Articles DOI: 10.1038/s41559-017-0293-5

A Devonian tetrapod-like fish reveals substantial parallelism in stem tetrapod evolution

Min Zhu 1,2*, Per E. Ahlberg 3*, Wen-Jin Zhao1,2 and Lian-Tao Jia1

The fossils assigned to the tetrapod stem group document the evolution of terrestrial vertebrates from lobe-finned fishes. During the past 18 years the phylogenetic structure of this stem group has remained remarkably stable, even when accommo- dating new discoveries such as the earliest known stem tetrapod Tungsenia and the elpistostegid (fish–tetrapod intermediate) Tiktaalik. Here we present a large lobe-finned fish from the Late Devonian period of China that disrupts this stability. It com- bines characteristics of rhizodont fishes (supposedly a basal branch in the stem group, distant from tetrapods) with derived elpistostegid-like and tetrapod-like characters. This mélange of characters may reflect either detailed convergence between rhizodonts and elpistostegids plus tetrapods, under a phylogenetic scenario deduced from Bayesian inference analysis, or a previously unrecognized close relationship between these groups, as supported by maximum parsimony analysis. In either case, the overall result reveals a substantial increase in homoplasy in the tetrapod stem group. It also suggests that ecological diversity and biogeographical provinciality in the tetrapod stem group have been underestimated.

he colonization of the land by animals during the mid-Palaeozoic in 2002 and described here, provides a first and highly sur- involved the evolution of complex suites of adaptations. prising glimpse of sarcopterygian diversity in the Devonian of The incidence and importance of evolutionary convergence North China (Figs. 1–4 and Supplementary Figs. 1–3). It com- T 17–26 in this process appears to have varied greatly between groups. bines characteristics of rhizodont fishes (supposedly a basal Several arthropod clades independently achieved terrestrial- branch in the stem group) with derived elpistostegid-like and ity during the Silurian period or earlier1. By contrast, tetrapods tetrapod-like characters, including a remarkably tetrapod- (defined here as vertebrates with limbs and digits)2 are mono- like shoulder girdle10,27, hinting at an unanticipated ecological phyletic, and their sister group relationship to the elpistostegids diversity and challenging the accepted consensus view of the Panderichthys, Elpistostege and Tiktaalik is robustly supported2–10, fish–tetrapod transition. suggesting that vertebrates underwent just a single transition from water to land. The lobe-finned fishes that form the lower part of Results the tetrapod stem group, below the elpistostegids, do not show Systematic palaeontology. Osteichthyes Huxley, 1880 convergent acquisition of terrestrial adaptations; although, there Sarcopterygii Romer, 1955 are repeated trends towards large body size and an elpistostegid- Tetrapodomorpha Ahlberg, 1991 like morphology2. The phylogenetic topology of the tetrapod stem Hongyu chowi gen. et sp. nov. group has remained essentially stable through repeated analyses Etymology. The generic name derives from hong (Chinese Pinyin), over the last 18 years2–9. which means large and yu (Chinese Pinyin), which means fish. The The North China Block, an ancient craton complex, was a small specific is in honor of Min-Chen Chow. continent located near the Equator during the Devonian period11–13. Holotype. IVPP V17681, a three-dimensionally preserved and par- The distribution of regionally endemic groups of Devonian verte- tially articulated specimen. brates, such as galeaspids and sinolepid antiarchs, indicates close Locality. A quarry at Shixiagou, Qingtongxia, Ningxia, China. proximity or even contact at this time between the North China Approximate coordinates: 37° 39′​ 18.4″ ​N, 105° 59′​ 34.2″​ E. Block, the South China Block and eastern Gondwana12–14. Silurian Horizon. Zhongning Formation, Famennian, Late Devonian deposits within the South China Block contain the earliest fossils of period. sarcopterygian (lobe-finned) fishes in the world, suggesting that the Diagnosis. Large fin-bearing tetrapodomorph with the following clade Sarcopterygii may have originated there15; early sarcopteryg- unique character combination: a jagged margin along the dermal ian fossils from neighbouring North China are therefore potentially intracranial joint, posterior margin of tabular anterior to that of the of great evolutionary and biogeographical interest. However, until postparietal, an extremely flat lower jaw with a large rectangular ret- now, the only Devonian sarcopterygian from the North China Block roarticular process, single large lateral line pore at extratemporal– that has been described, is the tetrapod Sinostega, represented by a supratemporal junction, hyomandibula with an opercular process at single incomplete lower jaw from the Famennian (latest Devonian) the distal end, a large plate-like scapulocoracoid without foramina, Zhongning Formation of the Ningxia Hui Autonomous Region16. cleithrum without ventral lamina, distinct atlas vertebra articulating The partly articulated skeleton of a large lobe-finned fish with occiput, vertebrae with ring centra, round thin scales without from the Zhongning Formation, discovered by P.E.A. and M.Z. an internal median boss.

