Meemannia Eos, a Basal Sarcopterygian Fish from the Lower Devonian of China – Expanded Description and Significance

Morphology, Phylogeny and Paleobiogeography of Fossil Fishes D. K. Elliott, J. G. Maisey, X. Yu & D. Miao (eds.): pp. 199-214, 8 figs. © 2010 by Verlag Dr. Friedrich Pfeil, München, Germany – ISBN 978-3-89937-122-2

Meemannia eos, a basal sarcopterygian fish from the Lower Devonian of China – expanded description and significance

Min Zhu, Wei Wang and Xiaobo Yu

Abstract

Additional morphological and histological features of a stem-group sarcopterygian fish Meemannia eos (Zhu et al. 2006) are provided, including dermal bone features, endocranial structures in the oto-occipital region, and details of the superimposed enamel + odontode layers bearing on the stepwise origin of cosmine in crown- group sarcopterygians. A lower jaw characterized by six infradentary foramina, a relatively straight dentary profile, and absence of parasymphysial tooth whorls is tentatively assigned to Meemannia . The distribution and phylogenetic significance of the lateral cranial canal, the endolymphatic duct of supraotic cavity, the horizontally-positioned coronoid-supporting face of the Meckelian bone, and the pore-canal network in dermal bone surface (integration of pore-canal network with multi-layered odontodes) are discussed in the context of the sequential acquisition of characters leading from stem-group osteichthyans to basal sarcopterygians. The histological condition in Meemannia indicates that stem-group sarcopterygians share two important histological features with stem-group osteichthyans and basal actinopterygians, i. e., the ability of an earlier generation of odontodes to induce the formation of future odontodes, and the absence of resorption. The multi-layered odontodes coexisting with the pore-canal network bring cosmine into alignment with surface covering in stem osteichthyans and actinopterygians.

Introduction

Recent studies on basal actinopterygians (e. g., Dialipina and Ligulalepis ) (Basden & Young 2001, Basden et al. 2000, Schultze & Cumbaa 2001) and basal sarcopterygians (e. g., Psarolepis , Achoania , and Styloichthys) (Zhu & Yu 2002; Zhu et al. 1999, 2001), have greatly improved our understanding of the origin and early diversification of osteichthyans. The earlier report of Meemannia eos, combining an actinopterygian-like skull roof and a cosmine-like dermal surface, outlined a possible morphotype for the common ancestor of actinopterygians and sarcopterygians, and highlighted its phylogenetic position as the most basal sarcopterygian fish so far known (Zhu et al. 2006). Due to space limitation, the earlier report focused on major features such as the actinopterygian-like dermal skull roof and the unique histological condition of the dermal covering. The present paper provides additional morphological and histological information such as endocranial features in the oto-occipital region and details of the surface covering, and describes a lower jaw specimen tentatively assigned to Meemannia . The paper discusses the implications of the unique histological condition in Meemannia and other features in the context of the stepwise acquisition of characters underlying the diversification of early sarcopterygians from their actinopterygian relatives. Material and faunal assemblage. The Meemannia material described here is housed in the Institute of Vertebrate Paleontology and Paleoanthropology (IVPP), Beijing. The specimens were collected from the middle part of the Xitun Formation (late Lochkovian, Early Devonian) at a locality close to Xitun village in the suburb of Qujing, Yunnan, southwestern China (Fig. 1). The material occurs in association with galeaspids Microholonaspis microthyris, Hyperaspis acclivis (Pan 1992), antiarchs Yunnanolepis chii, Y. parvus, Y. porifera, Phymolepis cuifengshanensis, P. guoruii, Chuchinolepis gracilis, C. qujingensis, C. sulcata, C. robusta,

199 D2 0 500 km

1000 m

0 m

shale conglomerate

mudstone muddy limestone

siltstone limestone

sandstone dolomite

Fig. 1. Locality map and stratigraphic position of the fossil bed yielding Meemannia eos.

Zhanjilepis aspratilis (Zhu 1996), arthrodire Szelepis yunnanensis (Liu 1979), and sarcopterygians Youngolepis praecursor, Diabolepis speratus, Psarolepis romeri, Achoania jarviki and Styloichthys changae (Chang & Yu 1981, 1984; Yu 1998; Zhu & Yu 2002; Zhu et al. 2001). The vertebrate microremains from the Xitun Formation include thelodonts Parathelodus scitulus, P. asiatica, P. catalatus, P. trilobatus, P. cornuformis, acanthodians Nostolepis sp., Youngacanthus gracilis, and chondrichthyans Gualepis elegans, Changolepis tricuspidus, Peilepis solida, and Ohiolepis ? xitunensis (Wang 1984, 1997). From the Xitun Formation of neighboring localities were described other galeaspids including Polybranchiaspis liaojiaoshanensis, Nanpanaspis microculus, Laxaspis qujingensis, ‘L ’. rostrata, Cyclodiscaspis ctenus (Liu 1965, 1975) and Siyingia altuspinosa (Wang & Wang 1982). All these findings, together with Meemannia as the most basal sarcopterygian, suggest that during the beginning of the Devonian, early vertebrates were highly diversified in the restricted coastal embayment along the coast of the Upper Yangtze Paleocontinent in South China (Wang 1991).

