Graham Budd

Uppsala University | UU · Department of Earth Sciences

Morphology usually serves as an effective proxy for functional ecology,1–5 and evaluating morphological, anatomical, and ecological changes permits a deeper understanding of the nature of diversification and macroevolution.5–12 Lingulid (order Lingulida) brachiopods are both diverse and abundant during the early Palaeozoic but decrease in diversity...

Trilobites are an iconic Paleozoic group of biomineralizing marine euarthropods that appear abruptly in the fossil record (c. 521 million years ago) during the Cambrian ‘explosion’. This sudden appearance has proven controversial ever since Darwin puzzled over the lack of pre-trilobitic fossils in the Origin of Species, and it has generally been as...

Fox genes represent an evolutionary old class of transcription factor encoding genes that evolved in the last common ancestor of fungi and animals. They represent key-components of multiple gene regulatory networks (GRNs) that are essential for embryonic development. Most of our knowledge about the function of Fox genes comes from vertebrate resear...

The popularity of MCMCTree for Bayesian inference of clade origin timings has generated several recent publications with focal results considerably older than the fossils of the clades in question. Here we critically examine two such clades; the animals (with focus on the bilaterians) and the mammals (with focus on the placentals). Each example dis...

Interview with Graham Budd, who studies anatomy and evolution in relation to the Cambrian explosion at Uppsala University.

Biramous appendages are a common feature among modern marine arthropods that evolved deep in arthropod phylogeny. The branched appendage of Cambrian arthropods has long been considered as the ancient biramous limb, sparking numerous investigations on its origin and evolution. Here, we report a new arthropod, Erratus sperare gen. et sp. nov., from t...

Background: Development of the nervous system and the correct connection of nerve cells requires coordinated axonal pathfinding through an extracellular matrix. Outgrowing axons exhibit directional growth toward or away from external guidance cues such as Netrin. Guidance cues can be detected by growth cones that are located at the end of growing...

Records of evolutionary stasis over time are central to uncovering large-scale evolutionary modes, whether by long-term gradual change or via enduring stability punctuated by rapid shifts. The key to this discussion is to identify and examine groups with long fossil records that, ideally, extend to the present day. One group often regarded as the q...

In his famous (if uncharacteristic) burst of lyricism at the end of the Origin Darwin described biodiversity as "endless forms most beautiful and wonderful". It is easy to agree with him when one considers red-lipped batfish or pelagic holothurians. But are they endless, or are there limitations to the variety of forms - and if there are, where do...

Background In the vinegar fly Drosophila melanogaster , the homeodomain containing transcription factor Teashirt (Tsh) appears to specify trunk identity in concert with the function of the Hox genes. While in Drosophila there is a second gene closely related to tsh , called tiptop ( tio ), in other arthropods species only one copy exists (called ti...

Excretion is an essential physiological process, carried out by all living organisms, regardless of their size or complexity. Both protostomes (e.g., flies and flatworms) and deuterostomes (e.g., humans and sea urchins) possess specialized excretory organs serving that purpose. Those organs exhibit an astonishing diversity, ranging from units compo...

Forkhead box (Fox) genes code for a class of transcription factors with many different fundamental functions in animal development including cell cycle control. Other important factors of cell cycle control are Cyclins and Cyclin-dependent kinases (CDKs). Here we report on the oscillating expression of three Fox genes, FoxM, FoxN14 (jumeaux) and Fo...

A widely (although not universally) accepted model of arthropod head evolution postulates that the labrum, a structure seen in almost all living euarthropods, evolved from an anterior pair of appendages homologous to the frontal appendages of onychophorans. However, the implications of this model for the interpretation of fossil arthropods have not...

The origin of angiosperms is a classic macroevolutionary problem, because of their rapid rise in the Early Cretaceous fossil record, beginning about 139 Ma ago, and the conflict this creates with older crown-group ages based on molecular clock dating. Silvestro et al. use a novel methodology to model past angiosperm diversity based on a Bayesian Br...

Animal phylogeny has always been controversial, but a new study brings some much-needed order for two infamous wandering groups, the ctenophores and the Xenacoelomorphs. The study introduces an innovative approach to dissect systematic errors in the underlying methodology of molecular phylogenies. Animal phylogeny has always been controversial, but...

A Correction to this paper has been published: https://doi.org/10.1038/s41586-020-03178-4.

