Ontogeny and Evolutionary Significance of a New Acrotretide Brachiopod Genus from Cambrian Series 2 of South China

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Ontogeny and evolutionary significance of a new acrotretide brachiopod genus from Cambrian Series 2 of South China

Zhiliang Zhang , Lars E. Holmer , Feiyang Chen & Glenn A. Brock

To cite this article: Zhiliang Zhang , Lars E. Holmer , Feiyang Chen & Glenn A. Brock (2020): Ontogeny and evolutionary significance of a new acrotretide brachiopod genus from Cambrian Series 2 of South China, Journal of Systematic Palaeontology, DOI: 10.1080/14772019.2020.1794991 To link to this article: https://doi.org/10.1080/14772019.2020.1794991

Published online: 07 Aug 2020.

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Ontogeny and evolutionary significance of a new acrotretide brachiopod genus from Cambrian Series 2 of South China a,b,c a,c a,b a,b Zhiliang Zhang , Lars E. Holmer , Feiyang Chen and Glenn A. Brock aState Key Laboratory of Continental Dynamics, Shaanxi Key Laboratory of Early Life & Environments, Early Life Institute, Department of Geology, Northwest University, Xi’an 710069, China; bDepartment of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia; cInstitute of Earth Sciences, Palaeobiology, Uppsala University, SE-752 36 Uppsala, Sweden (Received 5 March 2020; accepted 3 July 2020)

Micromorphic acrotretide brachiopods first appeared during Cambrian Epoch 2 and subsequently experienced a rapid diversification. However, our knowledge of acrotretide origins and early evolution is hampered by our poor understanding of their earliest representatives. Here, we describe one of the oldest known acrotretides from the Cambrian Series 2 Shuijingtuo Formation of southern Shaanxi and western Hubei, South China. The new genus Palaeotreta gen. nov. can be distinguished from all other genera, mainly by its unusual ontogeny and morphology; in Palaeotreta the pedicle foramen is located mostly outside of the metamorphic shell, the ventral intertrough is very short and the inclination of the ventral pseudointerarea changes from catacline to apsacline. Two ontogenetic stages (T1–T2) of post-metamorphic shell growth can be distinguished in the low cap-like Palaeotreta shannanensis gen. et sp. nov.; this type of development with a relatively long pedicle foramen forming stage (T1), a simple pedicle opening, weakly developed ventral apical process and dorsal median septum, can be considered to represent a plesiomorphy for the acrotretides. By contrast, the more derived Palaeotreta zhujiahensis (Li & Holmer, 2004) is characterized by paedomorphosis, expressed in an early enclosure of pedicle foramen and greatly decreased growth of the ventral intertrough during the intertrough-increasing stage (T3), producing a cap-like shape and retaining catacline inclination of the ventral pseudointerarea. Thus, heterochrony may have played an important role in the morphological divergence of acrotretides during the Cambrian evolutionary radiation, and promoted the subsequent radiation of acrotretides. The ontogenetic study of Palaeotreta gen. nov. also supports the notion that the ventral intertrough of acrotretide brachiopods may have formed by the ‘rolling up’ of the lingulide propareas. http://zoobank.org/urn:lsid:zoobank.org:pub:2C95FB13-7B15-43A2-B37C-AAA1B74A2D1C Keywords: micromorphic brachiopods; Acrotretida; ontogeny; Cambrian Epoch 2; pedicle foramen; heterochrony

Introduction origin, divergence and phylogenetic relationships with other brachiopod groups remain uncertain. Linguliform brachiopods first appeared at the beginning To date, only six acrotretide genera, including of the Cambrian, and they represent one of the key com- Eohadrotreta, Linnarssonia, Prototreta, Vandalotreta, ponents of benthic communities during the Cambrian Kuangshanotreta and Hadrotreta, are known from evolutionary radiation (Bassett et al. 1999; Z.-F. Zhang Cambrian Series 2 (Holmer & Popov 2000;Li&Holmer et al. 2008, 2016; Budd & Jackson 2016; Z.-L. Zhang 2004; Ushatinskaya 2010). Recently published works et al. 2020). The linguliform order Acrotretida, which is show that Eohadrotreta rapidly achieved a wide distribution over key palaeocontinents (South China, East uniquely characterized by a diminutive shell size and Gondwana, West Gondwana, North China), soon after coniform ventral valve, had a relatively late origination, their first appearance in Cambrian Epoch 2 (Wang et al. but subsequently diversified rapidly and became 2012; Popov et al. 2015; Z.-L. Zhang et al. 2016, 2017, extremely abundant with a cosmopolitan distribution 2018a;Panet al. 2019; Claybourn et al. 2020). Two spe- during the Cambrian and Ordovician (Williams & cies of Eohadrotreta (E. zhenbaensis and E.? zhujiahen- Holmer 1992; Holmer & Popov 2000; Williams et al. sis) were originally described from South China by Li & 2000; Ushatinskaya 2010; Topper et al. 2013; Z.-L. Holmer (2004) but the diagnostic features to discriminate Zhang et al. 2018a, b; Ushatinskaya & Korovnikov these taxa were not clearly defined, making it difficult to 2019). However, many questions concerning their early evaluate the biostratigraphy and phylogeny of this Corresponding author. Email: [email protected]