Description

Skull roof General features. As briefly mentioned in the earlier report (Zhu et al. 2006), the three skull roof specimens only preserved the portion behind the rostral region (Figs. 2, 3B), suggesting a loose connection between the unpreserved anterior rostral unit (rostral and nasal bones) and the dermal bones behind it. In this feature, Meemannia resembles Dialipina (Schultze 1992) and many placoderms (Goujet 1984, 2001), suggesting that the ‘loose nose’ condition may be characteristic of ancestral osteichthyans. The

200 pi Pros

p.soc n.orb p.soc n.orb

ptoc

pl.m pl.m

n.spir

St pl.p AB Fig. 2. Meemannia eos Zhu et al. 2006, reproduced at higher magnification for clarity in morphological details. Dorsal view of skull roof. A, holotype, IVPP V14536.1; B, IVPP V14536.2. Scale bars = 5 mm. Abbreviations: n.orb, orbital notch; n.spir, spiracular notch; pi, pineal opening; pl.m, pl.p, middle and posterior pit-lines; Pros, postrostral; ptoc, postorbital corner; soc, supraorbital canal; St, supratemporal. post-rostral unit of the skull roof is long and narrow, with the orbital notch (n.orb, Fig. 2A,B) relatively large and anteriorly positioned. Behind the postorbital corners (ptoc, Fig. 2A), the lateral margins run in parallel to the level of the spiracular notches (n.spir, Fig. 2A). The skull roof reaches its maximum width in the otico-occipital region, and presents an embayed posterior margin. No dermal intracranial joint exists between the parietal (P, Fig. 3A) and postparietal (Pp, Fig. 3A) shields which can barely be distinguished by vague indications of incomplete sutures. Dermal bone pattern. Meemannia has a large shield-shaped postrostral bone, whose sutures with neighboring bones are clearly detectable. The postrostral bone bears a round pineal opening (Fig. 2A) close to its posterior margin. The pineal opening is present in V14536.1 (Fig. 2A) and V14536.3 (Fig. 3B), but absent in V14536.2 (Fig. 2B), suggesting the variable distribution of this feature. Two series of dermal bones can be identified on the skull roof, the parietal-postparietal in the middle and the dermosphenotic-supratemporal along the lateral margin (Fig. 3A). The parietal is very long and narrow, with its length nearly 3.8 times its width. Anteriorly, the parietals are separated by the postrostral (Figs. 2, 3A,B). The postparietal is also rectangular, about half as long as the parietal. The parietal is flanked by an elongate longitudinal bone which is referred to the dermosphenotic (Dsp, Fig. 3A). Along the lateral margin of the postparietal is a single bone which is attributed to the supratemporal (St, Figs. 2B, 3A). Anteriorly the supratemporal is narrow and constitutes the upper margin of the spiracular opening. Behind the spiracular opening, the supratemporal is postero-laterally expanded, with its posterior margin forming the lateral portion of the embayed posterior margin of skull roof. Sensory canals. On the skull roof, two pairs of sensory canals and two pairs of pit-lines are detectable. The supraorbital canal (soc, Fig. 3A) extends posteromedially and traverses the anterior portion of the parietal without contacting the otic portion of main lateral line canal (lc, Fig. 3A). After passing through the center of the supratemporal, the main lateral line canal proceeds anteriorly along the lateral margin of the elongated dermosphenotic and exits at a point close to the posterior corner of the shallow orbital margin (Figs. 2, 3A). The trajectory of these two canals can be confirmed by the thin sections from V14534.3 (Fig. 3). The middle (horizontal) pit-line (pl.m, Figs. 2, 3A) and curved posterior (oblique) pit-line (pl.p, Figs. 2, 3A) are situated close to the median line of the skull roof, as in Dialipina. In other basal sarcopterygians such as Psarolepis and Achoania, these two pit-lines have more lateral positions.