The hypothesis that destructive mass extinctions enable creative evolutionary radiations (creative destruction) is central to classic concepts of macroevolution1,2. However, the relative impacts of extinction and radiation on the co-occurrence of species have not been directly quantitatively compared across the Phanerozoic eon. Here we apply machin...

A widely (although not universally) accepted model of arthropod head evolution postulates that the problematic labrum, a structure seen in almost all living euarthropods, evolved from an anterior pair of appendages homologous to the frontal appendages of onychophorans. However, the implications of this model for the interpretation of fossil arthrop...

Excretion is an essential physiological process, carried out by all living organisms regardless of their size or complexity(1–3). Most animals, which include both protostomes (e.g. flies, flatworms) and deuterostomes (e.g. humans, sea urchins) (together Nephrozoa(4, 5)), possess specialized excretory organs. Those organs exhibit an astonishing dive...

Important evolutionary events such as the Cambrian Explosion have inspired many attempts at explanation: why do they happen when they do? What shapes them, and why do they eventually come to an end? However, much less attention has been paid to the idea of a ‘null hypothesis’—that certain features of such diversifications arise simply through their...

Important evolutionary events such as the Cambrian Explosion have inspired many attempts at explanation: why do they happen when they do? What shapes them, and why do they eventually come to an end? However, much less attention has been paid to the idea of a 'null hypothesis' - that certain features of such diversifications arise simply through the...

The rich early fossil record of the echinoderms reveals surprisingly dynamic patterns of body plan evolution and suggests that currently popular theories about how the major features of the animal originated and were maintained are unlikely to be correct.

The Sp-family genes encode important transcription factors in animal development. Here we investigate the embryonic expression patterns of the complete set of Sp-genes in the velvet worm Euperipatoides kanangrensis (Onychophora), with a special focus on the Sp6–9 ortholog. In arthropods, Sp6–9, the ortholog of the Drosophila melanogaster D-Sp1 gene...

The fossil record of the origins of major groups such as animals and birds has generated considerable controversy, especially when it conflicts with timings based on molecular clock estimates. Here, we model the diversity of "stem" (basal) and "crown" (modern) members of groups using a "birth-death model," the results of which qualitatively match m...

Important evolutionary events such as the Cambrian Explosion have inspired many attempts at explanation: why do they happen when they do? What shapes them, and why do they eventually come to an end? However, much less attention has been paid to the idea of a “null hypothesis” – that certain features of such diversifications arise simply through the...

Tang et al. (2019) described new specimens of carbonaceous compression fossils from the early Cambrian Hetang Formation in South China, for which they established the new taxon Cambrowania ovata Tang and Xiao in Tang et al., 2019. Tang et al. (2019) interpreted these fossils as the remains of metazoans, representing either the carapaces of bivalve...

Background: One set of the developmentally important Doublesex and Male-abnormal-3 Related Transcription factors (Dmrt) is subject of intense research, because of their role in sex-determination and sexual differentiation. This likely non-monophyletic group of Dmrt genes is represented by the Drosophila melanogaster gene Doublesex (Dsx), the Caeno...

Posterior elongation of the developing embryo is a common feature of animal development. One group of genes that is involved in posterior elongation is represented by the Wnt genes, secreted glycoprotein ligands that signal to specific receptors on neighbouring cells and thereby establish cell-to-cell communication. In segmented animals such as ann...

The fossil record of the origins of major groups is of great interests to many biologists, especially when the fossil record apparently conflicts with timings based on molecular clock estimates. Here we model the diversity of 'stem' (basal) and 'crown' (modern) members of groups as seen in the fossil record, using a 'birth-death model'. Under backg...

The Upper Famennian (Upper Devonian) Strud locality has yielded very abundant and diversified flora as well as vertebrate and arthropod faunas. The arthropod fauna, mostly recovered from fine shales deposited in a calm, confined floodplain habitat including temporary pools, has delivered a putative insect and various crustaceans including eumalacos...

The fossilized traces of burrowing worms have taken on a considerable importance in studies of the Cambrian explosion, partly because of their use in defining the base of the Cambrian. Foremost among these are the treptichnids, a group of relatively large open probing burrows that have sometimes been assigned to the activities of priapulid scalidop...

Gastropods often show signs of unsuccessful attacks by durophagous predators in the form of healed scars in their shells. As such, fossil gastropods can be taken as providing a record of predation through geological time. However, interpreting the number of such scars has proved to be problematic—Would a low number of scars mean a low rate of attac...