# 2020 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License (http://creativecommons.org/ licenses/by-nc-nd/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way. Published online 07 Aug 2020 2 Z. Zhang et al. important genus (Li & Holmer 2004; Z.-L. Zhang et al. phosphatized shelly fossils have been reported from the 2017, 2018a, b; Z.-L. Zhang 2018). A subsequent lower part of the Shuijingtuo Formation at the detailed quantitative analysis of brachiopod ontogeny Xiaoyangba section, which are dominated by the eodis- demonstrated that the developmental pattern of the meta- coid trilobite Hupeidiscus orientalis, the hyolith morphic shell was quite different in these two species Paramicrocornus zhenbaensis and bradoriids (Li et al. (Z.-L. Zhang et al. 2018a), revealing heterochrony in the 2012; Z.-L. Zhang 2018; Z.-L. Zhang et al. 2018c). ontogeny of the earliest acrotretide representatives during Associated fossils include the brachiopods Eohadrotreta, the Cambrian radiation. Numerous morphological differ- Palaeobolus, Botsfordia and Lingulellotreta, the tommo- ences between E.? zhujiahensis and E. zhenbaensis indi- tiid Kelenella, hyoliths, molluscs along with chancellor- cate that they may belong to separate genera (Z.-L. iids, echinoderm plates and sponge spicules (Li & Zhang 2018; Z.-L. Zhang et al. 2018a). Holmer 2004; Yang et al. 2015; Z.-F. Zhang et al. This paper aims to describe the new acrotretide genus 2016). The new taxon Palaeotreta shannanensis gen. et Palaeotreta gen. nov. from the Cambrian Series 2 sp. nov. is described from a single layer (S4-3) at the Shuijingtuo Formation from southern Shaanxi and west- base of the Shuijingtuo Formation. ern Hubei provinces of South China. The ontogeny of In the Three Gorges area of western Hubei, the Aijiahe Palaeotreta shannanensis gen. et sp. nov. includes the section, approximately 25 km north-west of Yichang City formation of an enclosed pedicle foramen that is mostly (Fig. 1), has been well studied (e.g. Ishikawa et al. 2014; located outside of the metamorphic shell, as well as an Z.-F. Zhang et al. 2016; Z.-L. Zhang et al. 2016, 2018a). apsacline ventral pseudointerarea during later ontogen- The 68 m thick Shuijingtuo Formation (unconformably etic stages, which are unlike any other acrotretides from overlying the Yanjiahe Formation) is composed of three Cambrian Epoch 2. The problematic E.? zhujiahensis is parts. The 10 m thick basal part consists of condensed also referred to the new genus Palaeotreta. The new black shale intercalated with black limestone concretions, information on the development of the pedicle foramen, yielding the oldest known trilobite, Tsunyidiscus actus, pseudointerarea, apical process and median septum is from this region (Z.-F. Zhang et al. 2016). The 40 m thick also shown to be important for deciphering phylogeny. middle part of the succession is dominated by alternating Three ontogenetic stages (e.g. pedicle foramen-forming black shale and thin limestones, while the 18 m thick upper stage [T1], pedicle foramen-enclosing stage [T2] and part consists of greyish-black argillaceous limestones. intertrough-increasing stage [T3]) were identified by Abundant phosphatized shelly fossils have been described Z.-L. Zhang et al.(2018a) for E. zhenbaensis and can from the middle and upper parts of the Shuijingtuo also be identified in Palaeotreta. Formation at the Aijiahe section with the acrotretide brachiopod Eohadrotreta zhenbaensis, the eodiscoid trilobite Tsunyidiscus actus and hyoliths the most dominant groups Geological setting (Z.-F. Zhang et al. 2016; Z.-L. Zhang et al. 2018c). Other associated fossils include the brachiopods Palaeobolus, Neoproterozoic to Palaeozoic sedimentary successions Spinobolus and Lingulellotreta, archaeocyaths, molluscs, are well developed and distributed on the northern mar- bradoriids, chancelloriid sclerites and sponge spicules gin of the Yangtze Platform, South China. The acrotre- (Steiner et al. 2007;Z.-F.Zhanget al. 2016; Z.-L. Zhang tide brachiopods described here come from the lower et al. 2016, 2018a; Z.-L. Zhang 2018). Palaeotreta zhujia- part of the Shuijingtuo Formation of South China. In hensis (Li & Holmer, 2004) is found in the middle and southern Shaanxi, Precambrian to Cambrian strata are upper parts of the Shuijingtuo Formation in this section. well exposed at the Xiaoyangba section, approximately 106 km south-east of Hanzhong City (Fig. 1), including (in ascending order) the Ediacaran Dengying Formation, Material and methods the Cambrian Xihaoping Member of Dengying Formation, the Shuijingtuo Formation and the Shipai All specimens described and illustrated are from the Formation (Z.-L. Zhang et al. 2018c, 2020). The Shuijingtuo Formation (Cambrian Series 2) of South Shuijingtuo Formation (unconformably overlying the China (Fig. 1). To date, 22 ventral and 10 dorsal valves Xihaoping Member of the Dengying Formation) is char- of Palaeotreta shannanensis gen. et sp. nov. and 23 acterized by organic-rich and nodular limestones at the complete conjoined valves, 124 ventral and 115 dorsal lower boundary. The 31 m thick lower Shuijingtuo valves of Palaeotreta zhujiahensis have been collected Formation is comprised of dark, thin silty limestones, from the Xiaoyangba and Aijiahe sections, respectively. while the 85 m thick upper part consists of siltstones The specimens were obtained through acetic acid interbedded with thin limestones. Large quantities of (10%) maceration of samples from thin-bedded A new acrotretide brachiopod genus from the Cambrian of South China 3