201 Pros n.orb pi S14 n.orb S15 soc S12 S13 p.soc ptoc S10 S11

S8 S9 P S6 S7 Dsp

S4 n.spir S5 pl.m S2 S3 Pp

lc pl.p S1 St 5 mm B A

soc S15 e

S12

S9 lc

d S6 lc

b c

f lc S4 a

1 mm S1 lc C g

Fig. 3. Meemannia eos Zhu et al. 2006. A, reconstruction of skull roof; B, dorsal view of skull roof, IVPP V14534.3, a specimen sectioned at positions marked S1-S15; C, sketch drawings of six selected thin sections (S1, S4, S6, S9, S12, S15) of V14534.3. Histological details in boxed areas a-f are shown in Figure 6A-F; those in box area g are shown in Figure 5A. Abbreviations: Dsp, dermosphenotic; lc, otic portion of the main lateral line canal; n.orb, orbital notch; n.spir, spiracular notch; P, parietal; p.soc, pores for supraorbital canal; pi, pineal opening; pl.m, pl.p, middle and posterior pit-lines; Pp, postparietal; Pros, postrostral; ptoc, postorbital corner; soc, supraorbital canal; St, supratemporal.

202 cav.cr re.u am.a

am.e sca

lcc ge sac

scp

cav.so St pdf A B

cav.cr cav.cr am.a re.u sca

am.e

lcc sac

scp ge lcc cav.so pdf C pdf D Fig. 4. Endocranium of Meemannia eos (A,B), Ligulalepis (C) and Psarolepis (D). A, photo of IVPP V14536.4 with partially preserved oto-occipital ossification in ventral view; B, illustrative drawing of IVPP V14536.4; C, endocranium of Ligulalepis in ventral view (after Basden & Young 2001); D, oto-occipital ossification of Psarolepis endocranium in ventral view (after Yu 1998). Scale bars = 5 mm. Abbreviations: am.a, am.e, anterior and external ampullae; cav.cr, cranial cavity; cav.so, supraotic cavity; ge, groove for endolymphatic duct; lcc, lateral cranial canal; IX, exit of the ninth cranial nerve; pdf, posterior dorsal fontanelle; re.u, utricular recess; sac, sacculus; sca, anterior semicircular canal; scp, posterior semicircular canal; St, supratemporal.

203 Endocranium The endocranium is represented only by specimen V14536.4 (Fig. 4A,B), in which the orbitotemporal (or ethmosphenoid) portion is not preserved. The ventral (or occipital) part of the oto-occipital is missing, suggesting the existence of complete fissures separating the occipital portion from the otic portion. This resembles the condition in both basal actinopterygians (e. g., Ligulalepis , Fig. 4C) and basal sarcopterygians (e. g., Psarolepis , Fig. 4D), but differs from the condition in Mimia and Moythomasia in which the two portions of the oto-occipital are partly fused and the cranial fissure between them is not lined with perichondral bone (Basden & Young 2001, Basden et al. 2000, Gardiner 1984, Yu 1998). Because of the missing ventral (or occipital) part of the oto-occipital, the ventral surface of the specimen reveals the dorsal portion of structures in the cranial cavity and the otic region. In ventral view, specimen V14536.4 reveals a large lozenge-shaped median depression which forms the roof of the myelencephalon portion of the brain cavity (cav.cr, Fig. 4A,B), like Psarolepis (Yu 1998: figs. 3B, 4B). This lozenge-shaped area is posteriorly closed off by the medially-converging ridges. These posteromedially extending ridges define the lateral boundaries of the brain cavity and posteriorly con- tribute to the broad wall separating the brain cavity from the posteriorly-situated supraotic cavity (cav. so, Fig. 4A,B). Unlike Psarolepis , the large and long trapezoidal supraotic cavity is not divided by the medially converging ridges. Following the supraotic cavity is a large posterior dorsal fontanelle (pdf, Fig. 4A,B), which is triangular in shape and is roofed over by dermal bone. In Ligulalepis, the fontanelle is rather big (Fig. 4C), and occupies the region corresponding to the supraotic cavity and posterior dorsal fontanelle in Meemannia . The fontanelle is also present in Psarolepis (Fig. 4D), though smaller in size. The supraotic cavity of Meemannia has anteriorly diverging extensions (ge, Fig. 4B) connecting to the otic capsules, as in Ligulalepis (Fig. 4C) and Youngolepis (Chang 1982). The extensions define the position of the endolymphatic ducts which exit through the dorsal fontanelle. The ventral part of otic capsules is not preserved, and this exposes some incomplete dorsal structures of otic capsules. The most conspicuous are the paired fossae (lcc, Fig. 4B) lateral to the anterior extension of supraotic cavity or the groove for endolymphatic duct. The fossa with the same position is also found in Ligulalepis (Fig. 4C) and Psarolepis (Fig. 4D). In Psarolepis , the fossa is somewhat dorsal to the anterior extension of the supraotic cavity. Basden & Young (2001: figs. 3B, 9B) referred the fossa in Ligulalepis to the ‘anterior semicircular canal’, which may be more consistently interpreted as a lateral cranial canal comparable to those in Meemannia and Psarolepis . Lateral to the lateral cranial canal is the groove for the anterior and posterior semicircular canals (sca, scp, Fig. 4A,B). At the anterior ends of these canals are three obvious pits for the anterior and external ampullae (am.a, am.e, Fig. 4B) and the utricular recess (re.u, Fig. 4B) respectively. Lateral to the point where the anterior semicircular canal meets the posterior semicircular canal (Fig. 4B), the exposed ventral face of the otic capsule shows a pear-shaped shallow depression which probably represents the space for the sacculus (sac, Fig. 4B). Immediately behind the posterior semicircular canal lies the exit for the glossopharyngeal nerve (IX, Fig. 4B).

