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Conservation impacts of hybridization and introgression in symbionts: Measuring the magnitude and role in shaping eco-evolutionary variables

Periodic Reporting for period 2 - INTROSYM (Conservation impacts of hybridization and introgression in symbionts: Measuring the magnitude and role in shaping eco-evolutionary variables)

Reporting period: 2022-05-01 to 2023-04-30

Hybridization is becoming increasingly acknowledged as a process that has played (and often still plays) a major role in the Ecology and Evolution of many taxa. However, most studies of hybridization have been carried out in model taxa, such that much of the diversity of eco-evolutionary histories (e.g. coevolving species) and the potentially key role that hybridization plays across a variety of groups remain unstudied.

Symbionts (i.e. parasites, mutualists, and commensals that intimately interact with their hosts) comprise the most diverse group of organisms in the world. Symbionts are essential to ecosystems, comprising up to 75% of all ecological interactions. A major concern is that conservative estimates predict that up to 10% of symbiont species are expected to go extinct by 2070 due to climate change. In some cases, climate change causes species to change their distributions such that they overlap with other species with which they can hybridize. A dominant species may even hybridize a less dominant species into extinction. Despite their diversity, relevance, and conservation status, primary aspects of the Ecology, Evolution, and Conservation Biology of symbionts are yet to be understood, especially when compared to what is known about free-living organisms. This lack of knowledge is particularly acute when it comes to understanding the role of hybridization among symbiont taxa. The overall purpose of this project was to follow an integrative approach to disentangle how hybridization operates in symbionts, a group of taxa exhibiting unique eco-evolutionary trajectories, and for which hybridization has almost never been studied.

The main objective of this project was to disentangle how hybridization operates in symbionts. To achieve this, we leveraged already generated high coverage (>50X) whole-genome data of feather lice from at least 600 louse individuals belonging to around 500 species and 140 genera. This sampling represented around 90% of feather louse genera, and most host families.

Conclusions: Over the course of the project, we found that introgression is highly prevalent across all studied clades, hinting at its significance in symbiont evolution. Notably, we discovered patterns suggesting that hybridization might provide essential genetic material for colonizing new host species. The project's findings pave the way for deeper insights into symbiont evolution and provide crucial knowledge for conservation efforts.
We processed, assembled, and analyzed genomic data, aiming to understand the role of hybridization in symbionts focusing in bird feather lice

To support our endeavors, we developed a suite of scripts, enhancing the efficiency of our analytical processes, including new computational implementations and improvements in existing methods.

Intermediate analyses necessary for the introgression studies were performed for the majority of the clades and has led to derived research articles. We also established pipelines for microbiome and genome-resolved metagenomic studies. A dedicated Google Drive spreadsheet was created to track the progress and results, ensuring transparent and continuous reporting.

Our general introgression analyses have yielded significant findings, revealing the prevalence of introgression across all analyzed clades and its potential role in speciation events, particularly in relation to host-switching. Notably, our analyses have highlighted that introgression events often precede host-switching speciation events, suggesting that hybridization might be furnishing beneficial genetic material for the colonization of new host species.

We have so far ensured the dissemination of our findings:

Conferences: Co-organized a symposium at ESEB 2022 (RP1, https://www.eseb2022.cz) invited talk at the University of Arkansas (RP1), talk at ICP7 (FRP, https://darwin.biology.utah.edu/ICP7.html) and invited talk at AOS & SCO-SOC 2023 (FRP, https://meeting.americanornithology.org). I'm also co-organizing a symposium for ICE2024 in Kyoto (FRP, https://ice2024.org).
Publications: 4 papers published, more ongoing, and 2 preprints available.
Documentary: Collaboration with "Barrios Producciones" for platforms like Vimeo, YouTube, and my website (https://jdona.com/project/introsym/).
Our research has made substantial progress beyond the current state of the art in understanding the role of hybridization in symbionts. Key advancements and conclusions include:

- Prevalence of introgression in specialized symbionts: We've demonstrated that introgression is prevalent even in highly specialized and host-specific symbionts like bird lice, challenging traditional beliefs about reproductive barriers in these organisms.

- Broad range of hybridization partners: Contrary to previous assumptions, our data suggests that introgression doesn't solely occur between closely related species. This implies that reproductive isolation barriers might be weaker than previously believed, allowing for genetic exchange across diverse taxa.

- Introgression and host switching speciation dynamics: Our findings indicate that introgression events more frequently precede host-switching speciation events. This groundbreaking discovery supports the theory that hybridization might supply beneficial genetic material essential for the colonization of new host species.

- Introgression and extinction dynamics: We've identified a negative correlation between the levels of introgression and the cophylogenetic extinction rate. This implies that clades with reduced introgression levels might be at a higher risk of extinction.

Our research has broad implications. Firstly, it reshapes our understanding of the evolutionary dynamics of symbionts, offering a fresh perspective on the role of hybridization in speciation and adaptability. The findings also have potential socio-economic impacts, particularly in the context of conservation efforts (e.g. thanks to the derived research on introgression and extinction dynamics, we have found that host body size shapes symbiont effective population sizes). Recognizing the factors that influence the survival and adaptability of symbionts can inform strategies to protect biodiversity, especially given the looming threat of climate change and its impact on ecosystems.
Downy woodpecker