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Deuterostomes are the major division of animal life which includes sea stars, acorn worms, and humans, among a wide variety of ecologically and morphologically disparate taxa. However, their early evolution is poorly understood, due in part to their disparity, which makes identifying commonalities difficult, as well as their relatively poor early fossil record. Here, we review the available morphological, palaeontological, developmental, and molecular data to establish a framework for exploring the origins of this important and enigmatic group. Recent fossil discoveries strongly support a vermiform ancestor to the group Hemichordata, and a fusiform active swimmer as ancestor to Chordata. The diverse and anatomically bewildering variety of forms among the early echinoderms show evidence of both bilateral and radial symmetry. We consider four characteristics most critical for understanding the form and function of the last common ancestor to Deuterostomia: Hox gene expression patterns, larval morphology, the capacity for biomineralization, and the morphology of the pharyngeal region. We posit a deuterostome last common ancestor with a similar antero-posterior gene regulatory system to that found in modern acorn worms and cephalochordates, a simple planktonic larval form, which was later elaborated in the ambulacrarian lineage, the ability to secrete calcium minerals in a limited fashion, and a pharyngeal respiratory region composed of simple pores. This animal was likely to be motile in adult form, as opposed to the sessile origins that have been historically suggested. Recent debates regarding deuterostome monophyly as well as the wide array of deuterostome-affiliated problematica further suggest the possibility that those features were not only present in the last common ancestor of Deuterostomia, but potentially in the ur-bilaterian. The morphology and development of the early deuterostomes, therefore, underpin some of the most significant questions in the study of metazoan evolution.

The middle (Wuliuan Stage) Cambrian Burgess Shale is famous for its exceptional preservation of diverse and abundant soft-bodied animals through the “thick” Stephen Formation. However, with the exception of the Walcott Quarry (Fossil Ridge) and the stratigraphically older Tulip Beds (Mount Stephen), which are both in Yoho National Park (British Columbia), quantitative assessments of the Burgess Shale have remained limited. Here we first provide a detailed quantitative overview of the diversity and structure of the Marble Canyon Burgess Shale locality based on 16,438 specimens. Located 40 km southeast of the Walcott Quarry in Kootenay National Park (British Columbia), Marble Canyon represents the youngest site of the “thick” Stephen Formation. We then combine paleoecological data sets from Marble Canyon, Walcott Quarry, Tulip Beds, and Raymond Quarry, which lies approximately 20 m directly above the Walcott Quarry, to yield a combined species abundance data set of 77,179 specimens encompassing 234 species-level taxa. Marble Canyon shows significant temporal changes in both taxonomic and ecological groups, suggesting periods of stasis followed by rapid turnover patterns at local and short temporal scales. At wider geographic and temporal scales, the different Burgess Shale sites occupy distinct areas in multivariate space. Overall, this suggests that the Burgess Shale paleocommunity is far patchier than previously thought and varies at both local and regional scales through the “thick” Stephen Formation. This underscores that our understanding of Cambrian diversity and ecological networks, particularly in early animal ecosystems, remains limited and highly dependent on new discoveries.

The in situ preservation of animal behaviour in the fossil record is exceedingly rare, but can lead to unique macroecological and macroevolutionary insights, especially regarding early representatives of major animal clades. We describe a new complex ecological relationship from the middle Cambrian Burgess Shale (Raymond Quarry, Canada). More than 30 organic tubes were recorded with multiple enteropneust and polychaete worms preserved within them. Based on the tubicolous nature of fossil enteropneusts, we suggest that they were the tube builders while the co-preserved polychaetes were commensals. These findings mark, to our knowledge, the first record of commensalism within Annelida and Hemichordata in the entire fossil record. The finding of multiple enteropneusts sharing common tubes suggests that either the tubes represent reproductive structures built by larger adults, and the enteropneusts commonly preserved within are juveniles, or these enteropneusts were living as a pseudo-colony without obligate attachment to each other, and the tube was built collaboratively. While neither hypothesis can be ruled out, gregarious behaviour was clearly an early trait of both hemichordates and annelids. Further, commensal symbioses in the Cambrian may be more common than currently recognized.