Figure 1. Palaeogeographic map and fossil localities in southern Shaanxi and western Hubei, South China (modified from Z.-F. Zhang et al. 2016), noting the Xiaoyangba and Aijiahe sections. limestones following standard techniques (Jeppsson Class Lingulata Gorjansky & Popov, 1985 et al. 1985). Specimens were manually picked from the Order Acrotretida Kuhn, 1949 acid-resistant residues and selected specimens were Superfamily Acrotretoidea Schuchert, 1893 imaged using SEM facilities including a Zeiss Supra Family Acrotretidae Schuchert, 1893 35 VP field emission at Uppsala University and Genus Palaeotreta gen. nov. a JEOL JSM 7100F-FESEM at Macquarie University. Measurements of length and width of P. shannanensis Type species. Palaeotreta shannanensis gen. et sp. gen. et sp. nov. were made on the best-preserved speci- nov.; Cambrian Series 2 of southern Shaanxi, mens, while the measurement data for P. zhujiahensis South China. was illustrated in Z.-L. Zhang et al. 2018a (appendix Derivation of name. Palaeo, ‘old’, from the Greek S3–S4). Scatter plots of different specimens showing palaios, describing an ancestral representative of morphological variation were constructed using PAST v. acrotretide brachiopods, with the ending –treta, 3.14 (Hammer et al. 2001). ‘perforated’ from the Greek tretos. Description. Shell ventribiconvex, sub-circular to trans- Systematic palaeontology versely oval, ornamented with evenly distributed pits, about 1 mm in diameter covering the metamorphic shell, Phylum Brachiopoda Dumeril, 1806 and with finely concentric growth lines on the post- Subphylum Linguliformea Williams, Carlsson, metamorphic shell. Ventral valve cap-like to low Bruton, Holmer & Popov, 1996 conical, pseudointerarea vestigial, from catacline to 4 Z. Zhang et al. apsacline, with very short intertrough. Incipient pedicle Holmer & Popov 2000); but to date, this character is notch is open during the long pedicle foramen-develop- not known from early Cambrian Acrotretidae. ing stage. Adult pedicle foramen located outside of the metamorphic shell. Growth lines developed on a separ- Palaeotreta shannanensis gen. et sp. nov. ate area between the metamorphic shell and pedicle for- (Figs 2–7; Table 1) amen. Apical process vestigial, very close to the pedicle foramen. Cardinal muscle scars and vascula lateralia Derivation of name. After the occurrence in Shannan, weakly impressed. Dorsal valve slightly convex. southern Shaanxi Province. Pseudointerarea orthocline, short with narrow sub- Holotype. ELI-XYB S4-3 AU-01, ventral valve (Fig. triangular median groove. Median buttress generally 2I–L, length [L] ¼ 1196 mm, width [W] ¼ 1331 mm). well developed, while median septum vestigial. Cardinal muscle scars weakly impressed. Secondary shell layer Paratype. ELI-XYB S4-3 AV-18, dorsal valve (Fig. columns relatively short. 3H–K,L¼ 1008 mm, W ¼ 1226 mm). Remarks. The new genus is established for acrotretide Type locality. Shuijingtuo Formation (layer S4-3, 0.7 m 0 00 species that are similar to Eohadrotreta and above the base) at Xiaoyangba section (32 29 29 N, 0 00 Linnarssonia. However, the new genus differs from all 107 57 2 E), Zhenba County, south-eastern Shaanxi, other (especially from Cambrian Epoch 2) acrotretides South China. Cambrian Series 2. in having the following characters: (1) a catacline to Other material. A total of 21 ventral valves and nine apsacline inclination of ventral pseudointerarea with dorsal valves were recovered from the same layer short intertrough; (2) a pedicle foramen that is located (S4-3) in the Shuijingtuo Formation. mostly outside the metamorphic shell; (3) a vestigial apical process and median septum; and (4) weakly Description. Shell ventribiconvex, sub-circular in out- m impressed cardinal muscle scars. Eohadrotreta, line with round posterior margin (Figs 2, 3). 1.1 m Prototreta, Vandalotreta, Hadrotreta and Kotylotreta hemispherical pits evenly distributed on the whole mainly have procline pseudointerarea with a relatively metamorphic shell surface without overlapping (Fig. 4F, G), while the post-metamorphic shell is long intertrough. Although the apsacline ventral pseu- covered by finely circular growth lines and drape struc- dointerarea and internal structures (apical process, tures (Fig. 4H). Shell structure consists of thin-lamella median septum) of Palaeotreta can be compared with (2 mm) primary layer and thin-lamina (5 mm) secondary Cambrian Epoch 3 taxa, such as Aphelotreta and the columnar layers (Fig. 5H–M). Furongian Linnarssonella, the positions of pedicle for- Ventral valve sub-circular, on average 89% as long amen and ventral pseudointerarea are different. The ven- as wide with maximum width at mid-length (Table 1). The tral apical process and dorsal septum of Palaeotreta are valve is convex, with a cap-like shape (Fig. 2), on average very weakly defined, while Linnarssonia develops a 21% as deep as long, with maximum height almost at mid- high, boss-like apical process and has a high median sep- valve. Metamorphic shell pronounced at the apex (Fig. 2C, tum. Eohadrotreta has a relatively more well-developed N), occupying 13% of valve length. Pseudointerarea apical process and median septum. Vandalotreta has an weakly developed, catacline to apsacline. Intertrough apical process that forms a boss-like thickening anterior poorly defined, very short, occupying on average about to the internal foramen and Hadrotreta develops apical 2% of the length and 6% of the width of the valve (Fig. pits that are situated close to the apical process (Holmer 2I–P). Apical process vestigial, only observed in adult &Popov2000). Kuangshanotreta is difficult to compare specimens, close to pedicle foramen, occupying 20% of with the new genus in the absence of data on shell valve length (Fig. 4B, C). Enclosed pedicle foramen morphology and ornamentation (Wang et al. 2012). almost circular, about 50 mm in diameter, located mostly Palaeotreta is the third genus of the Acrotretida that directly outside of the metamorphic shell, until valve has been described from the Cambrian Series 2 of South reaches about 1100 mm in length. Growth lines developed China, and this region has a higher diversity of coeval at the posterior margin of the metamorphic shell and the acrotretides as compared to South Australia, Laurentia, lateral side of the pedicle foramen (Fig. 4C). Cardinal Antarctica and Siberia. The most unique character of muscle scars and vascula lateralia weakly impressed. Palaeotreta is the position of the pedicle foramen, Dorsal valve sub-circular, on average 87% as long which is located mostly outside of the metamorphic as wide, with maximum width almost at mid-valve shell from the T2 ontogenetic stage. In this feature it (Table 1). It is slightly convex (Fig. 5), on average has similarities to some Cambrian Ceratretidae and about 19% as deep as long. Pseudointerarea small, Ordovician Scaphelasmatidae species (Holmer 1989; orthocline, occupying 6% of the valve length and 36% A new acrotretide brachiopod genus from the Cambrian of South China 5

Figure 2. Ontogenetic development of ventral valve of Palaeotreta shannanensis gen. et sp. nov. from the Shuijingtuo Formation of southern Shaanxi. A–H, ventral valves demonstrating pedicle foramen forming stage (T1); A–D, juvenile with unrestricted pedicle notch, ELI-XYB S4-3 AU-06; E–H, small valve with pedicle opening, ELI-XYB S4s-3 AV-04; I–P, ventral valves demonstrating pedicle foramen-enclosing stage (T2); I–L, adult with enclosed pedicle foramen, ELI-XYB S4-3 AU-01; L, interior view, noting vascula lateralia (tailed arrow); M–P, larger valve with very short intertrough, ELI-XYB S4-3 AU-08. 6 Z. Zhang et al.

Figure 3. Ontogenetic development of dorsal valve of Palaeotreta shannanensis gen. et sp. nov. from the Shuijingtuo Formation of southern Shaanxi. A–D, juvenile with rudiment median buttress, ELI-XYB S4-3 AV-19; E–G, larger valve with developed median buttress, ELI-XYB S4-3 AU-12; G, oblique lateral view showing weakly developed median septum (arrow); H–K, adult valve with weakly developed median septum, ELI-XYB S4-3 AV-18. of valve width (Fig. 5E, H). Median groove sub-triangu- However, the new species has a low cap-like shape, lar, short, about 31% of the pseudointerarea width (Fig. small pseudointerarea with very short intertrough, 4E). Median buttress generally developed, fading anteri- apsacline pseudointerarea in the adult valve, prolonged orly (Fig. 4E, F). Median septum vestigial, only devel- pedicle foramen-forming stage and a pedicle oped in adult valve, extending anteriorly for 59% of foramen that is located outside of the metamorphic shell valve length (Fig. 5H–K). Cardinal muscle scars (Figs 6, 7). Furthermore, the new species has a less weakly impressed, occupying 17% of the length and developed intertrough as compared with E. zhenbaensis 45% of the width of the valve (Fig. 5D). (Z.-L. Zhang et al. 2018a); in the latter species the intertrough is becoming remarkably prominent in stage T3, Remarks. Palaeotreta shannanensis gen. et sp. nov. which does not happen in the new species. The shell shares a similar morphology in outline with structure of P. shannanensis is similar to that of E. Eohadrotreta zhenbaensis (from the same locality). zhenbaensis. However, the former species has a very A new acrotretide brachiopod genus from the Cambrian of South China 7

Figure 4. Ornamentation and ultrastructure of the earliest ontogeny of Palaeotreta shannanensis gen. et sp. nov. from the Shuijingtuo Formation of southern Shaanxi. A, enlarged ventral apex, note pronounced halo (arrow) and drape structures (tailed arrow), ELI-XYB S4-3 AU-08; B, oblique lateral view of A, showing the pedicle foramen (arrow) and protegulum (tailed arrow); C, posterior view of ventral apex, show enclosed pedicle foramen outside of metamorphic shell, ELI-XYB S4-3 AU-01; D, enlarged dorsal apex, note pronounced halo (arrow) and drape structures (tailed arrow), ELI-XYB S4-3 AV-15 E, obliquely lateral view of D, showing the protegulum (tailed arrow) and two pairs of larval setal sacs (arrows); F, evenly distributed pitting structures on metamorphic shell, ELI-XYB S4-3 AU-13; G, enlargement of F; H, growth lines and drape structures on post-metamorphic shell, ELI-XYB S4-3 AU-13. thin primary layer about 2 mm thick, and very thin sec- shell, ranging from 4 mmto8mm, and are quite short ondary columnar layers. The thickness of columns in compared to the columns of E. zhenbaensis. The sec- P. shannanensis is variable in different parts of the ondary layer insignificantly increases the overall 8 Z. Zhang et al.

