The hexamer hypothesis explains apparent irregularities in the plating of early and extant crinoids

In 2011, I proposed a new hypothesis for the evolution and development of the five-rayed structure of echinoderms, the Hexamer Hypothesis (Lussanet, 2011). According to this hypothesis, the five-rayed structure develops by reduction from a six-rayed Bauplan. Crinoids (sea lilies) are unique as the only extant clade with stalked representatives, s t reaching back at least to the early Ordovician. Their extraordinary rich fossil record and n i r the known embryology of recent forms make them ideal to test the Hexamer Hypothesis. It P

e is concluded that the plating of the calyx and the stalk can be explained by the new r

P hypothesis.

PeerJ PrePrints | http://dx.doi.org/10.7287/peerj.preprints.857v1 | CC-BY 4.0 Open Access | rec: 26 Feb 2015, publ: 26 Feb 2015 THE HEXAMER HYPOTHESIS EXPLAINS APPARENT IRREGULARITIES IN THE PLATING OF EARLY AND EXTANT CRINOIDS

Marc H.E. de Lussanet1 1 Institut für Sportwissenschaft, Westfälische Wilhelms-Universität Münster, Horstmarer Landweg 62b, 48149 Münster, Germany. e-mail: [email protected]

Keywords: Early crinoids, fossil, embryology, Bauplan, evolution, Extraxial axial theory (EAT)

INTRODUCTION

In 2011 I proposed a new hypothesis for the evolution and development of the five-rayed structure of echinoderms, the Hexamer Hypothesis (Lussanet, 2011). According to this hypothesis, the five-rayed structure develops by reduction from a six-rayed Bauplan. This six-rayed origin is reflected developmentally in the six coelomic spaces, which are, in the early larva, arranged symmetrically around the mouth and the larval mid-sagittal plane.

s According to the new hypothesis the mouth and five Anlagen for rays migrate to the left side of the larval t body, in a process well known as coelomic stacking. The sixth Anlage along with its coelom, the right

n hydrocoel either degenerates (for example, the dorsal sac in echinoids), or specializes into attachment i

r structures. Meanwhile, the mouth and the surrounding ray-Anlagen turn in an anti-clockwise direction. Thus the missing ray, recognizable by the closure point of the hydrocoel crescent, becomes located towards the P anus or periproct. e r In the original presentation of the new hypothesis I tried to collect evidence from the extant echinoderm

P clades, and the main focus was on the developmental deformations and on morphological features, such as the Lovén’s rule and symmetry planes. I showed that the missing ray originates from the CD interray (according to Mortensen’s encoding of the rays), on the side of the C-ray. Accordingly, the bivium-trivium arrangement of rays, typical for early crinoids and other paleozoic clades, is derived from a bivium-quartium arrangement, with the D-E bivium being derived from the rostral larval side.

Echinoderms are a rich phylum with a rich fossil record reaching back into the Cambrian. Of this richness, only five classes survive to date, four of which belonging to the same subphylum, the Eleutherozoa, and the fifth, the crinoids, as extant representatives of the once much more diverse subphylum of Crinozoa. Crinoids are unique as the only extant clade with stalked representatives, reaching back at least to the early Ordovician. Their extraordinary rich fossil record and the known embryology of recent forms make them ideal to test the Hexamer Hypothesis. This was proposed to me by Michel Roux, and the discussions with him and Marc Eléaume led to the considerations presented in the following.

EXISTING THEORIES

The extraxial-axial theory (EAT) refers primarily to the skeletal structures of the body wall and their patterns of development (David et al., 1996). According to David and Mooi, the skeletal plating of all echinoderms can be distinguished in three classes by the developmental pattern. The axial skeleton is arranged around the mouth and can be very prominent (Echinoidea) or almost absent (Holothuria). The perforate extraxial skeleton forms the rest of the body whereas the imperforate extraxial skeleton is typically related to stalk structures. In crinoids (in contrast, e.g., to blastoids), the arms are formed of both, axial and extraxial elements. The EAT was originally developed for echinoids, and subsequently extended to eleutherozoans and other echinoderms. Although widely accepted for eleutherozoans, its validity for other clades of echinoderms is still disputed. As far as I am aware, the Hexamer Hypothesis is compatible with the EAT, although the nature of the imperforate extraxial is unsure.

