Graham E. Budd

A critical reappraisal of the fossil record of the bilaterian phyla

It has long been assumed that the extant bilaterian phyla generally have their origin in the Cambrian explosion, when they appear in an essentially modern form. Both these assumptions are questionable. A strict application of stem‐ and crown‐group concepts to phyla shows that although the branching points of many clades may have occurred in the Early Cambrian or before, the appearance of the modern body plans was in most cases later: very few bilaterian phyla sensu stricto have demonstrable representatives in the earliest Cambrian. Given that the early branching points of major clades is an inevitable result of the geometry of clade diversification, the alleged phenomenon of phyla appearing early and remaining morphologically static is seen not to require particular explanation. Confusion in the definition of a phylum has thus led to attempts to explain (especially from a developmental perspective) a feature that is partly inevitable, partly illusory. We critically discuss models for Proterozoic diversification based on small body size, limited developmental capacity and poor preservation and cryptic habits, and show that the prospect of lineage diversification occurring early in the Proterozoic can be seen to be unlikely on grounds of both parsimony and functional morphology. Indeed, the combination of the body and trace fossil record demonstrates a progressive diversification through the end of the Proterozoic well into the Cambrian and beyond, a picture consistent with body plans being assembled during this time. Body‐plan characters are likely to have been acquired monophyletically in the history of the bilaterians, and a model explaining the diversity in just one of them, the coelom, is presented. This analysis points to the requirement for a careful application of systematic methodology before explanations are sought for alleged patterns of constraint and flexibility.

A palaeontological solution to the arthropod head problem

The composition of the arthropod head has been one of the most controversial topics in zoology, with a large number of theories being proposed to account for it over the last century. Although fossils have been recognized as being of potential importance in resolving the issue, a lack of consensus over their systematics has obscured their contribution. Here, I show that a group of previously problematic Cambrian arthropods from the Burgess Shale and Chengjiang faunas form a clade close to crown-group euarthropods, the group containing myriapods, chelicerates, insects and crustaceans. They are characterized by modified or even absent endopods, and two pre-oral appendages. Comparison with reconstructions of the crown-group euarthropod ground plan and recent investigations into onychophorans demonstrates that these two appendages are the first antenna (of extant crustaceans) and a more anterior appendage associated with an ocular segment. The latter appendage has been reduced in all crown-group euarthropods. Its most likely relic is as a component of the labrum. These fossils thus tie together results from disparate living groups (onychophorans and euarthropods).

The origin and evolution of arthropods

The past two decades have witnessed profound changes in our understanding of the evolution of arthropods. Many of these insights derive from the adoption of molecular methods by systematists and developmental biologists, prompting a radical reordering of the relationships among extant arthropod classes and their closest non-arthropod relatives, and shedding light on the developmental basis for the origins of key characteristics. A complementary source of data is the discovery of fossils from several spectacular Cambrian faunas. These fossils form well-characterized groupings, making the broad pattern of Cambrian arthropod systematics increasingly consensual.

Why are arthropods segmented

SUMMARY Segmentation as an attribute of organisms is being increasingly discussed in the recent literature because (1) new phylogenies suggest that organisms classically considered to be segmented may lie in separate clades; (2) the molecular basis of segmental development has been much studied; (3) various theories of bilaterian origins place weight on segmentation as a primitive character; (4) there has been recent stress on the importance of modularity as an evolutionary topic. However, the definition and extent of segmentation are highly ambiguous and usually typological. Here, segmentation is regarded as an attribute of organs, not organisms. The evolution of just one system, the arthropod epidermis, is examined on the basis of the fossil record and the extant euarthropods, tardigrades, and onychophorans. It may be seen to have become segmented in a complex pathway that necessitated shifts in function, redundancy, and changes in associated organs. This complexity must inevitably reflect on, and to an extent have primacy over, the genetic basis for the changes involved. Evolutionary functional morphology has been relatively little considered in the context of the evolution of development, but may play an important role in defining the framework within which this evolution occurs.