1​Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, PO Box 643, Beijing 100044, China. 2​College of Earth Science, University of Chinese Academy of Sciences, Beijing 100049, China. 3​Subdepartment of Evolution and Development, Department of Organismal Biology, Evolutionary Biology Centre, Uppsala University, Uppsala 752 36, Sweden. *e-mail: [email protected]; [email protected]

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ab

c d Surangular Prearticular Entopterygoid It Pa hy Unidentified bones Gular plate Angular Dentary Dentary po Cleithrum

Pq Pp St sc n.arch Ta sc Cleithrum Clavicle hy Et retro phbr retro cla.sp oa.sc chy scap pit cla.sp Glenoid cla.sp sc sq buttress ebr 1–2 at.v ebr 1–2 gle rad scap cbr 4–5 rad gle cbr 1–5 sc sc Scapular Anamestic Premaxillary process scap bone Glenoid buttress gle ac.gle sc Lepidotrichia Canal for Neural spine notochord 15th Attachment for haemal arch 15th vertebra Unidentified dermal bone vertebra Attachment for neural arch Rib attachment 10 cm 22nd vertebra 22nd vertebra

Fig. 1 | V17681, holotype of Hongyu chowi gen. et sp. nov. a, Dorsal view (photo). b, Ventral view (photo). c, Dorsal view (drawing). d, Ventral view (drawing). ac.gle, anterior cam of glenoid facet; at.v, atlas vertebra; cbr, ceratobranchial; chy, ceratohyal; cla.sp, clavicular spine; ebr, epibranchial; Et, extratemporal; gle, glenoid facet; hy, hyomandibula; It, intertemporal; n.arch, neural arch; oa.sc, area overlapped by scale; Pa, parietal; phbr, pharyngobranchial; po, lateral line pore; Pp, postparietal; Pq, palatoquadrate; rad, radial; retro, retroarticular process; sc, scale; scap, scapulocoracoid; sq, squamosal; St, supratemporal; Ta, tabular.

Taxonomic note. We use the name Tetrapodomorpha for the tet- displaced by flowing water: the left premaxilla, left squamosal and rapod total group28 and restrict Tetrapoda to the limbed vertebrates a third unidentified dermal bone are scattered to the right of the (limbed stem tetrapods plus the tetrapod crown group)4,10. Hongyu, vertebral column. Opercular and extrascapular bones are absent. like Tiktaalik, belongs to the finned stem tetrapods and is therefore The strongly ossified gill skeleton is well preserved, as is the partly a member of the Tetrapodomorpha, but not the Tetrapoda. disarticulated pectoral girdle. The vertebral column consists of ring centra with loosely attached, slender neural arches. A patch of lepi- Discussion dotrichia with long basal segments, and a couple of slender radial Mélange of characters. The specimen comprises the posterior part elements, represent the right pectoral fin. of the skull, the gill skeleton and pectoral girdle, and the anterior In many respects Hongyu resembles a rhizodont, a widely dis- vertebral column of a large fish (Fig. 1a,b). It is slightly compressed tributed group of large to very large predatory tetrapodomorph dorsoventrally but essentially three-dimensional. Unfortunately, fishes known from the Devonian and Carboniferous periods17–26. the snout region was not recovered (the specimen was found in Supratemporal–extratemporal contact is a derived rhizodont char- the working face of an active quarry and this part seems to have acter (albeit shared with onychodonts), as is the tall facial lamina of been lost to the quarrying process), but the posterior end of the the premaxilla19,22. A large robust shoulder girdle with a tall clavicu- ethmosphenoid is preserved along with the posterior half of the lar spine, thin round scales, and a proportionately broad head are left palatoquadrate, which is still in articulation with the lower jaw. also typical rhizodont features18,19,22–24. The shape of the squamosal, The dermal bones of the cheeks and snout appear to have been which resembles that of the rhizodont Screbinodus17,18, suggests that