Histology As reported in Zhu et al. (2006), the surface covering of Meemannia ’s skull roof is punctured by relatively large pore openings (though smaller than those in Styloichthys, Psarolepis and Achoania) (Zhu & Yu 2002; Zhu et al. 1999, 2001), often arranged in parallel grooves that reflect the overall contour of bone elements, especially in the marginal portions of the skull roof (Figs. 2, 3A). As revealed by 15 transverse sections of the skull roof specimen V14534.3 (Figs. 3B,C, 4, 5), the dermal skeleton contains three horizontal divi- sions. The most remarkable feature of Meemannia is a unique histological condition found in the upper division, combining features previously found separately in actinopterygians and basal osteichthyans and in many crown-group sarcopterygians. The upper division has a thickness of about 80 to 220 microns and occupies half of the dermal skeleton in thickness. It consists of three or four superimposed layers of enamel (e1-e4, Figs. 5, 6) and odontodes (od1-od4, Figs. 5, 6) separated by flask-shaped pore cavities (pc, Figs. 5, 6), interconnecting horizontal canals (hc, Figs. 5, 6), and pore openings (p, Figs. 5, 6). Each superimposed layer is composed of one layer of enamel with the thickness of several microns and one underlying layer of odontodes with the thickness varying from 10 to 70 microns, representing the occurrence of one generation.

204 The odontodes of the oldest generation (or the most basal layer) together with the overlying enamel covering, the row of main chambers of the flask-shaped pore cavities, and the interconnecting horizontal canals jointly present a picture of typical cosmine, a complicated ornamental tissue combination regarded by some authors as a defining feature of sarcopterygians (Janvier 1996, Miles 1977). The superimposed arrangement shown by the two or three younger generations (or more superficial layers) of enamel+odontodes, as well as the underlying of the dentinous layer directly by the lamellar bone, resemble the histological pattern of dermal skeleton found in stem-group osteichthyans (Lophosteus and Andreolepis) (Gross 1968, 1969), primitive actinopterygians (e. g., Cheirolepis and Moythomasia ) (Gardiner 1984, Richter & Smith 1995) and even some acanthodians (Gross 1971). The odontodes contain dentinal pulp cavities (puc, Figs. 5, 6), and dentine tubules running almost perpendicular to the contact surface with the overlying enamel layer. The pulp cavities exist not only in the odontodes of old generations, but also in the odontodes of young generations (Fig. 6). The pulp cavities are tree-like, from which dentine tubules radiate. Some of the dentine tubules ramify. The odontodes are layered with concentric striations visible even under the light microscope, indicating periodical deposition. Each overlying odontode is successively larger than the one below. The younger generations of odontodes do not have their own pore cavities and horizontal canals, and they are vertically superimposed in a way to provide passage to the upward-reaching necks of the pore cavities associated with the odontodes of the most basal layer. The pore cavities are flask-shaped cavities with a depth of 70-210 microns. The narrow neck of the flask-shaped cavity is relatively deep, going through the superimposed layers of enamel and odontode. The pore openings are comparatively large, and of varying diameter ranging from 30 to 90 microns, much greater than that in many crown-group sarcopterygians (Gross 1956, Thomson 1975). The main chambers of pore cavities connect with adjacent pore cavities and dentinal pulp cavities via connecting horizontal canals that lie on the same horizontal plane as the base of main chambers and odontodes of the oldest generation. The enamel layers are partially penetrated by the tips of the dentine tubules (dt, Figs. 5, 6). The enamel of the most superficial layer dips slightly into the pore openings, whereas the enamel of each underlying layer dips slightly into the sidewall of the pore cavities at different levels. This arrangement, together with the superimposition of three or four enamel+odontode layers, indicates that each layer (or successive generation) might be deposited without resorbing previously deposited layers and that the pore-canal network maintains its integrity during the subsequent deposition of overlying layers. The middle horizontal division of the dermal skeleton consists of vascular bone (Fig. 5) and is poorly developed, visible only in places where the dermal bone is thick, as in areas close to the sensory canals. This feature resembles the dermal bone features found in primitive actinopterygians, stem-group osteichthyans (for example, Andreolepis , Gross 1968) and some acanthodians (Gross 1971). The lowest horizontal division of the dermal skull roof consisting of lamellar bone (Figs. 5, 6) is well developed and often directly underlies the uppermost division. The thickness of the lowest division varies from 40 to 140 microns, and is about half of the thickness of the dermal skeleton.

