A tetrapod fauna from within the Devonian Antarctic Circle

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TETRAPOD EVOLUTION

A tetrapod fauna from within the Devonian Antarctic Circle

Robert Gess¹*and Per Erik Ahlberg²

Until now, all known fossils of tetrapods (limbed vertebrates with digits) and near-tetrapods (such asElpistostege,Tiktaalik, andPanderichthys) from the Devonian period have come from localities in tropical to subtropical paleolatitudes. Most are from Laurussia, a continent incorporating Europe, Greenland, and North America, with only one body fossil and one footprint locality from Australia representing the southern supercontinent Gondwana. Here we describe two previously unknown tetrapods from the Late Devonian (late Famennian) Gondwana locality of Waterloo Farm in South Africa, then located within the Antarctic Circle, which demonstrate that Devonian tetrapods were not restricted to warm environments and suggest that they may have been global in distribution.

T

he fossil locality at Waterloo Farm, near Grahamstown, South Africa (Fig. 1A), fea- tures an exceptionally preserved biota, including examples of soft-tissue preservation (1–4), deposited in the south polar region close to paleolatitude 70°S (Fig. 1B). In contrast, all previously known Devonian tetrapod and elpistostegid localities lie within about 30° of the palaeoequator (5). The Waterloo Farm fossils are metamorphosed and strongly flattened, with the bone tissue replaced by secondary meta- morphic mica, partially altered to chlorite. Two tetrapods—Tutusius umlambogen. et sp. nov.

andUmzantsia amazanagen. et sp. nov., both represented by disarticulated material (Figs. 2 and 3 and figs. S1 and S2)—are present in the assemblage and are described here (formal taxonomic descriptions are in the supplementary materials).Tutusiusis represented by a single

cleithrum (Fig. 2, A and B) with a broad, flat, un- ornamented blade, resembling that of the early Famennian Russian genusJakubsoniamore than the slender cleithra of the late Famennian IchthyostegaandVentastega(6–8) (Fig. 4).

Dermal bones ofUmzantsiacarry a distinctive ornament consisting of fine parallel ridges rem- iniscent of water ripples. This allows identification of a number of cranial bones and a cleithrum from one bedding plane as probably derived from a single individual, designated the holotype (Fig. 2, C to P). A lower jaw ramus from another bedding plane (Fig. 3) is also assigned to Umzantsia. Scaling the bones of theUmzantsia holotype to the skull reconstruction ofVentastega (8) suggests a head length of ~13 cm. The lower jaw is 17.9 cm long. The dermal ornament also covers much of the cleithrum ofUmzantsia; this fishlike characteristic contrasts with the unorna-

mented cleithra of other Devonian tetrapods, suggesting a phylogenetic position between those tetrapods andTiktaalik(9) (Fig. 4).

The largest skull bone is a jugal (Fig. 2, E to G), identifiable from the presence of an orbital margin and characteristic set of sutural margins (5,7,8). The orbital margin is short [suggesting a triangular orbit with a ventral apex, similar in shape to that ofAnthracosaurus(10), unless the eye was extremely small], the lacrimal is excluded from the orbital margin by a jugal- prefrontal contact, there is no distinct dorsal postorbital process, and the notch for the quadratojugal is deep. The preopercular (Fig. 2, H and I) is similar to that ofVentastega, with a rounded posterior margin that projects as a short process beyond the quadratojugal contact. The frontal resembles those of previously described Devonian tetrapods. A probable supratemporal is the only recovered skull table element.

The lower jaw is slender and gently curved.

The splenial is the longest of the infradentaries, occupying about half the jaw length. The left lower jaw ramus has five infradentaries, instead of the normal four. This may be an autapomorphy ofUmzantsia, but the associated infradentaries from the right ramus appear proportionately longer, raising the possibility that there were only four infradentaries on the right side and that this individual was asymmetrical. The infradentaries carry the typical tetrapod“star- burst”ornament, grading dorsally into a ripple- like ornament. A series of short tooth-bearing

1Albany Museum and Geology Department, Rhodes University, Grahamstown, South Africa.²Department of Organismal Biology, Uppsala University, Uppsala, Sweden.

