Early Cambrian Protomelission is a scleritomous eumetazoan but not a bryozoan or dasyclad alga

doi:10.21203/rs.3.rs-2947902/v1

Download PDF

Biological Sciences - Article

Early Cambrian Protomelission is a scleritomous eumetazoan but not a bryozoan or dasyclad alga

https://doi.org/10.21203/rs.3.rs-2947902/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

The origin of Bryozoa has long been an intriguing mystery, largely due to the dearth of unambiguous bryozoan fossils within Cambrian strata1-5. Recently reported earliest bryozoan Protomelission 2, an early Cambrian phosphatized microfossil from Australia and China, was subsequently contested and proposed as calcified dasyclad algae1. Our re-analysis of raw micro-CT data from Protomelission specimens, however, unveils previously unrevealed structures, indicating Protomelission to be neither bryozoan nor alga, but almost a complete scleritome of Cambroclavus, an early Cambrian microfossil typically found as disarticulated sclerites. The long-awaited scleritomes suggest that enigmatic cambroclaves likely represent an extinct group of epitheliozoan-grade eumetazoan, with spiny sclerites covering their epidermis for defense. The prevalence of bizarre animals like cambroclaves, lacking modern analogues, implies a greater disparity of animal body plans during the Cambrian Explosion than previously understood. Our findings underscore the absence of definitive early Cambrian bryozoan fossils, further highlighting the dilemma of the origin of Bryozoa.

Biological sciences/Evolution/Palaeontology

Earth and environmental sciences/Solid Earth sciences/Palaeontology

Protomelission

origin of bryozoan

cambroclaves

dasyclad algae

micro-CT

Molecular clock estimates^6-8 and fossil records^9-11 both suggest that metazoans originated before Ediacaran and subsequently underwent evolutionary radiation during the Ediacaran-Cambrian transitional period, giving rise to nearly all extant animal phyla^10,12,13. However, no definitive bryozoans have been found in Cambrian fossil records^1-5, leaving the question of whether bryozoans originated during the Cambrian Explosion unresolved.

In 2021, Zhang et al.² interpreted Protomelission¹⁴, a phosphatized modular microfossil from early Cambrian strata in South Australia and South China, as a stem group bryozoan, suggesting that bryozoans emerged simultaneously with other animal phyla during the early Cambrian. However, this study has recently been challenged by Yang et al.¹, who reported a new type of Protomelission-like macrofossils from the early Cambrian Xiaoshiba biota, South China. Based on observing these macroscopic fossils, the authors reinterpreted the microscopic Protomelission as a calcified dasyclad alga¹. This new interpretation refutes the assertion of reliable bryozoan fossil records in early Cambrian strata, further obscuring the enigmatic origin of bryozoans.

The specimens described by Yang et al.¹ are typical of Burgess Shale-type macrofossils. The authors claimed that they exhibit similarity in overall morphology to the three-dimensionally phosphatized microfossils of Protomelission, such as similar arrangement of modules. However, it is difficult to make precise comparisons of anatomical details between fossils from the two distinct taphonomic windows due to preservational bias. To elucidate whether Protomelission represents bryozoans or calcified dasyclad algae, detailed investigations of the morphology and anatomical features of the phosphatized specimens of Protomelission are required. Therefore, we reanalyzed the raw micro-CT data published by Zhang et al.² and reconstructed the three-dimensional structure of Protomelission.

Our new reconstructions indicate that Protomelission represents a more complete scleritome of Cambroclavus, and the “zooids with openings” observed by Zhang et al.² are actually broken hollow sclerites of cambroclaves. The original appearance of Protomelission consists of arrays of imbricated, spiny sclerites arranged in a barrel-like shape. It exhibits apical-basal polarity, with a smaller base and a larger apex, representing an extinct benthic bilaterian, which is neither a bryozoan nor a dasyclad alga. Thus, no definitive bryozoan fossils can be confirmed in the early Cambrian strata. Whether bryozoans emerged synchronously with other animal phyla during the Cambrian Explosion remains an unresolved mystery.

