Crown or modern sarcopterygians (coelacanths, lungfishes, and tetrapods) differ substantially from stem sarcopterygians, such as Guiyu and Psarolepis, and a lack of transitional fossil taxa limits our understanding of the origin of the crown group. The Onychodontiformes, an enigmatic Devonian predatory fish group, seems to have characteristics of both stem and crown sarcopterygians but is difficult to place because of insufficient anatomical information. We describe the new skull material of Qingmenodus, a Pragian (~409-million-year-old) onychodont from China, using high-resolution computed tomography to image internal structures of the braincase. In addition to its remarkable similarities with stem sarcopterygians in the ethmosphenoid portion, Qingmenodus exhibits coelacanth-like neurocranial features in the otic region. A phylogenetic analysis based on a revised data set unambiguously assigns onychodonts to crown sarcopterygians as stem coelacanths. Qingmenodus thus bridges the morphological gap between stem sarcopterygians and coelacanths and helps to illuminate the early evolution and diversification of crown sarcopterygians.

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INTRODUCTION

Living sarcopterygians fall into three major groups: coelacanths, lungfishes, and tetrapods (limbed vertebrates). Most of the recent molecular and morphological phylogenetic analyses place the lungfishes and tetrapods as extant sister groups—forming a clade that is sometimes termed “Rhipidistia”—and the coelacanths as the sister group to that clade (1–4). The subclass Sarcopterygii forms the sister group to the subclass Actinopterygii, which together constitute the class Osteichthyes. With the exception of the tetrapods, sarcopterygians have a long evolutionary history of diversity decline and are nowhere near as diverse today as they were at the beginning of their history. As a consequence, their early fossil record contains a number of groups that have proved more or less difficult to place in relation to the extant members, such as the onychodonts (1, 2, 5, 6).

Until recently, the onychodonts, which are an exclusively Devonian group of mostly marine sarcopterygians, were represented by only six named genera. The recently described Qingmenodus from the Early Devonian of China (7) is now the best known early representative. Of the other five genera, two are known from single specimens (Grossius and Luckeus) (8, 9) and one from dermal bone fragments (Bukkanodus) (10). The Strunius material from the Late Devonian (Frasnian) of Bergisch Gladbach in Germany is articulated but strongly flattened (11); near-contemporary Onychodus material from Gogo in Western Australia is perfectly three-dimensional and includes braincase components, but large parts of the braincase appear to have been unossified, and the preserved components are often more tantalizing than informative (12). Fragmentary jaw materials from the Lochkovian fauna of South China and northern Vietnam (13, 14) suggest that the fossil record of onychodonts may extend back to the earliest Devonian, almost coeval with the earliest rhipidistians (Youngolepis, Diabolepis, and Powichthys).

Onychodonts are characterized by a distinctive head morphology that includes large parasymphysial tooth whorls with sigmoid teeth on their lower jaws and commensurately large internasal pits on the ethmoid floor to accommodate the whorls (6, 12). In Onychodus, the ethmosphenoid region of the braincase has a series of distinctive features that all appear to form a functional complex with the strongly developed parasymphysial tooth whorls and internasal pits: notably, the vomers are absent, the parasphenoid is short, and the notochordal facet is extremely large (12).

This onychodont character complex has always been regarded as autapomorphic (12). Tooth whorls and internasal pits are also present in porolepiforms (for example, Porolepis and Holoptychius), Powichthys, and Youngolepis, which are Devonian members of the lungfish stem group (15–18), but these parts are smaller than those of onychodonts, and the associated cranial architecture is less extreme. However, the hypothesis that the onychodont character complex is specialized has recently been challenged by the discovery of three very early osteichthyans—Guiyu, Psarolepis, and Achoania—from the Late Silurian to Early Devonian (Ludlow to Lochkovian) of Yunnan, China (19–21). These genera combine onychodont-like ethmosphenoids, as well as lower jaws equipped with large parasymphysial tooth whorls, with primitive characteristics that suggest a placement in the sarcopterygian stem group or possibly the osteichthyan stem group (19, 22, 23). Some researchers have interpreted this character distribution as evidence that these early Chinese osteichthyans form a clade with onychodonts (6), but this conflicts with other characters such as the presence of a single humerus in Onychodus (and crown sarcopterygians) (12) but a multibasal pectoral fin in Psarolepis and Achoania (24). An alternative possibility is that the distinctive and seemingly specialized onychodont gestalt is, at least in part, primitive for the Sarcopterygii. Resolution of this problem requires a well-supported phylogenetic placement for the onychodonts.

Poor ossification of the character-rich neurocranium, along with conflicting character states, has until now resulted in disagreement about the placement of onychodonts in a sarcopterygian phylogeny (1–3, 5, 6, 25). The recent discovery of Qingmenodus, an Early Devonian (Pragian, ~409 million years ago) onychodont from China with a well-ossified braincase (7), has begun to remedy this deficiency in the data; notably, the otoccipital region of Qingmenodus shows a posteriorly large positioned attachment for the basicranial muscle reminiscent of the condition in coelacanths (7). However, until now, the cranial cavity and associated spaces of onychodonts have remained largely unknown, except for a few structures (the external semicircular canal tract, the mesial wall of the nasal cavity, and parts of the ethmosphenoid cranial cavity) visible in acid-prepared specimens of Onychodus from Gogo (12).

We describe here a newly discovered anterior cranial portion, permitting a completely reconstructed virtual cranial endocast of Qingmenodus. It provides the first detailed interpretation of internal neurocranial anatomy in onychodonts, allowing extensive comparisons with other sarcopterygians, in particular those that have been studied by serial grinding or computed tomography (CT) scanning (15–17, 26–33). This study sheds light on the relationships of onychodonts and helps us to understand the sequence of character acquisition in the early evolution of sarcopterygians. We show that onychodonts form a plesion in the coelacanth stem group, casting light on the earliest steps in the evolution of this morphologically distinctive and still extant sarcopterygian group.