The Burgess Shale Anomalocaridid Hurdia and Its Significance for Early Euarthropod Evolution

As the largest predators of the Cambrian seas, the anomalocaridids had an important impact in structuring the first complex marine animal communities, but many aspects of anomalocaridid morphology, diversity, ecology, and affinity remain unclear owing to a paucity of specimens. Here we describe the anomalocaridid Hurdia, based on several hundred specimens from the Burgess Shale in Canada. Hurdia possesses a general body architecture similar to those of Anomalocaris and Laggania, including the presence of exceptionally well-preserved gills, but differs from those anomalocaridids by possessing a prominent anterior carapace structure. These features amplify and clarify the diversity of known anomalocaridid morphology and provide insight into the origins of important arthropod features, such as the head shield and respiratory exites.

Tardigrades as ‘Stem-Group Arthropods’: The Evidence from the Cambrian Fauna

Abstract The Cambrian fauna can now reasonably be seen as containing many taxa that lie in the stem-groups of the extant phyla. As such, these fossils suggest how both the ‘body plans’ of extant phyla were assembled, and also how various ‘minor’ phyla relate to the larger groupings of today such as the arthropods and annelids. The various arthropod and lobopod taxa of the Cambrian faunas have been controversial and have generally been considered either as lying in the crown or (occasionally) stem groups of the euarthropods, onychophorans and tardigrades. However, phylogenetic analysis strongly suggests that many of even the most euarthropod-like taxa do not lie within the euarthropod crown-group but are more basal. Further, the commonly expressed view that Cambrian lobopods are in effect stem- or crown-group onychophorans also seems not to be well supported. Lobopods in the Cambrian appear to be diverse and not particularly closely related to one another, and certainly cannot be combined in a monophyletic clade. Both these advances offer hope that the tardigrades (placed as the sister group to the euarthropods in many analyses of extant taxa, here collectively named the Tactopoda) may be more closely related to some of these Cambrian taxa than others. The challenge for both neontologists and palaeontologists is to refine the systematic analysis of both living and fossil taxa in order to maximise the usefulness of the (admittedly few) characters that unite tardigrades to their Cambrian forbears.

The earliest fossil record of the animals and its significance

The fossil record of the earliest animals has been enlivened in recent years by a series of spectacular discoveries, including embryos, from the Ediacaran to the Cambrian, but many issues, not least of dating and interpretation, remain controversial. In particular, aspects of taphonomy of the earliest fossils require careful consideration before pronouncements about their affinities. Nevertheless, a reasonable case can now be made for the extension of the fossil record of at least basal animals (sponges and perhaps cnidarians) to a period of time significantly before the beginning of the Cambrian. The Cambrian explosion itself still seems to represent the arrival of the bilaterians, and many new fossils in recent years have added significant data on the origin of the three major bilaterian clades. Why animals appear so late in the fossil record is still unclear, but the recent trend to embrace rising oxygen levels as being the proximate cause remains unproven and may even involve a degree of circularity.

The morphology and phylogenetic significance of Kerygmachela kierkegaardi Budd (Buen Formation, Lower Cambrian, N Greenland)

Specimens of Kerygmachela kierkegaardi Budd are described, from the Lower Cambrian Sirius Passet fauna of N Greenland. The cephalic region is characterised by a pair of stout unsegmented appendages each bearing long spinose processes, and an anterior mouth. The trunk shows alternating rows of tubercles and transverse annulations along the axis, to which are attached 11 pairs of gill-bearing lateral lobes and lobopodous limbs. The caudal region is small, and bears two long tail spines. There is some evidence for circular musculature arranged around the trunk and a dorsal, longitudinal sinus, and several details of the muscular pharynx have been preserved. The combination of characters found in Kerygmachela allows it to be allied with the lobopods, represented in the extant fauna by the onychophorans, tardigrades, and possibly the pentastomids, and in the Cambrian fossil record by a morphologically diverse set of taxa, some of which are not assignable to the extant groupings. It also shares important characters with the previously problematic Burgess Shale forms Opabinia regalis Walcott and Anomalocaris Whiteaves, and the Sirius Passet form Pambdelurion Budd. These taxa together form a paraphyletic group at the base of the clade of biramous arthropods. The position of the so-called ‘Uniramia’ remains unclear. It can be demonstrated from the reconstruction of the arthropod stem-group that full arthropod segmentation has a different derivation from that of the annelids. In line with other recent analyses, this suggests that the ‘Articulata’ of Cuvier should be dismantled, and the arthropods considered to be a group of protostomes which are phylogenetically distinct from the classic spiralians. Arthropod affinities may rather lie with the other moulting animals, in the so-called ‘Ecdysozoa’.