Our reanalysis of the micro-CT data of two Protomelission specimens (SADME 10470, ELIXYB 4AN02) published by Zhang et al.² indicate that these millimeter-sized, erect specimens are composed of minute modules (Figs. 1-3; Extended Data Figs. 1-3). Each individual module exhibits more or less bilateral symmetry and has a dumbbell shape, with lateral swellings at both ends and a constriction in the middle (Fig. 1h-o; Extended Data Figs. 1, 2). These modules are arranged in an imbricated fashion along the longitudinal axis, forming a regular series of modules (Figs. 1a-j, 2a-c, Extended Data Figs.1, 2). Thanks to the morphology of the modules, adjacent parallel series can interlock almost seamlessly (Figs. 1a-c, 2a-c). The convex swelling at both ends of a module fits perfectly into the concave embayment (constriction) of the laterally adjacent modules (Fig.1c, 2c, Extended Data Figs. 1a, 1i, 2a, 2i). The two adjacent series of modules are displaced by a half-module length. Both the front and back sides of these two specimens preserve five parallel series of modules (Figs. 1a, 1b, 2a, 2b). These modular series ultimately assemble into a tightly integrated modular sheet.

Each module features an opening-like structure on its outer surface (Figs. 1, 2; Extended Data Figs. 1, 2). However, the "openings" of different modules exhibit considerable variation in size and morphology, with no discernible pattern (Fig. 1k-o; Extended Data Figs. 1, 2). This suggests that these "openings" are more likely artifacts of taphonomic origin, rather than biogenetic structures.

In specimen SADME 10470 (Fig. 1), the modular sheets on the front and back sides appear to be two separate layers that are back-to-back in the lateral view (Fig. 1d, e, r). However, this is likely due to damages occurred along the edges of the specimen. We precisely segmented all the modules in this specimen (Fig. 1, Extended Data Fig. 1). The morphology of the modules in the three central series is more or less bilaterally symmetrical (Fig. 1a-c, Extended Data Fig. 1c-e, h, k-m, p), while the outlines of the modules in the two series at the specimen's edges are incomplete (Fig. 1a-c; Extended Data Fig. 1b, f, g, j, n, o), appearing to be cut by the straight outer edges. In contrast, specimen ELIXYB 4AN02 has well-preserved outer edges on both sides without damage (Fig. 2a-e). Thus, in the lateral view, the modular sheets on the front and back of this specimen are hinged together (Fig. 2p). Therefore, the true form of the specimen is not a flat object composed of two separate, back-to-back modular sheets, but rather a barrel-shaped object enclosed by a single, continuous modular sheet. The flat morphology of the specimen SADME 10470 is likely a result of later compression.

A cavity within the two specimens can be clearly observed in both longitudinal and transverse sections (Figs. 1f, g, p, q; 2n, o). This cavity is also corroborated in top view (Fig. 2f). The swollen end of specimen ELIXYB 4AN02 (Fig. 2d, e), previously interpreted as a holdfast, actually inherits the original barrel-like shape.

In specimen ELIXYB 4AN02, we discovered some previously unrevealed spines (Fig. 2c, e, f-o). The segmented data show that they are typical sclerites of Cambroclavus^15,16, with two relatively well-preserved (Fig. 2g-k). Cambroclaves are enigmatic small shelly fossils that are quite common during the Cambrian period¹⁶. Their affinity has long been unclear^15,16. They are typically preserved as discrete sclerites (Fig. 3f-j; Extended Data Fig. 3p-t, w-z), but some are found as articulated sclerites (Extended Data Fig. 3aa-ac). For example, in some partially-preserved scleritomes of Cambroclavus, as well as those closely related to Cambroclavus, such as Deltaclavus and Deiradoclavus, longitudinally overlapping sclerites form regular series^15,16. Parallel series of sclerites interlock and can ultimately assemble into sclerite sheet similar to that of Protomelission (Extended Data Fig.3 ab-ad).

The modules of Protomelission are highly consistent with the morphology and size of the sclerites of Cambroclavus (Figs. 1-3; Extended Data Figs. 1-3). Statistical data indicates that their length-to-width ratios are also consistent (Extended Data Fig. 4). Considering that the "openings" on the outer surface of the modules in the two specimens are taphonomic artifacts, we propose that these modules are actually sclerites of Cambroclavus that have lost their spines secondarily. The discovery of spiny sclerites of Cambroclavus in specimen ELIXYB 4AN02 supports this interpretation.