*Corresponding author. Email: [email protected]

Fig. 1. Maps of the fossil locality.(A) Map of South Africa showing the Waterloo Farm fossil locality (black asterisk). (B) South-polar projection of Gondwana, modified from (20), showing Waterloo Farm (black asterisk) in relation to the reconstructed position of the South Pole 360 million years ago (21). Blue asterisks indicate the other two known Devonian tetrapod

localities in Gondwana—Genoa River [left; footprints (22)] and Jemalong [right;Metaxygnathus,a single lower jaw ramus (23)]—both in Australia. The landmass with a dashed outline below Waterloo Farm is an emergent part of the Falklands Plateau, forming the outer margin of the semi-enclosed Agulhas Sea (24). Brown denotes land; pale blue, shallow shelf; blue, deep shelf.

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ossifications appears to represent the coronoid series (Fig. 3C), implying that, of the three coronoids normally seen in tetrapods, at least the posterior one has been replaced by a chain of smaller elements in this taxon. An isolated element of this kind is also associated with the holotype (Fig. 2, N to P). The lateral line canals

of the skull and lower jaw appear as a combination of continuous and discontinuous grooves, similar to the condition in other Devonian tetrapods (5,8), though poorly preserved.

Waterloo Farm demonstrates that the early evolution of tetrapods did not play out exclu- sively in tropical and subtropical environments.

The late Famennian to Tournaisian witnessed a gradual transition from greenhouse to icehouse conditions, punctuated by an end-Famennian glaciation (11). Exact timing of this glaciation relative to Waterloo Farm deposition is uncertain, but late Famennian diamictites in South Africa are probably glaciogenic, and carbonates are

Fig. 2. Material ofTutusiusandUmzantsia.(AandB) Photograph and line drawing of AM7527, a left cleithrum, the holotype and only known specimen ofTutusius umlambo. (CtoP) AM7528a to -f, the bones of the holotype ofUmzantsia amazana, believed to represent one individual.

(C and D) AM7528a, right cleithrum (line drawing incorporates information from the counterpart); (E to G) AM7528b, left jugal, showing part, counterpart, and line drawing; (H and I) AM7528c, right preopercular;

(J and K) AM7528d, incomplete left frontal; (L and M) probable left

supratemporal; (N to P) AM7528e, a bone assemblage comprising a chain of two partial infradentaries, one near-complete infradentary, a probable premaxilla, and an unidentified tooth-bearing ossicle (see also Fig. 3). In all drawings, thick outlines denote true margins, and thin outlines denote broken or covered margins. In (D), gray shading indicates the dermal ornament. Anterior is to the left in (A), (B), (E) to (G), (J), and (K) and to the right in (C), (D), (H), and (I). All scale bars, 10 mm. (C) to (P) are shown to the same scale.

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entirely absent from the region (11). Thus, even though Waterloo Farm yields a rich terrestrial flora that rules out a truly polar climate (12), it cannot have been very warm, and proximity to the pole implies several months of complete winter darkness.

The presence of tetrapods in such an environ- ment raises the question of whether high- latitude environments played a distinctive role in

the fish-tetrapod transition—for example, as drivers of innovation or as refuges for archaic taxa. The combination of autapomorphic and primitive characters inUmzantsiahas bearing on this problem. All Devonian tetrapod cleithra described to date (6–8,13–15), including frag- mentary late Frasnian material associated with Elginerpeton(16), lack dermal ornament (Fig. 4).

This suggests thatUmzantsiarepresents a deep

but specialized branch of the tetrapod lineage that had been in existence since at least the Frasnian, a time interval of some 12 million years.

The Waterloo Farm tetrapod fossils and the Middle Devonian tetrapod trackways from Poland and Ireland (17–19) challenge the popular scenario of a tropical origin of tetrapods during the Late Devonian (5). Tetrapods originated no later than the Eifelian (early Middle Devonian), when they Fig. 3. The lower jaw ofUmzantsia.(AtoC) AM7529, left mandibular

ramus and infradentaries of the right mandibular ramus ofUmzantsia amazana. (A) Photograph of the specimen. The splenial of the left ramus partly overlies an infradentary of the right ramus; the area within the white box is shown on the left with the splenial in place and on the right as an excerpt box with the splenial removed. (B) Photograph

overlaid with interpretative line drawing. (C) Interpretative line drawing. Light gray shading indicates infradentaries of the right mandibular ramus; dark gray, the sensory canals on these bones.