Decay experiments are becoming a more widespread tool in evaluating the fidelity of the fossil record. Character interpretations of fossil specimens stand to benefit from an understanding of how decay can result in changes in morphology and, potentially, total character loss. We performed a decay experiment for the Class Enteropneusta to test the validity of anatomical interpretations of the Burgess Shale enteropneust Spartobranchus tenuis and to determine how the preservation of morphological features compares with the sequence of character decay in extant analogues. We used three species of enteropneust (Saccoglossus pusillus, Harrimania planktophilus, and Balanoglossus occidentalis) representing the two major families of Enteropneusta. Comparisons between decay sequences suggest that morphological characters decay in a consistent and predictable manner within Enteropneusta, and do not support the hypothesis of stemward slippage. The gill bars and nuchal skeleton were the most decay resistant, whereas the gill pores and pre-oral ciliary organ were unequivocally the most decay prone. Decay patterns support the identification of the nuchal skeleton, gill bars, esophageal organ, trunk, and proboscis in Spartobranchus tenuis and corroborate a harrimaniid affinity. Bias due to the taphonomic loss of taxonomically informative characters is unlikely. The morphologically simple harrimaniid body plan can be seen, therefore, to be plesiomorphic within the enteropneusts. Discrepancies between the sequence of decay in a laboratory setting and fossil preservation also exist. These discrepancies are highlighted not to discredit the use of modern decay studies but rather to underline their non-actualistic nature. Paleoenvironmental variables besides decay, such as the timeframe between death and early diagenesis as well as postmortem transport, are discussed relative to decay data. These experiments reinforce the strength of a comprehensive understanding of decay sequences as a benchmark against which to describe fossil taxa and understand the conditions leading to fossilization.

Summary Annelida is one of the most speciose (∼17,000 species) and ecologically successful phyla. Key to this success is their flexible body plan with metameric trunk segments and bipartite heads consisting of a prostomium bearing sensory structures and a peristomium containing the mouth. The flexibility of this body plan has traditionally proven problematic for reconstructing the evolutionary relationships within the Annelida. Although recent phylogenies have focused on resolving the interrelationships of the crown group [1–3], many questions remain regarding the early evolution of the annelid body plan itself, including the origin of the head [4]. Here we describe an abundant and exceptionally well-preserved polychaete with traces of putative neural and vascular tissues for the first time in a fossilized annelid. Up to three centimeters in length, Kootenayscolex barbarensis gen. et sp. nov. is described based on more than 500 specimens from Marble Canyon [5] and several specimens from the original Burgess Shale site (both in British Columbia, Canada). K. barbarensis possesses biramous parapodia along the trunk, bearing similar elongate and thin notochaetae and neurochaetae. A pair of large palps and one median antenna project from the anteriormost dorsal margin of the prostomium. The mouth-bearing peristomium bears neuropodial chaetae, a condition that is also inferred in Canadia and Burgessochaeta from the Burgess Shale, suggesting a chaetigorous origin for the peristomial portion of the head and a secondary loss of peristomial parapodia and chaetae in modern polychaetes.

Background The combination of a meager fossil record of vermiform enteropneusts and their disparity with the tubicolous pterobranchs renders early hemichordate evolution conjectural. The middle Cambrian Oesia disjuncta from the Burgess Shale has been compared to annelids, tunicates and chaetognaths, but on the basis of abundant new material is now identified as a primitive hemichordate. Results Notable features include a facultative tubicolous habit, a posterior grasping structure and an extensive pharynx. These characters, along with the spirally arranged openings in the associated organic tube (previously assigned to the green alga Margaretia), confirm Oesia as a tiered suspension feeder. Conclusions Increasing predation pressure was probably one of the main causes of a transition to the infauna. In crown group enteropneusts this was accompanied by a loss of the tube and reduction in gill bars, with a corresponding shift to deposit feeding. The posterior grasping structure may represent an ancestral precursor to the pterobranch stolon, so facilitating their colonial lifestyle. The focus on suspension feeding as a primary mode of life amongst the basal hemichordates adds further evidence to the hypothesis that suspension feeding is the ancestral state for the major clade Deuterostomia. Electronic supplementary material The online version of this article (doi:10.1186/s12915-016-0271-4) contains supplementary material, which is available to authorized users.