In light of this interpretation, we combined the spiny sclerite with a partially preserved base (Fig. 2i) and modules that had lost their spines to obtain complete sclerites (Fig. 3a-e). These reconstructed sclerites look almost the same as the sclerites of Cambroclavus (Fig. 3f-j, Extended Data Fig. 3p-t). Following this pattern, we reconstructed all broken modules and the three-dimensional structures of the two specimens of Protomelission (Fig. 3k-t). The results reveal that the two specimens are, in fact, the long-awaited scleritomes of Cambroclavus absonus^15,16 (Extended Data Fig. 3ad). The two scleritome specimens are much more complete than all the scleritome specimens reported previously^15,16.

Considering that the outward-facing spines likely served a defensive function, we believe that the upward orientation of the spines is more probable. Therefore, based on the direction of the spines, the top and bottom of the specimens can be inferred. The reconstructions exhibit a conical shape, with a larger top and a smaller bottom (Fig. 3k-t). The swollen end in specimen ELIXYB 4AN02, previously interpreted as a holdfast, is actually closer to the individual's apex rather than a true holdfast. A cavity develops in the middle of the conical body. It is worth noting that the specimen ELIXYB 4AN02 exhibit typical soft deformation (Fig.2d, p), indicating that it was not fully mineralized hard skeleton before phosphatization, but was likely weakly mineralized.

Based on the available data, we have summarized the morphology and anatomical features of this organism. It possesses an inverted cone-shaped body, with spiny sclerites covering its epidermis for defense. As the individual grows upward and increases in size, the sclerite chains proliferate through branching, transitioning from five chains to seven or even more². Moreover, in a single sclerite series, the newly produced upper sclerites become longer and wider (Fig. 1k-o, Extended Data Figs. 1c-d, k-m, 2b-f, k-n, 4b-d) but maintaining the same length-to-width ratio (Extended Data Fig. 4a, b), while growth, thus preserving the identical morphology between them.

Reappraising the competing interpretations of Protomelission

In their study, Zhang et al.² posited that the key evidence for interpreting Protomelission as a bryozoan lies in the conceptualization of each module (i.e., sclerite) as a "zooid with an opening." However, these so-called "zooids" are, in fact, hollow sclerites of Cambroclavus. The "openings" appear to be artifacts resulting from taphonomic processes, a preservational status commonly observed in cambroclave sclerites^15,16. These findings thoroughly refute the bryozoan interpretation. Similarly, Yang et al.¹ contended that the "zooid with an opening" is a taphonomic artifact, thereby excluding the possibility that they are bryozoans. Therefore, the enigmatic question of whether bryozoans emerged synchronously with other phyla during the Cambrian Explosion remains unresolved.

Given that Protomelission is not a bryozoan, the question arises as to what type of organism it truly represents. Yang et al.¹ compared Protomelission with a type of new macrofossils from the Xiaoshiba biota and concluded that they represent the same type of organism, preserved in different taphonomic windows. Therefore the authors assigned the Xiaoshiba macrofossils into Protomelission and interpreted them as calcified dasyclad algae¹. They had already recognized the significant differences in anatomy between the Xiaoshiba macrofossils and the cambroclaves, leading them to propose that the latter are relatives of Protomelission, representing a more strongly calcified form of dasyclad-like algae¹.

However, the new three-dimensional reconstructions presented in this study do not support the interpretation put forth by Yang et al.¹ Firstly, Protomelission gatehousei represents, in fact, a relatively well-preserved scleritome of Cambroclavus absonus. Protomelission gatehousei is therefore a junior synonym of Cambroclavus absonus. They are not relatives but the same species. Secondly, both extant and fossil dasyclad algae exhibit a honeycomb-like appearance (Extended Data Fig. 5), with their external surfaces composed of polygonal lateral heads (PLHs)^17,18. Unlike the cambroclave sclerites, these PLHs are not arranged in an imbricated fashion^17,18. Thirdly, the inner surface of the PLHs in dasyclad algae is connected to the central axis via an aperture^1,17,18, while each complete cambroclave sclerite is, in fact, closed off, with no internal or external openings(Figs. 1h-j; 3a-e)^15,16,19,20. Finally, the elongated, soft flanges on the PLHs of dasyclad algae are nonmineralized^1,17,18, in contrast to the short, stout mineralized spines found on sclerites of cambroclaves^15,16,19,20. In summary, Yang et al.’s proposal¹ that Protomelission and cambroclaves represent different taxa, as weakly and strongly calcified dasyclad algae respectively, lacks sufficient anatomical evidence for support.

