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TETRAPOD EVOLUTION
A tetrapod fauna from within theDevonian Antarctic CircleRobert Gess1* and Per Erik Ahlberg2
Until now, all known fossils of tetrapods (limbed vertebrates with digits) and near-tetrapods(such as Elpistostege, Tiktaalik, and Panderichthys) from the Devonian period have come fromlocalities in tropical to subtropical paleolatitudes. Most are from Laurussia, a continentincorporatingEurope,Greenland, andNorthAmerica,with onlyonebody fossil andone footprintlocality from Australia representing the southern supercontinent Gondwana. Here wedescribe 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 andsuggest that they may have been global in distribution.
The fossil locality at Waterloo Farm, nearGrahamstown, South Africa (Fig. 1A), fea-tures an exceptionally preserved biota, in-cluding 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 andelpistostegid localities lie within about 30° ofthe palaeoequator (5). TheWaterloo Farm fossilsare metamorphosed and strongly flattened, withthe bone tissue replaced by secondary meta-morphic mica, partially altered to chlorite. Twotetrapods—Tutusius umlambo gen. et sp. nov.and Umzantsia amazana gen. et sp. nov., bothrepresented by disarticulated material (Figs. 2and 3 and figs. S1 and S2)—are present in the as-semblage and are described here (formal taxo-nomic descriptions are in the supplementarymaterials). Tutusius is represented by a single
cleithrum (Fig. 2, A and B) with a broad, flat, un-ornamented blade, resembling that of the earlyFamennian Russian genus Jakubsonia morethan the slender cleithra of the late FamennianIchthyostega and Ventastega (6–8) (Fig. 4).Dermal bones ofUmzantsia carry a distinctive
ornament consisting of fine parallel ridges rem-iniscent of water ripples. This allows identi-fication of a number of cranial bones and acleithrum from one bedding plane as probablyderived from a single individual, designated theholotype (Fig. 2, C to P). A lower jaw ramus fromanother bedding plane (Fig. 3) is also assigned toUmzantsia. Scaling the bones of the Umzantsiaholotype to the skull reconstruction of Ventastega(8) suggests a head length of ~13 cm. The lowerjaw is 17.9 cm long. The dermal ornament alsocovers much of the cleithrum of Umzantsia; thisfishlike characteristic contrasts with the unorna-
mented cleithra of other Devonian tetrapods,suggesting a phylogenetic position between thosetetrapods and Tiktaalik (9) (Fig. 4).The largest skull bone is a jugal (Fig. 2, E to
G), identifiable from the presence of an orbitalmargin and characteristic set of sutural margins(5, 7, 8). The orbital margin is short [suggesting atriangular orbit with a ventral apex, similar inshape to that of Anthracosaurus (10), unlessthe eye was extremely small], the lacrimal isexcluded from the orbital margin by a jugal-prefrontal contact, there is no distinct dorsalpostorbital process, and the notch for the qua-dratojugal is deep. The preopercular (Fig. 2, Hand I) is similar to that of Ventastega, with arounded posteriormargin that projects as a shortprocess beyond the quadratojugal contact. Thefrontal resembles those of previously describedDevonian tetrapods. A probable supratemporalis 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 leftlower jaw ramus has five infradentaries, insteadof the normal four. Thismay be an autapomorphyof Umzantsia, but the associated infradentariesfrom the right ramus appear proportionatelylonger, raising the possibility that there wereonly four infradentaries on the right side andthat this individual was asymmetrical. Theinfradentaries carry the typical tetrapod “star-burst” ornament, grading dorsally into a ripple-like ornament. A series of short tooth-bearing
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1Albany Museum and Geology Department, RhodesUniversity, Grahamstown, South Africa. 2Department ofOrganismal Biology, Uppsala University, Uppsala,Sweden.*Corresponding author. Email: [email protected]
Fig. 1. Maps of the fossil locality. (A) Map of South Africa showing theWaterloo Farm fossil locality (black asterisk). (B) South-polar projection ofGondwana, modified from (20), showing Waterloo Farm (black asterisk) inrelation to the reconstructed position of the South Pole 360million 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.Thelandmass with a dashed outline below Waterloo Farm is an emergent part ofthe Falklands Plateau, forming the outer margin of the semi-enclosed AgulhasSea (24). Brown denotes land; pale blue, shallow shelf; blue, deep shelf.
