Introduction

The origins of crinoids remain debated in disparate approaches (most recently Guensburg, 2012; Ausich et al., 2015a, b; Guensburg et al., 2016; Sheffield and Sumrall, 2019a, b). Bearing on this issue are the earliest-known (Tremadocian, 485.4–477.7 Ma), crinoids, but the fossils are few and imperfect (Ubaghs, 1969; Guensburg and Sprinkle, 2003, 2009; Guensburg, 2012; Guensburg et al., 2016). Athenacrinus new genus, described here, adds clarity to our understanding of earliest-known crinoid arms. We use new morphologic data, together with those from other Tremadocian crinoids, to characterize this skeletal construction of arms and to compare similar anatomy outside the crinoid clade with that of more archaic echinoderms. This information invites a reanalysis of crinoid origin using a new phylogenetic dataset. Arm data from Tremadocian crinoids, combined with data from younger (Floian, late Early Ordovician) crinoids documents the events preceding the acquisition of typical Paleozoic crinoid morphology.

Athenacrinus n. gen. is the earliest-known crinoid to express so-called ‘biradial’ morphology. This type of cup plating characterizes many disparid crinoids in which fixed ray plating consists of single elements in some rays, and two plates in others. A new explanation for the origin of this morphology is offered.

The known crinoid record begins during the middle Tremadocian (excepting the problematic middle Cambrian fossil Echmatocrinus Sprinkle, 1973). Oldest in this succession are the camerate-like protocrinoids Glenocrinus Guensburg and Sprinkle, 2003 and Titanocrinus Guensburg and Sprinkle, 2003, along with the cladid-like form Apektocrinus Guensburg and Sprinkle, 2009. Titanocrinus is joined up-section by the camerate-like Eknomocrinus Guensburg and Sprinkle, 2003 and the earliest disparid-like crinoid, Alphacrinus Guensburg, 2010. Aethocrinus Ubaghs, 1969 and the earliest Athenacrinus n. gen. occur just below the Floian boundary. A broad picture of Tremadocian crinoid evolution based on these occurrences is characterized by standardization and reduction that accompanied emergence of camerate, cladid, and disparid clades.

Materials and methods

Taphonomy and preparation.—Syntaxial overgrowths and dissolution weathering, along with abrasion, require consideration in the context of the finely detailed morphology described here. Taphonomic effects are patchy and vary within and among specimens. Etching corrodes plate surfaces, whereas evidence of syntaxial overgrowths cover and fill fine details in many places. Because of the importance of these effects in interpretation, detailed preservation information is found in the section Hypodigm, preservation and localities under Systematic paleontology.

An air scribe was used for rough preparation; specimens were finished by hand with fine needles, a slow method needed for the indurated matrices. The paratype USNM 165237 was previously prepared by air abrasion. Most images are multifocus montages prepared at the Field Museum with a Leica DMS 300 digital microscope and software. Large field montage images were prepared at the Illinois Natural History Survey, Urbana. Imaging included dry, water-immersed, and ammonium chloride-coated views under various lighting.

Terminology.—Basic terms including theca, floor, and cover plates, and interradials are used consistently as homologous across all of the early echinoderms discussed here. Crinoid terminology is that of Ubaghs (1978) with the following exceptions: (1) the cup base circlet, ‘basals' according to the Treatise on Invertebrate Paleontology (Ubaghs, 1978), are here considered ‘infrabasals' (Guensburg and Sprinkle, 2003), and (2) biradial terminology used for disparids is not accepted; instead radials are the first ray plates. Subsequent plates are designated fixed cup-like (wide, similar to radials) or free brachials, regardless of relative position (see section Disproportionate cup ray plating in disparid crinoids: ‘Compound radials' and ‘biradials,’ below).

Two-tiered cover plating here refers to cover plates stacked in rows, as distinct non- or little-intercalated layers. Presumably these formed a continuous but slightly flexible sheet that was hinged at the contact with floor plates. This trait is not unique to crinoids, occurring elsewhere in certain edrioasterid edrioasteroids (e.g., Paredriophus Guensburg and Sprinkle, 1994, Pseudedriophus Sprinkle and Guensburg, 2015), more derived forms that retain axial anatomy similar to plesiomorphic nonblastozoan basal pentaradiates (e.g., Camptostroma Ruedemann, 1933, Stromatocystites Pompeckj, 1896, Kailidiscus Zhao et al., 2010). No standardized terminology exists for the two tiers of arm cover plating, and no terminology links cover plates of edrioasteroid-like basal pentaradiate echinoderms with those of early crinoids. ‘Primary' was used for lateral, and ‘secondary' for medial cover plates in previous work on the Cambrian basal pentaradiate Stromatocystites (Paul and Smith, 1984). ‘Inner' and ‘outer' were used by Brower (2006) for two-tiered Late Ordovician crinoids. The term ‘lappets' was applied to camerate crinoids with a single biserial tier (Kolata, 1982) and, in some cases, to extant crinoid cover plates (Clark and Clark, 1915). ‘Lateral' and ‘medial,' implemented here, apply to early crinoids and to cover plates of edrioasteroids and edriosteroid-like early taxa. Lateral cover plates can be considered homologous to ‘primary’ elements, and medial cover plates in part homologous to any other cover plate elements that occur more medially.