Figure 5. Internal morphology and ultrastructure of Palaeotreta shannanensis gen. et sp. nov. from the Shuijingtuo Formation of southern Shaanxi. A, enlarged ventral posterior end, showing cardinal muscle scars (arrows) and paired vascula lateralia (tailed arrows), ELI-XYB S4- 3 AU-07; B, oblique lateral view of A; C, enlarged ventral posterior end, ELI-XYB S4-3 AV-07; D, lateral view of dorsal posterior end, noting cardinal muscle scars by arrows, XYB S4-3 AV-18; E, enlarged dorsal pseudointerarea and median buttress, ELI-XYB S4-3 AU-12; F, enlargement of the terminal of median buttress of E, note weakly developed median septum; G, fine pores on the exterior of columnar lamella by exfoliation of the primary layer, ELI-XYB S4-3 AU-09; H, I, one layer of the secondary columnar structures on valve margin, ELI-XYB S4-3 AV-09, XYB S4-3 AU-07; J, K, remaining base of columns after exfoliation of the covering lamella of H; L, one lamella of very short secondary columns, ELI-XYB S4-3 AU-08; M, re-crystallization of the columns, note hollow in the centre, ELI-XYB S4-3 AV-13. A new acrotretide brachiopod genus from the Cambrian of South China 9

Figure 6. Ontogenetic development of pedicle foramen of Palaeotreta shannanensis gen. et sp. nov. from the Shuijingtuo Formation of southern Shaanxi. A, B, juvenile with unrestricted pedicle notch, note raised propareas (arrows), ELI-XYB S4-3 AV-09; C, D, juvenile with unrestricted pedicle notch, ELI-XYB S4-3 AV-17; E–G, semicircular pedicle foramen soon to be enclosed, ELI-XYB S4-3 AV-05; H, raised propareas (arrows), ELI-XYB S4-3 AV-11; I–L, pedicle foramen, just enclosed with very short intertrough, XYB S4-3 AU-07; M, N, adult with enclosed pedicle foramen, showing the successive growth of propareas at the posterior margin of the metamorphic shell (arrow), ELI-XYB S4-3 AU-01; O, enclosed pedicle foramen is mostly outside the metamorphic shell, ELI- XYB S4-3 AV-07. thickness of the ventral valve (Z.-L. Zhang et al. 2016), that is mostly located outside the metamorphic shell being composed of one to two columnar laminae, result- (Holmer et al. 1996, pl. 13; Ushatinskaya & ing in a low cap-like shape in P. shannanensis. Korovnikov 2019, pl. 4). P. shannanensis has a similar Palaeotreta shannanensis differs from Vandalotreta inclination of the ventral pseudointerarea as Aphelotreta djagoran (Kruse, 1990) and Linnarssonia rowelli khemangarensis (Popov et al. 2015), while the ornamen- (Pelman, 1973) in having a lower ventral valve, weakly tation of the metamorphic shell, pedicle foramen size developed apical process and median septum, apsacline and the median groove allow the distinction of the two ventral pseudointerarea, as well as a pedicle foramen species (Popov et al. 2015, fig. 21). 10 Z. Zhang et al.

Figure 7. Bivariate plots of ventral valves of Palaeotreta shannanensis gen. et sp. nov. from the Shuijingtuo Formation showing ontogenetic stage T1 (red) and stage T2 (blue). A, plots of valve width – length ratio (W/L), length at maximum width – valve length ratio (Lm/L), and valve height – length ratio (H/L). B, plots of apical process length – valve length ratio (La/L), pedicle foramen length – valve length ratio (Lf/L).

At the Xiaoyangba section, P. shannanensis occurs at Other material. A total of 23 conjoined valves, 124 the base of the Shuijingtuo Formation, while E. zhen- ventral and 115 dorsal valves from the middle and upper baensis first occurs 60 cm higher. Therefore, P. shanna- parts of the Shuijingtuo Formation at the Aijiahe section nensis represents the oldest known acrotretide (30 440 55.200 N, 111 030 58.500 E) of Yichang, western brachiopod in southern Shaanxi. The diachronous nature Hubei, South China. of the stratigraphic hiatus at the base of Cambrian Series 2 across southern Shaanxi and western Hubei Description. Shell ventribiconvex, transverse oval makes the biostratigraphic correlation between these in outline with slightly straightened posterior margin m regions imprecise, and more index fossils from new sec- (Fig. 8). 1.3 m hemispherical pits evenly distributed on tions are required to better constrain the time gap and the whole metamorphic shell surface without overlap- better resolve correlation. ping (Fig. 9N), while post-metamorphic shell covered by finely circular growth lines and drape structures (Fig. Palaeotreta zhujiahensis (Li & Holmer, 2004) 8I). Shell structure consists of thin-lamella (2 mm) pri- (Figs 8, 9) mary layer and thin-lamina (5–10 mm) secondary columnar layers (Fig. 9O, P). 2004 Eohadrotreta zhujiahensis Li & Holmer: 208, Ventral valve sub-circular, on average 83% as long as figs 14,15. wide with maximum width at the posterior half of valve. 2016 Eohadrotreta zhujiahensis Z.-F. Zhang et al.: 342, It is convex, with a low conical shape (Fig. 8I–N), on fig. 6. average 28% as deep as long, with a maximum height 2018a Eohadrotreta? zhujiahensis Zhang et al.: almost at mid-valve. Metamorphic shell pronounced at 187–197, figs 7–10. the apex (Fig. 8B, I), occupying 31% of the valve 2018b Eohadrotreta? zhujiahensis Zhang et al.: 4–8, length. Pseudointerarea weakly developed, almost cata- figs 2a, 4. cline, divided by a very short intertrough, which is on Holotype. Li & Holmer (2004), NIGP1351 77, con- average about 5% of the length and 11% of the width joined shell (W ¼ 1167 mm). of the valve (Fig. 8H, M). Apical process weakly developed, occupying on average 30% of valve length, close Type locality. Guojiaba Formation (uppermost) at the to pedicle foramen. Pedicle foramen is relatively large, Fucheng section of Zhenba County, south-eastern about 90 mm in diameter, enclosed and located directly Shaanxi, South China. Cambrian Series 2. outside the metamorphic shell until valve reaches about Paratype. ELI-AJH 8-2-1 CE-03, ventral valve (Fig. 650 mm in length. Growth lines distinctively developed 8I–N,L¼ 975 mm, W ¼ 1220 mm) from the upper at the posterior margin of the metamorphic shell (Fig. Shuijingtuo Formation at the Aijiahe section of 9D, E, L, M). Cardinal muscle scars and vascula latera- Yichang, South China. lia weakly impressed. Table 1. Average dimensions and ratios of ventral and dorsal valves of Palaeotreta shannanensis gen. et sp. nov. from the Cambrian Series 2 Shuijingtuo Formation.

