Fossil juvenile coelacanths from the Devonian of South Africa shed light on the order of character acquisition in actinistians

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1 bs_bs_banner Zoological Journal of the Linnean Society, 2015, 175, With 12 figures Fossil juvenile coelacanths from the Devonian of South Africa shed light on the order of character acquisition in actinistians ROBERT W. GESS 1 * and MICHAEL I. COATES 2 1 Evolutionary Studies Institute, University of Witwatersrand, Johannesberg 2050, South Africa 2 Department of Organismal Biology and Amatomy, University of Chicago, 1027 East 57th Street, Chicago, IL 60637, USA Received 11 August 2014; revised 14 March 2015; accepted for publication 24 March 2015 A new coelacanth genus from the Famennian (Upper Devonian) of South Africa is described, principally from presumed juveniles. Serenichthys kowiensis gen. et sp. nov. uniquely shares with Diplocercides a ventral expansion of the elbow-like lachrymojugal, as well as a symmetrical diphycercal tail supported by expanded neural and haemal spines and radials. Serenichthys is distinguished from Diplocercides by a number of derived characters, including possession of longer anterior parietals, a more crescent-shaped postorbital with a more anteriorly positioned infraorbital canal, and a far smaller squamosal, which is well separated from the skull roof. By contrast, Serenichthys appears to lacks a second dorsal fin lobe, a derived feature present in Diplocercides. Most specimens of Serenichthys are between 3 and 6 cm in length. They have large eyes, and dermal bones of the skull ornamented with long wavy ridges, similar to the dermal ornament of other Devonian coelacanths such as Gavinia. Larger isolated operculae also collected from the Waterloo Farm locality and attributed to Serenichthys indicate that with growth the ridges on the dermal bones transformed into elongate tubercles, reminiscent of those of Diplocercides and Carboniferous taxa. Phylogenetic analysis resolves Serenichthys as the sister group of Holopterygius and all known post-devonian coelacanths. The clade including the unusual leaf-shaped coelacanths, the Devonian Holopterygius and Carboniferous Allenypterus, branches from the coelacanth lineage immediately crownward of Serenichthys. The presence of abundant juveniles within an estuarine setting strongly parallels the discovery of similarly sized juveniles of Rhabdoderma exiguus together with eggs and yolk-sack larvae in the Upper Carboniferous Mazon Creek biota. It is therefore argued that Serenichthys, like Rhabdoderma, was using the sheltered estuarine environment as a nursery.. doi: /zoj ADDITIONAL KEYWORDS: estuary Famennian fish nursery ontogeny Waterloo Farm west Gondwana Witteberg Group. INTRODUCTION Coelacanths are the sister group of other living sarcopterygians (Rosen et al., 1981; Ahlberg, 1991; Friedman, 2007; Amemiya et al., 2013). As such, early coelacanths from the Devonian and Carboniferous provide an important perspective on conditions close to the base of the sarcopterygian crown group (e.g. *Corresponding author. robg@imaginet.co.za Friedman, Coates & Anderson, 2007). Although long considered as evolutionarily conservative (e.g. Huxley, 1861; Moy-Thomas & Miles, 1971; Jarvik, 1980; Amemiya et al., 2013), the record of Devonian and Carboniferous coelacanths is beginning to provide hints of initial morphological diversity. Among the earliest examples are seemingly plesiomorphic species lacking many characteristics of more crownward members (Cloutier, 1991, 1996; Long, 1999; Friedman, 2007), as well as apparently specialized leaf-shaped coelacanths with almost eel-like body forms 360

2 FOSSIL COELACANTHS FROM THE SOUTH AFRICAN DEVONIAN 361 (Lund & Lund, 1984, 1985; Friedman & Coates, 2006). Nonetheless, Devonian and Carboniferous coelacanths are represented by a limited data set of generally poorly known exemplars. As yet only five Devonian taxa, Diplocercides kayseri (Koenen, 1895; Stensio, 1922, 1937; Forey, 1998), Nesides (Diplocercides) heiligenstockiensis (Jessen, 1973; Cloutier, 1991), Miguashaia bureaui (Schultze, 1973; Cloutier, 1991, 1996), Gavinia syntrips (Long, 1999) and Holopterygius nudus (Jessen, 1973; Friedman & Coates, 2006) have been described from substantial skeletal remains. Additional taxa, Euporosteus eifeliensis (Jaekel, 1927), Euporosteus yunnanensis (Zhu et al., 2012), Chagrinia enodis (Schaeffer, 1962), Eoactinistia foreyi (Johanson et al., 2006), Styloichthys changae (Zhu & Yu, 2002, Friedman, 2007) and Shoshonia arctopteryx (Friedman et al., 2007), have been defined from no more than isolated fragments or impressions exhibiting very limited sets of characters. A small number of Carboniferous coelacanths have been described. Most species are attributed to the widespread and well-studied genus Rhabdoderma (Reis, 1888; Forey, 1981, 1998). Additional monospecific genera, Caridosuctor, Hadronector, Polyosteorhynchus, Lochmocercus and Allenypterus, have been described from the Bear Gulch locality in Montana (Lund & Lund, 1984, 1985). Later workers (e.g. Cloutier, 1991; Forey, 1998) have challenged aspects of the original descriptions of the Bear Gulch coelacanths and latex peels of key specimens have subsequently been reinterpreted. This paper reports new, whole-bodied, material derived from an Upper Devonian (Famennian) black shale lens bedded within quartzite strata of the Witpoort Formation (Witteberg Group, Cape Supergroup). Quartzites are interpreted as having been deposited in a barrier island complex, with the black shale representing anaerobic mud deposited in a back barrier lagoon of mixed marine and fresh water (Hiller & Taylor, 1992; Gess, 2002). The Waterloo Farm locality, near Grahamstown (Eastern Cape, South Africa), is the only known Upper Devonian locality in southern Africa to have yielded faunal remains. These include a diversity of fish taxa including a lamprey (Gess, Coates & Rubidge, 2006), arthrodire and antiarch placoderms (Long et al., 1997), acanthodians (Gess & Hiller, 1995; Gess, 2001), chondrichthyans (Gess & Coates, 2015), actinopterygians (R.W.G., pers. observ.) as well as dipnoan and tristichopterid sarcopterygians (Gess & Hiller, 1995). Although remains of small coelacanths were recognized in material excavated during the mid 1990s (Anderson, Hiller & Gess, 1994; Gess & Hiller, 1995), these specimens were not well enough preserved to allow a taxonomic analysis. Subsequent excavations have produced a far larger sample of specimens, including a small number in which anatomical features are preserved in exquisite detail. These latter specimens are all presumed juveniles. More fragmentary material of larger individuals provides evidence for ontogenetic change. MATERIAL AND METHODS The coelacanth fossils are compressions in which, during diagenesis, organic material was replaced by a silvery white phyllosilicate, which later altered to soft white kaolinite clay (Gess & Hiller, 1995). Superimposition of features from left and right sides of the body as well as from the internal skeleton and soft tissue structures occurs in some of the specimens. Material was studied under a binocular microscope using low-angle light to highlight details. This required frequent changes of light angle to highlight different features. Attempting to photographically illustrate all features within a single photographic image was therefore precluded. Attempts to improve photographic quality of Waterloo Farm fossils through the use of UV light have not been successful. The exeptionally delicate and friable nature of the specimens furthermore precludes submersion in alcohol. All specimens have been deposited in the palaeontological collection of the Albany Natural History Museum, Grahamstown, Eastern Cape Province, South Africa. Most of the known material appears to consist of juveniles. These include whole or partial body impressions (Figs 1 5) of 28 individuals all ranging from 3 to 6 cm in length (see Fig. 12). The whole-bodied material has generally large heads and eyes, and the ornamentation of dermal bones differs from that of larger individuals, approximately nine of which are represented, principally by isolated operculae (Fig. 6C, F). The anterior portion of a partially dissociated individual, which may have reached 15 cm in length, has operculae equal in size to the largest isolated example. These fragmentary remains of larger individuals provide important clues regarding ontogenetic change in early coelacanths. All coelacanth specimens from the Witpoort Formation conform to the anatomical and morphological constraints of a single genus and species. The interrelationships of early coelacanths were explored by including the new taxon in Forey s (1998) character matrix, as updated and extended by Friedman & Coates (2006). This matrix, augmented with further characters and taxa, was subjected to parsimony analysis, and results are included in the Phylogenetic Analysis section. ABBREVIATIONS a.f, anal fin; a.n, anterior nostril; ang, angular; ano, anocleithrum; c.f, caudal fin; cla, clavicle; cle, cleithrum;