Plates separating the axial complex from free brachials occur in the early cladid-like Apektocrinus and Aethocrinus, as well as the protocrinoid Titanocrinus. Here, these are called ‘extraxial lateral plates.' It is critical to recognize that these are not cover plates, which can be superficially similar. Extraxial laterals lie aboral to the floor plates, interradial elements extended from and contiguous with the tegmen field. Lateral cover plates are of axial origin and lie adoral to floor plates, extraxial laterals are aboral, being extended interradial elements. Similar plates are found in living crinoids, in which they are termed ‘laterals' (Roux and Lambert, 2011, and others), but have also been referred to as ‘adambulacrals’ (Breimer, 1978). The latter term is not preferred because it has long been used in extant forms such as asteroids for elements that are most likely not homologous (Mooi and David, 2000). These can be irregular plate fields, exemplified by the stalked Gephyrocrinus messingi (Roux and Lambert, 2011, fig. 3), or organized in a single row, exemplified by the comatulid Pachylometra inequalis (Clark and Clark, 1915, pl. 27, fig. 1168). These latter series superficially resemble lateral cover plates, but are, in fact, extraxial laterals.

Terminology for blastozoans follows Parsley (1982; Eumorphocystis Branson and Peck, 1940), Paul (1968; Macrocystella Callaway, 1877), Ubaghs (1968; Rhopalocystis Ubaghs, 1963), and Sprinkle (1973; Cambrian eocrinoids), except that we make the distinction that all extraxial morphology is treated as nonhomologous with crinoids, including terms such as ‘basals' and ‘radials’ that have been used interchangeably (see Guensburg and Sprinkle, 2007). Distinctions to this effect are created in the character list used in the phylogenetic analysis (see section Independent origins of crinoids and blastozoans among early radiate echinoderms, below).

Repositories and institutional abbreviations.—Athenacrinus broweri n. gen. n. sp. specimens are deposited in the Field Museum of Natural History (PE), Chicago, Illinois, and the National Museum of Natural History (formerly United States National Museum, USNM), Washington, DC. Figured specimens of other taxa are housed in the Field Museum; Museum of Comparative Zoology (MCZ), Harvard University, Cambridge, Massachusetts; Muséum National d'Histoire Naturelle (MNHN) Paris; Paleontology Repository, Sam Noble Museum (OU), University of Oklahoma, Norman; University of Illinois (UI X), Urbana; University of Iowa (SUI), Iowa City; Non-vertebrate Paleontology Laboratory (####TX###, NPL), University of Texas, Austin; and Yale Peabody Museum (YPM), New Haven, Connecticut.

Systematic paleontology

Figure 1.

Athenacrinus broweri n. gen. n. sp., holotype PE 52742, small calyx with short anal sac and proximal stalk: (1) entire, immersed; (2–5) AB, C, A, and E views, respectively, all immersed except coated E view, E radial proportionately shorter than other radials; (6, 7) AB and AE interrays and tegmen, several small cover plates extending over peristome area, small rounded plates filling tegmen interrays, dry uncoated images.

Figure 2.

Athenacrinus broweri n. gen. n. sp.: (1, 2) paratype PE 52750, large cup showing rays A, B, and E with proximal stalk: (1) entire specimen, coated; (2) cup and stalk, proximal two meres not reaching laterally adjacent meres, four primibrachials above short E radial, immersed; (3) paratype USNM 165237, flattened cup with short stalk segment, CD view, irregular posterior plating, small gaps between adjacent primibrachials accentuated by air abrasion, immersed; (4–8) paratype PE 52751, disarticulated cup with articulated arm, arm segments, and stalk: (4) entire specimen, coated; (5) disarticulated cup, cover plating showing tegmen to arm transition, immersed; (6) similar view with cup plates and proximal stalk pentamere ring in cross section (left) showing large round lumen and fine crenulae; (7) proximal stalk, slightly weathered showing marginal crenulae, coated; (8) two views of separate medial-distal stalk segment, above with short projections centered on pentameres, accessory ossicular covering, below weathered on right showing pentameres beneath ossicular layer, coated.

Figure 3.

Athenacrinus broweri n. gen. n. sp.: (1–4) paratype PE 52751 (continued from Fig. 2.1–2.4): (1) adjacent ramules or armlets, midarm, medial cover plates in regular alternating double biseries, immersed; (2, 4) well-preserved arm segment: (2) brachials just visible at bottom, then floor plates (small rectangular elements), large rectangular lateral cover plates, and alternating double or triple series along perradial suture above, coated; (4) specimen turned to accentuate cover plates, dry, raking light; (3) arm trunk with two branchings, irregular plating below; (5) paratype PE 52753, well-preserved collapsed proximal cup, BC view, anibrachial apparently primibrachial one, attached proximal stalk segment and detached medial stalk with small, ∼ 1 cm missing interval, pentameres with spinose processes, coated; (6–8) paratype PE 52752, associated arm and stalk segments: (6) medial stalk and adjacent arm segment, meres with attachment pits, coated; (7) distal stalk transitioning below to plate mosaic, coated; (8) much of surface with specimen segments showing articulated long arm segment with two branchings below, then long section without branchings, dry uncoated.

