Martin Smith

Timing the pace of the Cambrian Explosion

M.R. Smith

530 million years ago, the fossil record documents a step change in the complexity and abundance of life on Earth. Our understanding of this ‘Cambrian Explosion’ is fundamentally incomplete. Was it one event or multiple bursts? How did diversification relate to contemporary environmental changes? Can it be explained by presentday evolutionary processes?

The Leverhulme Trust have awarded us funding to develop mathematical techniques that integrate geological observations from across the globe, generating a single record of biological and environmental changes through time. This will establish the rate at which animal biodiversity arose, and the triggers and consequences of this riot of evolution.

To accurately reconstruct the evolutionary events of the Cambrian radiation, we will map the global record of palaeontological, sedimentological and geochemical change onto a common timeline, accounting for preservational biases. The first challenge is to fit independent rock deposits into a single timeline, which currently relies on subjective decision-making. We will construct an objective statistical model for precise stratigraphic correlation, adapting established archaeological techniques to establish the relative ages of rock sequences in the Cambrian and beyond. Secondly, a novel model of morphological evolution will link fossil finds of known ages to points in the tree of life, providing dates and rates of branching points and morphological innovation. Finally, applying our models to a detailed dataset of a major animal lineage will link evolutionary progress to environmental change. Testing the influence of different factors interpreted as contributors to, or results of, elevated evolutionary rates will establish the feedbacks and interactions between the planet and early animal life.

Pioneering bryozoan – or shelly seaweed?

Zhang et al. / Nature

Conventional wisdom holds that all major animal groups trace their origins to the Cambrian period. Our work has reinstated the moss animals (phylum Bryozoan) as the exception to this rule: we have shown that candidate bryozoan fossils from the Cambrian period are actually mineralizing seaweeds.

This pushes back the first occurrence of bryozoans – tentacle-bearing animals that lived in skyscraper-like underwater colonies – by millions of years, to the Ordovician. The delayed appearance of bryozoans suggests that the Cambrian was not as unique a period of innovation as conventionally thought; instead, new body plans continued to be carved out by evolution over a much longer time period.

Yang, J.; Lan, T.; Zhang, X.-G.; Smith, M.R. (2023). "Protomelission is an early dasyclad alga and not a Cambrian bryozoan". Nature, 615 (7952): 468–471.

Hermits hiding in hyolith shells

Zhiqian Zhang

Modern hermit crabs' habit of inhabiting vacant shells was presented as one indicator the Mesozoic Marine Revolution, an escalation in predation pressure during the time of the dinosaurs.

We showed that penis worms beat crabs to it by hundreds of millions of years. In the Cambrian Guanshan biota, every instance of the priapulan Eximipriapulus was snuggled inside a hyolith-shell home. This early invention of "hermiting" shows that predation pressure in the Cambrian was no less fierce than at later points in life history.

Yang, X.-Y., Smith, M.R., Yang, J., Li, W., Guo, Q.-H., Li, C.-L., Wang, Y. & Zhang, X.-G. (2021). "A 'hermit' shell-dwelling lifestyle in a Cambrian priapulan worm". Current Biology, 31 (21): R1420–R1421.

Comparing evolutionary family trees

M.R. Smith

Phylogenetic analysis is the science of reconstructing evolutionary relationships from observations such as morphology and genetic sequences. There are various methods of reconstructing relationships, each with different strengths and weaknesses. My work aims to improve the quality of data that is analysed, and the methods used in analysis. I have developed new ways to compare trees, a first step to testing how well different methods reconstruct true evolutionary patterns; and methods to extract the maximum information from the resulting 'forests' of evolutionary trees.

Smith, M.R. (2022). "Robust analysis of phylogenetic tree space". Systematic Biology, 71 (5): 1255–1270.

Smith, M.R. (2022). "Using information theory to detect rogue taxa and improve consensus trees". Systematic Biology, 71 (5): 1088–1094.

Smith, M.R. (2020). "Information theoretic Generalized Robinson–Foulds metrics for comparing phylogenetic trees". Bioinformatics, 36 (20): 5007–5013.

Brazeau, M.D., Guillerme, T. & Smith, M.R. (2019). "An algorithm for morphological phylogenetic analysis with inapplicable data". Systematic Biology, 68 (4): 619–631.

Smith, M.R. (2019). "Bayesian and parsimony approaches reconstruct informative trees from simulated morphological datasets". Biology Letters, 15:20180632.