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a d Scapular process Contact surface for cleiththrum do.hy Free area (not in contact with exoskeleton)

gle

1 cm Coracoid plate ac.gle

bc 1 cm Attachment area for dorsal (extensor) muscles of fin gle at.v scap cla.sp ac.gle ef Cleithrum

1 cm

Coracoid plate cla.sp

Clavicle scap Attachment area for ventral (flexor) muscles of fin scap

gle Glenoid buttress 1 cm gle ac.gle

Fig. 2 | Pectoral girdle and neck joint of Hongyu chowi gen. et sp. nov. a–c, Photographs of the left scapulocoracoid (holotype) in lateral (a), medial (b) and posterior (c) views. d, Close-up of the type specimen showing the neck joint. e,f, Reconstruction of the pectoral girdle in lateral (e) and medial (f) views. do.hy, distal opening of the hyomandibular canal; for other abbreviations, see Fig. 1. the jugal and quadratojugal were in contact. Comparison with the tetrapods27,33, while an occipital articulation with a modified atlas proportions of the complete rhizodont Gooloogongia22 suggests a vertebra is shared with post-Devonian tetrapods10 and convergently total body length for Hongyu of about 1.5 m, to be compared with with the derived tristichopterid Mandageria34. about 1 m for Gooloogongia and perhaps 7 m for Rhizodus, the larg- est known rhizodont18. Cladistic analysis. A maximum parsimony analysis of 169 mor- Other characters are unknown in rhizodonts and suggest a dis- phological characters scored for 33 tetrapodomorphs, including tinctive lifestyle. The lower jaw is robust, but extremely shallow Hongyu and 5 outgroup taxa (see Supplementary Information posteriorly, with a large rectangular retroarticular process; its ven- and Supplementary Figs. 4 and 5), yielded 74 trees of 330 steps, tral face carries thin unornamented infradentary bones without a with a reasonably well-resolved strict consensus topology (Fig. 5a) lateral line canal (Fig. 1c,d). Unlike rhizodonts29, the hyomandibula that resembles the topology of Ahlberg and Johanson2 and subse- ends distally at the opercular process and thus lacks a distal ramus quent analyses3–9, apart from one thing: the elpistostegid–tetrapod altogether (Figs. 1c and 3a). The anteriormost vertebral centrum clade, which previously occupied a position next to the tristichop- (at.v, Figs. 1c and 3b) articulates dorsally with the occiput by a pair terid clade, has moved down to become the sister group of the of processes. Most unusually, the cleithrum lacks a ventral lamina, rhizodonts (Fig. 5d,e). Hongyu forms an unresolved trichotomy leaving the large plate-like scapulocoracoid exposed in lateral view with rhizodonts and elpistostegids–tetrapods. This topology (Figs. 2a–c,e,f and 3a). We tentatively interpret these characters as implies that the elpistostegid-like characters of Hongyu, as well adaptations for a benthic lifestyle (Fig. 4), possibly involving rapid as the frequently noted resemblances between rhizodonts and mouth opening aided by dorsal rotation of the skull, as proposed elpistostegids and tetrapods21,24,27, are synapomorphies. However, for the derived temnospondyl Gerrothorax30, which has a similar at 331 steps we recover 312 trees that resemble the maximum lower jaw morphology and a well-developed occipital articula- clade credibility tree from the Bayesian inference analysis (Fig. 5c) tion. The scapulocoracoid lies flush against the medial surface of and place the elpistostegid–tetrapod clade in its conventional the cleithrum as in rhizodonts24, elpistostegids and tetrapods27. This position and Hongyu as the sister group of rhizodonts (Fig. 5b is in striking constrast to the scapulocoracoid in dipnomorphs28,31 and Supplementary Figs. 6–8), which implies that all these and osteolepiforms32, in which the scapulocoracoid is triradiate in characters are homoplasies35. We compare the unconstrained and shape with supraglenoid and supracoracoid foramina. The distally contrained maximum parsimonius trees using the Templeton’s shortened hyomandibula, large plate-like scapulocoracoid, glenoid nonparametric test36. With only one step difference, the present facet with a distinct anterior cam, and cleithrum without a ven- dataset cannot reject statistically either of the two tree topologies tral lamina are derived characters shared with elpistostegids and (Templeton test P >​ 0.85).

