Possible taphonomic and sampling biases

Taphonomic studies have shown that the fossil record can test the proposition that marine community structure has changed over time67,68. Ediacaran to Cambrian skeletal lophotrochozoans are represented by taxa of comparable millimetric sizes, forming part of the small shelly fauna as shells and disarticulated sclerites. These fossils are generally either replaced by phosphate or present in the form of inner and outer moulds. Only lingulate brachiopods and tommotiids are preserved as original shells, and only rhynchonelliform brachiopods retain their original low-Mg calcite mineralogy. In the lower Cambrian of the Siberian Platform, such fossils are restricted to argillaceous limestones (mostly wackestones and packstones), and some grainstones, all of which accumulated onshore above either normal wave or storm wave base69. All fossils are extracted by the same method of dissolution in buffered acetic acid to isolate phosphatic and phosphatized shells, or moulds and steinkerns (e.g.29). Worker bias is unlikely given that the assemblages reflect multiple different studies and no single worker or study dominates. We infer that taphonomic biases are minimized, and sampling biases present are shared by all small skeletal fossils.

Trends through time

Total lophotrochozoan biodiversity increases until the middle of Stage 2, but then there is a notable decline that extends to approximately the middle of Stage 3 (Fig. 3B). This interval coincides in part with an expansion of anoxic sea floor around ~525 Ma inferred from U isotopes70. Stem- and crown group lophotrochozoan species show distinctly different temporal distributions, with stem group lophophorate, brachiopod and mollusc taxa originating and radiating first. The preferential extinction of stem group species in early Cambrian Stage 4, at ~513 Ma coincides with the well-known Sinsk Event, an episode of widespread shallow marine anoxia on the Siberian Platform and other locations globally, which also coincides with the major extinction of the Archaeocyatha71. It is probable that Archaeocyatha represent a poriferan stem group, and indeed a similar temporal separation of stem and crown group diversification is observed among other metazoans at phyla level, including the Porifera (where crown group demosponges are known by Cambrian Stage 3), Cnidaria and Echinodermata54,72,73,74.

The first probable metazoan body fossils (rangeomorphs) appeared at ~570 Ma75. Rangeomorphs are complex, macroscopic eukaryotes, probably stem group metazoan taxa, although an affinity higher than Porifera has been proposed76. Rangeomorph-dominated assemblages were devastated by the Kotlin Crisis, which marks a turnover event15. After this we propose two phases of the Cambrian Explosion separated by the Sinsk Event extinction. The first was dominated by non-bilaterians (Porifera, Cnidaria and Ctenophora) joined by indeterminate bilaterian stem groups at ~ 560 Ma18 and lasted until ~513 Ma. The general increase in diversity may have been interrupted by the global expansion of anoxic sea floor around ~525 Ma. Notably, this diversification started before, and continues across, the Ediacaran/Cambrian boundary and the Basal Cambrian Carbon Isotope Excursion (BACE) interval (~541 to ~540 Ma). The BACE has been ascribed to a possible global perturbation of the carbon cycle12.

The second phase was marked by radiating non-bilaterian and bilaterian (here determined as brachiopod and mollusc) crown group species, and started from ~513 Ma. This second radiation phase may have been interrupted or even terminated by the late Cambrian SPICE event, which marked a further minor extinction (Fig. 4). Crown groups brachiopod species continued to diversify during the remainder of the Cambrian and into the Ordovician. Bivalves and gastropods also formed a significant part of total global lophotrochozoan diversity and were joined by the appearance of bryozoans and cephalopods around the Cambrian/Ordovician boundary77,78. From that time onwards their diversity remained higher than stem group lophotrochozoans, which continued to decline dramatically during the Cambrian51,59,71,79,80. The last stem group taxa (a few hyolith genera) went extinct in the Permian81.