Origin of the crinoid arm

Crinoid arms are not derived from blastozoan feeding appendages.—Crinoid and blastozoan feeding appendages are constructed in fundamentally distinct ways, with significantly different topologic relationships among only partly homologous body walls and body cavity systems (Ubaghs, 1953, 1978; Sprinkle, 1973; Mooi and David, 1998; Guensburg and Sprinkle, 2007; Guensburg et al., 2016). The character list and coding reflect these distinctions, which have not yet been fully implemented in a phylogenetic analysis. This interpretation is further supported by character evidence provided in this study. Briefly, blastozoan and crinoid arms express ambulacral floor and cover plates; no one has challenged the homology of these plate systems, and these are found in other major groups of echinoderms as well. Floor plates in blastozoans can form exposed primary appendage and brachiole structures. However, in crinoids, floor plates are thin, largely internal structures that the most crownward crinoids do not express at all as stereom; these are instead represented by the tissue shelf that lies adoral to the extensions of the right and left somatocoels, but still supports the water vascular system (Nichols, 1960, figs. 4, 5; Mooi et al., 2005). Crinoid appendages extend from the ambulacral rays on the tegmen, and are supported by brachials derived from the extraxial thecal wall. Crinoid appendages always house extensions of the left and right somatocoels entering the arm at the thecal shoulders, emanating from these coeloms from within the theca. Blastozoan appendages lack these thecal openings and therefore also lack left and right somatocoel components, although presumably they were present as coeloms within the theca.

Figure 4.

Athenacrinus broweri n. gen. n. sp., paratype PE 52752: (1, 4) two proximal arm segments: (1) entire, coated; (4) detail of best preserved lower right-hand portion, floor plates nestled into brachials, above series face on, below edge on, wedge-shaped podial basins, best preserved on left with faint rims and slotted articulating cover plates, three sequential small podial pores on right, coated, compare Figure 11.5 and 11.6, similar two-tiered cover plating and wedge-shaped podial basins; (2, 3, 5–7) polished surfaces of medial to distal arm cross sections at or near right angles to arm axes, with syntaxial overgrowths, hints of dark organic matter, immersed: (2) distal arm, floor plates in near original position; (3) overview of associated cross sections depicted at lower magnification, current oriented segments; (5–7) three medial arm cross sections, much enlarged, subsidiary groove at bottom of adoral groove, floor plates collapsed or disarticulated: (6) an ?axillary with dual subsidiary groove.

It has recently been proposed that a Late Ordovician blastozoan, Eumorphocystis multiporata Branson and Peck, 1940, constitutes a plesiomorphic sister group to crinoids (Sheffield and Sumrall, 2019a). A more complete response to this claim will be published elsewhere, but its relevance to the present work and the phylogenetic analysis require that a summary response be provided here. The putative sister-group claim is predicated on the observation that this taxon expresses arm cavities interpreted to have housed coeloms (left and right somatocoels). Therefore, the triserial arms of Eumorphocystis are assumed to be homologous with those of certain early crinoids (e.g., Athenacrinus n. gen, n. sp.). However, observation of 10 Eumorphocystis specimens other than the single example used in Sheffield and Sumrall (2019a) to hypothesize the existence of this homology indicates that these similarities are superficial. Most important among this evidence is that the specimen studied by Sheffield and Sumrall (2019a) provides incomplete information regarding putative coeloms. As preserved, the arms of this specimen do not reveal a situation in which these longitudinal appendage cavities are contiguous with the thecal cavity. Other specimens that we examined have appendages broken at their bases and preserve all of the elements necessary for an accurate portrayal of this relationship. These show that the large arm cavities of Eumorphocystis are confined to feeding appendages. These taper to form small pores in thecal floor plates that do not extend through the shoulder wall (Fig. 9). The function of such arm lumens is unclear. Earliest crinoids express large cavities that taper along the arms outward from the theca, with lateral plate fields separating the brachials from the floor plates (Guensburg and Sprinkle, 2003, pl 1.4; Guensburg and Sprinkle, 2009, figs. 1.2, 5.3; Fig. 10.1). It is this continuity, in conjunction with known patterns of early development in modern crinoids, which indicates the existence of left and right coelomic extensions throughout not only the full length of the arms, but also the pinnules as well (summarized by Hyman, 1955; Heinzeller and Welsch, 1994; and others). Eumorphocystis expresses biserial cover plating unlike the two-tiered patterns documented for earliest crinoids here. Every other trait of this taxon's skeleton indicates that it is a derived blastozoan, some anatomy of which is homoplastic with crinoids (see Parsley, 1982, for a similar interpretation).

Figure 5.