The Universal Elemental Homology (UEH) model was developed for the plating of the oral region of blastozoan echinoderms (Sumrall, 2012), and has recently been applied to crinoids (Kammer et al., 2013). The plating of the mouth region is not focus of the present study.

THE STALK

According to the Hexamer Hypothesis, the sixth ray was lost from the oral region to form attachment structures. Depending on the time of coelomic stacking, aboral plating regions may not be involved in the loss of the sixth ray and thus retain hexamery. Consequently, it is predicted that the plating of attachment structures, such as the crinoid stalk, resembles the axial growth pattern (so that the term „imperforate axial“ might be more appropriate than imperforate extraxial). PeerJ PrePrints | http://dx.doi.org/10.7287/peerj.preprints.857v1 | CC-BY 4.0 Open Access | rec: 26 Feb 2015, publ: 26 Feb 2015

Accepted Preprint: Progress in Echinoderm Palaeobiology (Spain 2015) Editor: S. Zamora. Figure 1. Application of the hexamer circlet rules to Aethocrinus moorei. Left: Ubaghs’ original interpretation (Ubaghs, 1969). Note the irregular „X“ and „Y“ plates. Middle: Hexamer circlet interpretation of the same schema and two views of the holotype (Right). Columns are indicated by thick curves (P is the C-D interray). Circlets are connected by thin grey curves. The plates of each circlet are given the same grey tone. The brachials of the top circlet alternate with thecal plates. Note, that the P column has lost connection to the lowest circlet, and interrupts the C and B columns. Also, the C ray is moved up due to this interference. s t n i A typical property of axial growth, as opposed to extraxial growth, is that new elements are added only r behind a terminal end plate. Indeed, the stalk of crinoids does grow in such manner (Améziane & Roux,

P 2005; Breimer, 1978; Ubaghs, 1978). Interestingly, new plates are added on the proximal side of the stalk, so that the sixth ray in effect growth towards the body, pushing it up. This might be a crucial factor in the survival e r of crinoids, enabling the stalk to regenerate after loss. Also, the direction of growth appears consistent with an axial pattern, because the growth is directed towards the extraxial border as in the axial plating. P

THE CALYX

If the stalk is axial, we predict that the calyx is not reduced and therefore has six rays. The calix of crinoids is composed of circlets of plates (Ubaghs, 1978). For the present study, the plating of the calyx was reinterpreted on the assumption that each circlet is composed of exactly six plates at least during some stage in development, and that each plate can be associated with one of six columns each of which is associated with a ray.

The taxonomy of these circlets has caused ample controversy. For example, the circlets of the very early Aethocrinus moorei from the Cambrian/Ordovician transition have been revised at least four times (Ubaghs, 1969; Simms, 1993; Ausich, 1996; Ausich, 1998; Guensburg & Sprinkle, 2003). Indeed, the plating pattern appears quite irregular (Figure 1). Indeed, Aethocrinus proved to possess one of the most complex plating schemas. The following five simple rules could be applied to a large number of early and recent crinoids.

First, it is hypothesized that each of the plates of a circlet also belongs to a columnar series. It is hypothesized that these columns tend to spiral in a leftward direction (when following the spirals in an upwards direction), as in the Cambrian helicoplacoids (Sprinkle & Wilbur, 2005), and as in the gut system of extant echinoderms (Breimer, 1978). Thus, starting from the lowest circlet, it is assumed that each column progresses into the left neighbor of the next circlet.

Second, that the sixth column is associated to the CD interray, according to the Hexamer Hypothesis.

Third, that the sixth ray, P, typically looses connection to the stalk and is therefore the source of perturbation in the plating pattern of the calyx. The rationale is that the sixth ray is involved in the formation of the stalk structures so that connection to the sixth column in the calyx may loose connection to the base of the stalk.

Finally, that each circlet is composed of exactly six plates. This may be impossible to prove in many-plated cups such as Titanocrinus (Guensburg & Sprinkle, 2003). Extant crinoids posses two circlets of calyx plates. The five radials are supplemented by a radianal plate (which is sometimes reduced in the adult). The circlet of basals seems to be formed of just five plates, but a sixth plate may be formed in early embryo.

