Investigating the genomic and phenotypic consequences of recurrent whole genome duplication in spiders

The duplication of genes provides new genetic material that can be used for novel functions, allowing plants and animals to evolve biological innovations and adapt to environmental conditions. Whole genome duplication (WGD) is arguably the most dramatic mechanism for duplication, resulting in the production of a new copy of every gene in the nuclear genome. Around 430 million years ago, spiders and scorpions diverged from a common ancestor that had experienced a WGD. The retained duplicated genes from this WGD event (genes called ohnologs) can still be found in the genomes of the approximately 45,000 species of these animals alive today and may have contributed to their adaptation and diversification. Since then, some families of Synspermiata spiders have undergone at least two additional WGDs within a single lineage, reflecting a similar series of WGDs in vertebrates. This presents an opportunity to compare these events to determine whether there are general principals shaping the outcomes of WGDs and their contribution to animal diversification. In addition, Synspermiata represent a wide diversity of spiders that are understudied and poorly understood Therefore, the aims of this project are to identify spider ohnologs after multiple WGDs, explore whether and how they have contributed to the evolutionary success of these animals, and compare the outcomes of these events to repeated WGDs in vertebrates. We will first collect and carry out the first large scale detailed study of the morphology of Synspermiata spiders to better understand their evolution and phenotypic diversity. In parallel, we will identify the ohnologs that have been retained in spider groups after WGDs by comparing the repertoire and arrangement of the duplicated genes in these animals with relatives where there is no evidence of additional WGDs. As part of this aim, we will sequence the genomes of Synspermiata spiders that have undergone one (Pholcus phalangioides, Scytodes thoracica and Loxosceles reclusa), and two (Oonops pulcher, Segestria senoculata and Dysdera crocata) WGD, as well as the transcriptomes of Caponiidae species with two (Orthonops zebra) or three (Calponia harrisonfordi) WGDs. Since relatively little is known about these spiders this will provide new insights into the biology of these animals as well as their genome evolution. We will then compare the repertoires of genes retained after WGD between spiders and vertebrates to determine whether there are any similarities in the aftermath of these events. This information will help us to better understand the general consequences of WGD and the principles underlying their outcomes in terms of genes being preferentially retained or lost again. Identification of ohnologs will also allow us to ask if these genes have been subject to sub-, neofunctionalisation or specialisation during spider development and if their expression is associated with morphological diversification. Overall our project will provide new insights into the genomes of spiders and how WGDs in these animals have contributed to their morphological evolution. Our data will also allow comparisons to WGD events in other animals, including vertebrates, to better understand the general consequences of these events and their contribution to animal adaptation and diversification.

This proposal will have a beneficial impact on individuals and organisations in both private and public sectors in four main groups.
International collaboration
This project involves collaboration with a range of UK and international partners with expertise in different areas of spider biology and genomics. To expand beyond these collaborations and build a stronger wider community, we will bring together around 100 international academics at a workshop focusing on multidisciplinary strategies to enhance the future of spider research. Thus, the project will benefit researchers in many different areas, from natural history and conservation to developmental biology and genomics, by unifying them in an integrative research community. This will facilitate new multidisciplinary collaborations leading to grant applications, publications, and improved higher education teaching in these areas.
Charities and societies
The creation of a new integrative arachnological community will also provide an improved platform to inform the strategies and policies of scientific charities involved in spider biology, such as the British Arachnology Society and the Field Studies Council by complementing their ecological and taxonomic interests with genomics. We have also initiated a collaboration with the Field Studies Council, with the aim of synthesising our work with their activities and goals. This will positively impact this charity through expansion of its public engagement provision to include genomics and development as well as improving the public understanding of (and attitude to) spider biology.
Public engagement
We will continue building our successful outreach and public engagement programme to disseminate the aims and importance of this research. The proposed outreach activities will help children, parents and teachers better understand how genomes contain information to build animals, and how this may evolve to generate biodiversity. LSR's position at the museum provides an excellent platform for public engagement that will further enhance reach and thus public benefit. Through the museum and OBU, we will lead Spider Safaris as part of our two planned public engagement events in Oxford. These will teach all involved how to find and identify recognisable British spider species, including the focal British species of the proposal. The total of four planned events associated with this collaboration will also enable us to increase the reach and impact of our public engagement by including activities designed to engage with blind and partially sighted people. These events will also impact a wider audience from press attendance and subsequent dissemination to improve scientific understanding and inform and develop educational and scientific policies.
Early-career researchers
The project will provide specialist cross-disciplinary training for AS through activities in the host labs and in the labs of international collaborators. This will provide an early career researcher able to address important research questions by developing and using state-of-the-art experimental approaches in the lab and in silico. As well as continuing to enhance her scientific training, this project will provide AS with opportunities for professional development such as skills in leadership, grant management, supervision, mentoring and public engagement to furnish her with all of the necessary attributes for an independent research career following this project. This will produce a well-trained scientist with a unique combination of cutting-edge skills and international experience, who will enhance the research output and culture of OBU and the UK more widely. This project will also provide excellent training and development opportunities for the Co-I to integrate her existing expertise in morphology with genomics and development, providing her with a comprehensive suite of skills to study the evolution of animal form from molecules through to organ systems.