Solving the riddle of the hyoliths

Danielle Dufault

Hyoliths are one of the most abundant fossils from the Palaeozoic, the era before the dinosaurs. Looking like an ice cream cone with a lid, their identity has long been a mystery: were they aberrant snails, or a long-extinct lineage with no close relatives – a 'failed evolutionary experiment'?

Amazing new fossils from North America and China have finally solved this 175 year old mystery. Preserving the body, not just the shell, these fossils reveal for the first time a crown of tentacles surrounding the mouth – a distinctive feature that links the fossils to modern brachiopods and horseshoe worms. This shows that Hyoliths lived on the sea floor, plucking food particles from passing water. Settling the affinity of hyoliths sheds new light on the origins of animal body plans during the sudden burst of evolution that is the Cambrian Explosion.

Smith, M.R. (2020). "Finding a home for hyoliths". National Science Review, 7 470–471.

Moysiuk, J., Smith, M.R. & Caron, J-B. (2017). "Hyoliths are Palaeozoic lophophorates". Nature 541: 394–397.

Sun, H.-J., Smith, M.R., Zeng, H., Zhao, F.-Z., Li, G.-X. & Zhu, M.-Y. (2018). "Hyoliths with pedicles illuminate the origin of the brachiopod body plan". Proc. Roy. Soc. B, 285: 20181780.

The humble fungus that brought life to land

M.R. Smith

These tiny branching filaments may look unremarkable, but they represent the oldest fossils of terrestrial organisms. New fossils collected in field excursions to Sweden, New York and Scotland allowed me to reconstruct how the hitherto enigmatic organism Tortotubus lived and grew.

These strands represent fragments of extensive subterranean networks, which would have stabilised and nourished the soils in which early plants took root.

Smith, M.R. (2016). "Cord-forming Palaeozoic fungi in terrestrial assemblages". Botanical Journal of the Linnean Society 180 (4): 452–460.

Mini fossils that pack a punch

T.H.P. Harvey / PalAss

Small Carbonaceous Fossils (SCFs) are a diverse suite of non-mineralized microfossils representing bits of early organisms. Widespread in space and time, these tiny elements provide an unrivalled view on the rate and tempo of Cambrian evolution. By establishing the identity of a range of problematic SCFs, my research is telling the evolutionary tales locked up in these beautiful fossils.

Smith, M.R., Hughes, G.M.G., Vargas, M.C. & de la Parra, F. (2016). "Sclerites and possible mouthparts of Wiwaxia from the temperate palaeolatitudes of Colombia, South America". Lethaia 49 (3): 393-397.

Smith, M.R., Harvey, T.H.P. & Butterfield, N.J. (2015). "The macro-and micro-fossil record of the Cambrian priapulid Ottoia". Palaeontology 58 (4): 705–721.

Smith, M.R. & Ortega Hernández, J. (2014). "Hallucigenia’s onychophoran-like claws and the case for Tactopoda". Nature 514 (5722): 363–366.

Caron, J.-B., Smith, M.R. & Harvey, T.H.P. (2013). "Beyond the Burgess Shale: Cambrian microfossils track the rise and fall of hallucigeniid lobopodians". Proceedings of the Royal Society B 280 (1767): 20131613.

The 'weird worm' Hallucigenia

M.R. Smith / Smithsonian

Hallucigenia has always baffled scientists. A 500-million-year-old enigma, this bizarre spiny worm is known from a handful of fossils and just two locations. A study with coauthors Tom Harvey and Jean-Bernard Caron revealed that, in fact, it had relatives all over the world. Whilst examining its defensive spines, we spotted a resemblance with a global family of small spiny fossils: both have a subtle surface ornament and a structure like a stack of ice-cream cones. It seems that quirky Hallucigenia was no recluse: along with its relatives, it formed a cosmopolitan community that spanned the Cambrian seas.

When Hallucigenia was first described in the 1970s, the spines along its back were mistaken for legs, and its head was mistaken for its tail. Now, state-of-the-art electron microscopes have yielded new details from the spines, claws and head of Hallucigenia, exposing its place in life’s evolutionary tree, and how it helps us to reconstruct the common ancestor of all moulting animals.

Smith, M.R. (2017). "Fossil Focus: Hallucigenia and the origin of animal body plans". Palaeontology Online 7 (5): 1–9

Smith, M.R. & Caron, J.-B. (2015). "Hallucigenia’s head and the pharyngeal armature of early ecdysozoans". Nature 523 (7558): 75–78.

Smith, M.R. & Ortega Hernández, J. (2014). "Hallucigenia’s onychophoran-like claws and the case for Tactopoda". Nature 514 (5722): 363–366.