Fine parallel gray lines on the left jaw ramus represent dermal ornament.

(D) Sketch reconstruction of the left mandibular ramus (AM7529).

Scale bars, 10 mm.

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were present in southern Laurussia; by the late Famennian (latest Devonian), they ranged from the tropics to the south polar regions. This geograph- ic pattern could still point to a tropical origin but may simply be a sampling artifact. Against this background, the continued investigation of nontropical localities such as Waterloo Farm must be a priority. Waterloo Farm is also the only known Devonian tetrapod locality to feature soft-tissue preservation, as exemplified by the earliest known lamprey,Priscomyzon (1). The locality thus has the potential not only to cast new light on early tetrapod biogeography and evolution, but also to illuminate unknown aspects of their morphology.

R E F E R E N C ES A ND NOT ES

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Fig. 4. Comparison of cleithra.A series of cleithra from the tetrapod stem group, spanning the fin-to-limb transition, placed on a simplified phylogeny that reflects recent analyses (8,9), illustrating the morphological transformation of the shoulder girdle and the tentative phylogenetic positions ofTutusiusandUmzantsia. Not to scale. For each taxon, the upper image shows the cleithrum in external view, and the lower image shows it in internal view. Anterior is to the left in all cases. Only for Eusthenopteron(25) is the entire scapulocoracoid shown; in other taxa, the projecting ventral part has been cut off. For comparison, a complete scapulocoracoid plus cleithrum ofIchthyostegais shown (bottom right).

The arrowhead branch of the phylogeny leads to the tetrapod crown group. Small gray arrows indicate the posteroventral buttress of the cleithrum. Character states at nodes: 1, the scapulocoracoid is small and concealed by the cleithrum in lateral view, and the cleithrum has a broad ventral lamina and is entirely covered with ornament (primitive condition, widely shared among Osteichthyes); 2, the cleithrum tapers to a point anteroventrally and attaches along the anterodorsal margin of the scapulocoracoid; 3, the dorsal end of the scapulocoracoid forms a v-shaped peak, and the cleithrum carries a posterodorsal buttress;

4, the cleithrum lacks ornament.

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AC K N OW L E D GM E N TS

The South African National Roads Agency Limited supported rescue of shale during roadworks. R.G. acknowledges useful early discussions with M. Coates and P. Janvier regarding the morphology and confirming the identity of AM7527. B. Nosilela (Department of African Languages, Rhodes University) advised on taxonomic names.Funding:R.G. acknowledges funding from the South African Millennium Trust and the South African DST-NRF Centre of Excellence in Palaeosciences (CoE-Pal). P.E.A. acknowledges a Wallenberg Scholarship from the Knut and Alice Wallenberg Foundation.Author contributions: Fieldwork, collection and preparation of material, initial identification of tetrapod specimens (cleithra), and project conceptualization and design, R.G.; identification of additional specimens, R.G. and P.E.A.; manuscript writing and

illustrations, P.E.A. and R.G.Competing interests:None declared.

Data and materials availability: Formal taxonomy is presented in the supplementary materials. Specimens are accessioned at the Albany Museum, Grahamstown, South Africa, as AM7511 to AM7513.

SUPPLEMENTARY MATERIALS

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9 October 2017; accepted 25 April 2018 10.1126/science.aaq1645

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A tetrapod fauna from within the Devonian Antarctic Circle

Robert Gess and Per Erik Ahlberg

DOI: 10.1126/science.aaq1645 (6393), 1120-1124.

360 Science

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which this important group was shaped.

Antarctica. Thus, the distribution of tetrapods may have been global, which encourages us to rethink the environments in group have been recovered from the tropics. Gess and Ahlberg now describe two fossil tetrapods from Devonian creatures emerging from the water into a wet tropical forest or swamp. Indeed, all previously described specimens of this

When we think of Devonian tetrapods, the ancestors of all modern vertebrates, we tend to picture amphibian-like Out of Antarctica

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