Athenacrinus broweri n. gen. n. sp., line drawings with radials in black: (1) paratype USNM 165237, plate tracing, CD view, irregular posterior plating, much enlarged; (2) cup plate layout, A on right, based largely on holotype PE 52742, D fixed primibrachials provided from USNM 165237, C and E ray primibrachials one cup-like, disproportionately larger than those of other rays, AE interradials extending upward to level of primibrachials three or four, A, B and D rays with unknown number of fixed primibrachials, much enlarged.

Figure 6.

Athenacrinus broweri n. gen. n. sp., paratype PE 52751, arm-to-tegmen transition, traced, arm medial elements not well-exposed, partly covered, not individually depicted; compare Figure 2.5 and 2.6. blue = lateral cover plates (axial); gray = brachials (extraxial); green = laterals, not present here (extraxial); orange = floor plates (axial); purple = medial cover plates (axial).

The earliest crinoid arms.—This discussion centers on recognition of a morphology characterizing the earliest crinoid arms from the middle Tremadocian (Figs. 2–4, 10, 11). As discussed above, modern crinoid anatomy reveals that arms are composite constructs—part axial, part extraxial (David et al., 2000; Mooi et al., 2005). Tremadocian crinoid skeletal anatomy reflects this duality even more than later taxa and begins to bring into focus the range of morphology present at that time. Data for their arm interiors are incomplete, but reasonably well-known for at least one taxon across the range of high-ranking taxa present at that time—disparid-like, cladid-like, and the camerate-like forms.

Figure 7.

Schematic cross sections of representative Tremadocian (1–3) and Sandbian (4–9) crinoid arms showing morphologic change through time, secondary grooves in aboral channels, much enlarged, homologous elements color coded as in Figure 6: (1) cladid-like Apektocrinus ubaghsi Guensburg and Sprinkle, 2009, 1983TX1; (2) camerate-like Titanocrinus sumralli Guensburg and Sprinkle, 2003, PE 52720; (3) disparid-like Athenacrinus broweri n. gen. n. sp., paratype PE 52753; (4) rhodocrinitid camerate Archaeocrinus snyderi Guensburg, 1984, unnumbered brachial on same slab with UI X-5738; (5, 6) disparid Doliocrinus pustulatus Warn, 1982, brachial outline from 1113TX51 and 1279TX177, showing transition from secondary groove to nearly fully enclosed foramen within brachial, cover plates added from Doliocrinus monilicaulis Guensburg, 1984, UI X-5716; (7) Columbicrinus crassus Ulrich, 1925, UI X-5711, brachial outline from Guensburg (1992); (8) hybocrinid cladid Hybocrinus bilateralis Guensburg, 1984, UI X-5867 and 5868, and (9) cladid Cupulocrinus crossmani Brower, 1992, SUI 62895A and 62895C, secondary groove based on unnumbered specimens of Cupulocrinus gracilis in Field Museum collections.

The ambulacral parts of the axial skeleton of earliest crinoids can be traced to the early Cambrian Camptostroma, an archaic edrioasteroid-like form with stubby arm-like structures (Durham, 1966, text-fig. 1; Derstler et al., 2018). A distinctive sequence orthogonal to the plane of the ray includes the podial basin and pore-bearing floor plates, and cover plates in rows diminishing in size as they meet from either side of the ambulacrum over the perradial suture. Initially in Camptostroma, these plate series are not as standardized or geometrically consistent, but the sequence is the same. This basic pattern occurs not only in the earliest, middle Tremadocian, crinoids (Guensburg and Sprinkle, 2003, 2009; Figs. 3.1, 3.2, 3.4, 4.2, 4.4–4.7, 10, 11.3, 11.4), but also edrioasterid edrioasteroids (Sprinkle and Sumrall, 2015) (e.g., compare Figs. 3.2, 3.4, 4.2, and 4.4–4.7 with Figs. 11.5 and 11.6) and the edrioblastoid Cambroblastus Smith and Jell, 1990 (Zhu et al., 2014).

Cover plates.—Earliest crinoid cover plates occur in two tiers—lateral and medial. It is important to recognize that two tiers refers to discrete layers or stories of cover plates, not a multiseries sequence within a single tier. Lateral cover plates are squared elements, whereas medials are lath- or wedge-shaped elements arranged in an alternating double biseries pattern. Relative sizes vary by taxon. The medial cover plates of Titanocrinus and apparently Eknomocrinus are larger than lateral cover plates (Figs. 7.2, 8.2, 10.3, 10.5, 10.6, 11.1), whereas lateral cover plates are larger than medials in Aethocrinus, Apektocrinus, Athenacrinus n. gen., and Alphacrinus (Figs. 3.1, 3.2, 3.4, 4.2, 4.5, 6, 7.1, 7.3, 8.1, 8.3, 8.4, 10.2, 10.8, 11.3, 11.4) (Note: cover plates in general were not illustrated with sufficient clarity to allow interpretation in the works of Guensburg and Sprinkle, 2003, 2009, and other earlier workers. Much of the earlier ambiguity in interpretation has resulted from preservational artifacts and unfavorable orientations. Preparation of previously collected and well-preserved material such as that of Athenacrinus n. gen. has helped to resolve this issue.) Floor plating is largely or fully internal in crinoid arms. They are fully internal in Titanocrinus and possibly Eknomocrinus (Figs. 8.2, 10.5, 10.6, 11.1). If exposed, these are exposed along the lateral margins of the ambulacra (Fig. 10.2, 10.7, 10.8). Podial basins range from round in the cladid-like Apektocrinus and possibly Aethocrinus (Guensburg and Sprinkle, 2009, fig. 7.3; Fig. 10.7) to wedge-shaped in the disparid-like Athenacrinus n. gen. described here (Fig. 4.4; Table 1).

