On the origin of animals
Erwin et al. review the fossil and molecular record of early animal evolution:
Molecular estimates suggest that the origin and earliest diversification of animals occurred during the Cryogenian Period. We estimate that the last common ancestor of all living animals arose nearly 800 Ma and that the stem lineages leading to most extant phyla had evolved by the end of the Ediacaran (541 Ma). Most phylum-level crown group divergences occurred coevally between the end of the Ediacaran and the end of the Cambrian (Figs. 1 and 3, large colored circles). This is the case both for taxa with robust fossil records (e.g., echinoderms, molluscs, arthropods) and those with sparse fossil records (e.g., nemerteans, nematodes). For taxa with robust fossil records, these coeval origination estimates are concordant with their first appearances in the rock record (Fig. 3), supporting both the general accuracy of our relaxed molecular clock analysis and the intuition of many paleontologists who argued that the known fossil record for crown groups of bilaterian phyla is largely robust (11)….
Much of this protein-coding repertoire—especially the developmental toolkit—is conserved throughout all metazoans and is even found today among single-celled opisthokonts (24, 52–54). The distribution of these genes in extant organisms (SOM text 3) implies that this toolkit evolved in a two-step pattern (Fig. 4, left): an initial diversification occurring at the base of the Metazoa before the split between sponges and eumetazoans deep in the Cryogenian (and possibly earlier), followed by a pronounced expansion at least in some families at the base of the Eumetazoa during the late Cryogenian (database S3). Thus, the last common ancestor of metazoans, and especially eumetazoans, was a genetically complex animal possessing all of the families of protein-coding genes used during development, save for the potential absence of Hox complex genes (55) needed to build the plethora of morphological structures found throughout the crown group….
Unlike the mRNA toolkit, which was largely established before the evolution of bilaterians (Fig. 4, left), miRNAs (database S4) seem to have been continuously added to eumetazoan genomes through time with very little secondary loss in most taxa (Fig. 4, right) (60). When loss did occur, it seems to have been associated with morphological simplification (20). For example, each of the extant animals put forth as putative biological models for late precambrian animals, including lophotrochozoan flatworms, acoel flatworms, and Xenoturbella (61), are characterized by extensive secondary loss of their miRNA complements as compared to more typical invertebrates like ambulacrarian deuterostomes, crustacean arthropods, and polychaete annelids (60). In contrast, large expansions in the number of miRNA families correlate to increases in the number of cell types and morphological complexity of animals, as seen, for example, at the base of the bilaterians and at the base of the vertebrates (60) (Fig. 4, right)….
Standard models of adaptive radiation (65) involve diversification from a single clade and cannot explain the polyphyletic nature, morphological and ecological breadth, or the extended duration of this event. Rather, we identify a suite of processes that facilitated the construction of biodiversity through positive feedback: ecosystem engineering of the environment, particularly by Cryogenian-Ediacaran sponges and later by burrowing bilaterians, and the formation of new ecological linkages including the evolution of zooplankton, which connected pelagic and benthic systems (64), and the advent of metazoan predation….
Predation was an important component of the growth of these ecological networks. The first appearance of predatory traces, and body fossils of predators, occurs near the Ediacaran-Cambrian transition (70). Animals evolved in response to predation pressures by developing novel defensive mechanisms such as biomineralized shells or developing new structures or capabilities that allowed movement into new habitats. The origin of predation can be assessed by mapping feeding modes onto the time-calibrated phylogeny (Fig. 3). Given the similarities between the sponge feeding cell (choanocyte) and choanoflagellates, the metazoan last common ancestor (LCA) was likely a microphagous suspension feeder, irrespective of whether sponges are monophyletic or not….
We see no evidence for a carnivorous lifestyle during the Cryogenian to mid-Ediacaran for any bilaterian lineage. Given that ecology and the physical environment are closely linked, it may be that the origin of animal carnivory, a metabolically expensive feeding strategy, was driven by increased oxygenation….
Our emerging understanding of early animal history shows that evolution is not always relentlessly opportunistic, taking advantage of evolutionary novelties as soon as they arise. Rather, the Cambrian explosion involved the construction of historically unique, and uniquely complex, feedbacks between biological potential and eco-environmental context, including the oxygenation of the ocean’s waters. These feedbacks relied on networks of gene regulatory interaction that were established long before the construction of metazoan ecosystems. Because of this long lag between the origin and eventual ecological dominance of clades, data on taxonomic occurrences alone are insufficient to understand evolutionary dynamics and must be accompanied by data on abundances and ecological impact, in addition to accurate and precise estimates of both evolutionary origin and geological first appearances. Macroevolutionary lags such as that which preceded the Cambrian explosion were not unique to animals, as similar dynamics seem to underlie plant evolution as well (24). Understanding both early animal and plant evolution requires an understanding of the processes that generate biodiversity and the expansion of ecological networks through deep time.