VLWHLm Lms Wms La Li Wi Lc Wc Lf Wf Lv L/W H/L

N 15 13 14 13 9 9 8 16 16 7 7 16 16 11 4 13 14 China South of Cambrian the from genus brachiopod acrotretide new A Mean 998 1130 208 561 142 199 235 8 70 146 423 45 47 417 88.64% 21.06% Min 707 750 120 410 101 161 147 0 40 77 258 28 25 274 82.32% 16.97% Max 1319 1533 282 778 179 240 311 25 99 249 587 68 68 566 94.67% 26.00% Median 1009 1190 213 538 145 195 221 0 72 129 417 43 48 413 88.07% 21.13% SD 200 258 38 134 28 26 64 10 15 61 115 10 13 129 3.95% 2.56%

VLm/L Lms /L La/L Li/L Wi/W Li/Wi Lf/Li Wf/Wi Lf/Wf Lc/L Wc/W N 13109 61277 15167 7 Mean 56.07% 12.44% 20.44% 1.55% 6.13% 24.71% 255.64% 66.07% 101.43% 13.86% 36.18% Min 48.76% 0.00% 0.00% 0.96% 3.34% 18.87% 172.73% 41.77% 47.06% 9.63% 31.64% Max 64.82% 18.42% 29.19% 2.09% 10.20% 33.33% 409.09% 95.77% 135.71% 20.82% 44.10% Median 55.63% 13.51% 22.42% 1.56% 5.65% 22.00% 228.57% 65.06% 112.67% 12.54% 34.40% SD 4.03% 5.01% 8.31% 0.39% 2.01% 5.63% 75.97% 16.68% 27.55% 4.01% 5.09%

DLWHLm Lms Wms Ls Lp Wp Lc Wc Lg Wg L/W H/L N 666655444334466 Mean 975 1127 180 537 144 212 602 59 425 172 548 58 189 86.8% 18.5% Min 890 996 146 490 118 198 354 57 392 145 485 57 156 82.2% 14.8% Max 1135 1311 225 604 185 230 743 62 465 221 599 59 218 91.3% 22.4% Median 961 1103 176 521 142 209 655 59 422 150 561 58 190 86.0% 17.7% SD 92 127 30 52 27 12 171 2 39 43 58 1 32 3.4% 3.2%

DLm/L Lms /L Lms /Wms Ls/L Lp/L Wp/W Lg/Lp Lg/Wg Wg/Wp Lc/L Wc/W N 65544444433 Mean 55.1% 14.7% 67.5% 59.0% 5.8% 36.3% 98.4% 31.4% 44.6% 16.6% 44.5% Min 49.5% 10.6% 55.8% 38.0% 5.2% 29.9% 93.5% 26.8% 34.5% 13.2% 39.6% Max 59.1% 18.7% 80.4% 75.1% 6.3% 38.8% 100.0% 37.2% 55.6% 22.3% 48.2% Median 55.6% 14.1% 68.6% 61.4% 5.9% 38.2% 100.0% 30.9% 44.2% 14.4% 45.7% SD 3.5% 3.2% 10.0% 15.9% 0.5% 4.3% 3.2% 5.3% 8.7% 5.0% 4.4%

All measurements are in lm. Abbreviations: D, dorsal valve; V, ventral valve; L, H, W, length, height and width of valve where not specified; La, length of ventral apical process; Lc,Wc, length and width of cardinal muscle scars; Lf,Wf, length and width of pedicle foramen; Lg,Wg, length and width of dorsal median groove; Li,Wi, length and width of ventral intertrough; Lm, length at maximum width; Lms ,Wms , length and width of metamorphic shell; Lp,Wp, length and width of dorsal pseudointerarea; Ls, length of dorsal median septum; Lv, length of vascula lateralia. 12 Z. Zhang et al.

Figure 8. Ontogenetic development of ventral valve of Palaeotreta zhujiahensis from the Shuijingtuo Formation of western Hubei. A–F, ventral valves demonstrating pedicle foramen forming stage (T1); A, oblique dorsal view of a very small conjoined specimen showing unrestricted pedicle notch, ELI-AJH 8-1-2-B AF12; B, lateral view of a small conjoined specimen, ELI-AJH 8-2-3 AD2-07; C, posterior view, box indicates the area shown in Figure 9E, ELI-AJH S05 AG07; D, interior view of C; E, oblique view of a larger juvenile, ELI-AJH 8-2-3 AC-27; F, posterior view of E, note ‘U’-shaped pedicle notch, box indicates the area shown in Figure 9D; G, lateral view, indicating pedicle foramen-enclosing stage (T2), showing enclosed pedicle foramen outside of the metamorphic shell, ELI-AJH 8-2-D AD2-12; H–N, intertrough-increasing stage (T3); H, posterior view, ELI-AJH S05 AF-16; I–N, adult with short intertrough, ELI-AJH 8-2-1 CE-03; I, exterior view; J, interior view; K, oblique lateral view; L, lateral view; M, posterior view, note the posterior migration of enclosed pedicle foramen, outside the metamorphic shell; N, oblique anterior view.

