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Dollo parsimony overestimates ancestral gene content reconstructions

Gàlvez-Morante, Alex; Guéguen, Laurent; Natsidis, Paschalis; Telford, Maximilian J; Richter, Daniel J; (2024) Dollo parsimony overestimates ancestral gene content reconstructions. Genome Biology and Evolution , 16 (4) , Article evae062. 10.1093/gbe/evae062. Green open access

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Abstract

Ancestral reconstruction is a widely-used technique that has been applied to understand the evolutionary history of gain and loss of gene families. Ancestral gene content can be reconstructed via different phylogenetic methods, but many current and previous studies employ Dollo parsimony. We hypothesize that Dollo parsimony is not appropriate for ancestral gene content reconstruction inferences based on sequence homology, as Dollo parsimony is derived from the assumption that a complex character cannot be regained. This premise does not accurately model molecular sequence evolution, in which false orthology can result from sequence convergence or lateral gene transfer. The aim of this study is to test Dollo parsimony's suitability for ancestral gene content reconstruction and to compare its inferences with a maximum likelihood-based approach which allows a gene family to be gained more than once within a tree. We first compared the performance of the two approaches on a series of artificial datasets each of 5,000 genes that were simulated according to a spectrum of evolutionary rates without gene gain or loss, so that inferred deviations from the true gene count would arise only from errors in orthology inference and ancestral reconstruction. Next, we reconstructed protein domain evolution on a phylogeny representing known eukaryotic diversity. We observed that Dollo parsimony produced numerous ancestral gene content overestimations, especially at nodes closer to the root of the tree. These observations led us to the conclusion that, confirming our hypothesis, Dollo parsimony is not an appropriate method for ancestral reconstruction studies based on sequence homology.

Type: Article
Title: Dollo parsimony overestimates ancestral gene content reconstructions
Location: England
Open access status: An open access version is available from UCL Discovery
DOI: 10.1093/gbe/evae062
Publisher version: http://dx.doi.org/10.1093/gbe/evae062
Language: English
Additional information: © The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/).
Keywords: Dollo parsimony, ancestral reconstruction, gene family evolution, maximum likelihood, phylogenomics
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences > Genetics, Evolution and Environment
URI: https://discovery.ucl.ac.uk/id/eprint/10190227
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