The Cambrian Conundrum: Early Divergence and Later Ecological Success in the Early History of Animals

Abstract

Diverse bilaterian clades emerged apparently within a few million years during the early Cambrian, and various environmental, developmental, and ecological causes have been proposed to explain this abrupt appearance. A compilation of the patterns of fossil and molecular diversification, comparative developmental data, and information on ecological feeding strategies indicate that the major animal clades diverged many tens of millions of years before their first appearance in the fossil record, demonstrating a macroevolutionary lag between the establishment of their developmental toolkits during the Cryogenian [(850 to 635 million years ago (Ma)], and the later ecological success of metazoans during the Ediacaran (635 to 541 Ma) and Cambrian (541 to 488 Ma) periods. We argue that this diversification involved new forms of developmental regulation, as well as innovations in networks of ecological interaction within the context of permissive environmental circumstances.

Ediacaran developmental biology

“…Initially, many Ediacaran taxa were considered members of extant animal clades (e.g. Glaessner, 1984), but more recently they have instead been grouped according to morphological similarity (Erwin et al ., 2011; Grazhdankin, 2014), with such groupings representing grades (rather than clades) of organism. We focus our study on fossils considered to belong to three widely recognised morphogroups that together include many of the most contentious members of the Ediacaran biota: the rangeomorphs, dickinsoniomorphs and erniettomorphs.…”

“…1) encompasses organisms that share a body plan comprising one or multiple fronds constructed of serially repeated, leaf‐like, self‐repeating branches [see supplementary online material (SOM) of Erwin et al ., 2011]. Rangeomorphs were seemingly sessile organisms that lived in deep‐ and shallow‐marine depositional environments, and are a stratigraphically long‐ranging morphogroup, spanning the interval ∼570–541 Ma (Boag, Darroch, & Laflamme, 2016; Pu et al ., 2016).…”

“…4) are defined as serially repetitive organisms with anterioposterior differentiation (Erwin et al ., 2011 SOM), and include the genera Dickinsonia , Yorgia , Windermeria and Andiva (Erwin et al ., 2011). However, there is divergence of opinion concerning the composition of this morphogroup, and alternative groupings have been proposed, some of which include taxa such as Spriggina (Dzik & Ivantsov, 1999; Grazhdankin, 2014).…”

“…5) are defined as serially repetitive organisms constructed entirely of tubular units arranged into fronds, ‘sac‐like’ or ‘canoe‐like’ benthic recliners, or flat‐lying mats (SOM of Erwin et al ., 2011); this definition clearly encompasses a broad range of morphologies. Erniettomorphs are prominent constituents of the latest Ediacaran macrofossil assemblages of Namibia (∼550–541 Ma) (Darroch et al ., 2015; Boag et al ., 2016), and Nevada (Smith et al ., 2017), yet their biology is little understood.…”

“…Erwin et al ., 2011; Cunningham et al ., 2017). Some of the most likely candidates for early animal fossils are found within the Ediacaran Biota; an enigmatic assemblage of largely soft‐bodied macroscopic organisms that spans the ∼40 million year interval immediately prior to the Cambrian Period (Fedonkin et al ., 2007; Cunningham et al ., 2017).…”