Figure 4 Schematic of hypothesised non-Bilaterian (total group Porifera, Cnidaria and Ctenophora) and Bilaterian diversification during the Ediacaran-Cambrian metazoan radaition, showing the fossil record of probable earliest metazoans (shown by a rangeomorph reconstruction), the Kotlin crisis, followed by two phases of Cambrian Explosion, separated by the Sinsk Event extinction (with a possible expanded interval of anoxia during Phase 1) and extending to the Ordovician Radiation through the SPICE extinction. Non-bilaterian stem group example is a stem group archaeocyath sponge; crown group is a crown group demosponge. Bilaterian stem group is shown by a tommotiid; crown group by a trilobite. Full size image

The Sinsk Event might therefore be considered a mass extinction, which appears to have preferentially removed skeletal stem group lophotrochozoans at a point when diversity was high. This rapid removal is in contrast to background extinctions that are expected to erode the base of a clade gradually through time. We note that crown group brachiopod and mollusc do not show a marked increase in diversity after the removal of stem group lophophorate, brachiopod and mollusc taxa, but continue their former diversity trajectory. This suggests that their radiation was not dependent upon the removal of incumbent stem group taxa, but rather that crown group taxa were in some way more resilient to shallow marine anoxia or other coeval environmental perturbations. Like other mass extinctions, the Sinsk Event led to significant and long-lasting changes in taxonomic composition and ecosystems22,79,82.

A similar sequential faunal replacement pattern of Phanerozoic metazoans has been established in the form of evolutionary marine faunas83, which are in part bounded by mass extinctions. During the Ediacaran to Cambrian interval, further distinguished were the Tommotian, Cambrian s.s. and Palaeozoic faunas84. All these faunas were discriminated by empirical and statistical analysis of family diversity patterns only without reference to phylogenetic relationships. Their existence was, however, challenged22 because their speciation/extinction trends could merely reflect replacement between major taxonomic groups that had coupled dynamics. But our analysis shows that evolutionary faunas may in fact be a manifestation of their composition, with the ‘Tommotian’ fauna being composed of mostly stem group lophotrophorates, molluscs and brachiopods, while the Cambrian s.s. and Palaeozoic faunas are dominated by crown group representatives of molluscs, brachiopods and many other phyla.

This pattern resembles the extinction of taxa at the Permo-Triassic boundary, when groups that originated in the early Palaeozoic either went extinct (tabulate and rugose corals, trilobites, cystoporates) or significantly declined (brachiopods, trepostomates, cryptostomates, conodonts) never to recover previous levels of diversity85. This is in contrast to the pattern shown by groups which appeared and diversified in the late Palaeozoic, such as gymnolaemates and new bivalve, gastropod and ammonoid orders85,86,87.

If ecological niches are relevant, the difference in maintaining the two phases of the Cambrian Explosion might be related to differences in ecospace that was actually “empty” for skeletal animals. During the earlier phase of stem taxa radiation (~543–513 Ma), speciation was most likely promoted by the lack of competition for existing niches. This is similar to the high rates of sympatric speciation, such as noted among modern benthic caenogastropods in lakes, where high phenotypic plasticity enables evolving ecophenotypes to diversify into different substrates (e.g.88). A similar pattern of early diversification as a result of adaptations to different substrates is shown by both helcionelloid mollusc and archaeocyath sponge species during the first phase of the Cambrian Explosion inferred here. The helcionelloids underwent rapid morphogenesis89, and archaeocyaths display extremely high inter-habitat diversity (that is, beta-diversity) in reef communities on the Siberian Platform90, which may also reflect high speciation rates. Niche partitioning is not inferred, as the alpha-diversity (species number per community) remains consistently low91. A similar effect as a result of low competition, and also correlated with a rise in beta-diversity, has been observed to be the main driver of general diversity increase in the early Cambrian92. This dynamic creates the unusual situation when the boundaries of even major lower Cambrian subdivisions have not been established due to an absence of cosmopolitan species. By contrast, even though stem group diversity was significantly reduced during the later crown group brachiopod and mollusc diversification (~513–508 Ma), older niches were not completely eliminated. Thus, in the aftermath of the Sinsk extinction, crown groups were able to diversify via competition for existing niches in order to incorporate into existing communities.