Figure 8.

Color-coded tracings of Early (Tremadocian) (1–4) and Late (Sandbian/Katian) (5–10) Ordovician crinoid mid-distal arm segments showing plating from one side: (1, 2) earliest-known crinoids, neither with exposed brachials: (1) Apektocrinus ubaghsi Guensburg and Sprinkle, 2009, 1984TX1, deeply weathered, many elements fragmentary, outlines incomplete, prepared from Figure 1.8; (2) Titanocrinus sumralli Guensburg and Sprinkle, 2003, PE 52720, weathered, most element outlines preserved, floor plates unexposed except on left where laterals have fallen away, traced from Figure 10.6; (3, 4) slightly younger taxa: (3) cladid-like Aethocrinus moorei Ubaghs, 1969, YPM 517777, latex cast, plate outlines partially exposed; (4) disparid-like Athenacrinus broweri n. gen. n. sp., paratype PE 52751, medial cover plates showing primary, secondary, and ?tertiary elements, plate outlines well preserved except for medial cover plates, these slightly weathered, traced from Figure 3.2; (5–10) line drawings modified from Brower (2006, fig. 1): (5) disparid Cincinnaticrinus varibrachialis Warn and Strimple, 1977, MCZ 136884; (6) disparid Ectenocrinus simplex (Hall, 1847), MCZ 133457; (7) camerate Euptychocrinus skopaios Brower, 1994, SUI 80173; (8) cladid Cupulocrinus crossmani Brower, 1992, SUI 62895C; (9, 10) cladid Hybocrinus conicus Billings, 1857: (9) SUI 49484, juvenile with single biseries, and (10) SUI 80030, mature specimen with two-tiered pattern. Color coding as in Figure 6. Scale bars = 1 mm.

Extraxial lateral plates.—The extraxial skeletal region of the earliest crinoids consists of brachials and lateral plate pavements, fields of small plates separating the brachials from the axial skeleton oral to these fields. The extraxial lateral plates are thin and extend to the arm tips in the camerate-like Titanocrinus (Fig. 10.5) and at least to the midarm in the cladid-like Aethocrinus and Apektocrinus (Guensburg and Sprinkle, 2009, figs. 1.2, 2; Guensburg et al., 2016, fig. 5E; Fig. 10.1). In these cases, the axial skeleton (cover and floor plates) lies oral to (above in life position) the brachial (adoral) channel. Extraxial lateral plate fields are lacking in Alphacrinus, Athenacrinus n. gen., and other early disparids (Figs. 3.1, 3.2, 3.4, 8.4, 11.3, 11.4). Floor plates are concealed beneath lateral plates in Titanocrinus, Eknomocrinus, Alphacrinus, and possibly an undescribed Floian disparid (Figs. 3.2–3.4, 10.3, 10.5, 10.6; Table 1), but their edges are laterally exposed in Apektocrinus, Aethocrinus, and most Athenacrinus n. gen. (Guensburg and Sprinkle, 2009, fig. 1.2; Figs. 3.1, 3.3, 3.4, 4.2, 4.5, 8.1, 8.3, 8.5, 10.8, 11.3, 11.4). In these instances, arm floor plates rest directly upon brachials and nestle into the adoral channel. The adoral channel in earliest crinoids contains a secondary medial groove that might have housed the brachial nerve (Figs. 4.5–4.7, 7.1–7.3).

Figure 9.

Eumorphocystis multiporata Branson and Peck, 1940, a diploporan blastozoan; OU 9048, view of E ray, broken surface adjacent to the thecal wall, no opening to the thecal interior.

Later transformations.—The Tremadocian pattern transitioned to more standard Paleozoic patterns during the Floian. Changes included: (1) extraxial lateral field size reduction or disappearance, (2) floor plates nestling into the adoral channel, but later not expressed as skeletal elements, and (3) medial cover plates consisting of a single biseries or entirely absent. This pattern persists into the Late Ordovician and beyond (Table 2). Diminutive taxa, and those with pinnulate morphology (e.g., Celtocrinus Donovan and Cope, 1989, Proexenocrinus Strimple and McGinnis, 1972) express a single cover plate tier or biseries. Juvenile Hybocrinus conicus Billings, 1857 are single-tiered, but the adults are two-tiered (Brower, 2006, fig. 1), suggesting paedomophosis as a mechanism for the reduction of tier numbers in other taxa. Patterns of taxonomic distribution suggest that cover plate transformations occurred asynchronously among major clades, these having emerged during the Tremadocian. The secondary medial groove submerges to become a longitudinal foramen fully encased in brachials by the Late Ordovician among disparids (Figs. 7.5–7.7), but not among cladids or camerates (Fig. 7.4, 7.8, 7.9).