Dorsal valve transversely oval, on average 82% as represent a second species of Eohadrotreta by Li & long as wide, with maximum width almost at mid-valve Holmer (2004). However, Z.-L. Zhang et al.(2018a) (see details in Z.-L. Zhang et al. 2018a)(Fig. 8A). demonstrated significant differences in ontogenetic Slightly convex (Fig. 8A, B), on average 17% as deep as growth between these two species. New material col- long. Pseudointerarea small, orthocline, occupying about lected from western Hubei demonstrates that P. zhujia- 7% of valve length and 38% of valve width. Median hensis has a lower ventral valve, straightened posterior groove subtriangular, short, on average 44% of pseudoin- margin, relatively larger pedicle foramen, late enclosure terarea width. Median buttress moderately developed, fad- of the pedicle foramen, smaller ventral pseudointerarea, ing anteriorly. Median septum vestigial, only developed much shorter intertrough, weakly developed growth in adult valve, extending anteriorly at mid-valve. Cardinal lines, apical process and median septum, thinner second- muscle scars gently impressed, occupying 22% of the ary layers and more weakly impressed cardinal muscle length and 51% of the width of the valve. scars than those of E. zhenbaensis. Furthermore, the Remarks. Based on their similar morphology, most characteristic feature of P. zhujiahensis is that Palaeotreta zhujiahensis was originally considered to the pedicle foramen is located directly outside of the A new acrotretide brachiopod genus from the Cambrian of South China 13

Figure 9. Ontogenetic development of pedicle foramen of Palaeotreta zhujiahensis from the Shuijingtuo Formation of western Hubei. A, enlarged pedicle notch of Figure 8A; B, juvenile with unrestricted pedicle notch, showing raised propareas (arrows), ELI- AJH 8-2-3 AC-11; C, posterior view of Figure 8B; D, ‘U’-shaped pedicle notch, note the growth of propareas at the posterior margin of metamorphic shell (arrow); E, F, ‘U’-shaped pedicle foramen is soon to be enclosed, note the growth of propareas (arrow); G, enclosed pedicle foramen with short intertrough, ELI-AJH 8-2-D AD2-12; H, larger adult showing pedicle foramen outside the metamorphic shell, ELI-AJH 8-2-3 CD2-02; I, enlargement of propareas growing at the posterior margin of metamorphic shell and lateral sides of pedicle foramen of G; J, lateral view of I, note propareas growth (arrow); K, posterior view, showing pedicle foramen mostly located outside the metamorphic shell, box indicates the area shown in L, ELI-AJH 8-2-3 AC-22; L, enlarged view showing propareas growth (arrow); M, enlargement of propareas at the posterior margin of metamorphic shell, note pedicle foramen (arrow), ELI-AJH 8-2-1 AE-09; N, pitting structures on metamorphic shell, ELI-AJH 8-2-1 AE-09; O, P, enlarged secondary columnar layer, ELI-AJH 8-2-1 AE-09, ELI-AJH 8-2-1 CE-03. 14 Z. Zhang et al.

