Host-symbiont-gene phylogenetic reconciliation

Motivation Biological systems are made of entities organized at different scales (e.g. macro-organisms, symbionts, genes…) which evolve in interaction. These interactions range from independence or conflict to cooperation and coevolution, which results in them having a common history. The evolution...

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Main Authors: Menet, Hugo, Trung, Alexia Nguyen, Daubin, Vincent, Tannier, Eric
Format: Article
Language:English
Published: Peer Community In 2023-05-01
Series:Peer Community Journal
Online Access:https://peercommunityjournal.org/articles/10.24072/pcjournal.273/
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author Menet, Hugo
Trung, Alexia Nguyen
Daubin, Vincent
Tannier, Eric
author_facet Menet, Hugo
Trung, Alexia Nguyen
Daubin, Vincent
Tannier, Eric
author_sort Menet, Hugo
collection DOAJ
description Motivation Biological systems are made of entities organized at different scales (e.g. macro-organisms, symbionts, genes…) which evolve in interaction. These interactions range from independence or conflict to cooperation and coevolution, which results in them having a common history. The evolution of such systems is approached by phylogenetic reconciliation, which describes the common patterns of diversification between two different levels, e.g. genes and species, or hosts and symbionts for example. The limit to two levels hides the multi-level inter-dependencies that characterize complex systems. Results We present a probabilistic model of evolution of three nested levels of organization which can account for the codivergence of hosts, symbionts and their genes. This model allows gene transfer as well as host switch, gene duplication as well as symbiont diversification inside a host, gene or symbiont loss. It handles the possibility of ghost lineages as well as temporary free-living symbionts. Given three phylogenetic trees, we devise a Monte Carlo algorithm which samples evolutionary scenarios of symbionts and genes according to an approximation of their likelihood in the model. We evaluate the capacity of our method on simulated data, notably its capacity to infer horizontal gene transfers, and its ability to detect hostsymbiont co-evolution by comparing host/symbiont/gene and symbiont/gene models based on their estimated likelihoods. Then we show in a aphid enterobacter system that some reliable transfers detected by our method, are invisible to classic 2-level reconciliation. We finally evaluate different hypotheses on human population histories in the light of their coevolving Helicobacter pylori symbionts, reconciled together with their genes. Availability Implementation is available on GitHub https://github.com/hmenet/TALE. Data are available on Zenodo https://doi.org/10.5281/zenodo.7667342.
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spelling doaj-art-3c4c6c620bdb49c59c7c0e5ca1f42c6e2025-02-07T10:16:49ZengPeer Community InPeer Community Journal2804-38712023-05-01310.24072/pcjournal.27310.24072/pcjournal.273Host-symbiont-gene phylogenetic reconciliation Menet, Hugo0https://orcid.org/0000-0002-6809-3878Trung, Alexia Nguyen1Daubin, Vincent2https://orcid.org/0000-0001-8269-9430Tannier, Eric3https://orcid.org/0000-0002-3681-7536Univ Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Évolutive UMR5558, F-69622 Villeurbanne, FranceUniv Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Évolutive UMR5558, F-69622 Villeurbanne, FranceUniv Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Évolutive UMR5558, F-69622 Villeurbanne, FranceUniv Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Évolutive UMR5558, F-69622 Villeurbanne, France; Inria, Centre de recherche de Lyon, 69622 Villeurbanne, FranceMotivation Biological systems are made of entities organized at different scales (e.g. macro-organisms, symbionts, genes…) which evolve in interaction. These interactions range from independence or conflict to cooperation and coevolution, which results in them having a common history. The evolution of such systems is approached by phylogenetic reconciliation, which describes the common patterns of diversification between two different levels, e.g. genes and species, or hosts and symbionts for example. The limit to two levels hides the multi-level inter-dependencies that characterize complex systems. Results We present a probabilistic model of evolution of three nested levels of organization which can account for the codivergence of hosts, symbionts and their genes. This model allows gene transfer as well as host switch, gene duplication as well as symbiont diversification inside a host, gene or symbiont loss. It handles the possibility of ghost lineages as well as temporary free-living symbionts. Given three phylogenetic trees, we devise a Monte Carlo algorithm which samples evolutionary scenarios of symbionts and genes according to an approximation of their likelihood in the model. We evaluate the capacity of our method on simulated data, notably its capacity to infer horizontal gene transfers, and its ability to detect hostsymbiont co-evolution by comparing host/symbiont/gene and symbiont/gene models based on their estimated likelihoods. Then we show in a aphid enterobacter system that some reliable transfers detected by our method, are invisible to classic 2-level reconciliation. We finally evaluate different hypotheses on human population histories in the light of their coevolving Helicobacter pylori symbionts, reconciled together with their genes. Availability Implementation is available on GitHub https://github.com/hmenet/TALE. Data are available on Zenodo https://doi.org/10.5281/zenodo.7667342. https://peercommunityjournal.org/articles/10.24072/pcjournal.273/
spellingShingle Menet, Hugo
Trung, Alexia Nguyen
Daubin, Vincent
Tannier, Eric
Host-symbiont-gene phylogenetic reconciliation
Peer Community Journal
title Host-symbiont-gene phylogenetic reconciliation
title_full Host-symbiont-gene phylogenetic reconciliation
title_fullStr Host-symbiont-gene phylogenetic reconciliation
title_full_unstemmed Host-symbiont-gene phylogenetic reconciliation
title_short Host-symbiont-gene phylogenetic reconciliation
title_sort host symbiont gene phylogenetic reconciliation
url https://peercommunityjournal.org/articles/10.24072/pcjournal.273/
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AT daubinvincent hostsymbiontgenephylogeneticreconciliation
AT tanniereric hostsymbiontgenephylogeneticreconciliation