The Scleritome of Eccentrotheca from the Lower Cambrian of South Australia : Lophophorate affinities and implications for tommotiid phylogeny

The first partially articulated scleritome of a tommotiid, Eccentrotheca sp., is described from the Lower Cambrian of South Australia. The Eccentrotheca scleritome consists of individual sclerites; fused in a spiral arrangement, forming a tapering tube-shaped skeleton with an inclined apical aperture and a circular to subcircular cross section. Traditionally, tommotiid sclerites have been assumed to form a dorsal armor of imbricating phosphatic plates in slug-like bilaterians, analogous to the calcareous sclerites of halkieriids. The structure of the Eceentrotheca scleritome is here reinterpreted as a tube composed of independent, irregularly shaped sclerites growing by basal-marginal accretion that were successively fused to form a rigid, protective tubular structure. The asymmetrical shape and sometimes acute inclination of the apical aperture suggests that the apical part of the scleritome was cemented to a hard surface via a basal disc, from which it projected vertically. Rather than being a vagrant member of the benthos, Eccentrotheca most likely represented a sessile, vermiform filter feeder. The new data suggest that the affinities of Eccentrotheca, and possibly some other problematic tommotiids, lie with the lophophorates (i.e., the phoronids and brachiopods), a clade that also possesses a phosphatic shell chemistry and a sessile life habit.

The origin of the animals and a ‘Savannah’ hypothesis for early bilaterian evolution

The earliest evolution of the animals remains a taxing biological problem, as all extant clades are highly derived and the fossil record is not usually considered to be helpful. The rise of the bilaterian animals recorded in the fossil record, commonly known as the ‘Cambrian explosion’, is one of the most significant moments in evolutionary history, and was an event that transformed first marine and then terrestrial environments. We review the phylogeny of early animals and other opisthokonts, and the affinities of the earliest large complex fossils, the so‐called ‘Ediacaran’ taxa. We conclude, based on a variety of lines of evidence, that their affinities most likely lie in various stem groups to large metazoan groupings; a new grouping, the Apoikozoa, is erected to encompass Metazoa and Choanoflagellata. The earliest reasonable fossil evidence for total‐group bilaterians comes from undisputed complex trace fossils that are younger than about 560 Ma, and these diversify greatly as the Ediacaran–Cambrian boundary is crossed a few million years later. It is generally considered that as the bilaterians diversified after this time, their burrowing behaviour destroyed the cyanobacterial mat‐dominated substrates that the enigmatic Ediacaran taxa were associated with, the so‐called ‘Cambrian substrate revolution’, leading to the loss of almost all Ediacara‐aspect diversity in the Cambrian. Why, though, did the energetically expensive and functionally complex burrowing mode of life so typical of later bilaterians arise? Here we propose a much more positive relationship between late‐Ediacaran ecologies and the rise of the bilaterians, with the largely static Ediacaran taxa acting as points of concentration of organic matter both above and below the sediment surface. The breaking of the uniformity of organic carbon availability would have signalled a decisive shift away from the essentially static and monotonous earlier Ediacaran world into the dynamic and burrowing world of the Cambrian. The Ediacaran biota thus played an enabling role in bilaterian evolution similar to that proposed for the Savannah environment for human evolution and bipedality. Rather than being obliterated by the rise of the bilaterians, the subtle remnants of Ediacara‐style taxa within the Cambrian suggest that they remained significant components of Phanerozoic communities, even though at some point their enabling role for bilaterian evolution was presumably taken over by bilaterians or other metazoans. Bilaterian evolution was thus an essentially benthic event that only later impacted the planktonic environment and the style of organic export to the sea floor.