A lower jaw tentatively assigned to Meemannia An isolated lower jaw (V14536.5, Fig. 7) from the Xitun Formation of Qujing reveals a unique combination of actinopterygian and sarcopterygian characters and bears evenly-distributed large pores on its external surface. The large pore dermal surface and the presence of infradentary foramina suggest a sarcopterygian affinity but the specimen differs remarkably from the lower jaws of all previously known sarcopterygians from the same site (Zhu & Yu 2004). Because of its general primitive features, its relatively small size, and the dermal surface covering comparable to that in the skull roof materials of Meemannia , the lower jaw is tentatively assigned to Meemannia , the only sarcopterygian form lacking lower jaw material from the site. The relative rareness and mode of preservation of the single lower jaw are also consistent with those of the Meemannia skull roof specimens. As there is only one specimen, the lower jaw has not been sectioned for histological comparison to the skull roof material. The lower jaw is about 13.2 mm in length and 3.8 mm in depth, with a profile similar to that of lower actinopterygians such as Mimia and Moythomasia (Gardiner 1984). The dorsal margin is fairly straight, and lacks the anteriorly ascending tip typical of the lower jaw of Psarolepis and Achoania (Zhu & Yu 2004). The dentary (De, Fig. 7B) has its teeth (de.t, Fig. 7B,D,F) reaching the anterior extremity of the lower jaw, suggesting the absence of parasymphysial tooth whorl. Small denticles (den, Fig. 7B), as those on the

205 lc lamellar bone

od2 e2 p od1 puc e3 hc

B pc hc pc

p od1 od2 od3 od4

e1 dt puc e2 e3 e4 pc hc and enamel of odontodes superimposed layers superimposed layers

bone pore- vascular vascular canal network lamellar bone C Fig. 5. Cosmine-like dermal surface in Meemannia combining 3 or 4 layers of odontodes and enamel with a pore-canal network. A, selected area of section S1 (box area g in Figure 3C); scale bar = 200 μm; B, detailed view of inset area from A; scale bar = 30 μm; C, reconstruction based on sections of IVPP V14534.3. Abbreviations: dt, dentine tubules; e1-e4, layers of enamel; hc, horizontal canal; od1-od4, layers of odontodes; p, pore opening; pc, pore cavity; puc, pulp cavity.

206 puc dt hc p p

pc pc pc

vascular bone lamellarlamellar bonebone A B puc e3 od3 e2 od2 e1 od1 od4 od3 od2 od1

pc pc pc hc

lamellarlamellar bonebone

vascular bone D

C od4 e3 e2 e1 od1 od2 od1 puc od2 p

pc pc hc

lamellarlamellar bonebone

vascular bone

E F Fig. 6. Photos showing histological details of Meemannia eos. A-F correspond to boxed areas a-f in Figure 3C. Scale bars = 30 μm. Abbreviations: e1-e3, layers of enamel; hc, horizontal canal; od1-od3, layers of odontodes; p, pore openings; pc, pore cavity; puc, pulp cavity. jaws of Lophosteus and Andreolepis (Botella et al. 2007), are distributed lateral to the dentary tooth row, mainly close to the lower jaw symphysis. The outer boundary of the adductor fossa (fo.add, Fig. 7D,F) is relatively short, and occupies about one fifth of the lower jaw length. This proportion is bigger than that of Mimia and Moythomasia (Gardiner 1984), but smaller than that of Psarolepis and Achoania , and much smaller than that of Styloichthys (Zhu & Yu 2004) and Youngolepis (Chang 1991). A groove extends antero- ventrally from the outer margin of adductor fossa and may represent the suture between the dentary and infradentaries (su, Fig. 7B).

207 den de.t De den su fo.6 art

A fo.1 B fo.2 gr fo.3 fo.gl fo.4 fo.5 p-mc fo.add de.t ar.Co

Mk C D for ar.Prea 5 mm

fo.gl fo.add ar.Co art de.t

E F Mk Fig. 7. A lower jaw tentatively assigned to Meemannia eos, IVPP V14536.5. Photos and illustrative drawings in lateral view (A,B), medial view (C,D) and dorsal view (E,F). Abbreviations: ar.Co, attachment area of coronoid; ar.Prea, attachment area of prearticular; art, articular portion of Meckelian bone; De, dentary; den, denticle; de.t, dentary teeth; fo.1-6, first to sixth infradentary foramen; fo.add, adductor fossa; fo.gl, glenoid fossa; for, foramen on Meckelian bone; gr, groove following infradentary foramen; Mk, Meckelian bone; p-mc, preoperculo-mandibular sensory canal; su, suture between dentary and infradentaries.

