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Exploring terra incognita: terrestrialization of arthropods in the era of genomics

Periodic Reporting for period 1 - TERRESTREVOL (Exploring terra incognita: terrestrialization of arthropods in the era of genomics)

Reporting period: 2018-01-15 to 2020-01-14

All animals come from the sea, and many of them managed to conquer terrestrial environments. The most successful of these lineages are arthropods, including insects, spiders or myriapods. The goal of this project was to understand how arthropods adapted to life on land. However, a series of questions needed to be addressed beforehand. For instance, arthropod phylogeny has been controversial, particularly in some of the lineages. How do different analyses affect the inferred phylogeny, particularly orthology inference? A second important question revolved around understanding how and when genes arose in this lineage. Are most genes ancient? Did they arise recently? And did they evolve through speciation or duplication? I tackled these questions through a bioinformatic spyglass.

Arthropods constitute the most successful animal phylum on our planet. By learning how their genomes evolved, we can hope to further our understanding on how to preserve specific lineages, or how to contain pests. For instance, in one of our publications we investigated how selection affected recent duplicated genes in the pea aphid, Acyrthosiphon pisum, an important pest. We showed that some genes involved in the maintenance of symbiotic relationships with bacteria (key for the aphid since they synthesize some essential amino acids) arose through recent gene duplication, and opens the door to the design of targeted drugs to contain this pest.

Overall objectives:
(1) How did arthropod genes evolve? Are most genes ‘old’ (i.e. gained in the Animal Tree of Life before arthropods arose) or ‘new’ (i.e. lineage-specific)? Did they evolve through speciation or duplication?
(2) How did selection reshaped genes recently duplicated in some arthropod lineages?

Conclusions of the action
- Most arthropod genes are very ancient and date back to the ancestor of animals and their relatives.
- Around one third of the genes in arthropod genomes evolved ‘recently’ (i.e. were gained in the branch leading to the phylum).
- Gene duplication was an important force shaping arthropod genomes, potentially facilitating adaptation to life on land.
- Genes recently duplicated were also important for pests, as in the case of the pea aphid, where recent duplicates facilitate symbiosis with bacteria.
WP1. Genome and transcriptome sequencing and assembly
Milestones: (1) we collected and sequenced all the specimens needed for the project and assembled their transcriptomes. (2) we explored when and how arthropod genes were gained, duplicated or lost in the context of the Animal Tree of Life.
Deliverables: (1) we created a large database of arthropods and inferred orthology/paralogy relationships for each gene in each genome. (2) we published a paper describing the patterns of gene gain, duplication and loss in the context of the Animal Tree of Life (Fernández & Gabaldón, 2020). (3) we wrote a book chapter about orthology inference, with special emphasis on how different methods affect the resulting topology in animals and some arthropod lineages, such as spiders (Fernández, Gabaldón & Dessimoz, 2019).

WP2 and WP3. Investigating cuticular composition and osmoregulation
Milestones: (1) we identified genes putatively involved in cuticular composition and osmoregulation in invertebrates. (2) we investigated when and how they arose in the context of the Animal Tree of Life.
Deliverables: (1) the generation of a database of orthologous genes related to cuticle composition and osmoregulation. I am currently analyzing these datasets and working on a manuscript on how these genes evolved in arthropods.

WP4. Understanding arthropod evolvability
Milestones: (1) we identified genes that evolved through recent gene duplication in the pea aphid. (2) we investigated how selection affected the new gene duplicates and interrogated their putative functions.
Deliverables: (1) in Fernández et al. (2019) we tested whether duplicates specific to the pea aphid Acyrthosiphon pisum were related to genomic innovation by combining comparative genomics, transcriptomics, and chromatin accessibility analyses.

To date, I already have published 3 research papers during the development of this action, and I am in the process of publishing 3 more soon. I attended 2 international conferences and three national one during the action, and I am attending a sixth one linked to this action already scheduled for next summer. 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 gave a talk in a high school during the International Day of Women and Girls in Science in Barcelona, and participated as an activity leader during the Open Day organized at the Barcelona Park of Biosciences.
So far, most studies aiming at understanding how genomes evolved used a gene family approach based on sequence homology, which provides a static picture of gene repertoire evolution. However, a phylogenomic approach had hardly ever been explored. The importance of this approach lies in that it allows us to generate an atlas of gene gain, duplication and loss to investigate how (by speciation or duplication), when (in which node) and how often (how many times) a gene has been gained, duplicated or lost. Our comprehensive phylogenomics analysis allowed us to tackle the history of duplicated genes to pave the road towards understanding the role of gene duplication in ecological adaptation and to further our understanding of the big picture of gene repertoire evolution across metazoans.
This action has already yielded several research publications, with several more in progress. Furthermore, the completion of all the deliverables is planned to be finished during 2020. The summary of the impacts is detailed on the 'Technical Report' (Part B) attached on the 'Project Periodic Report'.

Image description:
Caption: Schematic representation of the approach followed. In the center, an illustration showing genes (represented by lines) that are shared between lineages (represented by the color of the lines). In the outside, representatives of the main arthropod lineages.