993). Although neither flexible nor articulate crinoid taxa were included In the present analysis, our objective was to test the in the present analysis, our results also indicate the Cla- phylogenetic fidelity of Linnaean categories of crinoid dida has been a paraphyletic taxon since the Early higher taxa and to understand better the branching rela- Ordovician. Genera such as Apektocrinus, Aethocrinus, tionships among lineages. Consistent results were pro- Fresnedacrinus, Archaetaxocrinus and Compagicrinus were duced regardless of the analytical and/or taxon sampling consistently recovered as stem taxa with respect to strategy employed. All phylogenetic analyses recovered disparids, hybocrinids, cyathocrine cladids and more camerates, disparids, hybocrinids and protocrinoids as tipward dendrocrine cladids (Figs 2, 3A). Furthermore, a distinct, monophyletic lineages (note that the grouping minority of recovered tree topologies suggest that Cla- of protocrinoids was a precondition). This basically dida may be polyphyletic. Future studies investigating agrees with studies since Moore and Laudon (1943; with branching relationships among cladids and other crinoid AUSICH ET AL.: EARLY CRINOID PHYLOGENY 947

FIG. 5. Geological-time scaling of the best phylogenetic hypothesis (Fig. 3A) using the Datephylo function within strap (Bell and Lloyd 2015). lineages are necessary to identify monophyletic groups In addition to supporting the monophyly of most cri- and guide taxonomic revisions. Nevertheless, our analysis noid higher taxa, this study also provides new insight into supports the rapid branching and diversification of the phylogenetic relationships among these major groups. nearly all previously recognized higher taxa into Camerates are basal crinoids. From an Ordovician per- genealogically distinct lineages by the Early–Middle spective, the groups that emerge tipward from camerates Ordovician. are protocrinoids, cladids (paraphyletic), hybocrinids and Further, this result is consistent with crinoid mor- disparids. Neither protocrinoids nor Aethocrinus represent phospace studies (Deline and Ausich 2011), in which Tre- the most primitive crinoid morphology, but rather exhibit madocian crinoid lineages became established in distinct a combination of plesiomorphic and apomorphic charac- regions of morphospace. Subsequent radiation through ters. Regardless, with the exception of the relative posi- the Llandoverian primarily populated the same basic tions of camerates and protocrinoids, this fundamental regions of morphospace. The largest deviation was among topology agrees largely with that of Guensburg (2012), Llandoverian disparids, but the present results strongly and it contrasts with the conclusions of Ausich (1998a, support the disparids as a distinct clade. b), who recognized aethocrinids as plesiomorphic 948 PALAEONTOLOGY, VOLUME 58

FIG. 6. Stratigraphic congruence metrics for the best phylogenetic distribution (Figs 3A, 4). In each case, the observed value (dashed line) is compared to a null distribution produced using a Monte Carlo simulation based on 1000 trees. A, Stratigraphic Consistency Index (SCI); B, Relative Completeness Index (RCI); C, Gap Excess Ratio (GER); and D, Manhattan Stratigraphic Measure* (MSM*; see discussion in Bell and Lloyd 2015).