3 362 R. W. GESS AND M. I. COATES Figure 1. Serenichthys kowiensis gen. et sp. nov. Holotype, AM5754a & b, complete juvenile specimen. A, compression showing the right side of the body (a); B, counterpart (b); C, composite drawing of holotype based largely on AM5754a with details of jaw restored from AM5754b. Scale bar = 5 mm. co, coronoid; d.f1, first dorsal fin; d.f2, second dorsal fin; de, dentary; ex, extracleithrum, ext; extrascapular; ext.l, lateral extrascapular; ext.m, median extrascapular; gu, gular; gu.p.l, gular pit line; hr, haemal radial; hs, haemal arch spine; l.p.art, left prearticular, lj, lachrymojugal; lr, lateral rostral; n.c, nasal capsule; na; nasal; nr, neural radial; ns, neural arch spine; op, operculum; or, orbit; ot, otic capsule; p.co, principal coronoid; pa, parietal; pec.f, pectoral fin; pel.f, pelvic fin; pmx, premaxilla; po, postorbital; pop, preoperculum; pop.s.c, preopercular sensory canal; pp, postparietal; preo, preorbital; pt, pterygoid; r.ang, right angular; s.o, sclerotic ossicle; so, supraorbital; sop; suboperculum; spi, spiracular; spl, splenial; sq, squamosal; stt, supratemporal; sy, symplectic.

4 FOSSIL COELACANTHS FROM THE SOUTH AFRICAN DEVONIAN 363 Figure 2. Serenichthys kowiensis gen. et sp. nov. Holotype, AM5754a & b. A, compression showing the right side of the head; B, counterpart; C, composite drawing of head based largely on AM5754a with details of jaw restored from AM5754b; D, reconstruction of head (form of spiracular, lateral rostral and subopercular as well as number of supraorbitals conjectural). Scale bar = 5 mm. SYSTEMATIC PALAEONTOLOGY OSTEICHTHYES HUXLEY, 1880 SARCOPTERYGII ROMER, 1955 ACTINISTIA COPE, 1871 SERENICHTHYS GEN. NOV. JUVENILE COELACANTHS (GESS & HILLER, 1995) Type species: Serenichthys kowiensis sp. nov., Late Famennian, Witpoort Formation DIAGNOSIS Serenichthys is described from small, probably juvenile, individuals with large heads and eyes. With all other coelacanths it shares a single bone (lachrymojugal) beneath the eye, a tandem jaw articulation, a reduced dentary, two infradentaries of which the angular is largest and is dorsally expanded, a separate large anterior coronoid, absence of a maxilla (exceptionally present in Styloichthys), absence of submandibulars, a shoulder girdle free from the skull, presence of an extracleithrum, a caudal fin with a single series of radials distal to neural and haemal spines, and linear remodelling of oral denticles. In common with Diplocercides, Serenichthys has a symmetrical diphycercal tail. It uniquely shares with Diplocercides kayseri and D. jaekeli an elbow-like, ornamented, lachrymojugal with a posteroventral expansion, not found in any other coelacanths. Serenichthys differs from Diplocercides in possession of long anterior parietals approaching the size of the posterior parietals, in having a larger, more crescentshaped postorbital in which the infraorbital canal runs along the anterior margin, by the possession of a far

5 364 R. W. GESS AND M. I. COATES Figure 3. Serenichthys kowiensis gen. et sp. nov. Paratype, AM5756a & b. Compression of juvenile individual with dissociated anterior part of the body. A, imprint of the left side of the body (b); B, counterpart (a); C, composite drawing of AM5756 based largely on AM5756b with extremities of first dorsal and caudal fins restored from AM5756a. Scale bar = 5 mm.

