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

Okres sprawozdawczy: 2020-05-01 do 2022-04-30

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% 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 extinction6. 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 is 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 is to disentangle how hybridization operates in symbionts. To do so, I will leverage 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 represents around 90% of feather louse genera, and most host families. Specific objectives:

SO1. I will first investigate the pattern of introgression across the global tree of lice.
SO2-3. Next, I will research the role of introgression in shaping key eco-evolutionary variables related to dispersal and host-switching. I will focus on two specific variables: host-specificity (SO2) and microbiomes (SO3).
SO4. Finally, I will study the relationship between introgression levels and symbiont extinction rate.
We have processed and assembled most of the genomic data for the general analyses of the project (General analyses). In particular, for the aTRAM approach (2,395 single-copy orthologs per individual), 7 out of 8 clades are finished (590 species). For the whole genome-based approach, 5 out of 8 clades are completed, i.e. reference-based whole genome assemblies and SNP calling for 335 species. The remaining general analyses are expected to be done by August 2022.

We also generated a suite of scripts to either perform these required analyses (e.g. new computational implementations of theoretical methods, such as RND or Delta) or to improve efficiency and allow for some of these methods to work at a >100 taxa scale in a much shorter time (e.g. aTRAM phylogenomic pipeline). We have deposited all these scripts in a dedicated (still private) GitHub repository. The efficiency improvement has allowed us to increase the sample size for the project by adding more than 100 species.

We have performed all the intermediate analyses required for the introgression analyses (species delimitation, phylogenomic, dating, and cophylogenetic) for 5 out of 8 clades. Also, we set up the microbiome and genome-resolved metagenomic pipeline, used it for derived research, and ran it for one INTROSYM clade. Also, we have fine-tuned a bioinformatic pipeline to assemble endosymbiont genomes and retrieve phylogenomic markers (SO3). We have created a dedicated Google Drive spreadsheet containing all results, allowing tracking of the project status and continuous reporting (D1.1 report). The remaining intermediate analyses are expected to be done by September 2022.

We have also made the general introgression analyses (aTRAM based: phylogenetic networks, Delta; SNP-based: D statistics, f-branch statistic), identified potentially introgressed regions (RND + Gprofiler), and statistically analyzed (preliminary) the results of these 5 clades (SO1, SO2, and SO4). Notably, derived from this intermediate-generated data required for introgression analyses (e.g. clade-level phylogenies and cophylogenies), microbiome and genome-resolved-metagenomic pipelines, and the efficiency improvement in the phylogenomic pipeline (aTRAM based), we have published three derived papers and are working on more, some of which are on an advanced stage.

Preliminary results (from SO1, SO2, and SO4) indicate introgression is highly prevalent (positive signature in all analyzed clades so far, O1) and that it does not necessarily occur between closely related species (mean divergence time between hybridizing species = 8.9 mya, max=26.9 mya, min=1.6 mya, O1). Regarding the relationship between introgression and coevolutionary aspects, we have found a positive relationship between introgression level and host switching rate (R2=0.54 O2). Notably, we discovered that introgression events happen more often before host switching speciation events, i.e. a pattern congruent with hybridization providing useful genetic material for colonizing a new host species (O2). Furthermore, we found a strong negative relationship between introgression level and cophylogenetic extinction rate (i.e. clades with lower introgression levels have higher extinction rates, R2=0.75 O4). We are currently calculating two genome-wide individual heterozygosity metrics to see if clades with higher extinction rates and lower introgression levels also have lower individual heterozygosity values (as a proxy for species-level genomic diversity). We expect the remaining analyses to be finished by September, and then we will re-run the statistical analysis script including the final data.

We presented these results on patterns of introgression in lice (SO1) and the relationship between introgression and coevolutionary (SO2) and extinction (SO4) dynamics at an invited conference (April 29, 2022, University of Arkansas).
Based on our preliminary results:

- Introgression is also highly prevalent in highly specified and host-specific symbionts, such as bird lice
- Introgression does not necessarily occur between closely related species. Thus, reproductive isolation barriers are weaker than thought.
- Introgression events happen more often before host switching speciation events. This result supports that hybridization provides useful genetic material for colonizing a new host species.
- Introgression level is positively related to the host switching rate. Thus, suggesting that clades with higher levels of introgression are likely to have higher rates of host switching speciation events (in line with the previous statement).
- Introgression level is negatively related to the cophylogenetic extinction rate. Therefore, clades with lower levels of introgression are more likely to become extinct.
Downy woodpecker