Foreyia maxkuhni

Description A detailed description of Foreyia is available in online content (Supplementary Information and Figs S 2 – S 6). Only features departing from generalized coelacanths are mentioned herein. The skull roof of the posterior part of the otico-occipital portion of the neurocranium is circa 1.5 times longer than the skull roof of the ethmosphenoid portion. In most actinistians, the ethmosphenoid portion is significantly longer, between 1.5 to 2 times, than the otico-occipital portion. In a few Palaeozoic genera, the otico-occipital portion is almost as long as the ethmosphenoid portion (Caridosuctor, Rhabdoderma) or is even slightly longer (Miguashaia, Diplocercides, Sassenia), but never in the proportions seen in Foreyia (1.5 times longer). All the bones of the skull roof, the angular bone in the lower jaw and the clavicles are covered with densely packed large tubercles, while cheek and opercular bones are covered with smaller and less densely packed tubercles (Fig. 2 C). Foreyia is unique among coelacanths by its proportionally huge postparietal shield, which forms a dome in this fish and mirrors the ventral hypertrophied clavicle. No limits between ossifications are visible within the postparietal shield, neither with optical instruments nor with CT images (Figs 2 B, S 5, Smovie). We hypothesize that the postparietal shield is composed of a single, paired or unpaired ossification resulting from the complete fusion of the original ossifications (postparietals, supratemporals and extrascapulars). The skull roof of the parietonasal shield of Foreyia is typical for coelacanths, except the supraorbital sensory canal, which ran in a wide groove between the medial and the lateral series of bones and the ethmoid region, which is short. CT images of the paratype (PIMUZ A / I 4372) shows embedded in the matrix two rounded processes extending posteriorly from the postparietal shield and overpassing posteriorly the cleithra (Figs 2 B, S 5). They are interpreted as the posterior wings of the prootics, which have shifted backward before fossilization. These wings are associated with rod-like elements visible externally on the paratype that we tentatively identify as cranial ribs. A large triangular plate-like bone in the cheek is interpreted as a fused lachrymojugal and jugal. The lower jaw of Foreyia has an unusual general comma-shape, but the typical actinistian apomorphic organization is recognized (Fig. S 6). The dentary is hooked-shaped as in Latimeria and other derived coelacanths. The shoulder girdle of coelacanths is said to be remarkably conservative, except in Miguashaia 8 and, now, Foreyia. Contrary to all other coelacanths, which show a gap between the skull and the pectoral girdle, the cleithrum in Foreyia is situated at the level of the otico-occipital moiety. CT images show the dorsal extremities of the cleithra positioned against the postparietal shield (Figs 2 B, S 5), but the exact nature of the connection between the pectoral girdle and the skull cannot be observed. No anocleithra are visible externally, but the CT scan shows in the matrix a paired ossification oriented posteriorly and located on the internal side of the cleithrum in the mid-depth of the vertical branch (Fig. 2 B; Fig. S 5). Although the shape and the location are unusual for coelacanths, these bones are regarded as modified anocleithra. The ventral half of the cleithrum is hidden under the hypertrophied clavicle completely covered with the same strong ornamentation as present on the skull roof. A reniform extracleithrum covered by the same kind of tubercles borders a concavity of the posterodorsal corner of the clavicle. Its large ovoid shape is more reminiscent of the extracleithrum of the basal Miguashaia rather than that of the more derived genera, in which it is much slender 9, 10. A probable interclavicle is fused through a V-shaped suture to the anteroventral tips of both clavicles. Most coelacanths have no interclavicle, except Whitheia and Laugia, in which it is a small subdermal ossification of probable endochondral origin 8, and Miguashaia, in which it bears ornamentation and has a dermal origin 10. The scales bear two to four spines and those from the belly seem to form a paving-like structure, which may have acted as a kind of armoured protection. The postcranial skeleton of Foreyia fits the general Bauplan of coelacanths, except meristic features and fin size proportions. The paired fins are characterized by low number of fin rays: ten rays in the pectoral fins (only Allenypterus has less rays (9 )) and 12 rays in the pelvic fins (Allenypterus has less rays (6) and Hadronector has the same number). To the contrary, the dorsal and caudal fins are proportionally overdeveloped in Foreyia. The numbers of rays in these fins are in the range of other coelacanths, except for the anterior dorsal, which has the highest number together with Allenypterus (15). The total number of vertebrae is the lowest known among coelacanths due to an unusually low number of abdominal vertebrae (17).

Diagnosis As for genus, single species.

