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Molecular palaeobiology and comparative genomics of chelicerate terrestrialisation

Periodic Reporting for period 1 - CheliceLand (Molecular palaeobiology and comparative genomics of chelicerate terrestrialisation)

Periodo di rendicontazione: 2015-09-01 al 2017-08-31

What is the problem being addressed?
Animals have marine origins and only four lineages have adapted to life on land. These groups are the vertebrates (e.g. reptiles, mammals), molluscs (e.g. land snails, slugs), the onychophora (velvet worms) and the arthropods (e.g. insects, spiders). The water-to-land transition is referred as terrestrialisation, and is an extreme case of adaptation to a new environment. My research has been focused on the arthropod lineage, and I have been interested in knowing 'how' and 'when' these organisms have colonised the land. I am particularly interested in the comparative genomics of one of the groups that conform it, the chelicerates (e.g. spiders, scorpions, mites). Chelicerates contains marine and land representatives as well as abundant terrestrial fossil record. I combined the genomic and fossil information of these organisms to study the modifications that allowed marine chelicerates to adapt to life on land.

Why is it important for society?
This action is a blue skies project, however, studying the most extreme case of habitat colonization (i.e. invasion) can help understanding the biology of current invasive species, like the pest Drosophila suzukii – the containment of which is a EU priority. Chelicerates include pests (e.g. the spider mites) and species of biomedical relevance (e.g. the ticks – vectors of lyme disease). By identifying chelicerate–specific genomic adaptation to life on land, this project could potentially identify potential chelicerate–specific drug targets which may help the development of lineage–specific pesticides with low incidence on economically important arthropods, like the declining bees.

What are the overall objectives?
Two objectives have been set at the beginning of this action:
(1) To resolve and date the chelicerate radiation, estimate how many times the chelicerates colonised the land, and test whether their terrestrial diversification was a continuous or discontinuous (i.e. punctuated by diversification bursts and biotic crises) process.
(2) To identify the genes that underwent adaptive changes when chelicerates adapted to life on land.

Conclusions of the action
- The terrestrial chelicerates, Arachnida, have colonised the land just once.
- The colonisation of land happened during the Cambrian-Ordovician.
- The terrestrial diversification was marked by an initial explosive cladogenesis, giving origin to most of the extant arachnid orders.
- The fast and ancient diversification that took place during the origin of Arachnida, makes difficult the identification and interpretation of the adaptive changes to terrestrial environments that experienced this lineage.
"Three different work packages has been set to complete the objectives:

WORK PACKAGE 1: RNA–Seq data set assembly and phylogenomic analyses:

- Milestones: (1) The generation of all the genomic and RNA–Seq datasets. I generated two independent molecular datasets using hundreds of orthologus genes to test the relationships of chelicerates using Illumina transcriptomes for 95 taxa.
- Deliverables: (1) The generation of genomic and RNA–Seq data for Chelicerata. (2) The generation of a phylogenomic tree for the Chelicerata. I have completed the dataset and the phylogenomic analyses, and published a paper on the phylogeny of arthropods. A manuscript on the phylogeny of Chelicerata based on phylogenomics is currently under review, with results suggesting that Arachnida and Acari are monophyletic, reconciling previous results based on morphology, and suggesting a single terrestrialization event.

WORK PACKAGE 2: Merging fossils and molecules analyses:

- Milestones: (1) The completion of the morphological dataset. During my secondment at the Natural History Museum of London I completed this milestone.
- Deliverables: (1) The generation of a new morphological dataset for all chelicerates (fossils included). (2) The generation of a dated timetree illustrating the history of all chelicerates (including fossils). I used the fossil constraints to perform a node calibrated molecular clock. I already published a paper in which we inferred the terrestrialisation events in insects, myriapods and arachnids, and I am currently in the process of writing a paper using an extended datasets and more up-to-date methods just focused on arachnids.

WORK PACKAGE 3: Comparative genomics of terrestrialisation: I am doing comparative genomics focused on chelicerate species with the objective of detecting signatures of positive selection to terrestrial environments.

- Milestones: (1) The completion of all analyses necessary to complete the project. I started to analyze the genomic content of terrestrial and marine chelicerates, but this milestone has not been finished yet.
- Deliverables: (1) The Publication of a paper in the area of functional genomics illustrating the genomic changes that allowed chelicerates to adapt to life on land. I have not started yet the paper on functional genomics because I am still analyzing the data.

RESULTS, EXPLOITATION AND DISSEMINATION
To date, I already have published 5 research papers during the development of this action, and I am in the process of publishing 3 more soon. I attended 3 international conferences during the action, and a fourth one is scheduled after the end of it: In 2016 and 2017 I presented in the 'Annual Meeting of the Society for Molecular Biology and Evolution' (biggest event in the field of molecular evolution) and organised a symposium on ""Molecular clocks” in the 2017 meeting. I also attended in 2016 and 2017 the 'Annual Meeting of the Paleontological Association'. Furthermore, I assisted and presented my work in UK based conferences within the evolutionary biology and palaeobiological, such as ‘Dating species divergence using rocks and clocks’ organized by the Royal Society and held in London, and to the annual 'Young Systematists’ Forum’.
Apart from reaching colleagues of my area assisting and presenting in scientific conferences, I designed actions to reach wider audiences. I particularly focused on disseminating my research to young people. I acted as STEM ambassador in South-West England, attending severa events, and being an activity leader during the Bristol’s Bright Night' and during the Bristol Dinosaur week."
PROGRESS BEYOND THE STATE OF THE ART
This action has been largely based on up-to-date techniques in phylogenetics, the integration of fossil data and molecular clock dating. The advent of molecular biology and the development of the molecular clock theory allowed the use of genomes as a second record of life, in combination with the study of morphology, in which early phylogenetic studies mostly relied on. The integration of fossil data into a phylogenies with living species has become both a theoretical and computational challenge. To address this problems, I have been involved in the study the methods of implementing different phylogenetic signals, in order to use the most comprehensive information. In collaboration with Bristol colleagues we have published several papers dealing with the development of these methods.

EXPECTED RESULTS AND POTENTIAL IMPACTS
This action has already yield several research publications, with several more in progress, and the consecution of all the deliverables is plan to be finished during 2018. The summary of the impacts is detailed on the 'Technical Report' (Part B) attached on the 'Project Periodic Report'.
Schematic representation of the topic and tools used in this action