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From wrecks of ancient life to natural laboratories: Cave organisms as a testing ground for studying repeatability and predictability in evolution.

Periodic Reporting for period 1 - SPYCAVER (From wrecks of ancient life to natural laboratories: Cave organisms as a testing ground for studying repeatability and predictability in evolution.)

Okres sprawozdawczy: 2022-05-02 do 2024-05-01

The question being addressed in the SPYCAVER project is the investigation of parallel evolution in cave-dwelling organisms.

Parallel and convergent evolution have been considered to play contrasting roles in shaping biodiversity patterns. On the one hand, they promote speciation through natural selection, driving optimal solutions to similar problems repeatedly posed by the environment. On the other hand, they constrain ecological and phenotypical diversity and, consequently, homogenize the adaptive outcomes to similar niches.
In this project, I specifically focused on understanding the genomic mechanisms behind repeated phenotypic adaptations to extreme environmental conditions. In this context, subterranean environments and cave-dwelling organisms offer peculiarly advantageous experimental conditions to gain insight into the study of convergent evolution and the role of natural selection in speciation.

The project aims to explore whether similar environmental pressures lead to predictable genomic responses in different lineages of cave organisms.

This research is important for society for several reasons:
Conservation and Biodiversity: Understanding how organisms adapt to extreme environments and uncovering the genetic basis of these adaptations can help conserve unique species and fragile ecosystems, particularly in the face of global environmental changes.
Medicine and Biotechnology: Insights gained from studying convergent evolution can contribute to the development of medical treatments and technologies. For example, understanding how organisms cope with low oxygen levels or nutrient scarcity in caves could inspire innovations in human health.
Evolutionary Biology: Investigating convergent evolution sheds light on fundamental questions about the predictability of evolution and the role of natural selection in shaping biological diversity. This knowledge enhances our understanding of evolutionary processes more broadly.

The overall objectives of the SPYCAVER project are:
To quantify the extent of convergent evolution at the genomic level among distinct lineages of cave-dwelling organisms.
To identify specific genetic mechanisms and pathways associated with repeated adaptations to extreme environmental conditions.
To investigate the evolutionary history and divergence patterns of cave-dwelling species to discern between shared ancestral traits and traits that have evolved independently due to convergent evolution.
By achieving these objectives, the project aims to contribute significantly to our understanding of evolutionary biology, biodiversity conservation, and the potential applications of evolutionary insights in various fields, from medicine to ecology.
Milestones (M), Deliverables (D)
WP 1: DATA COLLECTION
M
I conducted extensive fieldwork in the Italian Western Alps cave systems, where I collected specimens for nine spider species of the genus Troglohyphantes, with the help of Dr. Marco Isaia. I specifically sampled species that inhabit different parts of the caves (entrance, shallow, and deep compartments, see figure 1 for a visual representation of compartment distribution) with different troglobitic phenotypic adaptations depending on the compartment.
D
My sampling design involved obtaining approximately 27 specimens representing 9 species, distributed as follows: three closely related species inhabiting each of the three main cave compartments.
WP 2: GENOMIC DATA GENERATION AND PROCESS
M
2.1. I extracted genomic DNA from Troglohyphantes pluto, a spider species inhabiting the entrance compartment of caves, to generate a high quality reference genome. A de novo Cantata Bio Hi-C sequencing approach was used to generate the genome assembly. Transcriptomic data was also retrieved from the same species to functionally annotate the genome.
2.2. I also generated whole-genome sequencing data from all the samples mentioned in WP1.
D
2.1. I generate a chromosome level reference genome with functional annotations, which will serve as a valuable resource for future studies in arthropod and particularly troglobitic fauna evolution.
2.2. I produced a genomic database of Troglohyphantes species, the most diverse spider genus in European caves, that will help to outgrow the knowledge on cave adaptation from this project and in future projects with new data being produced with collaborators.
WP 3 to 5: THE GENOMIC BASIS OF REPEATED ADAPTATION TO CAVES
M
3.2. Following a phylogenomic approach, I identified putative orthologs involved in the adaptation to the cave environment. I studied the role of natural selection in promoting independent evolution, specifically how the relaxation of selection on specific genes determined the evolution of cave-dwelling spiders.
3.3. Following a comparative structural variant detection approach, I determined that deletions and duplications play a key role in shaping the genetic diversity of cave-dwelling spiders.
D
3.2. The study revealed a set of genes that are under similar selective pressures in the species with total phenotipic adaptations to caves (from the deep cave environment).
3.3. I obtained a database of genes with deletions and genes with duplication in regions that could be affecting the expression of the genes, facilitating troglobitic adaptation.
WP 6: RESULTS DISSEMINATION AND OUTREACH ACTIVITIES
Based on the results obtained during the development of this action, a research paper is in preparation. I attended one national conference, and I will attend one national and one international conference during this and next year to disseminate our findings to a wider audience.
I gave two talks in high schools during the International Day of Women and Girls in Science in Barcelona and Montpellier. I was selected to present my research at an international conference in Uruguay, but unfortunately, I couldn't go for personal reasons. I was also selected to participate as a student at the EMBO "Hands-on course in genome sequencing, assembly, and downstream analyses" course (https://meetings.embo.org/event/22-gen-seq-analysis(odnośnik otworzy się w nowym oknie)) in 2022, to improve my skills in genome assembly and annotation, where I also had the opportunity to network with other researchers in the field.
Parallel and convergent evolution shape biodiversity by either promoting speciation through natural selection or homogenizing adaptive outcomes in similar niches. This project specifically focused on the genomic mechanisms behind repeated phenotypic adaptations to extreme environmental conditions, using natural populations of cave-dwelling spider species as a model to study these evolutionary processes. I am still evaluating the potential mechanisms driving parallel and independent phenotypic evolution in these species. However, to date, the findings of this study enhance the role of relaxed selection in driving parallel evolution in cave-dwelling species. Moreover, the shared structural variants (such as deletions and duplications) between these spider species suggest a common genetic basis for adaptations to cave environments. Overall, I generated genomic resources for cave organisms, adding value to previously-generated systematic and ecological resources, and the integration of novel methodologies at the crossroads of comparative genomics, phylogenetic, and population genomics. These resources will enable further exploration and understanding of the genetic diversity and evolutionary history of subterranean organisms.
Graphical methodology
Project's logo
Model system
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