Earliest Ontogeny of Early Cambrian Acrotretoid Brachiopods — First Evidence for Metamorphosis and Its Implications Zhiliang Zhang1,2, Leonid E
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Zhang et al. BMC Evolutionary Biology (2018) 18:42 https://doi.org/10.1186/s12862-018-1165-6 RESEARCHARTICLE Open Access Earliest ontogeny of early Cambrian acrotretoid brachiopods — first evidence for metamorphosis and its implications Zhiliang Zhang1,2, Leonid E. Popov3, Lars E. Holmer2,1 and Zhifei Zhang1* Abstract Background: Our understanding of the ontogeny of Palaeozoic brachiopods has changed significantly during the last two decades. However, the micromorphic acrotretoids have received relatively little attention, resulting in a poor knowledge of their ontogeny, origin and earliest evolution. The uniquely well preserved early Cambrian fossil records in South China provide a great new opportunity to investigate the phylogenetically important ontogeny of the earliest acrotretoid brachiopods, and give new details of the dramatic changes in anatomy of acrotretoid brachiopods during the transition from planktotrophic larvae to filter feeding sedentary juveniles. Results: Well preserved specimens of the earliest Cambrian acrotretoid brachiopods Eohadrotreta zhenbaensis and Eohadrotreta? zhujiahensis (Cambrian Series 2, Shuijingtuo Formation, Three Gorges area, South China) provide new insights into early acrotretoid ontogeny, and have significance for elucidating the poorly understood early phylogeny of the linguliform brachiopods. A more comprehensive understanding of the applied terminology based on new observation, especially in definition of the major growth stages (embryo, planktotrophic larva, post-metamorphically sessile juvenile and adult), is established. The so-called acrotretoid “larval shell” of both valves of Eohadrotreta demonstrates evidence for metamorphosis (shedding of the larval setae and transitions of shell secretion), during the planktotrophic stage. Therefore, it is here termed the metamorphic shell. The inferred early acrotretoid larval body plan included a bivalved protegulum, secreted at the beginning of the pelagic stage, which later developed two pairs of larval dorsal setal sacs and anterior–posterior alignment of the gut during metamorphosis. Conclusion: The primary larval body plan of acrotretoid Eohadrotreta is now known to have been shared with most early linguliforms and their relatives (including paterinates, siphonotretoids, early linguloids, the problematic mickwitziids, as well as many early rhynchonelliforms). It is suggested that this type of earliest ontogeny can be considered as plesiomorphic for the Brachiopoda and probably first evolved in stem group brachiopods with subsequent heterochronic changes. Keywords: Earliestontogeny,Metamorphosis,Acrotretoidea,EarlyCambrian,Heterochrony,SouthChina Background clades [1–6]. However, the micromorphic acrotretoids The outstanding early Cambrian fossil Lagerstätten of have received relatively little attention in these studies South China have had a major impact on our current [7–11]. The group first emerged in the fossil record to- understanding of the first brachiopods and other lopho- gether with other early lingulates in the Unnamed Cam- phorates; in particular, new information on their soft brian Stage 3, and went extinct in mid Devonian [2, 8]. body anatomy have been most valuable in tracing the Consequently, their origin, earliest evolution and on- initial radiation of major brachiopod and lophophorate togeny are still poorly known, and can be examined only based on the fossil record. * Correspondence: [email protected] The larval developments of living linguloid [12, 13], 1Shaanxi Key laboratory of Early Life and Environments and Department of discinoid [14, 15], terebratulid [16–19] and craniiform Geology, State Key Laboratory of Continental Dynamics, Northwest University, Xi’an 710069, China [20] brachiopods have been well documented with Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zhang et al. BMC Evolutionary Biology (2018) 18:42 Page 2 of 15 detailed accounts of their embryogenesis, fertilization, from one publication to other, and in particular common free swimming stage, and larval settlement. terms – including, the protegulum, embryonic shell, first Numerous previous studies have also shown that it is formed shell, larval shell, etc. – have been used in widely possible to discriminate planktotrophic and lecitho- different ways (compare, e.g. [24–27, 32, 38, 42]). trophic larval life histories in the