6 FOSSIL COELACANTHS FROM THE SOUTH AFRICAN DEVONIAN 365 Figure 4. Serenichthys kowiensis gen. et sp. nov. Paratype, AM5755a & b. Compression of complete juvenile specimen. A, imprint of the right side of the body (a); B, counterpart (b); C, composite drawing of AM5755 based largely on AM5755a. Scale bar = 5 mm. smaller squamosal which does not approach the skull roof and by the probable absence of a lobe on the second dorsal fin. Serenichthys is distinguished from coelacanths more plesiomorphic than Diplocercides, such as Miguashaia and Gavinia, by possession of two pairs of parietals, the presence of a pre-orbital, a diphycercal tail and unbranched fin rays. It is distinguished from more crownward coelacanths, other than Holopterygius, by the presence of broad neural and haemal spines and radials in the caudal skeleton. Serenichthys is easily distinguished from Holopterygius by its more conventional overall form and lack of keel scales.

7 366 R. W. GESS AND M. I. COATES A pa?sp pp stt ext.m ext.l so B pmx D de spl a.n preo lr or or po pt co ang C s.o E lj or op po sq pop Figure 5. Serenichthys kowiensis gen. et sp. nov. Details of Holotype, AM5754 (A D) and paratype, AM5756 (E). C and E are transposed to give all parts a common orientation. For line drawing explanations of specimens in A D see Figures 1C, D and 9E. For line drawing explanations of specimen in E see Figure 3C. A, skull roof; B, anterior of snout; C, cheek, orbit and lachrymojugal; D, anterior of jaw; E, caudal fin. Scale bars =2mm.

8 FOSSIL COELACANTHS FROM THE SOUTH AFRICAN DEVONIAN 367 Figure 6. Compression fossils of coelacanth operculae from Waterloo Farm, showing a progressive change in ornament with increasing size. Scale bar = 3 mm. ETYMOLOGY The generic name honours the valuable support of Serena Gess to this project. TYPE MATERIAL Holotype: AM 5754 (a & b), a slightly disrupted whole-bodied specimen preserved in part and counterpart, approximately 50 mm in length (Figs 1, 2, 5A D). Paratypes: AM 5756 (a & b) (Fig. 3, 5E), AM5755 (a & b) (Fig. 4). Other material examined: AM4889 (Fig. 6C), AM5757 AM5781, AM4912(BPCr1001) (Fig. 6B) AM4912(BPCr1002) AM4912(BPCr1007), AM4912 (BPCr1010), AM4912(BPCr1045). SERENICHTHYS KOWIENSIS SP. NOV. Diagnosis and type material: as for the genus. All material from a single shale lens at Waterloo Farm, Grahamstown/Rhini, Eastern Cape Province, South Africa. ETYMOLOGY The specific name refers to the Kowie River, which drains the hills from which the material was collected.

9 368 R. W. GESS AND M. I. COATES DESCRIPTION Serenichthys is described from presumed juvenile individuals, primarily from specimen AM5754 (Figs 1, 2, 5A D), except where stated. The dorsal profile of the skull is convex (Figs 2, 7), with a parietonasal shield marginally longer than the postparietal shield and extrascapulars combined. The postparietal shield alone is approximately 68% the length of the parietonasal shield, measured along the mid-line. This closely resembles the condition in Diplocercides, in which it is 65%. The dermal joint between the parietal and postparietal shields is slightly undulating in Serenichthys, neither as straight as that of Diplocercides kayseri (fig. 1, Stensio, 1937) nor as deeply notched as those of Hadronector (fig. 44, Lund & Lund, 1985) and Rhabdoderma (Forey, 1981), but approaching the condition reported in Caridosuctor (fig. 24, Lund & Lund, 1985). Two pairs of parietals are present; the anterior pair being slightly smaller. In contrast, Miguashaia has only one pair of parietals (Cloutier, 1996). In Diplocercides kayseri the anterior parietals are very small compared with the posterior ones (Stensio, 1937). Two pairs of parietals are found in Carboniferous and more recent taxa, the anterior pair commonly approaching the size of the posterior pair (Forey, 1998). The Carboniferous Caridosuctor (fig. 24, Lund & Lund, 1985) provides a marked exception in which the anterior pair is substantially smaller than the posterior pair. Details of the anterior portion of the snout of Serenichthys are not clear (Fig. 5B). However, a number of individual dermal bones are apparent and two pairs of large nasals are preserved in AM5756 (Fig. 3). There is no evidence of internasal bones, unlike the condition found in Diplocercides kayseri (Stensio, 1937) and Hadronector (Lund & Lund, 1985; Forey, 1998). This reflects the pattern in the remaining Carboniferous and later coelacanths (Forey, 1998). Three, or possibly four, supraorbitals are situated between the anterior parietal and the orbit. This differs from the condition in Diplocercides kayseri in which there are six (Stensio, 1937) and more recent taxa in which the number of supraorbitals is very variable, although generally greater than four (Forey, 1998). The more basally branching genus Miguashaia, however, has only four supraorbitals (Cloutier, 1996). There are five extrascapulars in Serenichthys (Figs 1, 2, 5A), as opposed to only three in Miguashaia (Cloutier, 1996) (Figs 8A, 9A) and Diplocercides kayseri (Stensio, 1937) (Figs 8B, 9C) but in common with Rhabdoderma (Forey, 1981) (Figs 8E, 9F) and Caridosuctor (Lund & Lund, 1985) as well as most Permo-Triassic taxa (Forey, 1998). Intriguingly, Lund & Lund (1985) recorded an extra pair of small, post-temporal bones, in contact with the lateral extrascapular and opercular of Hadronector (fig. 2, Lund & Lund, 1984; figs 35, 43, 44, 1985), which probably represent an extra lateral extrascapular pair (giving Hadronector, likewise, five extrascapulars). Forey (1998) interpreted Allenypterus as having only three extrascapulars, whereas Lund & Lund (1985) interpreted it as having five. Supratemporals are set into the postparietal shield. This matches conditions in Diplocercides kayseri (Stensio, 1937) (Fig. 9C), Diplocercides heiligenstockiensis (Jessen, 1973) (Fig. 9B), Hadronector, Caridosuctor and Allenypterus (Forey, 1998), but differs from Rhabdoderma (Forey, 1981) (Fig. 9F) in which the supratemporals are situated ventral to the postparietal shield. The premaxilla (Figs 2, 5B) is large and contains a circular structure interpreted as the anterior opening of the rostral organ. An anterior notch in the lateral rostal partially accommodated the anterior nostril, which was positioned between the lateral rostral and the premaxilla. Posteriorly the lateral rostral seems to extend ventral to the anterior portion of the lachrymojugal. Its exact posteroventral outline is lost as a result of rock breakage, but its ventral extent is suggested by an imprint on the pterygoid. The preorbital is large, but its exact shape is difficult to determine. Figure 7. Serenichthys kowiensis gen. et sp. nov. Reconstruction based on AM5754, AM5755 and AM5756. Scale bar = 5 mm.