Caron, J.-B., Smith, M.R. & Harvey, T.H.P. (2013). "Beyond the Burgess Shale: Cambrian microfossils track the rise and fall of hallucigeniid lobopodians". Proceedings of the Royal Society B 280 (1767): 20131613.

The 'maybe mollusc' Wiwaxia

M.R. Smith M.R. Smith / Royal Society

The loveable fossil Wiwaxia bears an intimidating coat of scale-mail armour punctuated with lengthy spines. But what is the animal underneath this tough exterior? Could it be a slug, related to the molluscs? Or does it really represent an 'earthworm in disguise'? I've focussed on two clues to assess its affinity. Firstly, its mouthparts have several similarities with the teeth of modern molluscs - and look nothing like worm teeth. Secondly, the animal grows just like some slug-like molluscs that inhabit modern rock pools. However, compelling links with annelid worms suggest that Wiwaxia has a deep evolutionary position and might tell us how both these two body plans became established.

Zhang, Z.-F., Smith, M.R. & Shu, D.-G. (2015). "New reconstruction of the Wiwaxia scleritome, with data from Chengjiang juveniles". Scientific Reports 5: 14810.

Zhao, F.-C., Smith, M.R., Yin, Z.-J., Zeng, H., Hu, S.-X., Li, G.-X. & Zhu, M.-Y. (2015). "First report of Wiwaxia from the Cambrian Chengjiang Lagerstätte". Geological Magazine 152: 378–382.

Yang, J., Smith, M.R., Lan, T, Hou, J.-B., Zhang, X.-G. (2015). "Articulated Wiwaxia from the Cambrian Stage 3 Xiaoshiba Lagerstätte". Scientific Reports 4: 4643.

Smith, M.R. (2014). "Ontogeny, morphology and taxonomy of the soft-bodied Cambrian “mollusc” Wiwaxia", Palaeontology 57 (1): 215-229.

Smith, M.R. (2012). "Mouthparts of the Burgess Shale fossils Odontogriphus and Wiwaxia: implications for the ancestral molluscan radula", Proceedings of the Royal Society B: Biological Sciences 279 (1745): 4287-4295.

The 'squishy squid' Nectocaris

M.R. Smith / Nature

From 1911, only a single specimen of Nectocaris was known. But since the 1980s, Royal Ontario Museum collectors have recovered dozens more. This new material transformed our idea of what Nectocaris looked like, and colleague Jean-Bernard Caron and I estabilshed that it resembled a modern-day squid or cuttlefish. This was astonishing: such cephalopods aren't meant to have evolved until much, much later. This could mean that there’s a huge (200 million year) gap in the fossil record, which would turn the conventional concept of cephalopod evolution on its head. Alternatively, Nectocaris may represent an incredible example of convergent evolution - the independent invention of a modern body plan. This question hinges on how far we trust the fossil record; for now, at least, the jury is out.

Smith, M.R. (2020). "An Ordovician nectocaridid hints at an endocochleate origin of Cephalopoda". Journal of Paleontology 94 (1): 64–69.

Smith, M.R. (2013). "Nectocaridid ecology, diversity and affinity: early origin of a cephalopod-like body plan". Paleobiology 39 (2): 345–357.

Smith, M.R. & Caron, J-B. (2011). "Nectocaris and early cephalopod evolution: Reply to Mazurek & Zatoń". Lethaia 44 (4): 369–372.

Smith, M.R. & Caron, J.-B. (2010). "Primitive soft-bodied cephalopods from the Cambrian", Nature 465 (7297): 469–472.

The 'soggy seaweed' Nematothallus

M.R. Smith / Palaeontology

Tiny fragments of fossilized cuticle, referred to as Nematothallus, have long been implicated in the origin of land plants. Cuticle was an essential adaptation before plants could invade the land – without it, they'd dry up far too quickly. But plants are not the only organisms to have cuticle – so do some seaweeds, lichens, fungi, and animals. How can you tell the difference based on fossil scraps that are less than a millimeter in size?

With co-author Nick Butterfield, I recovered new details of Nematothallus’s reproductive organs, some of which were even preserved with spores attached. Details of these organs allowed our fossils to be reinterpreted as coralline red algae, a type of seaweed that forms parts of coral reefs today. But unlike their modern counterparts, our fossils did not lay down limestone in their skeletons — filling an interesting gap in the evolutionary history of seaweeds.

Smith, M.R. & Butterfield, N.J. (2013). "A new view on Nematothallus: coralline red algae from the Silurian of Gotland". Palaeontology 56 (2): 297-321.