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A Devonian Tetrapod-Like Fish Reveals Substantial Parallelism in Stem Tetrapod Evolution

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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] 1470 NatURE ECOLOGY & EVOLUTION | VOL 1 | OCTOBER 2017 | 1470–1476 | www.nature.com/natecolevol © 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. © 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. NATURE ECOLOGY & EVOLUTION ARTICLES 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 NatURE ECOLOGY & EVOLUTION | VOL 1 | OCTOBER 2017 | 1470–1476 | www.nature.com/natecolevol
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