10 FOSSIL COELACANTHS FROM THE SOUTH AFRICAN DEVONIAN 369 A B C D E F Figure 8. Comparison of body forms of a number of coelacanth taxa (not to scale): A, Miguashaia bureaui, Shultze 1973, Upper Devonian (Frasnian), Migausha, Canada; B, Diplocercides heiligostockiensis, Jessen (1966), Upper Devonian (Frasnian), Bergisch-Gladbach, Germany; C, Serenicthys kowiensis gen. et sp. nov., Upper Devonian (Famennian), Grahamstown, South Africa; D, Allenypterus montanus Melton 1969, Lower Carboniferous (Namurian), Montana, USA; E, Rhabdodema elegans (Newberry, 1856), Upper Carboniferous (Westphalian), Linton, Ohio, USA;F, Latimeria chalumnae Smith 1939, recent, east coast of Africa. (Images modified after Cloutier, 1996 (A), Jessen, 1973 (B), Forey, 1998 (D), Forey, 1981 (E), Millot and Anthony, 1958 (F).) Dermal bones completely cover the cheek, closely abutting one another, as in all Palaeozoic actinistian taxa (Forey, 1998). Their arrangement is shown in Figures 2 and 9 where they are compared with those of select other taxa. In Serenichthys the postorbital, squamosal and preopercular are arranged one below the other (Figs 2, 5C), resembling the condition in Carboniferous coelacanths and differing from that in Diplocercides, in which the squamosal is situated posterior to the postorbital (Fig. 9). The lachrymojugal, like that of Diplocercides kayseri (Fig. 9C, D) and D. jaekeli (Stensio, 1937), but possibly not D. heiligenstockiensis (Jessen, 1973; Cloutier, 1991) (Fig. 9B), has an elbow-like shape with a ventral expansion that, in Serenichthys (Figs 2, 5C), is more posteriorly situated and less acute than in the Diplocercides species (Fig. 9). The jugal canal extends dorsally parallel to the posterior edges of the postorbital and squamosal before turning sharply, through the squamosal, to join the infraorbital canal. The infraorbital canal thereafter follows the anterior edge of the postorbital (Fig. 9E). This agrees with the condition found in known Carboniferous coelacanths (Forey, 1998) (Fig. 9F), and represents a further departure from the condition found in Miguashaia (Fig. 9A) and Diplocercides kayseri (Fig. 9C) in which the infraorbital canal runs through the centre of the postorbital (Stensio, 1937; Cloutier, 1996). A subopercular is not clearly apparent in the holotype of Serenichthys (Fig. 2A) as the relevant portion of the head is badly damaged because of breakage into the gill chamber. In the counter specimen (Fig. 2B) ornamented bone is present in this area. In AM5756 (Fig. 3) an ornamented bone in close contact with the anterior ventral edge of the operculum is interpreted to be a subopercular. The operculum is very large, with an overlap area along its anterodorsal edge, and a slight posterior overlap of the pectoral girdle (Figs 2, 3, 6). The exact outlines of the operculum are not clear in AM5754 (Figs 1, 2), but its form is clear in a number of examples (Fig. 6), including AM5756 (Fig. 3). A small spiracular is most probably present (Figs 2A, C, 5A), although it is only fragmentally preserved and its exact shape (Fig. 2D) is speculative. Ornamentation on the head of Serenichthys, in specimens within the predominant size range, consists of anteriorly posteriorly arranged wavy parallel ridges that are visible on the postparietal and posterior parietal. Arising on the posterior portions of the cheek bones, similar ridges extend continuously in an approximately anterior to posterior direction towards and within the operculum (Fig. 2C). These ridges are similar to those on the cheek and operculum of Gavinia from

11 370 R. W. GESS AND M. I. COATES A B pmx C E de pa lr pt pa p.co ang gu po pop sq sp sop pp stt op ext Figure 9. Comparison of the dermal skull of various early coelacanths. A, Miguashaia bureaui, Shultze 1973, Upper Devonian (Frasnian), Migausha, Canada; B, Diplocercides heiligostockiensis, (Jessen, 1966), Upper Devonian (Frasnian), Bergisch-Gladbach, Germany; C, D, Diplocercides kayseri (v. Koenen 1895), Upper Devonian (Frasnian), Gerolstein, Germany; E, Serenicthys kowiensis gen. et sp. nov., Upper Devonian (Famennian), Grahamstown, South Africa; F, Rhabdoderma elegans (Newberry, 1856), Upper Carboniferous (Westphalian), Linton, Ohio, USA. (Images modified after Cloutier, 1996 (A), Jessen, 1973 (B), Stensio, 1937 (C), Forey, 1998 (D), Forey, 1981 (F).) D F