The Ecdysozoa is a major animal clade whose main uniting feature is a distinctive growth strategy that requires the periodical moulting of the external cuticle. The staggering diversity within Ecdysozoa has prompted substantial efforts to reconstruct their origin and early evolution. Based on palaentological and developmental data, we proposed a sc...

run_experiments_SI.R gives the R commands necessary to produce each of the figures in the manuscript (excluding figure 3). fossil_trees_SI.R contains the source code necessary to perform all the mathematical analyses described in the manuscript, and should be ‘sourced’ prior to running the commands in run_experiments_SI.R

Background: Morphogen signalling represents a key mechanism of developmental processes during animal development. Previously, several evolutionary conserved morphogen signalling pathways have been identified, and their players such as the morphogen receptors, morphogen modulating factors (MMFs) and the morphogens themselves have been studied. MMFs...

Survivorship biases can generate remarkable apparent rate heterogeneities through time in otherwise homogeneous birth‐death models of phylogenies. They are a potential explanation for many striking patterns seen in the fossil record and molecular phylogenies. One such bias is the “push of the past”: clades that survived a substantial length of time...

Cruziana is one of the most recognizable trace fossils ascribed to arthropods. It ranges throughout the Phanerozoic and encompasses a diverse set of morphologies. The distinct features of Cruziana have incited fierce debate regarding its mode of formation. Here, we discuss critical aspects of trace fossil formation, namely epibenthic versus endoben...

Gastropods often show signs of unsuccessful attacks by predators in the form of healed scars in their shells. As such, fossil gastropods can be taken as providing a record of predation through geological time. However, interpreting the number of such scars has proved to be problematic - would a low number of scars mean a low rate of attack, or a hi...

Phylogenies may be modelled using “birth-death” models for speciation and extinction, but even when a homogeneous rate of diversification is used, survivorship biases can generate remarkable rate heterogeneities through time. One such bias has been termed the “push of the past”, by which the length of time a clade has survived is conditioned on the...

The early Cambrian (ca. 518 Ma) Sirius Passet Lagerstätte of North Greenland is one of the most celebrated sites bearing fossils of soft-bodied organisms, and provides key insights into the Cambrian explosion of animal life. Unlike the younger Burgess Shale (508 Ma), the Sirius Passet biota does not preserve original carbonaceous material because o...

The ancestral state of animal gastrulation and its bearing for our understanding of bilaterian evolution still is one of the most controversially discussed topics in the field of evolutionary and developmental biology. One hypothesis, the so-called amphistomy scenario, suggests the presence of a slit-like blastopore in the last common ancestor of B...

The study of evolution in a palaeontological context is chiefly the study of change in shape and form. This requires data sets that quantify morphology and morphological variation. Historically morphology has been described using discrete characters or more recently using various morphometric approaches. Elliptical Fourier analysis (EFA) is an appr...

Omnidens is a large feeding apparatus composed of circlets of teeth, first documented from the early Cambrian of China. Originally interpreted as the oral cone of a radiodontan, it was later reinterpreted as the introvert of a priapulan. In both cases the Omnidens mouthparts underpinned estimates of gigantic (c. 2 m) body size. Recent evidence has...

Delta/Notch (Dl/N) signalling is involved in the gene regulatory network underlying the segmentation process in vertebrates and possibly also in annelids and arthropods, leading to the hypothesis that segmentation may have evolved in the last common ancestor of bilaterian animals. Because of seemingly contradicting results within the well-studied a...

Recent studies have clarified the segmental organization of appendicular and exoskeletal structures in the anterior region of Cambrian stem-group Euarthropoda, and thus led to better understanding of the deep evolutionary origins of the head region in this successful animal group. However, there are aspects of the anterior organization of Palaeozoi...

Simulation studies of the early origins of the modern phyla in the fossil record, and the rapid diversification that led to them, show that these are inevitable outcomes of rapid and long-lasting radiations. Recent advances in Cambrian stratigraphy have revealed a more precise picture of the early bilaterian radiation taking place during the earlie...

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...

Understanding the evolution of early nervous systems is hazardous because we lack good criteria for determining homology between the systems of distant taxa; the timing of the evolutionary events is contested, and thus the relevant ecological and geological settings for them are also unclear. Here I argue that no simple approach will resolve the fi...

Animals make up only a small fraction of the eukaryotic tree of life, yet, from our vantage point as members of the animal kingdom, the evolution of the bewildering diversity of animal forms is endlessly fascinating. In the century following the publication of Darwin's Origin of Species, hypotheses regarding the evolution of the major branches of t...

