Phylochronology of early metazoans: combined evidence from molecular and fossil data

Abstract

Timing the evolutionary appearances of early Metazoa on Earth may rely on the combined information of fossil occurrences, molecular divergences and the geological background. Recent advances in the studies of Neoproterozoic and earliest Cambrian strata in South China and elsewhere, together with numerous works on molecular dating, provide an opportunity to draw a more precise timescale for the early metazoan evolution. This study presents a synthesis of available molecular and fossil dating results, placed in the palaeoenvironmental background, which leads to the recognition of the following time events for early metazoan cladogenesis: (1) Animal multicellularity occurred most probably during early to middle Neoproterozoic times (between $1000 and $660 Ma) during the geological period of gradual increase in oxygen content; (2) Eumetazoans and sponges (or sponge-like organisms) parted from each other during the Neoproterozoic glaciation interval (ca. 750-580 Ma), but both experienced adaptive radiation after the glaciations as evidenced by the Doushantuo Biota (ca. 635-551 Ma); (3) A great metazoan radiation event (MRE) occurred during the late Ediacaran and earliest Cambrian periods (ca. 550-530 Ma), interpreted here as a metazoan radiation at higher taxonomic levels, as compared with the early Cambrian radiation representing one at lower taxonomic levels (lower than subphylum or class). In order to better constrain the phylochronology of early metazoans, we present evidence for the divergences of arthropod subgroups on the basis of molecular dating results and the fossil record. It is shown that the arthropod stem group diverged from its sister taxon at between $700 and $565 Ma and major arthropod subgroups originated coevally with MRE. The MRE is probably correlatable with the d 13 C negative anomaly in the late Ediacaran Period.Although the phylochronology of early Metazoa is gradually emerging, a great deal of research still will be needed in the following directions in order to reduce uncertainties in, and discrepancies among, dating results: (1) Evaluate different molecular dating techniques so as to establish a proper set of standard procedures for dating early metazoan events; (2) Set up a standard set of fossil calibration points suitable for dating early metazoan divergences; (3) Use both molecular and fossil constraints as far as possible; (4) Place the time sequence in the geological and palaeoecological background so that one can visualize a logical evolutionary scenario. We suggest that the fossil record plus the geological background should serve to construct a general timeframe for evolution, while molecular dating will supplement and probably increase the precision of the chronology.

Molecular dating of the blood pigment hemocyanin provides new insight into the origin of animals

“…The emergence of the Hc superfamily during the Neoproterozoic Era corroborates modern molecular dating of an age between 1,000 and 650 Ma for the origin of metazoans (Dohrmann & Wörheide, 2017;Erwin et al, 2011;Lozano-Fernandez et al, 2017;Peterson et al, 2004;Qun et al, 2007;dos Reis et al, 2015). In addition, these results suggest that earlybranching animals may have already possessed blood pigments (Hc-like), which may have enhanced their respiratory capacity in a hypoxic environment at that time.…”

“…Fossil records of early animal life have generated considerable controversy over the years, especially when they conflict with timings based on molecular clock estimates (Budd & Mann, 2020a, 2020b. Current estimates for molecular origins for crown-group Metazoa range from 1,000 Ma to 615 Ma (Dohrmann & Wörheide, 2017;Peterson et al, 2004;Qun et al, 2007;dos Reis et al, 2015). From a biological perspective, the fossil record provides the only direct insight into evolutionary history (Wood et al, 2020); however, with recent advancements of molecular clock methodologies, estimates of divergence of major animal lineages are becoming more accurate, and the disparity between molecular dating and fossil evidence of clade age minima has reduced (dos Reis et al, 2015).…”

Decline and fall of the Ediacarans: late‐Neoproterozoic extinctions and the rise of the modern biosphere

“…However, recent analyses based on exceptionally preserved soft tissues (Hoyal Cuthill & Han, 2018) and developmental patterns (Dunn, Liu & Donoghue, 2018;Dunn et al, 2019bDunn et al, , 2021Dunn, Liu & Gehling, 2019a) suggest that at least some Ediacarans may lie on the stem of Eumetazoathe clade of tissue-grade animals comprising the vast majority of present-day metazoan biodiversity (Runnegar, 2022). As the earliest credible palaeontological window on animal evolution, the Ediacaran Biota illuminates its tempo and mode, helping to reconcile fossil evidence with molecular clocks hinting at a cryptic Neoproterozoic (1000-539 Ma) history (Cunningham et al, 2017;Yang et al, 2007). This Neoproterozoic rise of animals unfolded amid some of the most pronounced biogeochemical upheavals in Earth history (Butterfield, 2015b).…”

Different phylogenomic methods support monophyly of enigmatic ‘Mesozoa’ (Dicyemida + Orthonectida, Lophotrochozoa)

“…The early radiation of Lophotrochozoa (549–535 Ma; [13]), a major clade of protostome metazoans including annelids, molluscs, brachiopods, bryozoans, flatworms and rotifers among others, has been especially challenging to uncover [5,8,9,14,15]. This is probably owing to relatively rapid diversification [16] and fast evolutionary rates in some lineages, leading to long terminal branches in phylogenetic analyses possibly prone to LBA.…”