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How Do Genomes Create Novel Phenotypes? Insights from the Loss of the Worker Caste in Ant Social Parasites

A central goal of biology is to uncover the genetic basis for the origin of new phenotypes. A particularly effective approach is to examine the genomic architecture of species that have secondarily lost a phenotype with respect to their close relatives. In the eusocial Hymenoptera, queens and worker...

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Autores principales: Smith, Chris R., Helms Cahan, Sara, Kemena, Carsten, Brady, Seán G., Yang, Wei, Bornberg-Bauer, Erich, Eriksson, Ti, Gadau, Juergen, Helmkampf, Martin, Gotzek, Dietrich, Okamoto Miyakawa, Misato, Suarez, Andrew V., Mikheyev, Alexander
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4651238/
https://www.ncbi.nlm.nih.gov/pubmed/26226984
http://dx.doi.org/10.1093/molbev/msv165
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author Smith, Chris R.
Helms Cahan, Sara
Kemena, Carsten
Brady, Seán G.
Yang, Wei
Bornberg-Bauer, Erich
Eriksson, Ti
Gadau, Juergen
Helmkampf, Martin
Gotzek, Dietrich
Okamoto Miyakawa, Misato
Suarez, Andrew V.
Mikheyev, Alexander
author_facet Smith, Chris R.
Helms Cahan, Sara
Kemena, Carsten
Brady, Seán G.
Yang, Wei
Bornberg-Bauer, Erich
Eriksson, Ti
Gadau, Juergen
Helmkampf, Martin
Gotzek, Dietrich
Okamoto Miyakawa, Misato
Suarez, Andrew V.
Mikheyev, Alexander
author_sort Smith, Chris R.
collection PubMed
description A central goal of biology is to uncover the genetic basis for the origin of new phenotypes. A particularly effective approach is to examine the genomic architecture of species that have secondarily lost a phenotype with respect to their close relatives. In the eusocial Hymenoptera, queens and workers have divergent phenotypes that may be produced via either expression of alternative sets of caste-specific genes and pathways or differences in expression patterns of a shared set of multifunctional genes. To distinguish between these two hypotheses, we investigated how secondary loss of the worker phenotype in workerless ant social parasites impacted genome evolution across two independent origins of social parasitism in the ant genera Pogonomyrmex and Vollenhovia. We sequenced the genomes of three social parasites and their most-closely related eusocial host species and compared gene losses in social parasites with gene expression differences between host queens and workers. Virtually all annotated genes were expressed to some degree in both castes of the host, with most shifting in queen-worker bias across developmental stages. As a result, despite >1 My of divergence from the last common ancestor that had workers, the social parasites showed strikingly little evidence of gene loss, damaging mutations, or shifts in selection regime resulting from loss of the worker caste. This suggests that regulatory changes within a multifunctional genome, rather than sequence differences, have played a predominant role in the evolution of social parasitism, and perhaps also in the many gains and losses of phenotypes in the social insects.
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spelling pubmed-46512382015-11-25 How Do Genomes Create Novel Phenotypes? Insights from the Loss of the Worker Caste in Ant Social Parasites Smith, Chris R. Helms Cahan, Sara Kemena, Carsten Brady, Seán G. Yang, Wei Bornberg-Bauer, Erich Eriksson, Ti Gadau, Juergen Helmkampf, Martin Gotzek, Dietrich Okamoto Miyakawa, Misato Suarez, Andrew V. Mikheyev, Alexander Mol Biol Evol Discoveries A central goal of biology is to uncover the genetic basis for the origin of new phenotypes. A particularly effective approach is to examine the genomic architecture of species that have secondarily lost a phenotype with respect to their close relatives. In the eusocial Hymenoptera, queens and workers have divergent phenotypes that may be produced via either expression of alternative sets of caste-specific genes and pathways or differences in expression patterns of a shared set of multifunctional genes. To distinguish between these two hypotheses, we investigated how secondary loss of the worker phenotype in workerless ant social parasites impacted genome evolution across two independent origins of social parasitism in the ant genera Pogonomyrmex and Vollenhovia. We sequenced the genomes of three social parasites and their most-closely related eusocial host species and compared gene losses in social parasites with gene expression differences between host queens and workers. Virtually all annotated genes were expressed to some degree in both castes of the host, with most shifting in queen-worker bias across developmental stages. As a result, despite >1 My of divergence from the last common ancestor that had workers, the social parasites showed strikingly little evidence of gene loss, damaging mutations, or shifts in selection regime resulting from loss of the worker caste. This suggests that regulatory changes within a multifunctional genome, rather than sequence differences, have played a predominant role in the evolution of social parasitism, and perhaps also in the many gains and losses of phenotypes in the social insects. Oxford University Press 2015-11 2015-07-29 /pmc/articles/PMC4651238/ /pubmed/26226984 http://dx.doi.org/10.1093/molbev/msv165 Text en © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
Smith, Chris R.
Helms Cahan, Sara
Kemena, Carsten
Brady, Seán G.
Yang, Wei
Bornberg-Bauer, Erich
Eriksson, Ti
Gadau, Juergen
Helmkampf, Martin
Gotzek, Dietrich
Okamoto Miyakawa, Misato
Suarez, Andrew V.
Mikheyev, Alexander
How Do Genomes Create Novel Phenotypes? Insights from the Loss of the Worker Caste in Ant Social Parasites
title How Do Genomes Create Novel Phenotypes? Insights from the Loss of the Worker Caste in Ant Social Parasites
title_full How Do Genomes Create Novel Phenotypes? Insights from the Loss of the Worker Caste in Ant Social Parasites
title_fullStr How Do Genomes Create Novel Phenotypes? Insights from the Loss of the Worker Caste in Ant Social Parasites
title_full_unstemmed How Do Genomes Create Novel Phenotypes? Insights from the Loss of the Worker Caste in Ant Social Parasites
title_short How Do Genomes Create Novel Phenotypes? Insights from the Loss of the Worker Caste in Ant Social Parasites
title_sort how do genomes create novel phenotypes? insights from the loss of the worker caste in ant social parasites
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4651238/
https://www.ncbi.nlm.nih.gov/pubmed/26226984
http://dx.doi.org/10.1093/molbev/msv165
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