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Many Options, Few Solutions: Over 60 My Snakes Converged on a Few Optimal Venom Formulations

Gene expression changes contribute to complex trait variations in both individuals and populations. However, the evolution of gene expression underlying complex traits over macroevolutionary timescales remains poorly understood. Snake venoms are proteinaceous cocktails where the expression of each t...

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Autores principales: Barua, Agneesh, Mikheyev, Alexander S
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6736290/
https://www.ncbi.nlm.nih.gov/pubmed/31220860
http://dx.doi.org/10.1093/molbev/msz125
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author Barua, Agneesh
Mikheyev, Alexander S
author_facet Barua, Agneesh
Mikheyev, Alexander S
author_sort Barua, Agneesh
collection PubMed
description Gene expression changes contribute to complex trait variations in both individuals and populations. However, the evolution of gene expression underlying complex traits over macroevolutionary timescales remains poorly understood. Snake venoms are proteinaceous cocktails where the expression of each toxin can be quantified and mapped to a distinct genomic locus and traced for millions of years. Using a phylogenetic generalized linear mixed model, we analyzed expression data of toxin genes from 52 snake species spanning the 3 venomous snake families and estimated phylogenetic covariance, which acts as a measure of evolutionary constraint. We find that evolution of toxin combinations is not constrained. However, although all combinations are in principle possible, the actual dimensionality of phylomorphic space is low, with envenomation strategies focused around only four major toxin families: metalloproteases, three-finger toxins, serine proteases, and phospholipases A2. Although most extant snakes prioritize either a single or a combination of major toxin families, they are repeatedly recruited and lost. We find that over macroevolutionary timescales, the venom phenotypes were not shaped by phylogenetic constraints, which include important microevolutionary constraints such as epistasis and pleiotropy, but more likely by ecological filtering that permits a small number of optimal solutions. As a result, phenotypic optima were repeatedly attained by distantly related species. These results indicate that venoms evolve by selection on biochemistry of prey envenomation, which permit diversity through parallelism, and impose strong limits, since only a few of the theoretically possible strategies seem to work well and are observed in extant snakes.
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spelling pubmed-67362902019-09-16 Many Options, Few Solutions: Over 60 My Snakes Converged on a Few Optimal Venom Formulations Barua, Agneesh Mikheyev, Alexander S Mol Biol Evol Discoveries Gene expression changes contribute to complex trait variations in both individuals and populations. However, the evolution of gene expression underlying complex traits over macroevolutionary timescales remains poorly understood. Snake venoms are proteinaceous cocktails where the expression of each toxin can be quantified and mapped to a distinct genomic locus and traced for millions of years. Using a phylogenetic generalized linear mixed model, we analyzed expression data of toxin genes from 52 snake species spanning the 3 venomous snake families and estimated phylogenetic covariance, which acts as a measure of evolutionary constraint. We find that evolution of toxin combinations is not constrained. However, although all combinations are in principle possible, the actual dimensionality of phylomorphic space is low, with envenomation strategies focused around only four major toxin families: metalloproteases, three-finger toxins, serine proteases, and phospholipases A2. Although most extant snakes prioritize either a single or a combination of major toxin families, they are repeatedly recruited and lost. We find that over macroevolutionary timescales, the venom phenotypes were not shaped by phylogenetic constraints, which include important microevolutionary constraints such as epistasis and pleiotropy, but more likely by ecological filtering that permits a small number of optimal solutions. As a result, phenotypic optima were repeatedly attained by distantly related species. These results indicate that venoms evolve by selection on biochemistry of prey envenomation, which permit diversity through parallelism, and impose strong limits, since only a few of the theoretically possible strategies seem to work well and are observed in extant snakes. Oxford University Press 2019-09 2019-05-20 /pmc/articles/PMC6736290/ /pubmed/31220860 http://dx.doi.org/10.1093/molbev/msz125 Text en © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Discoveries
Barua, Agneesh
Mikheyev, Alexander S
Many Options, Few Solutions: Over 60 My Snakes Converged on a Few Optimal Venom Formulations
title Many Options, Few Solutions: Over 60 My Snakes Converged on a Few Optimal Venom Formulations
title_full Many Options, Few Solutions: Over 60 My Snakes Converged on a Few Optimal Venom Formulations
title_fullStr Many Options, Few Solutions: Over 60 My Snakes Converged on a Few Optimal Venom Formulations
title_full_unstemmed Many Options, Few Solutions: Over 60 My Snakes Converged on a Few Optimal Venom Formulations
title_short Many Options, Few Solutions: Over 60 My Snakes Converged on a Few Optimal Venom Formulations
title_sort many options, few solutions: over 60 my snakes converged on a few optimal venom formulations
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6736290/
https://www.ncbi.nlm.nih.gov/pubmed/31220860
http://dx.doi.org/10.1093/molbev/msz125
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