Figure 10.

Cover and floor plates of Tremadocian crinoids: (1, 2, 4) cladid Aethocrinus moorei Ubaghs, 1969: (1, 4) MNHN A49684: (1) tegmen to arm transition showing collapsed delicate platelet pavement separating brachials from floor plates that line the arm interior; (4) floor plate series above brachials, showing podial pores; (2) YPM 517777, brachials, floor plates, large lateral cover plates, medial cover plates partly disarticulated, with chevrons = position of Figure 6.3; (3) camerate-like protocrinoid Titanocrinus sp., PE 52722, medial arm, brachials weathered away revealing floor plates with podial pores or basins; (5, 6) Titanocrinus sumralli Guensburg and Sprinkle, 2003, holotype PE 52720, dry uncoated: (5) distal arm showing flattened, splayed lateral pavement, isotomous branching, with arrow = brachials, chevrons = position of Figures 1.6 and 5.2; (6) enlargement from (5); plating, in order from below: laterals, exposed floor plates indicated by arrows at left, lateral cover plates, medial cover plates, and medial cover plates of opposite side; (7) Titanocrinus sp., PE 52727, arm weathered through from back revealing floor plates; (8) Apektocrinus ubaghsi Guensburg and Sprinkle, 2009, 1983TX1, large lateral cover plates, alternating double biseries of medial cover plates on left, floor plates with podial pores on right, coated, with chevrons = position of Figure 8.1.

Figure 11.

Axial construction of early crinoids, edrioasterid edrioasteroids, and a representative early blastozoan brachiole: (1) Eknomocrinus wahwahensis Guensburg and Sprinkle, 2003, holotype PE 52734; (2, 3) Alphacrinus mansfieldi Guensburg, 2012, holotype PE 52743: (2) tegmen showing articulating cover plates, coated; (3) medial arm detail, two-tiered cover plating, medial cover plates with double alternating biseries, uncoated, dry; (4) undescribed Early Floian iocrinid, PE 52757, naturally etched showing, from below, brachials, floor plates, lateral and medial cover plates; (5) Paredriophus elongatus Guensburg and Sprinkle, 1994, PE 52755, exposed floor plates, podial basins with pores on right, coated; (6) Pseudedriophus guensburgi Sprinkle and Sumrall, 2015, 1778TX16, large rectangular lateral cover plates over partly exposed floor plates, smaller medial cover plates arranged with larger elements contacting laterals and much smaller elements along the perradial suture, coated; (7) Gogia sp., NPL 93360, brachiole showing single biseries of cover plates.

Disproportionate cup ray plating in disparid crinoids: ‘Compound radials’ and ‘biradials'

Athenacrinus n. gen. is the oldest crinoid expressing disproportionate cup-ray plating, and evidence from this taxon provides a hypothesis for the origin of this morphology. This unusual trait of many early disparids is a tendency to express disparate, uneven cup plating in which some rays possess one or two offset plates forming interlocking patterns with adjacent rays. Moore and Laudon (1943) created compound radial (‘biradial') terminology for those rays with two cup plates; proximal elements were termed ‘inferradials,' and distal elements ‘superradials.’ This terminology has become entrenched in family-level taxonomy in disparids and remains in common usage today (Ausich, 2018), yet there is no evidence that this interpretation is correct. Initial ray plates in Athenacrinus n. gen. are all large, similar to those of iocrinid radials. The second, more distal, C ray plate is smaller than the radial but still cup-like, carrying both an arm and anal column above. If multiple fixed-ray plating constitutes an emergent crinoid apomorphy as is now supported by the Tremadocian crinoid record, then this plate should be termed the first fixed primibrachial, with its cup-like appearance inherited from deeper in crinoid phylogeny. The same reasoning can be used for the E ray of Athenacrinus n. gen. (Figs. 1.5, 5.2).

Table 1.

Summary of earliest crinoid axial morphologies. Compagicrinus is early or middle Floian in age, younger than the other taxa listed here. The undescribed iocrinid is late Tremadocian and associated with specimens of Aethocrinus moorei Ubaghs, 1969 from Morocco.

Independent origins of crinoids and blastozoans among early radiate echinoderms

Basis of phylogenetic analysis.—A parsimony analysis using PAUP (Swofford, 2003) was constructed expressly to: (1) test the independent monophyly of crinoids and blastozoans and how these major clades are related to each other, and (2) reconstruct phylogenetic relationships among the earliest, Tremadocian, crinoids. This analysis is not intended to establish crinoid phylogeny beneath the subclass level. It differs from that of Ausich et al. (2015b) whose assumptions concerning crinoid origin lead to rooting on multiple blastozoan taxa. It also differs from the analyses of Guensburg (2012), Cole (2017), and Wright (2017), all of which are rooted on Tremadocian crinoids, but omit, or make unsupported assumptions concerning crucial early crinoid taxa.

