SUPPLEMENTARY INFORMATION (SI)

An early Cambrian agglutinated tubular lophophorate with

brachiopod characters Z.-F. Zhang1,2*, G.-X. Li2, L. E. Holmer3, G. A. Brock4, U. Balthasar5, C. B. Skovsted6, D-J. Fu1, X.-L. Zhang1, H.-Z. Wang3, A. Butler3, Z.-L. Zhang1, C.-Q. Cao2, J. Han1, J.-N. Liu1& D.-G. Shu1 1Early Life Institute, State Key Laboratory of Continental Dynamics and Department of

Geology, Northwest University, Xi’an, 710069, China.

2LPS, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences,

Nanjing, 210008, China.

3Uppsala University, Department of Earth Sciences, Palaeobiology, Villavägen 16, SE-752

36 Uppsala, Sweden.

4Department of Biological Sciences, Macquarie University, Sydney, New South Wales

2109, Australia.

5University of Glasgow, Department of Geographical and Earth Sciences, Gregory

Building, Lilybank Gardens, G12 8QQ, Glasgow, United Kingdom.

6Department of Palaeobiology, Swedish Museum of Natural History, Box 50007, SE-104

05 Stockholm, Sweden.

To whom correspondence should be addressed.

E-mail: elizf@nwu.edu.cnor zhangelle@126.com (Z.F.Z)

Taxonomic remarks on Yuganotheca. Yuganotheca is an abundant component in the Chengjiang fauna. It occurs in at least 10 localities in Chengjiang, Jinning, Anning counties and as well as in Haikou southwest of Kunming (Fig. S1), suggesting that Yuganotheca was a generalist adapted to a range of environmental settings in early Cambrian marine environments. Due to its typical occurrence as fragmented yellowish-brown arenaceous pieces, even in large clusters on single slabs (Fig. S2), Yuganotheca did not attract attention of Chengjiang research scientists1-4 until the specimens with pedicles were recovered5,6. Nevertheless, this bizarre animal has not formally been described up to this point. In earlier publications5-7, Y. elegans was informally referred to as “Wangyuia chengjiangensis Jin et al. 2004”, but the genus name was found to be preoccupied by a Silurian orthid8; “Wangyuia chengjiangensis” has never been formally established and therefore represents a nomen nudum.

Figure S1. a, map showing localities where Yuganotheca elegans gen. et sp. nov. has been collected. b, stratigraphic column showing the mud-rich deposits yielding the Chengjiang fauna including Y. elegans in the Jianshan section at Haikou, Kunming, China. The map image and stratigraphic column were created using CorelDraw 9.0 and converted to TIF format by Z. Zhang.

FigureS2. A gregarious occurrence of Yuganotheca elegans gen. et sp. nov. in a slab from Erjie Section in Anning around Kunming, China (also see Fig. S1). Comparison with fossil and recent lingulids

Yuganotheca elegans gen et sp. nov. resembles lingulid brachiopods in having a U-shaped digestive tract and a stalk-like pedicle with distinct annulations and central lumen9. However it differs markedly in possessing pinnate mantle canals in both valves, which is most unlike the vascular system in most lingulid-like taxa which is usually bifurcate or baculate. Moreover, Yuganotheca also lacks a typical lingulid pseudointerarea with characteristic pedicle groove and flexure lines. Yuganotheca also has a very unusual and distinctive helical disposition of the lophophore with thickened, widely spaced tentacles. The unique quadripartite tubular bauplan consists of a pair of soft (unmineralized) valves forming an enclosed lophophoral cavity, in addition to a flexible median collar and rigid conical tube terminated by a slender pedicle with central lumen used for anchorage to the substrate (Figs.1-2, S3-S5). Apart from the lowermost pedicle and the rigid conical tube, all other body parts are covered by relatively fine siliceous (mostly quartz) grains (Fig. S3), interpreted to have been biologically mediated as part of protective agglutination, a feature unknown in all other coeval Chengjiang brachiopods6,9.

Notes on preservation

In life, this animal was evidently a semi-infaunal sessile benthic filter

feeder attached in the sediment by the terminal bulb of the pedicle. The

annulated median collar appears to have been flexible and contractible,

presumably for orientating and reorienting the bivalved shell into prevailing

currents. The lower conical tube is considerably more rigid (possibly lightly

mineralized or chitinous) (Fig. S3e-h, S4) and probably functioned to elevate

the body of Yuganotheca above the muddy seafloor.

The median collar is preserved in various states of compaction, size and

appearance, from smooth with parallel lateral margins (Figs. 1, 2a, c, d) to

annulated with bent and buckled lateral margins, in most case showing a

similar preservation mode to the anterior valves (Figs.1, 2a, c, d). The size,

shape, extent of the pedicle and presence of a central lumen is generally

similar to other Chengjiang lingulids such as Lingulellotreta malongensis6,9-11.