The most conspicuous feature of the lower jaw is the presence of six infradentary foramina on the external surface (Fig. 7A,B). The first one (fo.1, Fig. 7A) lies at the ventral margin of lower jaw, and makes a notch on the ventral margin. The rest of the foramina have their positions increasingly removed from the ventral margin, with the last one (fo.6, Fig. 7B) close to the posterodorsal margin of the lower jaw. Each of these foramina (except the first one) bears a long groove extending posteroventrally to the ventral or posteroventral margin of lower jaw (gr, Fig. 7B). The presence of the infradentary foramina on the external surface of lower jaw is a feature of some sarcopterygians, although the biological nature of these foramina is still not clear. However, the number of the foramina is three or fewer in previously known sarcopterygians, regardless whether the number is stabilized as in basal sarcopterygians (e. g., Psarolepis, Achoania, Styloichthys and Youngolepis) or variable as in Gogonasus (Long et al. 1997). In the sarcopterygian lineage, these foramina were independently lost in different groups. In lingual view, only the Meckelian cartilage (Mk, Fig. 7D,F) supporting the dermal bones is preserved. In some basal sarcopterygians (e. g., Psarolepis, Achoania, and Styloichthys), the dermal bones of the coronoid series are only loosely attached to the Meckelian cartilage. Posterodorsally, the Meckelian cartilage bears a depression which represents the glenoid fossa (fo.gl, Fig. 7D,F). The adductor fossa is partly lined by the Meckelian cartilage in front of the glenoid fossa. At the posterior extremity of lower jaw, the posterior exit of the mandibular canal (p-mc, Fig. 7D) is close to the ventral edge of the Meckelian cartilage which forms a distinct line on the internal side of the infradentaries and exhibits several small openings anteriorly (for, Fig. 7D). The Meckelian cartilage is getting deeper anteriorly, and can be distinguished into two faces in front of the adductor fossa. The planes of the two faces are roughly at 90 degrees to each other. The upper face forms the floor for the coronoid series (ar.Co, Fig. 7D,F), while the lower face provides the attachment area for the prearticular (ar.Prea, Fig. 7D). In this feature, the lower jaw is more sarcopterygian-like than actinopterygian-like. In actinopterygians, the coronoids are situated in front of

208 the prearticular, and the Meckelian cartilage supporting them does not form an angled base in front of the adductor fossa (Gardiner 1984). The floor for the coronoid series becomes broader anteriorly. As judged by shallow depressions on the floor, the coronoid bones of this lower jaw may exceed three. However, there is no element which could correspond to the attachment area for the parasymphysial tooth whorl, which was present in Psarolepis and other basal sarcopterygians.

Discussion

Unique combination of features revealed by Meemannia and Ligulalepis (Basden & Young 2001, Basden et al. 2000, Zhu et al. 2006) as well as recent work assigning Lophosteus and Andreolepis to stem-group osteichthyans (Botella et al. 2007) suggest that basal actinopterygians and sarcopterygians display many common osteichthyan features that were variably modified or lost in later members, leading to subsequently widened morphological gaps between the two lineages. As the significance of major features in Meemannia was briefly discussed in the earlier report (Zhu et al. 2006), the discussion below will touch on additional cranial and lower jaw features described in this paper and will focus on the implications of Meemannia on the origin of typical cosmine in crown-group sarcopterygians.

Lateral cranial canal as a general osteichthyan feature The lateral cranial canal found in many basal actinopterygians used to be considered a synapomorphy of actinopterygians by Gardiner & Schaeffer (1989: char. 5, C1), Coates (1998: char. C1, 1999: char. 32), and Cloutier & Arratia (2004: char. 1). Although its biological significance or its possible relation to a haemopoietic organ remains uncertain (Coates 1998, 1999; Nielsen 1942; Patterson 1975; Rayner 1948), this structure always takes the form of a pocket or a canal in front of the posterior semicircular canal and carries a posterior connection into the cranial cavity (Cloutier & Arratia 2004). In Meemannia (and in Psarolepis ) (Fig.4) there is an endocranial dorsal pocket medial to the crus commune of anterior and posterior semicircular canals. Topologically, it is comparable to the lateral cranial canal of actinopterygians including Ligulalepis (Basden & Young 2001). Thus, the lateral cranial canal should be viewed as a general feature of crown-group osteichthyans, rather than a derived feature defining actinopterygians.