We report the occurrence of organically preserved microfossils from the subsurface Ediacaran strata overlying the East European Platform in Poland, in the form of sclerites and cuticle fragments of larger organisms. They are morphologically similar to those known from Cambrian strata and associated with various metazoan fossils of recognized phyla....

Exceptionally preserved fossils provide major insights into the evolutionary history of life. Microbial activity is thought to play a pivotal role in both the decay of organisms and the preservation of soft tissue in the fossil record, though this has been the subject of very little experimental investigation. To remedy this, we undertook an experi...

The ancestral states of bilaterian development, and which living groups have conserved them the most, has been a controversial topic in biology for well over a hundred years. In recent years, the idea that gastrulation primitively proceeded via the formation of a slit-like blastopore that then evolved into either protostomy or deuterostomy has gain...

Onychophorans (velvet worms) are closely related to the arthropods, but their limb morphology represents a stage before arthropodization (i.e., the segmentation of the limbs). We investigated the expression of onychophoran homologs of genes that are involved in dorso-ventral (DV) and proximo-distal (PD) limb patterning in arthropods. We find that t...

Fig. S1. Negative control with Euperipatoides decapentaplegic (dpp) sense probe. Anterior is to the left. 16 h of staining. A: Dorsal view. Stage 17. Artificial signal in the yolk (y) and the head cavities (arrow). B: Dorsal view. Stage 19. Artificial signal in the frontal appendages (asterisk), the head cavities (arrow) and the cavity between yolk...

Fig. S2. Overview over anti-sense mRNA probes for the detection of Euperipatoides decapentaplegic (dpp). The probe that is marked with an asterisk (*) represents the best-working probe (best ratio of signal to background and fastest staining-time). The “transcriptome probe” detected the same pattern as the “3′RACE probe”. The short “PCR probe” did...

Fig. S3. Phylogenetic analysis of E. kanangrensis Decapentaplegic and T-box genes. The conserved T-box sequences have been used for the analyses of the T-box genes. Each phylogram represents the unrooted majority rule consensus computed from 1000 intermediate trees produced with the Quartet Puzzling Method (Strimmer and von Haeseler 1996). Numbers...

Fig. S4. Expression of Cephalofovea clandestina H15. In all panels, anterior is to the left. A: Lateral view. Stage 15. B: Ventral view. Magnification of walking limb. Note that at this stage expression is restricted to the mesoderm (mes). The ectoderm (ect) of the limb is free from expression. C: Lateral view. Stage 17. Arrow points to expression...

A new notostracan crustacean, Strudops goldenbergi gen. et sp. nov., is described from the well-preserved terrestrial arthropod fauna of the Upper Devonian of Strud, Belgium. The fossil notostracan bears a close resemblance to modern notostracans in possessing a large, simple head shield covering almost half of the whole body, a set of phyllopodous...

A new bivalved arthropod Erjiecaris minusculo gen. et sp. nov. is described from the Lower Cambrian Chengjiang Lagerstätte, Yunnan, southwest China. It possesses mosaic features, such as the reduced shield that is dorsoventrally flattened, dorsally positioned eyes, ring-shaped somites and broad furcal rami. These provide an important link for asses...

The Onychophora are a probable sister group to Arthropoda, one of the most intensively studied animal phyla from a developmental perspective. Pioneering work on the fruit fly Drosophila melanogaster and subsequent investigation of other arthropods has revealed important roles for Wnt genes during many developmental processes in these animals. We sc...

The morphology of Isoxys auritus Jiang, 1982 is reinterpreted in the light of abundant new specimens from the Early Cambrian Chengjiang biota, South China. I. auritus was a bivalved arthropod, its shield armed with two cardinal spines sub-equal in length. Two morphotypes (shield with and without ornamentation) which are of several original differen...

Onychophora is a relatively small phylum within Ecdysozoa, and is considered to be the sister group to Arthropoda. Compared to the arthropods, that have radiated into countless divergent forms, the onychophoran body plan is overall comparably simple and does not display much in-phylum variation. An important component of arthropod morphological div...

A new study quantifies rates of morphological and molecular evolution for arthropods during the critical Cambrian explosion. Both morphological and molecular evolution are accelerated - but not so much to break any speed limits.

In Cambrian fossil Lagerstätten like the Burgess Shale, exceptionally preserved arthropods constitute a large part of the taxonomic diversity, providing opportunities to study the early evolution of this phylum in detail. The anomalocaridids, large presumed pelagic predators, are particularly relevant owing to their unique combination of morphologi...