The lower conical tube differs from all the other parts of Yuganotheca in terms

of rigidity and relief in that it retains its shape and morphology (Figs. S3f-h;

S4a-f). The anterior valves, median collar, and lower conical tube are usually

preserved on the same bedding plane whereas the pedicle commonly dips at a

low angle into underlying bedding laminae (Figs.1, 2a, c, d and Fig. S4a-f)

suggesting it was normally completely inserted into the soft substratum.

Figure S3. SEM micrographs of the early Cambrian agglutinated lophophorate Yuganotheca elegans gen. et sp. nov. from the early Cambrian Chengjiang Lagerstätte, southern China. a, entire individual, a composite of SEM micrographs. b, anterior margin of the upper “shell” valves. c-d, close-up view of the siliceous grains on the surface of valves. e, Detail of the median collar. f-h, SEM micrographs of the lower conical tube and pedicle; note the border between the lower cone and pedicle (marked by arrows). f, General view. g, Detail of (f). h, Close-up view of the proximal pedicle with annulations.

Figure S4. Compressed specimens of the agglutinated lophophorate Yuganotheca elegans gen. et sp. nov. from the early Cambrian Chengjiang Lagerstätte, southern China. Note the variable preservation of different elements; arrows indicate the border of different elements. a, ELI BLW-0066A, an internal mold with the upper valves in some relief; b, ELI BLW-0200, contracted median collar and oblique marginal growth of the lower conical tube with a sharply bent pedicle; c, ELI BLW-0119, a specimen probably close to life position; note the distorted upper valves, median collar, rigid lower conical tube and slender pedicle bending into the sediment. d, ELI BLW-0590A, close-up of the annulated median collar; e, ELI BLW-0069A, a dorso-laterally compressed specimen, showing the rigid lower conical tube and the connection point with the emerging pedicle; f, ELI BLW-0005B, a specimen with posteriorly compressed shell valves, showing the median collar as an extension of the posterior part of the ventral valve, box indicating position of Fig.1g; g, ELI BLW-0472A, close-up view of marginal setae in a strongly compressed specimen.

Figure S5.The agglutinated lophophorate Yuganotheca elegans gen. et sp.

nov. from the early Cambrian Chengjiang Lagerstätte, southern China. Scale

bars in mm; arrows indicate the boundary of different elements. a-d, ELI

BLW-0475B and 473A, photos and interpretive sketches drawn by Z. Zhang in

CorelDraw 9.0 showing the ventral mantle canals; e-f, NIPS IMG-0220a, photo

and interpretative drawing of well-preserved dorsal mantle canals; g, ELI

BLW-0092, a specimen with an antero-posteriorly crushed valves with

sediment intruded into the space between the valves, and with compressed

median collar; h, ELI BLW-0058A, a dorso-ventrally compressed mould

showing slightly displaced valves with some relief; note the borders of the

valves, median collar and lower conical tube. The sketch drawings were made

in CorelDraw 9.0 and converted to TIF format by Z. Zhang.

Figure S6. Comparison of the Lophophore organization of Yuganotheca elegans gen. et sp.nov. with those seen in other lingulids from the early Cambrian Chengjiang Lagerstätte, southern China. a-g, Y. elegans. a-b, Part and counterpart, ELI BLW-0580AB. c, interpretive drawing of b. d, ELI BLW-0537A, note the thick widely spaced tentacles. e-f, Lingulellotreta malongensis, showing spirally coiled lophophore arms fringed with thin and closely spaced tentacles from Chengjiang11. e, ELI L-0014A. f, ELI L-0033. g, ELI C-0031, showing the cilia-like tentacles of Lingulella chengjiangensis from the Chengjiang fauna12. h, L. chengjiangensis, ELI L-0413, flattened preserved spiral lophophore and posteriorly extended tube-like digestive tract far beyond the hinge line5,10. The sketch drawings were made in CorelDraw 9.0 and converted to TIF format by Z. Zhang.

Figure. S7. Cross section of the unmineralized valves of Yuganotheca elegans gen. et sp. nov. from the early Cambrian Chengjiang Lagerstätte, southern China. a-e, SEM photos of a cross section through two valves, showing that the siliceous grains are only associated with the outer layer of the two valves. a, a combined SEM micrograph. b, BSEM of A. c, close-up view of b. d, details of c. e, Enlargement of d, showing details of intruded sediments between valves. f, Detailed view of siliceous grains covering the surface of a valve.

Figure S8. Element maps of cross section of the two valves of Yuganotheca elegans gen. et sp. nov. from the early Cambrian Chengjiang Lagerstätte, China (compare to Fig.S6), showing the valve-related grains have major content of silicon (d) strikingly contrast to the surrounding and infilled muddy matrix, and small amount of Mg (b), O (c), Al (e) and Fe (h) as the result of the surrounding clay that hosts the animals. However, C (f) and Cu (g) have no profile of the section. (a) SEM micrograph of the section.