DISCUSSION

Crinoids are not the earliest stalked echinoderms. Crinoids have the advantage to have direct, extant ancestors. Moreover, already early crinoids are very well documented and have a rich fossil record. Potentially this study can be a starting point for investigating further and earlier clades of the earliest echinoderms. PeerJ PrePrints | http://dx.doi.org/10.7287/peerj.preprints.857v1 | CC-BY 4.0 Open Access | rec: 26 Feb 2015, publ: 26 Feb 2015

Accepted Preprint: Progress in Echinoderm Palaeobiology (Spain 2015) Editor: S. Zamora. Page !2 The Hexamer Hypothesis gives an explanation for the origin of the stalk, and why it is consistently clearly set apart from the calyx. I argue that the stalk resembles an axial structure in its development, not only by having a single growth zone of plate addition, but also because this growth zone faces the extraxial plating of the calyx. There remains potential for speculation of the origin of holdfast structures which are manifold and which differ markedly from the stalk itself.

CONCLUSIONS

The calyx plating of crinoids shows a clear and regular hexamery as predicted by the Hexamer Hypothesis. The axial region is clearly pentamer in structure, with one ray (P) missing in the CD interray. The axial elements of the P-ray seem to be not missing in crinoids but instead involved with the formation of the stalk.

Acknowledgements

I thank Michel Roux and Marc Eléaume for inspiring discussions and advise, as well as the reviewers, W. Ausich and S. Zamora for their clever and constructive comments.

REFERENCES s Améziane, N. and Roux, M. (2005). Environmental control versus phylogenic fingerprint in ontogeny: The t example of the development of the stalk in the genus Guillecrinus (stalked crinoids, Echinodermata). Journal n i of Natural History, 39(30), 2815–2860. r

P Ausich, W. I. (1996). Crinoid plate circlet homologies. Journal of Paleontology, 70(6), 955-964. e r Ausich, W. I. (1998). Early phylogeny and subclass division of the Crinoidea (Phylum Echinodermata). Journal of Paleontology, 72(3), 499-510. P

Breimer, A. (1978). General morphology recent crinoids. In R. C. Moore and C. Teichert (Ed.), Treatise on invertebrate paleontology, 2, T9-T58.

David, B. and Mooi, R. (1996). Embryology supports a new theory of skeletal homologies for the phylum Echinodermata. Comptes rendus de l'Académie des sciences. Série 3, Sciences de la vie, 319, 577-584.

de Lussanet, M. H. E. (2011). A hexamer origin of the echinoderms' five rays. Evolution and Development, 13(2), 228-238.

Guensburg, T. E. and Sprinkle, J. (2003). The oldest known crinoids (Early Ordovician, Utah) and a new crinoid plate homology system. Bulletins of American Paleontology, 364, 1-43.

Kammer, Thomas, W., Sumrall, Colin, D., Zamora, Samuel, Ausich, William, I., and Deline, Bradley (2013). Oral region homologies in paleozoic crinoids and other plesiomorphic pentaradial echinoderms. PLoS ONE, 8(11), e77989.

Simms, M. J. (1993). Reinterpretation of thecal plate homology and phylogeny in the class Crinoidea. Lethaia, 26(4), 303-312.

Sprinkle, J. and Wilbur, B. C. (2005). Deconstructing helicoplacoids: reinterpreting the most enigmatic Cambrian echinoderms. Geological Journal, 40(3), 281–293.

Sumrall, C. D. (2012). A model for elemental homology for the peristome and ambulacra in blastozoan echinoderms. In C. Johnson (Ed.), Echinoderms in a changing world, 13, 269-276.

Ubaghs, G. (1969). Aethocrinus Moorei Ubaghs, N. Gen., N. Sp., le plus ancien crinoide dicyclique connu. Kansas: University of Kansas Publications.

Ubaghs, G. (1978). Skelettal morphology of fossil crinoids. In R. C. Moore and C. Teichert (Ed.), Treatise on invertebrate paleontology, 2, T58-T216.

PeerJ PrePrints | http://dx.doi.org/10.7287/peerj.preprints.857v1 | CC-BY 4.0 Open Access | rec: 26 Feb 2015, publ: 26 Feb 2015

Accepted Preprint: Progress in Echinoderm Palaeobiology (Spain 2015) Editor: S. Zamora. Page !3