Animal origins: The record from organic microfossils

Accumulated records of organic microfossils span billions of years of Earth history. The majority of this record consists of prokaryotes plus eukaryotes of a protistan grade, yet this type of fossilisation is also capable of capturing the organically preserved remains of animals. Recently, it has become apparent that non-biomineralizing animal groups, otherwise known only from rare instances of exceptional fossilisation, can preserve in this fashion. Given this high taphonomic fidelity combined with the temporal continuity of organic microfossil preservation, it is clear this style of fossilisation has the potential to circumvent some of the major biases that afflict the current early animal fossil record. Despite this, there have been no attempts to survey recorded instances of animal-derived organic microfossils. We constructed a global database comprising 394 studies of organic microfossils covering 399 sedimentary rock formations spanning the Tonian–Cambrian Stage 5/Wuliuan Stage (1 Ga to 505 Ma). The database consolidates scattered reports and provides a first appraisal for how a record of metazoans emerges within the broader archives of organic microfossils. Scrutiny of the current record reveals that organic microfossils contain the oldest body fossil evidence for a number of key metazoan clades, including the Chaetognatha, Annelida, Priapulida, ‘lobopods’ and Panarthropoda, Crustacea, Pterobranchia, and potentially even the Bilateria. Also detected among this record are the fossilised remains of poriferans, chancelloriids, palaeoscolecids, loriciferans, bradoriids, trilobites, wiwaxiids, molluscs, hyoliths, brachiopods and chordates. Our data shows that metazoan-derived remains are relatively common constituents of palynological preparations from sediments of a Cambrian age or younger. Such metazoan remains are also detected in organic microfossil assemblages from several formations of late Ediacaran age, but are entirely absent from the large number of equivalent preparations from older sediments, throughout the Proterozoic. In this view, signs of animal diversification emerge as a unidirectional signal embedded within a deeper record of organic microfossils. We argue here that the absence of animal remains among the large number of equivalent studies from Tonian, Cryogenian and early Ediacaran strata weakens the case for the existence of a cryptic animal biosphere during the Tonian and Cryogenian.