Figure S9. EDX element maps of the upper valves of Yuganotheca elegans gen. et sp. nov. from the Chengjiang fauna (taken by UB at Glasgow), showing higher concentration of silica and iron,but lower Al content on the valves, with big contrast in color to the surrounding muddy matrix.

Figure S10. Elemental EDS maps of a cross section through the proximal conical tube. a-e, maps of Al, Fe, K, Si, and O, respectively.f, light photograph of a complete individual (ELI BLW0711) before cutting, with the arrow indicating the position of elemental maps at the upper part of the median collar; g, SEM backscatter image of the mapped region; note the central cavity which probably represents the lumen of the now collapsed tube.

Phylogenetic analysis: To examine the phylogenetic position of Yuganotheca among brachiopods, phoronids and other Cambrian lophotrochozoan fossils (Eccentrotheca, Cotyledion, Micrina, Wiwaxia and Halkieria), we compiled a character matrix data set with 13 brachiopod taxa and total group phoronids and 25 characters (Appendix 2; Table S2). Most of the characters used were adopted from existing matrices 13,14, in addition to data on soft anatomy discovered from Chengjiang5-7,10,11,15-18.

Character 1: Body shape: 0 vermiform body 1 dorsoventrally flattened with ventral locomotory sole 2 vertical body with benthic and sessile life style Character 2: Shape and arrangement of sclerite on body 0 absent 1 presence of scale-like elements on whole body 2 sclerite scoalesced to cone or tube 3. conjoined shell valves Character 3: Shell or valves 0 absent 1 shell by shell glands, unopposed and separated, overlapped 2 opposed shell valves Character 4: Fully developed scleritome composed of multiple exoskeletal elements 0 absent 1 scleritome composed of spinous elements (sclerites, tubes spicules, spines), with or without shells, covering the entire dorsal surface Character 5: Shell (whole body wall) composition 0 soft organic composition 1 chitinous hardening 2 protected by agglutinatation 3 phosphatic 4 carbonaceous composition Character 6: Coelomic cavity in lophophore 0 one coelomic cavity 1 two

Character 7: Arrangement of lophophore tentacles 0 one row 1 double row in post-trocholophe 2 double row in trocholophe Character 8: Mantle enclosing isolated cavity 0 absent 1 present Character 9: Mantle canals directed peripherally and medially 0 no mantle canals 1 peripheral and medial 2 peripherally only Character 10: Gut disposition 0 straight gut with posterior anus 1 U-shaped with anteriorly placed anus 2 straight, blind Character 11: Dermal muscles 0 absent or weakly developed 1 strongly developed Character 12: Transmedian muscle 0 absent 1 present Character 13: Number of other oblique muscles 0 one pair 1 more than one pair Character 14: Diductor muscles 0 absent 1 oblique muscles acting as diductors 2 oblique muscles attached posteriorly to inner side of homeodeltidium Character 15: Outside lateral muscles attached anteriorly to body wall 0 absent 1 present Character 16: Distal attachment structure - Pedicle (stalk) 0 absent 1 present

Character 17: Attachment through apical perforation or colleplax 0 present 1 absent Character 18: Pedicle coelom 0 no pedicle 1 present of coelomic lumen 2 cartilage infillings Character 19: Pedicle (stalk) forming from posterior part of body wall 0 absent 1 present Character 20: Pedicle (stalk) as outgrowth of ventral mantle lobe 0 absent 1 present Character 21: Phosphatic mineralization 0 absent 1 present Character 22: Calcareous mineralization 0 absent 1 present Character 23: Body sheltered or protected with agglutinated tube 0 present 1 absent Character 24: Larval shell 0 absent 1 present Character 25: Pseudodeltidium and delthyrium 0 absent 1 present