Figure 10. Ontogenetic scheme of Palaeotreta and Eohadrotreta from Cambrian Series 2 of South China, demonstrating transitions of important characters during different ontogenetic stages (modified from Z.-L. Zhang et al. 2018a, Claybourn et al. 2020). metamorphic shell, which fits closely with the diagnosis the second species discovered in southern Shaanxi and of the new genus Palaeotreta. The valve shape and western Hubei (after E. zhenbaensis), but E. zhenbaensis ontogenetic development of the pedicle foramen in P. has a much wider palaeogeographical distribution (Z.-L. zhujiahensis can be compared with that of P. shanna- Zhang et al. 2017). nensis (Figs 6, 9). However, the former has a catacline inclination of the ventral pseudointerarea and a relatively longer intertrough, which is two times longer than Discussion that of P. shannanensis. The shell structure of P. zhujiahensis is comparable Ontogenetic development of Palaeotreta with that of P. shannanensis. Both have a very thin pri- Recent study of the earliest ontogeny of Cambrian mary layer about 2 mm thick, but P. shannanensis has Epoch 2 acrotretide brachiopods has revealed that the relatively thinner columnar layers. The thickness of col- primary larval body plan of acrotretides is shared with umns in P. zhujiahensis is variable in different shell most early linguliforms, and that the metamorphic shell regions, ranging from 5 mmto10mm(Fig. 9O, P), is formed at the end of the planktotrophic stage (Z.-L. which is quite short compared to the columns in E. Zhang et al. 2018b). The same kind of early ontogenetic zhenbaensis (Zhang et al. 2017, fig. 5E, H). characters can also be observed in Palaeotreta shanna- At the Aijiahe section, P. zhujiahensis co-occurs with nensis gen. et sp. nov. The raised lobes at the posterior E. zhenbaensis at the middle part of the Shuijingtuo end of both the ventral and dorsal valves of P. shanna- Formation. Compared to the biostratigraphy with south- nensis are about 50 mm in size (Fig. 4B, D), which is ern Shaanxi (Z.-F. Zhang et al. 2016), P. zhujiahensis is comparable to the protegula of Eohadrotreta zhenbaen- slightly younger than P. shannanensis. P. zhujiahensis is sis. They are probably secreted initially as a bivalved, A new acrotretide brachiopod genus from the Cambrian of South China 15 organic shell by the larval mantle lobes (Paine 1963; pedicle notch changes from semicircular to circular (Fig. Chuang 1977; Balinski 2001; Z.-L. Zhang et al. 2018b). 6B–D). In the subsequent T2 pedicle foramen-enclosing During subsequent peripheral growth of the brephic stage (enclosure of pedicle notch to form a foramen and shell at the planktotrophic stage, two pairs of lobes are development of an incipient apical process and median preserved as imprints of larval setal sacs on the dorsal septum; Z.-L. Zhang et al. 2018a, pp. 191–197), the mar- side of the larval body (Fig. 4E). Pits with an average ginal accretionary growth increases the length and width diameter of 1 mm evenly cover the whole surface of the of both valves, while the ventral valve maintains a low metamorphic shell (Fig. 4F, G), which may represent cap-like form (Fig. 2I–O). At the same time, cardinal imprints of mineralized tablets that potentially protected muscle scars are weakly impressed, while the apical pro- the larvae against ultraviolet radiation penetrating sur- cess and median septum are weakly developed (Fig. face waters (Luter€ 2004; Williams & Cusack 2007; 5A–E). The inclination of the ventral pseudointerarea Z.-L. Zhang et al. 2018b). The metamorphic shell is changes from catacline to apsacline (Fig. 6F, L), and the separated from the post-metamorphic shell by a pro- accelerated shell growth along the posterior margin of nounced halo when the shell reached about 200 mmin the metamorphic shell produces a posterior migration of width (Fig. 4A, D; Table 1), which likely represents the the enclosed pedicle foramen (Fig.6B,M,O). It is completion of larval metamorphosis. A narrow belt important to note that the stage T2 of P. shannanensis is about 20 lm wide, outside the metamorphic shell, lack- much delayed until valves reach about 1100 mm in length, ing drape structures indicates the secretion of the neanic which is twice the size compared to E. zhenbaensis. shell (Fig. 4A, D). Subsequently, the mature shell is Furthermore, the boundary delineating the pedicle foramen developed by accretionary growth outside the neanic from the metamorphic shell is developed early in stage shell, exhibiting all major characters of the adult shell T1 (Fig. 6B), and successive growth lines of the propareas including drape structures (Fig. 4A, D) and a three-layer near the posterior margin of the metamorphic shell and shell (Fig. 5I–K). The growth of the mature shell indi- lateral sides of pedicle foramen are well developed in cates the development of marginal mantle after comple- stage T2 (Fig. 6M, O). These remarkable ontogenetic var- tion of metamorphosis (Z.-L. Zhang et al. 2018b). iations are also well demonstrated in the entire three onto- Detailed investigation of the earliest ontogeny of P. zhu- genetic stages of P. zhujiahensis (Fig. 9C, E, H–J, M). jiahensis has previously been documented by Z.-L. The morphology of juvenile shells is quite similar Zhang et al.(2018b). The closely similar features of between Palaeotreta and Eohadrotreta, which makes it metamorphosis between Eohadrotreta and Palaeotreta difficult to distinguish them when a complete ontogeny is imply that Palaeotreta probably had a life cycle similar lacking (Li & Holmer 2004;Z.-F.Zhanget al. 2016;Z.- to the early Cambrian acrotretide Eohadrotreta and lin- L. Zhang 2018). However, the heterochronic process gulide Eoobolus, which are interpreted to have had a probably occurred in later ontogenetic stages, resulting in relatively prolonged free-swimming stage (Popov et al. quite different morphologies in adults of Palaeotreta and 2007; Balthasar 2009; Ushatinskaya 2016; Z.-L. Zhang Eohadrotreta (Fig. 10; Klingenberg, 1998, 2016; Webster et al. 2017, 2018b). &Zelditch2005). A strong allometric growth pattern was For the later post-metamorphic ontogeny, Z.-L. Zhang verified in E. zhenbaensis especially during the T3 inter- et al.(2018a) demonstrated a strong allometric growth trough-increasing stage (complete development of ventral pattern in Eohadrotreta zhenbaensis by quantifying the intertrough, apical process, median septum and imprint of ontogenetic variations in size and shape in successive vascula lateralia; Z.-L. Zhang et al. 2018a,p.197)bythe ontogenetic stages. This also revealed that Palaeotreta rapid increase in the ventral intertrough length (Z.-L. zhujiahensis experienced three stages during the entire Zhang et al. 2018a). Nonetheless, this ontogenetic vari- ontogenetic sequence, which can be well compared with ation in stage T3 for P. shannanensis is completely lack- the almost coeval E. zhenbaensis (Fig. 10; Z.-L. Zhang ing, resulting in a very small ventral pseudointerarea and et al. 2018a; Claybourn et al. 2020). When compared to short intertrough (Fig. 2L, N). As the growth of the inter- the ontogeny of E. zhenbaensis, however, only two onto- trough is an important event in acrotretide brachiopods, genetic stages (T1–T2) can be distinguished during the the relatively slow development of the intertrough (c. growth of P. shannanensis (Figs 2, 6, 7). During the T1 1.6% length of ventral valve) in P. shannanensis results pedicle foramen-forming stage (pedicle opening is not in a change in inclination of the ventral pseudointerarea enclosed as a foramen and the ventral intertrough is not from catacline to apsacline, producing a low, cap-like developed; Z.-L. Zhang et al. 2018a,pp.187–191), the valve shape (Fig. 2J, O; Table 1). In contrast, the ventral shape of the ventral valve remains low and cap-like and valve of E. zhenbaensis becomes more conical with a the cardinal muscle scars, apical process and median sep- very long intertrough (c. 24.5% length of ventral valve) tum are vestigial (Figs 2A–H, 3A–G), while the incipient and the inclination of the ventral pseudointerarea changes 16 Z. Zhang et al. from catacline to procline during stage T3 (Z.-L. Zhang apical process and often a raised median septum in the et al. 2018a). Compared with the slightly older P. shanna- dorsal valve (Williams & Holmer 1992; Holmer & nensis, P. zhujiahensis demonstrates a relatively rapid Popov 1996, 2000; Williams et al 2000; Holmer et al. growth during ontogenetic stage T1, as the pedicle for- 2008). Recent studies have revealed that bearing an amen is enclosed at an earlier time when the ventral valve incipient pedicle notch in the juvenile, pitted meta- reaches 650 mm in length, contrasting with 1100 mminP. morphic shell and the presence of columnar shell struc- shannanensis. Thus, there is an earlier termination of tures in acrotretides demonstrates a close relationship shape change in the younger P. zhujiahensis during onto- with the oldest known lingulide brachiopods (Holmer & genetic stage T1 (Webster & Zelditch 2005). Moreover, Popov 1996; Ushatinskaya & Korovnikov 2014; Z.-L. the growth of the ventral pseudointerarea greatly decreases Zhang 2018; Z.-L. Zhang et al. 2018a, 2020). As the during ontogenetic stage T3 (increasing 0.8% of the position of the developing pedicle foramen in relation to length and 3.5% of the width of the ventral valve; Z.