Proposed affinity of Protomelission (= Cambroclavus)

As no complete soft tissues or organs of cambroclaves have been discovered to date, previous discussions of their phylogenetic affinity have largely remained speculative^15,16,19,20. However, the consensus is that cambroclaves represent a type of metazoan adorned with spiny sclerites on its surface^15,16. Here, we propose that they represent erect cone-shaped organisms, living a benthic and sessile lifestyle. Their epidermic integuments were completely covered with a suite of dumbbell-shaped, spiny sclerites for defense, while their internal cavity provided space for soft tissues and organs. Such complexity suggests that Protomelission (= Cambroclavus) represents at least an epitheliozoan-grade eumetazoan.

Like the enigmatic contemporaneous chancelloriids^21,22 and other problematic animals (e.g. halkieriids and wiwaxiids)^23-29, sclerite-covering Cambroclavus represents an extinct enigmatic animal with no extant analogues. The Cambrian Explosion witnessed the emergence of numerous problematic animals that are difficult to assign to extant phyla, indicating that the disparity of animal body plans during this period far exceeded that of the modern era^30,31. In this context, the absence of bryozoan fossils in early Cambrian strata becomes even more prominent.

The fossil materials and data analyzed in this study are derived from the work of Zhang et al.² Information on the sample localities and stratigraphic sections can be found in their paper. Temporally, these two fossils likely originate from the Cambrian Series 3, contemporaneous with the Chengjiang biota. We re-analyzed the raw micro-CT data of the two specimens using VGStudio Max 3.5. The processed data, along with the rendering models can be found in GBDB database at https://doi.org/XXXX/fossilontology.XXXX.

Acknowledgment

We would like to thank Dr. Zhang Zhiliang for providing the raw volume data of the two specimens of Protomelission. This work is founded by the National Key Research and Development Program of China (2022YFF0800100), the National Natural Science Foundation of China (42022010, 41921002), and the Youth Innovation Promotion Association of the CAS.

Authors’ Contributions

Z.Y. designed the research; Z.Y., K.X., W.L., F.Z., and M.Z. performed research; K.X. and W.L. processed the tomographic data supervised by Z.Y.; Z.Y. wrote the paper with inputs from all the other authors.

Competing interests

The authors declare that they have no competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Data availability

The datasets generated and/or analysed during the current study are available on the 3D model database of NIGPAS at https://doi.org/XXXX/fossilontology.XXXX.