12 FOSSIL COELACANTHS FROM THE SOUTH AFRICAN DEVONIAN 371 the Devonian of Australia (Long, 1999). The fine linear ornament on the dermal bones of the skull is seen in an ontogenetic series of isolated operculae (Fig. 6) to transform with growth into elongate tubercles, not dissimilar to those seen in specimens of Diplocercides kayseri (Stensio, 1937, plate 1). In Serenichthys (at least within the studied age group) the general linear pattern of the dermal bone is extended by finer ridges on the scales. Ridges continue, in parallel, across the entire width of the exposed portion of the scales, and align with those on previous and subsequent scales. These ridges are of even prominence and may reach eight or nine in number. They are similar to those of Diplocercides kayseri (fig. VI-1, Stensio, 1937), although in this taxon some scale ridges are not continuous across the entire width of the exposed surface. A ring of small, fairly evenly sized sclerotic ossicles is preserved within the orbit of AM5754. This reflects a general sarcopterygian condition found in early coelacanths such as Miguashaia from the Devonian of eastern Canada (Cloutier, 1996). A dark mineralized orbicular body underlying the posterior margin of the spiracular in AM5744 (Fig. 2) probably represents the trace of an otolith. A similar body, paired in dorsal view, is visible in a number of specimens of Serenichthys. Amongst Devonian coelacanths otoliths have previously been reported only in Holopterygius (Friedman & Coates, 2006). The lower jaw of Serenichthys is long and shallow (Fig. 2). The dentigerous surface of the dentary is 34% of the length of the jaw, angled anteriorly, with between 15 and 25 teeth (Fig. 5D). An anterior coronoid series of simple tooth plates is present, the hindmost of which overlaps the posterior margin of the dentary (Fig. 2C, co). The principal coronoid is triangular, large and extends forward to almost meet the dentary. Many specimens of Serenichthys, including AM5744, exhibit sub-parallel lines on the principal coronoid (Fig. 2C). These are interpreted as denticle rows impressed through from the lingual surface. Such parallel denticle rows characteristically line much of the oral cavity of early coelacanths (Friedman, 2007). Denticle rows were already present on the prearticular of Styloichthys, the most plesiomorphic known coelacanth (Friedman, 2007). They have been recorded on the lingual surface of the principal coronoid of Diplocercides kayseri (plate 3, Stensio, 1937) but the pattern of their arrangement differs from that on the coronoid of Serenichthys. In Diplocercides kayseri (fig. 8, Stensio, 1937), the dentary is, similarly to Serenichthys, slightly below 35% of the jaw length. In Diplocercides kayseri (fig. 8, Stensio, 1937) (Fig. 9C) and Diplocercides heiligenstockiensis (fig. 3, Jessen, 1973) (Fig. 9B) the dentary is similarly angled. There is, furthermore, a similarity in shape between the angulars of Diplocercides kayseri (fig. 8, Stensio, 1937) and Serenichthys, but the principal coronoid of Diplocercides kayseri (fig. 8, Stensio, 1937) is not as large as that of Serenichthys (Fig. 2) and does not approach the dentary (fig. 8, Stensio, 1937). The gular plates of Serenichthys exhibit pit lines. The gulars are about the same length as the lower jaw, but are offset posteriorly and thus project behind the level of the jaw articulation (Fig. 2C). The gulars and the lower jaw, like the cheek and operculum, are ornamented with longitudinal ridges, which on the gular plate are coarser and concentric. Both in form and in ornament the gular plates are reminiscent of those of Diplocercides kayseri (Stensio, 1937, plate 1), as well as isolated gular plates from the Holy Cross mountains attributed thereto (Szrek, 2007). Those of Serenichthys, however, exhibit far fewer ridges, which are unbroken. This difference might be attributable to their younger ontogenetic age. The urohyal of Serenichthys, best preserved in AM4912(BPCr 1045) (fig. 59C E, Gess & Hiller, 1995), is narrow anteriorly, diverging into a gradual fork posteriorly. It has broad, well-rounded lateral wings that extend from near the anterior extremity and broaden posteriorly. This matches the conserved form of the urohyal in coelacanths (Forey, 1998). This specimen has been subsequently damaged. The pectoral girdle, consisting of a cleithrum, anocleithrum and extracleithrum, is broad, like that of Diplocercides kayseri (Stensio, 1937), but because of its poor preservation the girdle is difficult to reconstruct. The pectoral fin is situated low on the girdle (Figs 1C, 8C). This is the condition seen in Diplocercides heiligenstockiensis (Jessen, 1973; Cloutier, 1996) (Fig. 8B), Miguashaia (Fig. 8A) and Shoshonia (Friedman et al., 2007) as well as in most early sarcopterygians and actinopterygians (Janvier, 1996). Pectoral fin position is unknown in other Devonian coelacanths, whereas in Carboniferous (Fig. 8D, E) and more recent taxa it assumes a position approximately half way up the flank, as in the extant coelacanth Latimeria (Fig. 8F) (Forey, 1998). The first dorsal fin of Serenichthys has nine fin rays, which are unbranched, smooth and segmented distally (Figs 1, 3, 7). At least eight fin rays are found in the second dorsal fin of AM5756 (Fig. 3). It echoes the first dorsal fin in the apparent absence of a basal lobe, and possibly in the number of fin rays. It is, however, far less commonly preserved than the first dorsal fin and evidently was less robust. No evidence for a basal lobe is to be found in any of the material examined, and we consider it most likely that it was absent. The poor preservation of the material, however, precludes demonstration of this character with absolute certainty