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ossifications appears to represent the coronoidseries (Fig. 3C), implying that, of the threecoronoids normally seen in tetrapods, at leastthe posterior one has been replaced by a chainof smaller elements in this taxon. An isolatedelement of this kind is also associated with theholotype (Fig. 2, N to P). The lateral line canals
of the skull and lower jaw appear as a combina-tion of continuous and discontinuous grooves,similar to the condition in other Devoniantetrapods (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 agradual transition from greenhouse to icehouseconditions, punctuated by an end-Famennianglaciation (11). Exact timing of this glaciationrelative to Waterloo Farm deposition is uncertain,but late Famennian diamictites in South Africaare probably glaciogenic, and carbonates are
Gess et al., Science 360, 1120–1124 (2018) 8 June 2018 2 of 5
Fig. 2. Material of Tutusius and Umzantsia. (A and B) Photograph andline drawing of AM7527, a left cleithrum, the holotype and only knownspecimen of Tutusius umlambo. (C to P) AM7528a to -f, the bones ofthe holotype of Umzantsia amazana, believed to represent one individual.(C and D) AM7528a, right cleithrum (line drawing incorporates informationfrom 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 chainof two partial infradentaries, one near-complete infradentary, a probablepremaxilla, and an unidentified tooth-bearing ossicle (see also Fig. 3). In alldrawings, thick outlines denote true margins, and thin outlines denotebroken or covered margins. In (D), gray shading indicates the dermalornament. Anterior is to the left in (A), (B), (E) to (G), (J), and (K) and tothe right in (C), (D), (H), and (I). All scale bars, 10 mm. (C) to (P) areshown to the same scale.
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entirely absent from the region (11). Thus, eventhough Waterloo Farm yields a rich terrestrialflora that rules out a truly polar climate (12), itcannot have been very warm, and proximity tothe pole implies several months of completewinter 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, asdrivers of innovation or as refuges for archaictaxa. The combination of autapomorphic andprimitive characters in Umzantsia has bearingon this problem. All Devonian tetrapod cleithradescribed to date (6–8, 13–15), including frag-mentary late Frasnianmaterial associated withElginerpeton (16), lack dermal ornament (Fig. 4).This suggests that Umzantsia represents a deep
but specialized branch of the tetrapod lineage thathad 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 Polandand Ireland (17–19) challenge the popular scenarioof a tropical origin of tetrapods during the LateDevonian (5). Tetrapods originated no later thanthe Eifelian (early Middle Devonian), when they
Gess et al., Science 360, 1120–1124 (2018) 8 June 2018 3 of 5
Fig. 3. The lower jaw of Umzantsia. (A to C) AM7529, left mandibularramus and infradentaries of the right mandibular ramus of Umzantsiaamazana. (A) Photograph of the specimen. The splenial of the leftramus partly overlies an infradentary of the right ramus; the area withinthe white box is shown on the left with the splenial in place and onthe right as an excerpt box with the splenial removed. (B) Photograph
overlaid with interpretative line drawing. (C) Interpretative linedrawing. Light gray shading indicates infradentaries of the rightmandibular 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 lateFamennian (latest Devonian), they ranged from thetropics to the south polar regions. This geograph-ic pattern could still point to a tropical originbut may simply be a sampling artifact. Againstthis background, the continued investigation ofnontropical localities such as Waterloo Farm mustbe a priority. Waterloo Farm is also the onlyknown Devonian tetrapod locality to featuresoft-tissue preservation, as exemplified by theearliest known lamprey, Priscomyzon (1). Thelocality thus has the potential not only to castnew light on early tetrapod biogeography andevolution, but also to illuminate unknown aspectsof their morphology.