Yang, J., Lan, T., Zhang, X. G. & Smith, M. R. Protomelission is an early dasyclad alga and not a Cambrian bryozoan. Nature (2023). https://doi.org:10.1038/s41586-023-05775-5
Zhang, Z. et al. Fossil evidence unveils an early Cambrian origin for Bryozoa. Nature 599, 251-255 (2021). https://doi.org:10.1038/s41586-021-04033-w
Taylor, P. D., Berning, B. & Wilson, M. A. Reinterpretation of the Cambrian ‘bryozoan’ Pywackia as an octocoral. Journal of Paleontology 87, 984-990 (2015). https://doi.org:10.1666/13-029
Taylor, P. D., Waeschenbach, A. & Smith, A. Phylogeny and diversification of bryozoans. Palaeontology 58, 585-599 (2015). https://doi.org:10.1111/pala.12170
Hageman, S. J. & Ernst, A. The last phylum: Occupation of Bryozoa morpho-ecospace (colony growth habits) during the early phase of the Great Ordovician Biodiversification Event. Palaeogeography, Palaeoclimatology, Palaeoecology 534 (2019). https://doi.org:10.1016/j.palaeo.2019.109270
Cunningham, J. A., Liu, A. G., Bengtson, S. & Donoghue, P. C. The origin of animals: Can molecular clocks and the fossil record be reconciled? Bioessays 39, 1-12 (2017). https://doi.org:10.1002/bies.201600120
dos Reis, M. et al. Uncertainty in the Timing of Origin of Animals and the Limits of Precision in Molecular Timescales. Current Biology 25, 2939-2950 (2015). https://doi.org:10.1016/j.cub.2015.09.066
Budd, G. E. & Mann, R. P. Survival and selection biases in early animal evolution and a source of systematic overestimation in molecular clocks. Interface Focus 10 (2020). https://doi.org:10.1098/rsfs.2019.0110
Zhang, X. & Shu, D. Current understanding on the Cambrian Explosion: questions and answers. PalZ (2021). https://doi.org:10.1007/s12542-021-00568-5
Budd, G. E. & Jackson, I. S. Ecological innovations in the Cambrian and the origins of the crown group phyla. Phil. Trans. R. Soc. B 371, 20150287 (2016).
Budd, G. E. The cambrian fossil record and the origin of the phyla. Integr Comp Biol 43, 157-165 (2003). https://doi.org:10.1093/icb/43.1.157
Erwin, D. H. Was the Ediacaran-Cambrian radiation a unique evolutionary event? Paleobiology 41, 1-15 (2015). https://doi.org:10.1017/pab.2014.2
Erwin, D. H. et al. The Cambrian Conundrum: Early Divergence and Later Ecological Success in the Early History of Animals. Science 334, 1091-1097 (2011). https://doi.org:10.1126/science.1206375
Brock, G. A. & Cooper, B. J. Shelly fossils from the Early Cambrian (Toyonian) Wirrealpa, Aroona Creek, and Ramsay Limestones of South Australia. Journal of Paleontology 67, 758-787 (2016). https://doi.org:10.1017/s0022336000037045
Morris, S. C. & Chen, M. Cambroclaves and paracarinachitids, early skeletal problematica from the lower Cambrian of South China. Palaeontology 34, 357–397 (1991).
Bengtson, S., Conway Morris, S., Cooper, B. J., Jell, P. A. & Runnegar, B. N. Early Cambrian fossils from South Australia. Association of Australasian Palaeontologists Memoir 9, 1-364 (1990).
Beadle, S. C. Dasyclads, cyclocrinitids and receptaculitids: comparative morphology and paleoecology. Lethaia 21, 1-12 (1988).
Berger, S. Photo-Atlas of living Dasycladales. (Carnets de Geologie, 2006).
Na, L., Li, G. Nail-shaped sclerite fossils from the lower Cambrian Xihaoping Member of Fangxian, Hubei Province. Acta Micropalaeontologica Sinica 28, 284-300 (2011).
Qian, Y. Early Cambrian small shelly fossils of China with special reference to the Precambrian-Cambrian Boundary. (Nanjing University Press, 1989).
Yun, H., Zhang, X., Brock, G. A., Li, L. & Li, G. Biomineralization of the Cambrian chancelloriids. Geology 49, 623-628 (2021). https://doi.org:10.1130/g48428.1
Cong, P. Y. et al. Naked chancelloriids from the lower Cambrian of China show evidence for sponge-type growth. Proc Biol Sci 285 (2018). https://doi.org:10.1098/rspb.2018.0296
Jensen, S., Gehling, J. G. & Droser, M. L. Ediacara-type fossils in Cambrian sediments. Nature 393, 567-569 (1998). https://doi.org:10.1038/31215
Caron, J. B., Scheltema, A., Schander, C. & Rudkin, D. A soft-bodied mollusc with radula from the Middle Cambrian Burgess Shale. Nature 442, 159-163 (2006). https://doi.org:10.1038/nature04894
Morris, S. C. & Caron, J. B. Halwaxiids and the early evolution of the lophotrochozoans. Science 315, 1255-1258 (2007). https://doi.org:10.1126/science.1137187
Pates, S., Wolfe, J. M., Lerosey-Aubril, R., Daley, A. C. & Ortega-Hernandez, J. New opabiniid diversifies the weirdest wonders of the euarthropod stem group. Proc Biol Sci 289, 20212093 (2022). https://doi.org:10.1098/rspb.2021.2093
Shu, D. G. et al. Lower Cambrian vendobionts from China and early diploblast evolution. Science 312, 731-734 (2006). https://doi.org:10.1126/science.1124565
Zhang, Z., Smith, M. R. & Shu, D. New reconstruction of the Wiwaxia scleritome, with data from Chengjiang juveniles. Sci Rep 5, 14810 (2015). https://doi.org:10.1038/srep14810
Zhao, F. et al. Orthrozanclus elongata n. sp. and the significance of sclerite-covered taxa for early trochozoan evolution. Sci Rep 7, 16232 (2017). https://doi.org:10.1038/s41598-017-16304-6
Briggs, D. E. G. & Fortey, R. A. Wonderful strife: systematics, stem groups, and the phylogenetic signal of the Cambrian radiation. Paleobiology 31, 94-112 (2005). https://doi.org:Doi 10.1666/0094-8373(2005)031[0094:Wsssga]2.0.Co;2
Briggs, D. E. The Cambrian explosion. Current Biology 25, R864-R868 (2015).
Li, L., Zhang, X., Yun, H. & Li, G. New occurrence ofCambroclavus absonusfrom the lowermost Cambrian of North China and its stratigraphical importance. Alcheringa: An Australasian Journal of Palaeontology 40, 45-52 (2015). https://doi.org:10.1080/03115518.2015.1085749