13 372 R. W. GESS AND M. I. COATES Pelvic fins of AM5755 (Fig. 4), situated slightly posterior to the first dorsal fin, display a small basal lobe. The anal fin has a similarly sized basal lobe, which in AM5756 and AM5755 (Figs 3, 4) is situated slightly posterior to the second dorsal fin. This fin position is similar to that in Diplocercides heiligenstockiensis (Fig. 8B) and Carboniferous coelacanths (such as Rhabdoderma) (Fig. 8E), with the exception of Allenypterus (Lund & Lund, 1984, 1985; Forey, 1998) (Fig. 8D), in which the pelvic and anal fins are situated more posteriorly and lack basal lobes. Serenichthys (Fig. 8C) also differs from Miguashaia (Fig. 8A) in which the pelvic fin is situated substantially more posteriorly, and a slight lobe on the anal fin is only developed in adult specimens (Cloutier, 1996). The caudal fin is most clearly preserved in AM5756 (Figs 3, 5E). It is diphycercal and symmetrical with 12 fairly robust fin rays, dorsally and ventrally. The anteriormost of these rays is short and unsegmented. Posterior to these 12 rays, after a gap, a number of far more delicate rays are preserved, interpreted as those of the caudal lobe. The caudal neural and haemal radials of AM5754 (Fig. 1) are broad and abutting. They appear to differ from pre-caudal neural and haemal spines which are long, narrow and well spaced (Fig. 1). In at least the anterior half of the caudal fin of AM5754, each radial supports two fin rays. The fin rays are more closely associated with each other towards the leading edge of the caudal fin. PHYLOGENETIC ANALYSIS To explore phylogenetic relationships amongst early coelacanths, Serenichthys was analysed using a matrix of 118 characters (115 informative) and 30 taxa (28 ingroup and two outgroup). Characters in the analysis were derived from Forey s data matrix for coelacanths (Forey, 1998) as updated by Friedman & Coates (2006). A number of other, more recent, variations of this data set have been used to incorporate and test the relationships of Mesozoic coelacanths (summarized and discussed in Dutel et al., 2012), but the focus of the present analysis concerns Palaeozoic branching events. For this purpose, character 111 was added from Cloutier s analysis of coelacanths (character 42, Cloutier, 1991). Characters are from Friedman s (2007) analysis of early sarcopterygians, numbered originally as 52, 50, 38 and 160, respectively (see Appendix 1). Four noval characters (110, 112, 113, 114) were added to the matrix, and brief justifications of these are provided below: Character 110: absence (0) or presence (1) of a ventral extension of an elbow-like lachrymojugal ; this refers to a ventrally directed extension of the lacrymojugal beneath the orbit. This was previously only observed in Diplocercides kayseri (Fig. 9C) and D. jaekeli (Fig. 9D). It is now also recognized in Serenichthys (Fig. 9E). Character 112: anal fin without (0) or with a basal lobe (1) and Character 113: second dorsal fin without (0) or with (1) a basal lobe ; these refer to the presence or absence of fleshy basal lobes on the dorsal and anal fins. Character 114: preopercular distant from (0) or adjacent to/abutting (1) lachrymojugal is a character added to reflect changes in the organization of the cheek, congruent with changes in the relative proportions of the skull in early coelacanths. Character 34 (Forey, 1998) deals with related but non-concurrent changes in the shape and orientation of the squamosal. The complete list of characters and character scores for taxa are provided in Appendix 1. Cladistic (maximum-parsimony) analysis of the character matrix was performed using the software PAUP*4.0b10 (Swofford, 1998, 2002), using the branch and bound algorithm. We report tree lengths treating polytomies as soft. Characters are coded as multistate and were treated as unweighted and unordered in the analysis. Bremer decay indices (Bremer, 1988) were calculated to assess support for the resolved nodes in the strict consensus of the most parsimonious cladograms. Actinopterygians and porolepiforms were used as outgroups to root resultant trees. Actinopterygian scores are an amalgam of conditions coded from Mimipiscis (Gardiner & Bartram, 1977; Gardiner, 1984; Choo, 2011) and Cheirolepis (Pearson & Westoll, 1979). Porolepiform scores were obtained from Porolepis (Jarvik, 1972; Clement, 2004) and Glyptolepis (Ahlberg, 1989, 1991). Analysis of the data matrix yielded 20 most-parsimonious cladograms of 276 steps. A strict consensus of these (Fig. 10) places Serenichthys among other Devonian coelacanths, crownward of a basal tritomy subtending Miguashaia, Gavinia and Styloichthys (paired as sister taxa: a noval result), and the clade of all other coelacanths used in the analysis. Notably, searches of the data set failed to resolve branching patterns among a suite of Mesozoic genera and Latimeria, but this anomaly has not been explored further because the taxonomic focus is beyond the scope of the present analysis. Although available data are patchy for early coelacanths, the present result provides a rudimentary branching sequence and character distribution relative to which less complete taxa, such as Eoactinistia, Chagrinia and Shoshonia, can be compared. DISCUSSION PHYLOGENETIC ANALYSIS RESULTS The resultant trees indicate that Serenichthys represents the sister group of the clade including

14 FOSSIL COELACANTHS FROM THE SOUTH AFRICAN DEVONIAN 373 Porolepiformes Actinopterygii Miguashaia Gavinia Styloichthys Diplocercides Serenichthys Allenypterus Holopterygius Lochmocercus Polyosteorhynchus Hadronector Caridosuctor Rhabdoderma Sassenia Spermatodus Coccoderma Laugia Coelacanthus Whiteia Holophagus Undina Latimeria Macropoma Garnbergia Libys Diplurus Chinlea Axelrodichthys Mawsonia 2 B 2 F K 3 M A 4 C Holopterygius and Allenypterus, and the clade of all post-devonian taxa (Figs 10, 11). The stratigraphic age of Holopterygius indicates that it diverged from Allenypterus by the late Givetian if not earlier (Friedman & Coates, 2006), and likewise for the divergence of this clade from the post-devonian coelacanth clade. Thus two lineages, at least, survived beyond the end Devonian (Hangenberg) extinction event, which brought about significant biotic turnover (Sallan & Coates, 2010). Earlier splits in coelacanth phylogeny, including that between Diplocercides and Serenichthys plus all more crownward coelacanths (Fig. 11), seem likely to have occurred before the Givetian. Moreoever, the possibility of a modest, evolutionary radiation of coelacanths early in the Devonian is supported by the recent description of a coelacanth neurocranium of apparently similar overall proportion to Diplocercides from the Pragian of China (Zhu et al., 2012), and the possibility that Styloichthys (Yu, 1990; Zhu & Yu, 2002) represents a further early lineage of this enigmatic clade (Friedman, 2007). MORPHOLOGY Cheek proportions Uniquely amongst Devonian coelacanths Serenichthys exhibits the cheek arrangement seen in Carboniferous and more crownward coelacanths. Early coelacanth history is characterized by a progressive extension of the anterior portion of the skull D E G H I 4 J 2 L N O P Crown group coelacanth Stem group coelacanths Out group Bremer support/decay values Figure 10. Strict concensus tree of coelacanths generated after phylogenetic analysis utilizing PAUP. that increased the size of the gape (Forey, 1998). Forey demonstrated this trend by comparing the relative lengths of the parietonasal and postparietal dermal armour as a proxy for a relationship between the anterior and posterior portions of the neurocranium (Forey, 1991). Increase in the length of the anterior portion of the skull was accompanied by a reduction in the postorbital portion, a change that has not previously been explored. The relative contribution of the postorbital region of the dermal skull to its total length was calculated by comparing the length of an arc extending from a mid-anterior position on the premaxilla to the furthest point on the opercular with the difference between this length and that of a similar arc extending to the posterior of the orbit. The measured trend towards reduction is consistant with the phylogenetic branching sequence. The postorbital regions of basal taxa, Miguashaia (after Cloutier, 1996) and Gavinia (after Long, 1999) contributed 74 and 71%, respectively, to total head length. In Diplocercides (after Jessen, 1973), this contribution was reduced to 55%. In Carboniferous taxa (after Forey, 1981; Lund & Lund, 1984, 1985; Cloutier, 1991) it was further reduced to between 38 and 47 % of the total head length. This range matches the equivalent proportions of post-carboniferous crania, and is close to the postorbital proportion of 48% (of total lateral head length) found in Serenichthys. Two rearrangements of the relative positions of the postorbital, squamosal and preopercular bones are linked 3 Q 2 R 5 T S