There remains no known immediate crinoid sister group. Taxa chosen for this analysis, with three exceptions, are Tremadocian, Early Ordovician, or earlier, this constraint intended to minimize effects of homoplasy caused by the origination of more crownward apomorphies. This is an important consideration given that stalked echinoderms—both blastozoans and crinoids—occupied similar ecologic niches and diversified rapidly during the Ordovician (Guensburg et al., 2016).

Table 2.

Characteristic arm types and cover plates among diverse Late Ordovician crinoids (primarily from Brower, 2006 and Sprinkle, 1982a, b).

As ever, central to the dispute over crinoid origins is the question of whether given features are homologous or homoplastic. Historically, very similar terminologies have been used interchangeably for blastozoans and crinoids (for summaries, see Guensburg and Sprinkle, 2007; Sumrall and Waters, 2012). Argumentation challenging potential homologies based on congruency, conjunction, and similarity arguments (ambulacral floor and cover plating excepted, see subsequent paragraph) has been laid out in detail (Guensburg and Sprinkle, 2007, 2009; Guensburg et al., 2010, 2016). These findings are accepted here.

The analysis was rooted on a middle Cambrian edrioasteroid-like form, Stromatocystites pentangularis Pompeckj, 1896 (see Zamora et al., 2015). This taxon is here considered to approximate an archaic, pentaradiate level of organization. Another early pentaradiate, Kailidiscus chinensis Zhao et al., 2010, was included because of its atypical ambulacral morphology and exceptional preservation. Camptostroma roddyi Ruedemann, 1933, an early difficult-to-interpret archaic radiate taxon is included because it is an edrioasteroid-like form, but with short arms (Durham, 1966, text-fig. 1; 1967, fig. 396, 1b). This fossil is under fuller and more accurate revision (Derstler et al., 2018), but information is now sufficient to analyze most salient features that significantly improve upon previous interpretations (Durham, 1966; Paul and Smith, 1984). We do not accept the reconstruction of Paul and Smith (1984, fig. 5), and instead conclude, based on more complete material, that Camptostroma was a low, biscuit-shaped form with a short, projecting, pedunculate aboral extension and with coelomate arms projecting along the margins of the theca (Derstler, et al., 2018). Two edrioasterid edrioasteroids—‘Totiglobus' lloydi Sprinkle, 1985, from the middle Cambrian, and Pseudedriophus guensburgi Sprinkle and Sumrall, 2015, from the Early Ordovician—were included based on similar axial expressions with earliest crinoids. Blastozoans cited by some to include the crinoid ancestor and six diverse taxa, spanning a long stratigraphic range, were coded. These include: (1, 2) the stem early Cambrian forms Kinzercystis durhami Sprinkle, 1973 and Lepidocystis wanneri Foerste, 1938 (see Sprinkle, 1973); (3) the middle Cambrian gogiid Gogia kitchnerensis Sprinkle, 1973; (4) the Tremadocian, Early Ordovician ‘eocrinoid’ Rhopalocystis destombesi Ubaghs, 1963 (see Ubaghs, 1968); (5) the rhombiferan-like Macrocystella (see Paul, 1968); and (6) the Sandbian diploporan blastozoan Eumorphocystis multiporata (see Parsley, 1982). The last taxon constitutes an exception to our stratigraphic constraint but was included because of recent claims that it represents a sister taxon to the Crinoidea (see above discussions concerning the origin of the crinoid arm). All crownward blastozoans express highly derived autapomorphies in thecal plating that have no supportable homologies among crinoids, and these were omitted from the data matrix. The early stylophoran Ceratocystis perneri Jaekel, 1901 (see Ubaghs, 1967) was included to extend the range of morphologies tested in the analysis. All seven described Tremadocian crinoids were coded: (1) Aethocrinus moorei Ubaghs, 1969; (2) Alphacrinus mansfieldi Guensburg, 2012; (3) Apektocrinus ubaghsi Guensburg and Sprinkle, 2009; (4) Athenacrinus broweri n. gen. n. sp.; (5) Eknomocrinus wahwahensis Guensburg and Sprinkle, 2003; (6) Glenocrinus globularis Guensburg and Sprinkle, 2003; and (7) Titanocrinus sumralli Guensburg and Sprinkle, 2003. Hybocrinus nitidus Sinclair, 1945 (see Sprinkle, 1982a) and Carabocrinus treadwelli Sinclair, 1945 (see Sprinkle, 1982b), of the Late Ordovician Sandbian, have been described as plesiomorphic taxa whose axial morphologies provide homologies and phylogenetic linkages with Eumorphocystis (most recently, see Sheffield and Sumrall, 2019a, b). Therefore, we also included these exceptions to our stratigraphic constraint. A total of 21 taxa from all groups were included in this analysis.