There is NO Competing Interest.

ExtendedDataFig.1.tif
Extended Data Fig. 1 | Microtomographic reconstruction of Protomelission gatehousei from Australia (SADME 10470). a, Front view showing segmented modules. The numbers label different rows. b-f, Five modular chains from a. g, Front view showing two modular chains along the edge. h, Front view showing three central modular chains. c1-e3, Individual modules from different columns and rows. i, o, p, Back view showing modular chains. j-n, Five modular chains from i. k1-m4, Individual modules from different columns and rows.
ExtendedDataFig.2.tif
Extended Data Fig. 2 | Microtomographic reconstruction of Protomelission gatehousei from South China (ELI XYB4 AN02). a, Front view showing segmented modules. The numbers label different rows. b-f, Five modular chains from a. g, Front view showing two modular chains along the edge. h, Front view showing three central modular chains. i, o, p, Back view showing modular chains. j-n, Five modular chains from i. c1-m4, Individual modules from different columns and rows.
ExtendedDataFig.3.tif
Extended Data Fig. 3 | Reconstructed modules of Protomelission and discrete sclerites of Cambroclavus. a-o, reconstructions of 15 modules of specimen SADME 10470. p-t, discrete sclerites of Cambroclavus (reproduced from ref.) . u, v, a sclerite from ELI XYB4 AN02, showing the internal structure. w-z, discrete sclerites of Cambroclavus, reproduced from ref.¹⁶. aa, two sclerites (Cambroclavus absonus), reproduced from ref.¹⁶. ab, ac, articulated series of sclerites (Deltaclavus graneus), reproduced from ref.¹⁵ ad, Hypothetical reconstruction of partial portions of the scleritome of Cambroclavus absonus (reproduced from ref.¹⁶).
ExtendedDataFig.4.tif
Extended Data Fig. 4 | Plots of module size of Protomelission and sclerites of Cambroclavus. a, Boxplot of length/width ratio of modules of Protomelission and sclerites of Cambroclavus. b, Scatter diagram showing length and width of modules of Protomelission and sclerites of Cambroclavus. c, Scatter diagram showing length and width of well-preserved modules from specimen SADME 10470. d, Scatter diagram showing length and width of well-preserved modules from specimen ELI XYB4 AN02. The size of sclerites of Cambroclavus absonus and Cambroclavus fangxianensis were collected from ref.^16,19,20,32
ExtendedDataFig.5.tif
Extended Data Fig. 5 | Extant and fossil dasyclad algae. a, Bornetella oligospora, extant, an immature cell. b, Neomeris annulata, extant, a mature cell. c, d, magnifications of the boxed areas in a and b, respectively. e, Fossil dasyclad alga Receptaculites biconstrictus from Middle Ordovician. f, Fossil dasyclad alga Cyclocrinites pyriformis from Middle Ordovician. a and b were reproduced from ref.¹⁸ e and f were reproduced from ref.¹⁷

Download PDF

Version 1

posted

You are reading this latest preprint version

Early Cambrian Protomelission is a scleritomous eumetazoan but not a bryozoan or dasyclad alga

Status:

Version 1

Abstract

Figures

Introduction

Results

Discussion

Materials and methods

Declarations

References

Additional Declarations

Supplementary Files

Status:

Version 1