Lower jaw features in early sarcopterygians Although the assignment of the lower jaw to Meemannia is tentative and subject to test when additional specimens reveal further histological and morphological details, it provides interesting information re- garding lower jaw features in early sarcopterygians. The presence of six foramina on the external surface of the lower jaw suggests that these foramina represent an early character of sarcopterygians (Zhu & Yu 2004) later lost independently in different groups. Another noteworthy feature of the lower jaw is the loose attachment of coronoids and prearticular on the Meckelian cartilage. Similar preservation is also found in other basal sarcopterygians, such as Psarolepis, Achoania and Styloichthys (Zhu & Yu 2004). This loose attachment may be partly correlated with the shallow root of coronoid tusks and thus have indirect phylogenetic significance. In addition, the presence of a horizontal coronoid-supporting face of the Meckelian bone should be considered a synapomorphy of sarcopterygians.

Cosmine – stepwise origin and alignment with surface covering in stem osteichthyans and actinopterygians Cosmine with its characteristic arrangement of enamel, pore-canal network, and single-layered dentine denticles or odontodes (Fig. 8C) has long been regarded a unique feature distinguishing sarcopterygians from actinopterygians. Cosmine-like surface covering has also been reported in osteostracans (Denison 1951) and acanthodians (Gross 1956), but it was hardly considered to be homologous with that of sarcopterygians (Meinke 1984, Rosen et al. 1981). In osteostracans, the pore-canal network is morphologically distinct, and is found in mesodentine and bone (Gross 1956, Schultze 1969) rather than in dentine and enamel (Schultze 1993). Prior to the discovery of the unique histological condition in Meemannia , cosmine tends to be regarded as a unique complicated tissue with special sensory and/or glandular functions (Denison 1966; Thomson 1975, 1977; Meinke 1984) and a major gap separated cosmine from the surface covering of stem-group

209 Andreolepis A

Orvikuina B no resorption actinopterygians

Meemannia

C Psarolepis 1 D Miguashaia partial 2 resorption Onychodus

Styloichthys sarcopterygians E

Diabolepis

Youngolepis

complete Powichthys resorption

3 Porolepis rhipidistians F Kenichthys Fig. 8. Cladogram showing the tentative position of Meemannia as the most basal sarcopterygian (after Zhu et al. 2006) and the step-wise origin of cosmine in crown-group sarcopterygians. Inserts compare the histological features of Meemannia (C) with those found in (A) stem-group osteichthyans ( Andreolepis), (B) actinopterygians ( Orvikuina), (D) stem-group sarcopterygians ( Psarolepis), and (E,F) crown-group sarcopterygians ( Styloichthys and Porolepis) . Nodes 1-3 represent three stages of cosmine evolution. Node 1: integration of pore-canal network and multi- layered odontodes. Node 2: partial resorption of odontodes of earlier generation before the redeposition of new odontodes; note that the odontodes of old generations are within the pore-canal network. Node 3: complete resorption of odontodes before the redeposition of new odontodes. The odontodes of old generations, if present, are the relicts buried in the vascular bone beneath the pore-canal network.

osteichthyans and early actinopterygians which has enamel-like ganoine and superimposed odontodes, but no pore-canal network (Fig. 8A,B). As was noted in Zhu et al. (2006), the multiple layers of superimposed odontodes coexisting with one pore-canal network in Meemannia indicates that the pore-canal network does not have a one-to-one relationship to any single odontode-enamel layer, thereby casting serious doubt on previous beliefs that cosmine bears sensory and/or glandular function, which was inferred from the unique association of the pore-canal network with one single layer of odontodes and enamel. Instead, the condition in Meemannia lends significant support to Bemis & Northcutt (1992), who presented a novel interpretation of the function of cosmine in dipnoans and proposed that the pore-canal network may represent vascular structures involved in the deposition of odontodes and enamel, rather than a network of cutaneous sensory or glandular structures.