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a Opercular facet of hyomandibula Neural spine Trigeminal notch Articulation between exoccipital and atlas vertebra

Ascending process of Pq

Premaxillary Pq

cbr 1–5 Cleithrum

Clavicle Glenoid buttress scap gle Exposed area of endopterygoid Gular plate Retroarticular process ac.gle ‘Pre-glenoid buttress’ of articular b Premaxillary

It Pq Pa

Hyomandibula Quadrate po St Glenoid fossa Articular Et mpl Pp Dentary ppl Ta ebr 1 Canal (nerve?) cbr 1 Muscle scar cbr 2 ebr 2 chy cbr 3 phbr

cbr 5 eo cbr 4 Clavicle at.v scap

Cleithrum

Centrum

n. arch

Fig. 3 | Interpretive skeletal reconstruction of Hongyu chowi gen. et sp. nov. a, Lateral view. b, Dorsal view. eo, exoccipital; mpl, middle pit-line; ppl, posterior pit-line; for other abbreviations, see Fig. 1.

Parallelism in stem tetrapod evolution. We conclude that the phy- range of tetrapodomorph fishes by showing, to our knowledge, logenetic importance of Hongyu cannot be fully resolved at present. the first example of a Gerrothorax-like morphology that probably It could be either a rhizodont convergent on elpistostegids and tet- reflects a benthic ‘fish trap’ lifestyle (Fig. 4). rapods or evidence that rhizodonts are closely related to elpistoste- It is remarkable that the first reasonably complete Devonian gids and tetrapods. In either case, the overall result is an increase in tetrapodomorph fish from the North China Block should be so homoplasy in the tetrapod stem group, because under the second morphologically specialized. Other tetrapodomorphs and lung- hypothesis the well-documented similarities between elpistostegids fishes from the Zhongning Formation that are currently under and tristichopterids become convergent. Hongyu therefore gives fur- study show equally unexpected characteristics, raising the possi- ther support to the hypothesis of multiple convergences towards an bility that biogeographical diversity in Devonian sarcopterygians elpstostegid-like morphology within the tetrapod stem group2,34. At has been underestimated. Together with the recent discovery of the same time it expands the known morphological and ecological large tetrapod footprints in the early Middle Devonian period of

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Fig. 4 | Life restoration. Hongyu chowi gen. et sp. nov. and associated antiarchs (Ningxialepis spinosa) from the Zhongning Formation (Famennian, Late Devonian period), Ningxia, China. Credit: B. Choo, Adelaide.

Poland37, and diversified sarcopterygian assemblages from the late we conducted additional analyses using the same algorithm (Supplementary Silurian period of South China15,38–40, these findings suggest that Figs. 6–8). early sarcopterygian evolution may have been an earlier, more MacClade v.4.044 was used to trace the character transformation in the regionally complex, and more homoplastic phenomenon than selected cladogram, based on one of the 74 most parsimonious trees 35 (Supplementary Fig. 5). Bremer decay indices (Supplementary Fig. 4a) were previously thought . obtained using the heuristic search algorithm in TNT45. The original dataset was also subjected to Bayesian inference analysis (Fig. 5c) using MrBayes v3.2.646,47. Diabolepis was set as the outgroup, and Methods priors were kept at their default settings for standard (morphological) analyses. Phylogenetic analysis. To explore the phylogenetic position of The analysis was run for 1 × 10​ 7 generations. Samples were taken every 1 × 10​ 2 Hongyu (Fig. 5 and Supplementary Figs. 4–8) and the impact of its generations, resulting in a total of 1 × 10​ 5 samples for each of the parallel characters on the phylogeny of stem tetrapods, we conducted phylogenetic analyses. The first 2.5 × 10​ 4 samples for each run, representing the ‘burn-in’ analysis using a dataset with 169 morphological characters and 38 taxa. 41 period, were discarded. The 50% majority-rule consensus tree was computed Te character data entry and formatting was performed in Mesquite (v.2.5) . for the sampled generations. Te dipnomorph taxa Youngolepis, Diabloepis, Powichthys, Porolepis Differences in tree topologies were compared between the unconstrained and Glyptolepis were designated as the outgroup. All characters, except and constrained most parsimonious trees (Supplementary Table 1) using the four (ch. 10, ch. 20, ch.63, and ch. 130), were treated as unordered and Templeton test36,48 implemented in PAUP* (v.4.0b10)42. weighted equally. The dataset was subjected to the parsimony analysis in PAUP* (v.4.0b10)42 following the algorithm used that was used previously43 (Supplementary Figs. 4, 5). Data availability. The specimen on which this study is based is housed in the Heuristic searches were initially run for 25 random sequence additions to collections of the Institute Vertebrate Paleontology and Paleoanthropology estimate the length of the shortest tree (TS). The value TS +​ 1 was then used (IVPP), Chinese Academy of Sciences. Taxonomic data have been deposited in as the ‘chuckscore’ (the treescore at and above which a fixed number of trees ZooBank (http://zoobank.org/) under the following LSIDs: urn:lsid:zoobank. were kept). A more comprehensive heuristic search was then run using 100,000 org:pub:D80955F3-7C21-457C-BA68-9C70F466E913 (article); urn:lsid:zoobank. random sequence additions, keeping 500 trees greater than or equal to the org:act:F7EDD4EB-6700-4583-8569-9BAC89B3A945 (genus); and chuckscore (CHUCKSCORE =​ TS +​ 1, NCHUCK =​ 500) for each random urn:lsid:zoobank.org:act:6ACCB5D2-E0D7-4BFD-85D6-9C8250515614 addition replicate42. (species). The Nexus format files for the maximum parsimony analysis and the In order to detect the respective impact of including Hongyu, Bayesian inference analysis are available on DRYAD; files are temporarily hosted and of constraining a tristichopterid–elpistostegid–tetrapod relationship, at: http://dx.doi.org/10.5061/dryad.m5p42.