Characters in this analysis are described below using body region terminology from the Extraxial Axial Theory (EAT) (Mooi and David, 1998; David et al., 2000). An important issue of this study is the definition of so-called ‘true arms,’ these involved in the coding of at least 16 characters. We concur with previous studies (Mooi and David, 1998; Guensburg et al., 2010, 2016) that identified the absence of somatocoel-bearing arms as arguably the key character separating blastozoans from all other pentaradiate echinoderms, including crinoids. This crucial distinction is manifested in the axial skeletons of blastozoan and crinoid arms. The primary supports in blastozoan appendages are axial elements (floor plates, brachiolars), whereas the primary supports in crinoid arms are extraxial (brachials). In addition, the well-documented complexity of ontogeny and anatomy seen in crinoid arms (Heinzeller and Welsch, 1994; Guensburg et al., 2016; and others), and the interplay of skeletal, water vascular, and coelomic elements in their formation make feeding appendages such as arms character-rich sources of homology that are more likely to carry phylogenetic signal. Therefore, the number and source of characters upon which our analysis relies reflect both the complexity and the fundamental differences among major echinoderm clades. Thirty-four characters were coded:

Figure 12.

Strict and 50% majority rule consensus trees for parsimony analysis of matrix in Table 3. All node frequencies occur in 100% of trees except where indicated, and bootstrap values are indicated by numbers in parentheses.

Table 3.

Matrix used in phylogenetic analysis.

These 34 characters were assembled for scoring using Mesquite Version 3.2 (build 801), and the nexus file run on PAUP 4.0a (build 165) for Macintosh. All characters were unordered and unweighted, but two characters were parsimony uninformative. The analysis employed the branch-and-bound algorithm, consensus trees were computed, and a bootstrap analysis of 10,000 replicates was run using a fast heuristic search.

Phylogenetic position of Athenacrinus n. gen. and comments on crinoid phylogeny

The phylogenetic analysis resulted in 120 most parsimonious trees of length 61, consistency index (CI) of 0.721, retention index of 0.856, rescaled CI of 0.617, and a homoplasy index of 0.279. The strict and 50% majority rule consensus trees are shown in Figure 12, along with the results of the bootstrap analysis. Figure 13 maps known stratigraphic ranges onto this tree.

In general, the axial skeleton has been considered the more conserved because it is consistently associated with suspension feeding (Mooi and David, 1998; Kammer et al., 2013). This suggestion is at least partially borne out by our analysis. The most important features of the discovered topology revolve around the placement of Camptostroma, the distinctiveness of the blastozoans from crinoids, and the placement of Eumorphocystis. The last not only receives strong support as belonging to the blastozoan clade, it does so as a highly derived blastozoan. As discussed above, the significance of features obtained by detailed analysis of appropriate material of the latter taxon will be treated in a separate work, but its supposed significance in possessing plesiomorphic crinoid features is not supported by our analysis. Otherwise, the crinoids and blastozoans have very little in common, and each forms a separate clade. Camptostroma retains many plesiomorphic features. In part because the origin of brachials, which characterize most true arms, comes later in the crinoid clade, there remains only weak support for the recovery of Camptostroma as sister to the crinoids.

Resolution among crinoid clades is weakly supported. However, it is clear that there is a robust clade consisting of crinoids including even the earliest known taxa. The relationships among camerate, cladid, and disparid clades remains poorly understood, largely because pervasive trends of cup plate simplification in cladids and disparids increase potential for homoplasy. Distinctive posterior morphologies extend deep in crinoid phylogeny, and traditionally provide reliable data for parsing major clades later in crinoid diversification (Guensburg, 2012). We think that this skeletal complex represents underlying, fundamental differences in anatomy, in particular of the hindgut. As such, it is more informative than traits associated with overall simplification of the calyx during radiation of the crinoid clade.

Recently, Wright (2017) applied a Bayesian statistical analysis to early crinoid phylogeny. That study was directed toward early and middle Paleozoic diversification of noncamerate crinoids. Resultant findings inform some aspects of crinoid diversification during that extended time frame, including a Late Ordovician clade consisting of Porocrinus and similar cladid taxa with oral surfaces dominated by large ‘oral’ plates. However, exclusion of any earliest camerate-like taxa and prior assumptions in that analysis produced results favoring a cladid-disparid clade, without consideration of potential alternatives.

As previously noted, our focus lies in identifying the most parsimonious crinoid ancestor, and in establishing the relationships among earliest crinoids, including camerate-like, cladid-like, and disparid-like taxa. Our findings rely on comparative analyses from which a new foundational understanding of earliest crinoid and other aspects of early radiate anatomy have emerged. These discoveries result in fundamentally different interpretations of crinoid ancestry. We suggest that future applications of Bayesian methods targeting these questions should begin with a different set of prior assumptions based upon these discoveries. It is through inclusion of these new data that potential for the Bayesian application as a tool for addressing this basal portion of the echinoderm record can be maximized.

Figure 13.

Evolutionary tree based on phylogenetic analysis with stratigraphic occurrence mapped onto it. Earliest occurrence of genera is indicated by dots. In most cases, the known range is as indicated. The crinoid branch includes taxa with feeding appendages supported by extraxial brachials that housed left and right somatocoel extensions. Epispire-bearing aboral plating in Camptostroma “arms” suggests the presence of somatocoels, but without brachial supports. Blastozoan ambulacra extend off of the theca as ‘arms’ or brachioles, with axial constructs lacking communication with the thecal interior. Series and stage nomenclature follow Geissman et al. (2018). This is an online version of the Geological Society of America Geologic Time Scale, ver. 5.0.