210 The existence of superimposed odontodes in Meemannia brings cosmine into closer alignment with the components (superimposed odontodes) of surface covering in stem osteichthyans and early actinopterygians (Gross 1968, 1969; Botella et al. 2007). Meemannia as a basal sarcopterygian shares two important histological features with stem-group osteichthyans and basal actinopterygians, i. e., the ability of an earlier generation of odontodes to induce the formation of future odontodes, and the absence of resorption. In Meemannia, the odontodes overlap each other with no sign of resorption and the newer odontodes appear to be built by odontoblasts invading from side-ways, as if moving in around the existing odontodes. As each odontode superimposes on earlier odontodes, the height of the dentine layer increases, resulting in corresponding increase in the depth of pore cavities. Superimposed odontodes can be seen in Psarolepis and Styloichthys but on a less regular basis than in Meemannia, suggesting reduced ability of earlier generations to induce future odontodes. In Meemannia , superimposed odontodes of different generations coexisting with the pore-canal network lie above the vascular and/or lamellar bone and show no sign of resorption or reworking. In crown-group sarcopterygians, previous generations of odontodes may occasionally exist in forms such as Porolepis (Gross 1956) and Uranolophus (Denison 1968). However, these isolated previous odontodes represent the relicts buried in the vascular bone beneath the pore-canal network – they exist at a lower level that has been resorbed and reworked, with the newly deposited cosmine forming a uniform layer on an elevated plane. With Meemannia , the deposition of odontodes in association with the pore-canal network appeared as an apomorphy for the sarcopterygian lineage while the absence of resorption represents the retention of a primitive gnathostome feature. Typical cosmine in crown-group sarcopterygians evolved when the ability for complete resorption was gradually acquired. Meemannia (Fig. 8C) provides the first documented fossil evidence for a step-wise origin of typical cosmine in crown-group sarcopterygians, i. e., the acquisition or modified retention of a pore-canal network and the subsequently acquired ability to resorb previous generations of odontodes (Zhu et al. 2006).

Remarks on possible synapomorphies for sarcopterygians and osteichthyans Recent research demonstrated that Lophosteus and Andreolepis from Late Silurian, once assigned as primitive actinopterygians (Cloutier & Arratia 2004, Friedman & Blom 2006, Janvier 1996), are stem-group osteichthyans (Botella et al. 2007). This provides a new phylogenetic context to study the sequence of character acquisition leading from basal osteichthyans to basal sarcopterygians. With the latest findings of a series of basal sarcopterygians (Zhu & Yu 2002; Zhu et al. 1999, 2001, 2006), the morphological and histological gap between sarcopterygians and actinopterygians has been greatly reduced. Our data suggest that the synapomorphies of sarcopterygians include pore-canal network in dermal bone surface (integration of pore-canal network with multi-layered odontodes), endolymphatic duct of supraotic cavity, and dorsally-facing coronoids. Botella et al. (2007) proposed that the clade can be defined by “largest teeth (‘fangs’) on coronoids, ectopterygoids, dermopalatine and vomers”. However, this cannot be corroborated in the mandible tentatively assigned to Meemannia , which seems to lack fangs based on available data. Combining the data from Zhu et al. (2006) and Botella et al. (2007), we can divide the osteichthyan synapomorphies relating to dentate bones into those for the Osteichthyes and those for crown-group Oste- ichthyes. The synapomorphies of Osteichthyes include the presence of maxilla, the presence of premaxilla and dentary, and the presence of tooth-like denticles on the edge of jaw bones. Only one character can definitely define crown-group Osteichthyes, i. e., broad medial horizontal lamina of dentary and maxilla bearing larger monolinear tooth row (Botella et al. 2007). Although the parasymphysial tooth whorl is likely to be a general gnathostome feature, the presence of coronoids and prearticular is an innovation of either Osteichthyes or crown-group Osteichthyes. Because we still lack the data about the endocranium of Lophosteus and Andreolepis , the endocranial morphotype of crown-group Osteichthyes can only be inferred from basal actinopterygians and basal sarcopterygians. Comparison between Meemannia and basal actinopterygians suggests that the following features can define crown-group Osteichthyes: supraotic cavity proper, lateral cranial canal, processus descendens of sphenoid or otico-sphenoid bridge, basipterygoid articulation, and endochondral bone. It is possible that some of these characters were acquired before the sarcopterygian- actinopterygian split, and more should be known of the endocrania of stem-group osteichthyans.

211 Acknowledgements

This paper is dedicated to Professor Chang Meemann in recognition of her outstanding contribution in many areas of paleoichthyology and vertebrate systematics. We thank Yang Mingwan and Huang Jinling for artwork, Zhang Jie for photographic work, Lu Xiufen for specimen preparation, and Zhang Wending for making thin sections. This work was supported by the Major Basic Research Projects of MST of China (2006CB806400), the Chinese Foundation of Natural Sciences (Grant 40332017 and 40572021), and the CAS/SAFEA International Partnership Program for Creative Research Teams. This paper is also a contribution to IGCP491. We are grateful for many useful remarks and suggestions of the reviewers.

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Authors’ addresses: Min Zhu (corresponding author) and Wei Wang, Key Laboratory of Evolutionary Systematics of Verte- brates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, P. O. Box 643, Beijing 100044, China. E-mail: [email protected] Xiaobo Yu, Department of Biological Sciences, Kean University, Union, NJ 07083, USA. E-mail: [email protected]

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