REFERENCES AND NOTES
1. R. W. Gess, M. I. Coates, B. S. Rubidge, Nature 443, 981–984(2006).
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Fig. 4. Comparison of cleithra. A series of cleithra from the tetrapodstem group, spanning the fin-to-limb transition, placed on a simplifiedphylogeny that reflects recent analyses (8, 9), illustrating the morphologicaltransformation of the shoulder girdle and the tentative phylogeneticpositions of Tutusius and Umzantsia. Not to scale. For each taxon, theupper image shows the cleithrum in external view, and the lower imageshows it in internal view. Anterior is to the left in all cases. Only forEusthenopteron (25) is the entire scapulocoracoid shown; in other taxa,the projecting ventral part has been cut off. For comparison, a completescapulocoracoid plus cleithrum of Ichthyostega is shown (bottom right).
The arrowhead branch of the phylogeny leads to the tetrapod crowngroup. Small gray arrows indicate the posteroventral buttress of thecleithrum. Character states at nodes: 1, the scapulocoracoid is small andconcealed by the cleithrum in lateral view, and the cleithrum has abroad ventral lamina and is entirely covered with ornament (primitivecondition, widely shared among Osteichthyes); 2, the cleithrum tapersto a point anteroventrally and attaches along the anterodorsal margin ofthe scapulocoracoid; 3, the dorsal end of the scapulocoracoid forms av-shaped peak, and the cleithrum carries a posterodorsal buttress;4, the cleithrum lacks ornament.
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21. T. H. Torsvik, L. R. M. Cocks, “The Palaeozoic palaeogeographyof central Gondwana,” in The Formation and Evolutionof Africa: A Synopsis of 3.8 Ga of Earth History, D. J. J. VanHinsbergen, S. J. H. Buiter, T. H. Torsvik, C. Gaina,S. J. Webb, Eds. (Special Publication 357, Geological Societyof London, 2011), pp. 137–166.
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23. K. S. W. Campbell, M. W. Bell, Alcheringa 1, 369–381 (1977).24. T. McCarthy, B. S. Rubidge, The Story of Earth & Life: A
Southern African Perspective on a 4.6-Billion-Year Journey(Struik Publishers, 2005).
25. E. Jarvik, Basic Structure and Evolution of Vertebrates(Academic Press, 1980), vol. 1.
ACKNOWLEDGMENTS
The South African National Roads Agency Limited supportedrescue of shale during roadworks. R.G. acknowledges useful earlydiscussions with M. Coates and P. Janvier regarding themorphology and confirming the identity of AM7527. B. Nosilela(Department of African Languages, Rhodes University) advised ontaxonomic names. Funding: R.G. acknowledges funding from theSouth African Millennium Trust and the South African DST-NRFCentre of Excellence in Palaeosciences (CoE-Pal). P.E.A. acknowledgesa Wallenberg Scholarship from the Knut and Alice WallenbergFoundation. Author contributions: Fieldwork, collection andpreparation of material, initial identification of tetrapod specimens(cleithra), and project conceptualization and design, R.G.; identificationof 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 thesupplementary materials. Specimens are accessioned at the AlbanyMuseum, Grahamstown, South Africa, as AM7511 to AM7513.
SUPPLEMENTARY MATERIALS
www.sciencemag.org/content/360/6393/1120/suppl/DC1Materials and MethodsSystematic PaleontologyFigs. S1 and S2Reference (26)
9 October 2017; accepted 25 April 201810.1126/science.aaq1645
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A tetrapod fauna from within the Devonian Antarctic CircleRobert Gess and Per Erik Ahlberg
DOI: 10.1126/science.aaq1645 (6393), 1120-1124.360Science
, this issue p. 1120Sciencewhich 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 Devoniancreatures 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-likeOut of Antarctica
ARTICLE TOOLS http://science.sciencemag.org/content/360/6393/1120
MATERIALSSUPPLEMENTARY http://science.sciencemag.org/content/suppl/2018/06/06/360.6393.1120.DC1
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