-L. the metamorphic shell is one of the most taxonomically Zhang et al. 2018a, appendix S3), producing a cap-like important characters in acrotretides (Rowell 1977; shape, catacline ventral pseudointerarea and posterior Holmer & Popov 2000; Topper et al. 2013; Z.-L. Zhang migration of the pedicle foramen outside of the meta- et al. 2018a), investigation of the ontogeny of the ped- morphic shell as well (Fig. 8G–N). The morphological icle foramen provides a new way of considering acrotre- similarity between the adult valves (650–1600 mm) of P. tide phylogeny. The incipient pedicle notch in juvenile zhujiahensis and juvenile valves (< 1110 mm) of P. shan- specimens of Palaeotreta during ontogenetic stage T1 is nanensis indicates paedomorphosis (progenesis) of P. zhu- interpreted to represent a similar ancestral type of pedicle jiahensis (Fig. 10;Z.-L.Zhanget al. 2018a). Thus, opening between the ventral and dorsal valves that occurs heterochrony plays an important role in the differentiation in linguliform brachiopods (Figs 6A–C,8A,B;seealso of species in the new genus Palaeotreta. Beecher 1891;Rowell1977; Popov 1992). The weakly Changes in shape through ontogeny and the different developed ventral pseudointerarea is comparable with the growth patterns in the two species of Palaeotreta may raised pseudointerarea above the valve floor in older lingu- correspond to subtle modification in life mode during lides such as Eoobolus (Ushatinskaya & Holmer 2001; the gradual cumulative increase in size (Gould 1966; Ushatinskaya & Korovnikov 2014;Z.-L.Zhanget al. Raup & Stanley 1971; Tomasovych et al. 2008; Baker 2020). In forming a high conical ventral valve, the cardinal & Logan 2011; Z.-L. Zhang et al. 2018a). However, the muscles move posteriorly to the raised pseudointerarea in life habit of extinct acrotretides is still not well under- acrotretides (Fig. 5A, B). During later ontogeny, the slow stood (Popov & Holmer 1994; Williams et al. 2000). growth of the intertrough results in a catacline pseudointer- Rare but exquisitely preserved fossils may suggest that area in P. zhujiahensis, whilst the lack of major growth of acrotretides attached to shell fragments or even to other the intertrough changes the pseudointerarea from catacline benthic animals like sponges to achieve secondarily to apsacline in P. shannanensis (Fig. 10). In contrast, the tiered niches (Mergl 2002; Holmer et al. 2005; rapid growth of the intertrough in E. zhenbaensis results in Henderson & Dann 2010; Wang et al. 2012; Topper a significant gradual transition of the ventral valve pseu- et al. 2015a, b). The low cap-like shape and apsacline dointerarea from catacline to procline (Fig. 10). The new ventral pseudointerarea indicate that P. shannanensis is evidence presented here supports the hypothesis that the likely to have had a mode of life similar to Treptotreta ventral intertrough in acrotretide brachiopods evolved by with a thin pedicle anchorage at the apex of the ventral the gradual and variable ‘rolling up’ of the lingulide prop- valve (Henderson & Dann 2010). The development of a areas along the posterior margin of the ventral valve in slightly longer intertrough whilst maintaining a catacline association with changes in the inclination of the ventral pseudointerarea in P. zhujiahensis may have aided stable intertrough (Popov 1992; Holmer & Popov 2000;Li& attachment to the substrate. Holmer 2004;Z.-L.Zhanget al. 2018a). A distinct evolutionary lineage from basal botsfordiids that developed an open delthyrium and vestigial ventral pseudointerarea to Phylogenetic implications more derived acrothelids which have an enclosed pedicle foramen and raised ventral pseudointerarea probably indi- The phylogenetic relationships of the Order Acrotretida cates that this monophyletic clade is derived from the lin- to other groups within the Class Lingulata are still gulides (Popov et al. 2015; Smith et al. 2016; Claybourn poorly resolved, though acrotretides possess many et al. 2020; Zhang et al. 2020). important unique characters, such as diminutive body There are three main positions of the pedicle foramen size, conical shape of the ventral valve with enclosed in the fossil record of acrotretides concerning its pos- pedicle foramen, simplified muscular system, developed ition related to the metamorphic shell. Type 1 is not A new acrotretide brachiopod genus from the Cambrian of South China 17 enclosed in the metamorphic shell, Type 2 is completely Tomasovych et al. 2008; Baker & Carlson 2010; Baker enclosed in the metamorphic shell and Type 3 is mostly & Logan 2011). These adaptations contributed to the located outside of the metamorphic shell. The first type, success of younger acrotretide brachiopods, especially where the pedicle foramen is partly enclosed in the during the transition from Cambrian Epoch 2 to Epoch metamorphic shell, occurred widely across genera begin- 3 and their subsequent radiation during the Great ning in Cambrian Epoch 2, such as Linnarssonia, Ordovician Biodiversification Event. Prototreta (or Homotreta), Eohadrotreta, Hadrotreta and Vandalotreta (Holmer & Popov 2000; Ushatinskaya 2010). The second and third types (Type 2–3), where Acknowledgements accelerated shell growth along the posterior margin of The authors would like to thank Zhifei Zhang from Northwest metamorphic shell resulted in anterior or posterior University for his original contribution to this project and migration of the pedicle foramen respectively, become valuable discussion. We are also grateful to Qingchun Feng common later in Cambrian Epoch 3 and the Ordovician for sample preparation in Xi’an, and Michael Streng at (e.g. Apsotreta and Scaphelasma; see also Holmer 1989; Uppsala University, Sue Lindsay and Chao Shen of the Holmer & Popov 2000; Topper et al. 2013; Popov et al. Microscopy Unit at Macquarie University for assistance with 2015). However, this is the first discovery of the Type 3 SEM imaging. Financial support for this project was during Cambrian Epoch 2 in Palaeotreta from South provided by Macquarie University Research Fellowships China (Figs 6, 9, 10). (2019 MQRF), National Natural Science Foundation of The morphological diversity amongst acrotretide bra- China (41425008, 41720104002, 41621003, 41890844), chiopods in Cambrian Stage 2 of South China includes Strategic Priority Research Program of Chinese Academy of great variation in the position of the pedicle foramen, Sciences (XDB26000000), Ministry of Science and 111 shell growth patterns and inclination of the ventral pseu- project of Ministry of Education of China (D17013), dointerarea (Fig. 10). The low cap-like shape, vestigial Zhongjian Yang Scholarship, Swedish Research Council apical process and median septum, very short inter- (VR 2018-03390), Opening Foundation of Shaanxi Key trough and longer pedicle foramen-forming stage (T1) Laboratory of Early Life and Environments and 1000 Talent probably imply that P. shannanensis is one of the ances- Shaanxi Province Fellowship. Financial support from the tral stocks of acrotretides. This is also supported by its China Scholarship Council (CSC 201806970026) for F.-Y. early occurrence in the Shuijingtuo Formation of south- Chen to have a 14-month study at Macquarie University is ern Shaanxi. Compared with the other two species P. acknowledged. We are also very grateful to Associate Editor zhujiahensis and E. zhenbaensis (Z.-L. Zhang et al. Rebecca L. Freeman and one anonymous reviewer whose 2018a), P. shannanensis has a more restricted distribu- constructive comments greatly improved the manuscript. tion and lower abundance, which may indicate this ancestral acrotretide was not suited to life in distal mixed clastic platforms. By contrast, E. zhenbaensis has ORCID more derived characters exemplified by faster growth rates during accretionary shell growth, especially during Zhiliang Zhang http://orcid.org/0000-0003-2296-5973 stage T3, enabling a wider geographical distribution and Lars E. Holmer http://orcid.org/0000-0003- increased abundance in shallow carbonate environments 3629-0049 (Li & Holmer 2004; Betts et al. 2017; Z.-L. Zhang Feiyang Chen http://orcid.org/0000-0001-8994-4187 et al. 2018a; Claybourn et al. 2020). The evidence pre- Glenn A. Brock http://orcid.org/0000-0002- sented here suggests evolutionary modification to onto- 2277-7350 genetic changes resulted in the early divergence of Palaeotreta and Eohadrotreta, and played an important role in the early evolution of acrotretides. The early Cambrian widespread acrotretides Hadrotreta and References Prototreta, developing a long ventral intertrough and Baker, P. G. & Carlson, S. J. 2010. The early ontogeny of dorsal median septum, may have a similar heterochronic Jurassic thecideoid brachiopods and its contribution to the process to E. zhenbaensis during the T3 intertrough- understanding of thecideoid ancestry. Palaeontology, increasing stage. Heterochrony also probably drove 53(3), 645–667. doi:10.1111/j.1475-4983.2010.00941.x rapid morphological variation in acrotretides, explaining Baker, P. G. & Logan, A. 2011. Support from early juvenile Jurassic, Cretaceous and Holocene thecideoid species for a their subsequent radiation and optimal adaptation across postulated common early ontogenetic development pattern a wide range of shallow marine depositional environ- in thecideoid brachiopods. Palaeontology, 54(1), 111–131. ments (Klingenberg 1998; Bassett et al. 1999, 2002; doi:10.1111/j.1475-4983.2010.01023.x 18 Z. Zhang et al.

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