15 374 R. W. GESS AND M. I. COATES Devonian Carboniferous E L M E Spk Vis Tou Fam Frs Giv Eif Ems Pra Loc Styloichthys Gavinia Holopterygius Miguashaia Diplocercides to this cheek-shortening trend. In genera that branch from the base of the coelacanth clade, such as Miguashaia (fig. 5, Cloutier, 1996) and Gavinia (Long, 1999), the postorbital, squamosal and preopercular are arranged one behind the other in an anterior to posterior series (Fig. 9A) as in outgroup sarcopterygians (Janvier, 1996). The Miguashaia squamosal dominates and spans the entire cheek, extending from the ventral margin to abut or nearly abut the lateral rim of the skull roof. However, in Diplocercides (Fig. 9B D) the cheek is anteroposteriorly shortened, and the squamosal reduced to a subtriangular plate, allowing the subjacent preopercular to contact the lachrymojugal (Stensio, 1937). Nevertheless, the squamosal continues to contribute to the dorsal margin of the cheek, and thus lies in close proximity to the skull roof. Significantly, this feature is absent in Serenichthys (Fig. 9E), and the squamosal is situated below the postorbital rather than behind, and has ceased to approach the skull roof. This derived arrangement, in which the postorbital, squamosal and preopercular are arranged one below the other, with the pre-opercular approaching or contacting the lachrymojugal, is characteristic of post-devonian coelacanths. Thus far, Serenichthys is the only known Devonian taxon in which Serenichthys Allenypterus Lochmocercus Polyosteorhynchus Hadronector Caridosuctor post Carboniferous Coelacanths Rhabdoderma Figure 11. Stratocladogram demonstrating the relationship between Serenichthys and other Devonian and Carboniferous coelacanths. both of these cheek modifications, characteristic of more crownward coelacanths, may be observed. Notable exceptions to this trend include the Triassic Sassenia (Stensio, 1921; Forey, 1998), in which the squamosal once more dominates the cheek, separating the pre-opercular from the lachrymojugal, and the crown genus Latimeria, in which cheek bone reduction increases their degree of separation. The unusually large squamosal of the Carboniferous Rhabdoderma (Newberry, 1856; Forey, 1981) apparently separates the preopercular from the lachrymojugal (fig. 7.1, Forey, 1998) (Fig 9F), and in the Carboniferous Hadronector (Lund & Lund, 1984, 1985; Cloutier, 1991; Forey, 1998), the squamosal extends dorsally as far as the spiracular, suggesting a degree of cheek pattern reversal. Relative length and orientation of the dentary The progressive shortening and increased anterior inclination of the dentary is a striking and visibly clear morphological trend in the evolution of coelacanth mandibles. Teeth on the dentary comprise a single row of individual teeth in early coelacanths whereas in more derived coelacanths teeth are clustered in groups on dentary tooth plates, or are lost completely. Serenichthys and Diplocercides are noteworthy as the only