0111111111122222 Phoronis 20002000011????010000000?

1234567891123456789012345

Yuganotheca 2221200111?????101111000? Lingula 232031211111000111101011? Lingulellotreta 232031211111000111101011? Siphonotreta 23203??11111000?0?101011? Acrotreta 23203??11?110001?1101011? Paterinida 232031?12?0??20?0???1011? Novocrania 23204111200010110?0101100 Craniopsida 23204??12000101???0101100 Obolellids 23204??12?001101020101101 Kutorginids 23204??120001101021001102 Terebratulina 2320411122001101?20101101 Longtancunella 23201??111?????10201001?? Lingulosacculus 23203??11111000111001011? Cotyledion 210110-0011????1?1--101-- Mickwitzia 23203??1??-----00---1011- Eccentrotheca 22?13?????-----??---1011- Wiwaxia 11010----0----------001-- Annelida 00000----0----------001-- Halkieria 11110----0----------011-- Acoel l00000---------------001- Table S1. Statistics for Yuganotheca elegans gen. et sp. nov. based on ELI collection from the Chengjiang fauna, Yunnan, South China. All measurements are in mm. The following abbreviations are used: Ls, Length of the upper shell valves; Ws, Width of the upper shell valves; Hm, the height of median collar; Dm, Diameter of the median collar; Hc, the height of the Lower conical tube; Lp, the length of pedicle; Dp, the diameter of pedicle, the body height of Yuganotheca based on ELI collection. Ls Ws Hm Dm Hc Lp Dp Max 14 17.5 7 6.3 21 30 2.1 Min 2.3 2.8 1.1 1 3.1 4 0.6 Count 207 207 222 227 212 38 13 Mean 7.4 9.4 3.1 3.2 9.4 15.7 1.5

References

1 Chen, J.-Y & Zhou, G.-Q. Biology of the Chengjiang fauna. Bulletin of the National Museum of Natural science 10, 11-106 (1997).

2 Hou, X., Bergström, J., Wang, H. F., Feng, X. H. & Chen, A. The Chengjiang fauna: exceptionally well-preserved fauna from 530 million years ago. Yunnan Science and Technology Press (1999).

3 Luo, H., Hu, S., Chen, L., Zhang, S. & Tao, Y. Early Cambrian Chengjiang fauna from Kunming region, China. Yunnan Science and Technology Press (1999).

4 Hou, X.-G. et al. The Cambrian fossils of Chengjiang, China: the flowering of early animal life. Wiley (2004).

5 Zhang, Z. F. et al. Note on the gut preserved in the Lower Cambrian Lingulellotreta (Lingulata, Brachiopoda) from southern China. Acta Zool-Stockholm 88, 65-70 (2007).

6 Zhang, Z. F., Robson, S. P., Emig, C. & Shu, D. G. Early cambrian radiation of brachiopods: A perspective from south china. Gondwana Res 14, 241-254 (2008).

7 Balthasar, U. & Butterfield, N. J. Early Cambrian "soft-shelled" brachiopods as possible stem-group phoronids. Acta Palaeontol Pol 54, 307-314 (2009).

8 Zhang, N. Wenlockian (Silurian) brachiopods of the Cape Phillips Formation, Baillie Hamilton Island, Arctic Canada: Part I. Palaeontographica Abteilung A 206, 49-97 (1989).

9 Jin, Y. G., Hou, X. G. & Wang, H. Y. Lower Cambrian Pediculate Lingulids from Yunnan, China. J Paleontol 67, 788-798 (1993).

10 Zhang, Z. F., Shu, D. G., Han, J. & Liu, J. N. Morpho-anatomical differences of the Early Cambrian Chengjiang and Recent lingulids and their implications. Acta Zool-Stockholm 86, 277-288 (2005).

11 Zhang, Z. F., Han, J., Zhang, X. L., Liu, J. N. & Shu, D. G. Soft-tissue preservation in the Lower Cambrian linguloid brachiopod from South China. Acta Palaeontol Pol 49, 259-266 (2004).

12 Zhang, Z.-F., Shu, D.-G., Han, J. & Liu, J.-N. New data on the lophophore anatomy of Early Cambrian linguloids from the Chengjiang Lagerstätte, Southwest China. Carnets de Géologie/Notebooks on Geology, Brest, Letter 4, 1-7 (2004).

13 Holmer, L. E., Popov, L. E., Bassett, M. G. & Laurie, J. Phylogenetic analysis and ordinal classification of the Brachiopoda. Palaeontology 38, 713-741 (1995).

14 Conway Morris, S. & Caron, J. B. Halwaxiids and the early evolution of the lophotrochozoans. Science 315, 1255-1258 (2007).

15 Zhang, Z. F. et al. Architecture and function of the lophophore in the problematic brachiopod Heliomedusa orienta (Early Cambrian, South China). Geobios-Lyon 42, 649-661 (2009).

16 Zhang, Z. F., Holmer, L. E., Popov, L. & Shu, D. G. An Obolellate Brachiopod with Soft-Part Preservation from the Early Cambrian Chengjiang Fauna of China. J Paleontol 85, 460-463 (2011).

17 Zhang, Z. F. et al. Rhynchonelliformean brachiopods with soft-tissue preservation from the early Cambrian Chengjiang lagerstatte of South China. Palaeontology 50, 1391-1402 (2007).

18 Zhang, Z. F., Holmer, L. E., Ou, Q., Han, J. & Shu, D. G. The exceptionally preserved Early Cambrian stem rhynchonelliform brachiopod Longtancunella and its implications. Lethaia 44, 490-495 (2011).