Comparative genomics of sponges (Porifera) gives insight into early animal evolution

Abstract

The emergence of animals (Metazoa) was a pivotal event in the evolution of life, posing a
major puzzle in evolutionary biology. The last common ancestor of animals evolved from a
single-celled precursor in the Precambrian oceans. Subsequently, modern metazoans
underwent a radiation, shaping the diverse animal body plans seen today and contributing to
contemporary biodiversity. During the transition from the Ediacaran to the Cambrian period
(635-485.4 million years ago), animals evolved tissue-level organization, developed organs
and systems (e.g., nervous, muscular, and gut systems), and acquired skeletal elements like
shells and spicules. Despite increasing knowledge about animal evolution, unresolved
questions persist. For example, we still do not know when crown group Metazoa emerged
and what was the ancestral body plan of the last common animal ancestor. Sponges represent
a major animal lineage that diverged close to the root of the metazoan tree. Sponges are key
to understand early animal evolution, particularly the timing of the animal radiation as
putative sponge fossils (including biomolecular fossils) represent the oldest possible fossil
evidence for animals.
The aim of this thesis is to elucidate the evolutionary history of the sponges using a
combination of omics techniques, such phylogenomics, comparative genomics, and
transcriptomics. Using NGS data, I built a new sponge phylogeny, which I then used as
framework to establish a new sponge timetree. By turn, I then used the timetree to perform
ancestral character state reconstruction and test hypotheses about the origin of the sponge
spicules, and the nature of the fossil record of the sponge spicules. To further test hypotheses
of spicule and sponge evolution, I then turned my attention to biomineralization processes
studying the evolution of genes involved in siliceous spicule assembly. Finally, I explored light
reception in sponges. Understanding sponge light reception is crucial for unravelling the
origins of photoreceptors, which can help us better understand the origin of the nervous
system more broadly.
I find the sponges to constitute a monophyletic group, resolving almost all the internal
relationships of the phylum. The timetree I inferred suggests a late Precambrian origin of
sponges, and my ancestral character state reconstructions suggest that siliceous spicules
evolved multiple times independently, with the last common sponge ancestor being soft
bodied. Overall, my ancestral character state reconstruction and molecular clock analyses
fully reconcile the molecular and fossil estimates of sponge evolution. Moreover, I found that
siliceous spicules were not fundamental for the success of demosponges and did not drive
radiation events. The biomineralization toolkit of sponges is much more diverse than
previously thought, with the demosponges having many enzymes, scaffolding proteins, and
membrane transports that create a complex system for spicule production.
Finally, my study of light reception suggeststhat calcareans, similarly to demosponges
and hexactinellids, use a blue light reception system based on cryptochromes to recognize
light.
In conclusion, this work highlights the importance of considering sponges when
thinking of early animal evolution: they are key to understand the origin of animal
biodiversity.

Date of Award	19 Mar 2024
Original language	English
Awarding Institution	University of Bristol
Supervisor	Davide Pisani (Supervisor), Philip C J Donoghue (Supervisor) & Ana Riesgo (Supervisor)