16 FOSSIL COELACANTHS FROM THE SOUTH AFRICAN DEVONIAN 375 Devonian taxa displaying the characteristic forwardly angled dentary of Carboniferous and later coelacanths. The dentaries of Serenichthys (Fig. 9E) and Diplocercides species (fig. 7, Stensio, 1937; fig. 3, Jessen, 1973) (Fig. 9B) have dentigerous surfaces equivalent in length to 33 35% of the length of their mandibles. This proportional length is close to those of most other mid- to late Devonian examples, with the exception of Miguashaia in which the dentary is reduced to 18% in adults (fig. 5, Cloutier, 1996) (Fig. 9A), although it is a more typical 27% in juveniles of the same species (fig. 1, Cloutier, 1996). By contrast, in the Early Devonian Styloichthys (Zhu & Yu, 2002), the toothbearing portion of the jaw represents almost 50% of its length (fig. 1, Zhu & Yu, 2002; fig. 5, 2004). Serenichthys and Diplocercides resemble post- Devonian coelacanths in having forwardly angled dentaries. Conversely they overlap with all other known Devonian taxa by the possession of a single row of individual teeth on the dentary. Thus far amongst post- Devonian taxa only Lochmocercus (fig. 69, Lund & Lund, 1985; Forey, 1998) displays this condition. All remaining post-devonian coelacanths bore dentary teeth on separate toothplates (Forey, 1998), with the exception of Allenypterus which was probably edentulous (Friedman & Coates, 2006). Dermal ornament of the head Identification of juvenile specimens of Serenichthys with linear ornament resembling that of juvenile Rhabdoderma material and of adult Gavinia (Long, 1999) has systematic and biostratigraphic implications. Linear ornament on the cheek bones and operculae of juvenile Rhabdoderma (Schultze, 1972; Forey, 1998) from the Upper Carboniferous Mazon Creek biota of Illinois (e.g. UC14389 in the Field Museum, Chicago: R.W.G., pers. observ.) is markedly different from the elongate tubercles surrounded by ridges (Forey, 1998) considered to be diagnostic of adult Rhabdoderma. Likewise, a small coelacanth from the Carboniferous Freeport Coal of Ohio (UF 270 in the Field Museum, Chicago: R.W.G., pers. observ.) identified as Rhabdoderma elegans (Newberry, 1856; Moy-Thomas, 1937) also exhibits an opercular ornament of parallel, continuous wavy ridges. These observations suggest that the adult Rhabdoderma dermal bone ornament pattern was derived through ontogeny from a more general condition of linear ornament as in Serenichthys, and that such ornament is a potentially misleading taxonomic indicator among Palaeozoic coelacanths. Thus, it is noteworthy that the only post-devonian species of Diplocercides, D. davisi (Moy-Thomas 1937; Cloutier, 1991), consists of small isolated head bones from the Lower Carboniferous of Ireland, and that these specimens were removed from Rhabdoderma because of ornament similarity to that of Diplocercides (Cloutier, 1991; Forey, 1998). We argue otherwise: that Diplocercides davisi is more likely to be a subadult specimen of Rhabdoderma, and that no definite evidence therefore exists for Diplocercides having survived the end-devonian biotic crisis. Caudal fin The genera Diplocercides, Serenichthys, Holopterygius, Allenypterus and Lochmocercus are characterized by having non-heterocercal tails (in common with all more derived coelacanths), whilst retaining more than one fin ray per caudal fin radial (in common with all less derived taxa). This combination is also seen in Chagrinia (Schaeffer, 1962) from the Famennian of Ohio. By contrast, Gavinia (Long, 1999) and Miguashaia (Schultze, 1973; Cloutier, 1996), the least derived taxa in which the caudal fin is known, have heterocercal caudal fins more closely resembling those of early actinopterygians such as Moythomasia (Woodward & White, 1926; Gardiner, 1984). Gavinia and Miguashaia also exhibit bifurcation of lepidotrichia in all fins, a character otherwise seen in the pectoral fin of Shoshonia (Friedman et al., 2007) and more generally among non-specialized osteichthyans. Jessen records a branched caudal lepidotrichium (Jessen, 1973, p. 169) in Diplocercides heiligenstockiensis. Bifurcation of lepidotrichia is, by contrast, not seen in any of the fins of Serenichthys or post-devonian coelacanths. Rate of morphological change Results presented here add to the ongoing revision of the classic view that the distinctive characteristics of coelacanths evolved rapidly and early, and then remained largely static throughout subsequent clade history (e.g. Huxley, 1861; Moy-Thomas & Miles, 1971; Jarvik, 1980; Zhu et al., 2012). It appears that the rearrangement of the cheek pattern, the transformation of the lower jaw and the modifications of the axial skeleton in coelacanths were incrementally acquired. Extending upon Friedman & Coates (2006) quantified analysis of anatomical disparity among early coelacanths, as well as demonstrations that coelacanths have not remained morphologically static since the Devonian (Cloutier, 1991; Forey, 1998), the present result contributes to a growing concensus that the actinistian morphotype did not arise suddenly during the Late Devonian, but evolved gradually and sequentially. REPRODUCTION AND ECOLOGY Adult female specimens of the extant coelacanth Latimeria have been collected with near-full-term juveniles within the reproductive tract (Smith et al., 1975;

17 376 R. W. GESS AND M. I. COATES Figure 12. Graph illustrating the size distribution of specimens attributed to Serenichthys kowiensis gen. et sp. nov. Bruton, Cabral & Fricke, 1992), indicating that they give birth to live young. Interestingly, the association of coelacanths with live bearing had already been proposed on the basis of fossil data, following Watson s (1927) discovery of anterior facing juveniles in the abdominal cavity of the Upper Jurassic species Undina penicillata. However, evidence from large numbers of eggs, yolk sac juveniles and juveniles of Rhabdoderma (Schultze, 1972) in the Upper Carboniferous Mazon Creek fauna indicates that coelacanths were not always ovoviviparous and that Rhabdoderma, at least, was probably oviparous. Moreoever, lack of non-juvenile coelacanths as well as scarcity of adult elasmobranch remains suggest that the Mazon Creek estuarine environment provided a safe spawning ground and nursery for a variety of fish (Schultze, 1972, 1980; Sallan & Coates, 2014). Therefore, it is significant that the Waterloo Farm shale is interpreted as having been deposited in a quiet embayment of a back-barrier lagoonal estuary (Gess & Hiller, 1995) on the shores of the Agulhas Sea. In addition, more than 75% of Serenichthys specimens belong to a single age group, ranging in size between 3 and 6 cm (Fig. 12). This strongly suggests an estuarine breeding-ground or nursery, probably in the shallow embayment where the shale was deposited. Such use of estuaries as a safe haven for juveniles of predominantly marine species is common in recent environments. Along the Eastern Cape coast of South Africa, for example, 34 of 80 fish species occurring in estuaries are, to a varying extent, utilizing this strategy (Whitfield & Bok, 1998). Although the Serenichthys specimens are of approximately the same size range as those of Rhabdoderma exiguum (Schultze, 1980), it is not possible to recognize any trace of yolk sacs. However, the possibility that the somewhat bloated state of many specimens derives taphonomically from the presence of a partially resorbed yolk sac cannot be unambiguously rejected. Finally, we note that in certain instances, several whole-bodied specimens of Serenichthys have been found on the same horizon, suggesting that they died as a result of a sudden stress within the environment. Considering the anoxic nature of the sediment (Gess, 2002), at a time of globally low oxygen levels (Algeo, Scheckler & Maynard, 2001) this stress may have been an oxygen deficiency. Alternatively, considering the markedly high latitude position of southern Africa during the late Devonian (Scotese & McKerrow, 1990), temperature fluctuations are not unlikely to have killed shoals of juvenile fish sheltering in shallow water. CONCLUSION Serenichthys provides an important addition to the scant record of early coelacanths, adding to an increasing morphological diversity of Devonian genera (cf. Friedman & Coates, 2006). The resemblance of many of the skeletal components of Serenichthys to those of Diplocercides suggests that binning of generalized Late Devonian and even Early Carboniferous fragmentary remains within this genus may have concealed some of the early diversity of coelacanths. Ontogenetic transformations of the dermal skeletal ornament of Serenichthys highlight the unreliability of such data as a diagnostic character. Records of Diplocercides from the Carboniferous, based upon dermal ornament type, are therefore unreliable. The growing array of early coelacanths demonstrates that characters associated with Mesozoic genera and the living Latimeria were neither rapidly nor simultaneously acquired towards the end of the Devonian. Rather, they were sequentially evolved. Moreover, towards the end of the Devonian a number of diverse lineages probably coexisted. These included seemingly plesiomorphic taxa such as Miguashaia; the group from which most post-devonian coelacanths probably descended, including Diplocercides and Serenichthys;