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a b c Youngolepis Tungsenia Diabolepis Kenichthys Powichthys Gooloogongia Sauripterus Porolepis 1.0 0.91 0.95 Barameda Glyptolepis 0.61 Screbinodus Tungsenia 0.90 0.97 0.70 Rhizodus 0.83 Kenichthys Strepsodus Rhizodontida Hongyu Strepsodus Gyroptychius Rhizodus 0.99 Osteolepis Screbinodus Gogonasus Barameda Medoevia Sauripterus 0.60 Cladarosymblema Rhizodontida Gooloogongia Ectosteorhachis 1.0 Megalichthys Hongyu Beelarongia Medoevia 0.79 Canowindra Osteolepis 0.60 Koharalepis Gogonasus 69 Marsdenichthys Cladarosymblema 54 Spodichthys Tristichopterus Ectosteorhachis 0.59 Eusthenopteron Megalichthys 0.67 0.60 Jarvikina 0.84 Beelarongia 0.97 Platycephalichthys 0.89 Canowindra 0.66 Mandageria 0.99 Koharalepis 0.98 Eusthenodon Tristichopteridae Cabonnichthys Gyroptychius Diabolepis Panderichthys Marsdenichthys Elpistostege Elpistostegalidae Youngolepis 1.0 Spodichthys 1.0 Tiktaalik 77 0.71 Powichthys Acanthostega Tristichopterus 69 Porolepis 0.93 1.0 1.0 Ichthyostega Eusthenopteron 1.0 Glyptolepis Jarvikina 77 ‘Osteolepiformes’ 85 Cabonnichthys de 92 Platycephalichthys Osteolepiformes Mandageria Eusthenodon Strepsodus Rhizodus Megalichthyidae Tristichopteridae Elpistostegalidae Canowindridae Dipnomorph a Rhizodontida Gyroptychius Tetrapoda Kenichthys Gogonasus Osteolepis Screbinodus Medoevia Barameda Sauripterus Elpistostegalidae Tristichopteridae Megalichthyidae Canowindridae Dipnomorph a Rhizodontida Gyroptychius Tetrapoda Kenichthys Gogonasus Tungsenia Osteolepis Medoevia Hongyu

Gooloogongia Rhizodontida Hongyu Panderichthys Elpistostege Tiktaalik Acanthostega Ichthyostega

Fig. 5 | Phylogenetic position of Hongyu chowi gen. et sp. nov. a, Strict consensus of 74 trees at 330 steps. b, The 50% majority-rule consensus of 312 trees at 331 steps that show elpistostegids and tetrapods in their conventional position near tristichopterids. Numbers at the nodes indicate percentage of trees containing that node. Nodes without numbers were recovered in all trees. c, Maximum clade credibility tree from the Bayesian analysis. Values associated with the nodes indicate the frequency with which those bipartitions occur among sampled trees. d,e, Comparison of the strict consensus trees presented here (d) and in ref. 2 (e). In e, the shift of the elpistostegid–tetrapod clade from the recovered position to the position sister to the Rhizodontida will yield the tree typology resembling the one presented in d.

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