Discussion Phylogenetic relationships. At first sight, the highly-modified coelacanth Foreyia recalls basal Palaeozoic coelacanths. In particular, its general head morphology and some meristic features are reminiscent of the Carboniferous Allenypterus, such as a steep and convex profile of the anterior moiety in lateral view and a proportionally short and deep mandible. Its pectoral girdle shares superficial characters with the Devonian Miguashaia. However, a cladistic analysis places Foreyia as the sister-taxon of Ticinepomis 11, a genus recovered from the same formation at a nearby locality 12 (Figs 3 A, S 7). Both genera are nested within the latimeriids. The node supporting the Latimeria – Foreyia clade is weakly supported but Ticinepomis shares with Foreyia other characters not included in the cladistic analysis (Fig. 2 B, C). These are: 1) The postparietal shield of Ticinepomis is proportionally smaller than in Foreyia, but no sutures are visible between the postparietal and supratemporal ossifications as in Foreyia; 2) The lachrymojugal and squamosal are poorly preserved and fragmented in the holotype of T. peyeri. A possible reconstruction based on direct observation of the holotype is to regard these fragments as belonging to a single large triangular plate corresponding to the fusion of the lachrymojugal and squamosal, as in Foreyia; 3) The lower jaw of Ticinepomis is less derived than that of Foreyia. However, the dentary and the splenial of the former are both angled, reminiscent of the curved mandible of the latter; 4) The ornamentation of most of the dermal bones consists in both genera of tubercles, although in Ticinepomis they are smaller; 5) A broad dorsal extremity of the cleithrum is present in both genera; 6) A massive ornamented clavicle is present in both genera, but in a much more important proportion in Foreyia than in Ticinepomis. Heterochronic evolution and its developmental basis. Most of the shared features in Ticinepomis and Foreyia are more weakly developed in the former than in the latter genus, and they indicate a possible heterochronic evolution at the origin of Foreyia. This hypothesis is strengthened by the fact that the general coelacanth skeletal organization is not altered in Foreyia, but only relative bone sizes vary compared to the generalized coelacanths Bauplan (hypertrophied occipital and clavicular regions, comma-shaped mandible, few abdominal vertebrae and rays in paired fins, and dense covering of large tubercles on the dermal bones and denticles on the scales). Several of these features are developmentally linked in sarcopterygians and, compared with extant models, partly under the control of the same genes. In the chick embryo, the anterior most somites give rise to part of the otic capsule and the exoccipital bone (somite 1) and to the basioccipital bone (somites 2 – 4) 13. The occipital lateral plate mesoderm at the level of somites 1 – 3 gives rise to the ventromedial extremity of the clavicle in amniotes, which is regarded in part as homologous to the dermal clavicle of bony fishes 3, 4. Although numerous developmental patterning genes have a control on these features, the best candidate is the paired box gene 9, or Pax 9, widely distributed among vertebrates and present in Latimeria 14, 15 (alternative genes, such as Prrx 1 / Prrx 2, HoxD, Tbx 14 are discussed in Supplementary Information). In extant bracketing clades of coelacanths, chondrichthyans and amniotes, the embryonic expression of Pax 9 occurs at the level of the head mesoderm, of the sclerotomes (those from the first somites give rise to the occipital bones), of the postotic mesoderm (gives rise to the clavicle) and of the trunk mesoderm (gives rise to paired limbs), as well as at the level of the neural crest (give rises to odontodes) 16, 17. Pax 9 expression on the neural crest at the level of the first rhombomeres also affects the palatine and the coronoid regions in the mouse 16, two anatomical domains also modified in Foreyia. Although Pax 9 in deficient mice does no show phenotypic features directly linkable to the peculiar morphology of Foreyia, the targeted embryological tissues make this gene potentially at the origin of its heterochronic evolution (Fig. 3 D, E). Pax 9 regulates synergetically the development of the vertebral column with Pax 1. The latter has a more limited expression than Pax 9 in amniotes and has an effect on the development of the pectoral girdle, particularly on the acromion, which is a process on the scapula connecting the clavicle 18, 19. The acromion is mesodermal in origin 3, as is the hypertrophied clavicle of Foreyia. It is possible that in coelacanths the expression Pax 1 and Pax 9 are more similar between them than they are in amniotes, as it is the case in the ray-fin fish Medaka 20. In this case, both genes should be considered together in their effects on the phenotype. The search of a single genetic source is an oversimplification since we know that Pax genes work in cooperation with Hox genes 21, 22. The developmental and genetic pathways proposed here suggest that the bizarre morphology of Foreyia (Fig. 4) might be the consequence of a rapid heterochronic evolution.

Etymology The generic name honors late Peter L. Forey for his contribution on the study of coelacanth fishes. The specific epithet refers to Max Kuhn, who kindly supported for 12 years the preparation and study of fossils from the Middle Triassic of Graubünden and especially the specimens described here.

Holotype A complete specimen preserved in left lateral view (PIMUZ A / I 4620) (Figs 1, 2 C, S 2, S 4, S 6). Paratype A specimen comprising the head and the tail in left lateral view (PIMUZ A / I 4372) (Figs 2 A, B, D, S 3, S 5, S 6). Type locality and horizon Site DF 4 near the Ducanfurgga (Graubünden, Switzerland), upper part of the Prosanto Formation, Middle Triassic (early Ladinian, 240.91 million years ago) 6, 7 (Fig. S 1).