earliest ontogenies of Moreover, our understanding of the ontogeny of fossil brachiopods, including extinct linguliforms [7, 21– Palaeozoic brachiopods has changed significantly in the 30], craniiforms [31, 32] and rhynchonelliforms [32–38]. last two decades, since the first brachiopod volume of The main objective of this paper is to provide the first the revised ‘Treatise on Invertebrate Paleontology, Part detailed account of the earliest ontogenetic development H, Brachiopoda’ [43] was published. The simplistic con- for two acrotretoid species Eohadrotreta zhenbaensis cept that recent (and probably extinct) linguliforms are and Eohadrotreta? zhujiahensis from the lower Cam- all planktotrophic, while craniiforms and rhynchonelli- brian Shuijingtuo Formation of the Three Gorges area in forms are lecithotrophic was challenged first by [27, 35], South China, which are among the earliest known repre- who advocated that lecithotrophy had evolved only in sentatives of the Acrotretoidea. Our results indicate that the crown group rhynchonelliform brachiopods. Subse- the acrotretoids had a metamorphic shell with two pairs quently planktotrophic larvae were described in the of dorsal setal sacs and a straight anterior–posterior gut orthoids [33], strophomenoids [44], orthotetidines [38, alignment – a type of ontogeny that has already been re- 44], polytoechioids [36]; however, at least some orthoids corded from other early Cambrian brachiopods and car- [34], clitambonitoids [36] and triplesioids were most rying important implications for the understanding of likely characterised by lecithotrophic larvae, which prob- their phylogeny and relationship to other brachiopod ably evolved independently from those in the crown lineages. Detailed information on the post-metamorphic group rhynchonelliforms. shell growth patterns of these species have been recently Lüter [45] pointed to the fact that lingulids are charac- investigated [39]. terised by having a direct development, and thus lost a ‘true’ larval stage. Indeed, the planktotrophic larvae of Methods Early Palaeozoic brachiopods, including both linguli- All specimens described and illustrated here are from the forms and rhynchonelliforms, have little in common Shuijingtuo Formation at Aijiahe section, Sandouping with living juvenile lingulids at their free swimming County in the Three Gorges area, South China ([40], stage (e.g. [24–26, 28, 29, 31, 32, 46–48]). Thus, a more Figure 1). The geological and geographical setting was de- comprehensive discussion of the applied terminology, scribed in detail by [5, 40]. A total of 75 conjunct valves, especially in definition of the major growth stages (em- 2536 ventral valves and 2517 dorsal valves of E. zhenbaen- bryo, planktotrophic larva, post-metamorphically sessile sis, and 23 conjunct valves, 102 ventral valves and 115 juvenile and adult) is needed. The most recent reviews dorsal valves of E.? zhujiahensis were found in the middle of the terminology currently applied to the morpho- and upper part of the Shuijingtuo Formation. The speci- logical characters observed on juvenile brachiopod shells mens were dissolved from limestones by applying 7% con- can be found in several publications e.g. [31, 35, 38, 39, centrated acetic acid, 63% water and 30% buffering 42], but here we follow the terminology of the two pa- solution formed after the dissolution of previous samples pers [38, 39]. to avoid chemical damage, as proposed by [41]. Scanning The earliest shell, identifiable through the brachiopod electron microscope (SEM) images of uncoated fossils ontogeny, is called protegulum. The term was first intro- were taken with a Philips Fei Quanta 400-FEG with 20 KV duced by [49] and traditionally was defined (e.g. [43]) as and 70–80 Pa at State Key Laboratory of Continental Dy- the ‘first-formed shell of periostracum and mineralised lin- namics, Northwest University, Xi’an. Some uncoated spec- ing secreted simultaneously by both mantles’. However, imens were taken to Sweden and SEM imaging was this definition is problematic due to the fact that there are carried out with a Zeiss Supra 35 VP field emission with 5 a large number of brachiopods (e.g. craniids, strophome- KV at the Evolutionary Biology Centre of Uppsala Univer- nates, siphonotretoids), in which the secretion of the ven- sity. No permissions were required for collecting of the tral valve is considerably delayed towards the end of fossils discussed in the study from the Shuijingtuo Forma- metamorphosis. Therefore, only the dorsal protegulum can tion at the Aijiahe