TABLE 4. Summary of significance tests assessing stratigraphic 1990; among others, see Ubaghs 1978b) and do not sup- congruence of the best phylogenetic hypothesis. port the hypothesis that crinoids were derived from a non-blastozoan echinoderm (Sprinkle 1973; David et al. Stratigraphic congruence Calculated value p-Value 2000; Guensburg and Sprinkle 2003, 2007, 2009; Guens- measure burg et al. 2010; Guensburg 2012). À Stratigraphic Consistency 0.556 4.1 9 10 2 Apektocrinus is the basal cladid in all analyses. In the Index analyses of Tremadocian–Dapingian taxa, Archaetaxocrinus À Relative Completeness 36.7 1.8 9 10 6 is immediately tipward of Apektocrinus (Fig. 2A); but in Index analyses of Tremadocian–Darriwilian crinoids, Aethocrinus 9 À6 Gap Excess Ratio 0.7 5.4 10 and Fresnedacrinus form the branch immediately tipward 9 À12 Manhattan Stratigraphic 0.143 4.3 10 of Apektocrinus (Figs 2B, 3A). With additional cladids and Measure* hybocrinids, Hoplocrinus is the basal hybocrinid, and the basal cyathocrinid is Illemocrinus (Fig. 3A). In analyses herein, if Heviacrinus is not included in an crinoids. The present results support the hypothesis that analysis (Fig. 2A), Alphacrinus is the basal disparid. Alter- crinoids were derived from within blastozoans (Bather natively, if Heviacrinus is included, it is the most basal 1900; Paul and Smith 1984; Smith 1984; Smith and Jell disparid (Figs 2B, 3A). The key primitive characters for AUSICH ET AL.: EARLY CRINOID PHYLOGENY 949 disparids appear to be either the extra fixed plating in homoplastic and may only be the result of high rates of Alphacrinus or the lack of compound radials in Heviacrinus. character change in Early Ordovician crinoids. For camerates, the monobathrid Celtocrinus is basal. Further analyses of only disparids and only camerates are required to clarify the base of the disparid and camerate CONCLUSIONS trees, respectively. Synapomorphies that separate crinoids from their blas- The phylogenetic results from this study provide a new tozoan ancestry include both the loss of blastozoan-grade view of early crinoid evolution. In previous analyses, the characters and the acquisition of novel characters. These ancestral morphology was assumed a priori, either as a include the loss of brachioles and loss of any thecal tricyclic form (Aethocrinus, Ausich 1998a, b)orasa respiratory structures (epispires or pore rhombs). Novel multiplated form (protocrinoids, e.g. Guensburg 2012). In structures at the base of the crinoid tree include acquisi- contrast, as stated above, the outgroup taxa used in this tion of arms, which are extensions away from the body study were chosen because they are representatives of taxa comprised of both ambulacral and calyx plating; and most closely related to crinoids based on analysis of radi- openings in the theca where the arms are articulated. Five ate echinoderms using universal elemental homology infrabasal plates, a radial circlet interrupted in the CD characters (Sumrall 2014, 2015). Further, the cladograms interray, and a pentameric column are also novel struc- generated here resulted from computational methods tures that separate crinoids from their immediate ances- using unweighted and unordered characters, with a con- tors. However, it is noteworthy that all of the newly certed effort to include only independent characters. acquired synapomorphies were subsequently lost in one Crinoids were derived from a blastozoan-grade ancestor. or more lineages. This is true even among the Ordovician Our fundamental understanding of the basic crinoid groups taxa studied here, as well as in other taxa throughout the (camerates, cladid paraphyly, disparids, hybocrinids and Palaeozoic. For example among Early and Middle Ordovi- protocrinoids) is confirmed, but their relationships during cian crinoids, Tripatocrinus has only recumbent ambu- the initial crinoid radiation is changed. In this view, camer- lacra fixed into the thecal wall; CD interray interruption ates are basal, with progressively more tipward groups is lost in disparids; infrabasal plates are lost in disparids, (from an Ordovician perspective) being protocrinoids, stem hybocrinids and monobathrid camerates; and a pen- cladids, hybocrinids and disparids. Camerates, disparids tameric column was lost in camerates and many other and hybocrinids are monophyletic groups, but cladids are a crinoids. Further, some crinoids (e.g. Porocrinus) redevel- paraphyletic group that include monophyletic hybocrinids oped pore structures (e.g. goniospires) during the and cyathocrine cladids as sister groups. The Protocrinoida Ordovician. This serves to emphasize the mosaic nature should be retained, but its mode of calyx growth is apomor- of crinoid evolution and the high degree of character phic. With Aethocrinus considered a primitive cladid, the plasticity that results from the modular, mesodermal Aethocrinida should be subsumed into the Cladida, pend- echinoderm skeleton. Character reversals are not unex- ing further discovery of additional tricyclic crinoids. This pected (Marshall et al. 1994; Wright in press); and also, study establishes the major crinoid groupings during the this illustrates the idea of character state exhaustion Early Palaeozoic and the phylogenetic relationships among (Wagner 2000; and others). them. Further, more detailed analyses are required to estab- Other characters, such as only circlets of plates, a radial lish phylogenetic relationships within each group. plate supporting a column of fixed plates, and exothecal appendages are persistent crinoid characters. However, Acknowledgements. We thank Andrew Smith for inviting this these characters were also novel acquisitions in some contribution and improving the results; J. Bohaty and G. D. Sev- blastozoan lineages; and, thus, potential plesiomorphies astopulo improved an earlier version of this manuscript; and S. for the Crinoidea. R. Cole, C. D. Sumrall and B. Deline for discussions of various As noted by Strimple and Watkins (1955) and Ausich ideas leading to this manuscript. Also, we thank the following et al. (1998), some Ordovician disparids have an unusual (in alphabetical order) for assistance with curated specimens: posterior interray similar to disparids with a compound Tiffany Adrain, University of Iowa; Roger Burkhalter, Sam Noble Oklahoma Museum of Natural History University of Oklahoma; C radial and the super-radial plate giving rise to the anal Jessica Cundiff, Museum of Comparative Zoology, Harvard series and an arm. Gahn (2015) recognized this condition University; Jean Dougherty, Geological Survey of Canada, on undescribed early Tremadocian camerates. Gahn Ottawa; Tim Ewin, Natural History Museum, London; Kathy (2015) suggested this single character could indicate a Hollis, US National Museum of Natural History; Brenda Hunda closer phylogenetic relationship between camerates and Cincinnati Museum Center; Kathy Leacock, Buffalo Museum of disparids than indicated by the results of this study. Our Science; Franz-Josef Lindemann, Natural History Museum, results, based on a parsimony analysis of a broad swath University of Oslo; Paul Mayer, Field Museum of Natural of morphological characters, suggest that this character is History; Ann Molineux, University of Texas, Austin; Sergey 950 PALAEONTOLOGY, VOLUME 58

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