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Evolution of five environmentally responsive gene families in a pine‐feeding sawfly, Neodiprion lecontei (Hymenoptera: Diprionidae)

A central goal in evolutionary biology is to determine the predictability of adaptive genetic changes. Despite many documented cases of convergent evolution at individual loci, little is known about the repeatability of gene family expansions and contractions. To address this void, we examined gene...

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Autores principales: Vertacnik, Kim L., Herrig, Danielle K., Godfrey, R. Keating, Hill, Tom, Geib, Scott M., Unckless, Robert L., Nelson, David R., Linnen, Catherine R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10542623/
https://www.ncbi.nlm.nih.gov/pubmed/37791292
http://dx.doi.org/10.1002/ece3.10506
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author Vertacnik, Kim L.
Herrig, Danielle K.
Godfrey, R. Keating
Hill, Tom
Geib, Scott M.
Unckless, Robert L.
Nelson, David R.
Linnen, Catherine R.
author_facet Vertacnik, Kim L.
Herrig, Danielle K.
Godfrey, R. Keating
Hill, Tom
Geib, Scott M.
Unckless, Robert L.
Nelson, David R.
Linnen, Catherine R.
author_sort Vertacnik, Kim L.
collection PubMed
description A central goal in evolutionary biology is to determine the predictability of adaptive genetic changes. Despite many documented cases of convergent evolution at individual loci, little is known about the repeatability of gene family expansions and contractions. To address this void, we examined gene family evolution in the redheaded pine sawfly Neodiprion lecontei, a noneusocial hymenopteran and exemplar of a pine‐specialized lineage evolved from angiosperm‐feeding ancestors. After assembling and annotating a draft genome, we manually annotated multiple gene families with chemosensory, detoxification, or immunity functions before characterizing their genomic distributions and molecular evolution. We find evidence of recent expansions of bitter gustatory receptor, clan 3 cytochrome P450, olfactory receptor, and antimicrobial peptide subfamilies, with strong evidence of positive selection among paralogs in a clade of gustatory receptors possibly involved in the detection of bitter compounds. In contrast, these gene families had little evidence of recent contraction via pseudogenization. Overall, our results are consistent with the hypothesis that in response to novel selection pressures, gene families that mediate ecological interactions may expand and contract predictably. Testing this hypothesis will require the comparative analysis of high‐quality annotation data from phylogenetically and ecologically diverse insect species and functionally diverse gene families. To this end, increasing sampling in under‐sampled hymenopteran lineages and environmentally responsive gene families and standardizing manual annotation methods should be prioritized.
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spelling pubmed-105426232023-10-03 Evolution of five environmentally responsive gene families in a pine‐feeding sawfly, Neodiprion lecontei (Hymenoptera: Diprionidae) Vertacnik, Kim L. Herrig, Danielle K. Godfrey, R. Keating Hill, Tom Geib, Scott M. Unckless, Robert L. Nelson, David R. Linnen, Catherine R. Ecol Evol Research Articles A central goal in evolutionary biology is to determine the predictability of adaptive genetic changes. Despite many documented cases of convergent evolution at individual loci, little is known about the repeatability of gene family expansions and contractions. To address this void, we examined gene family evolution in the redheaded pine sawfly Neodiprion lecontei, a noneusocial hymenopteran and exemplar of a pine‐specialized lineage evolved from angiosperm‐feeding ancestors. After assembling and annotating a draft genome, we manually annotated multiple gene families with chemosensory, detoxification, or immunity functions before characterizing their genomic distributions and molecular evolution. We find evidence of recent expansions of bitter gustatory receptor, clan 3 cytochrome P450, olfactory receptor, and antimicrobial peptide subfamilies, with strong evidence of positive selection among paralogs in a clade of gustatory receptors possibly involved in the detection of bitter compounds. In contrast, these gene families had little evidence of recent contraction via pseudogenization. Overall, our results are consistent with the hypothesis that in response to novel selection pressures, gene families that mediate ecological interactions may expand and contract predictably. Testing this hypothesis will require the comparative analysis of high‐quality annotation data from phylogenetically and ecologically diverse insect species and functionally diverse gene families. To this end, increasing sampling in under‐sampled hymenopteran lineages and environmentally responsive gene families and standardizing manual annotation methods should be prioritized. John Wiley and Sons Inc. 2023-10-01 /pmc/articles/PMC10542623/ /pubmed/37791292 http://dx.doi.org/10.1002/ece3.10506 Text en © 2023 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Vertacnik, Kim L.
Herrig, Danielle K.
Godfrey, R. Keating
Hill, Tom
Geib, Scott M.
Unckless, Robert L.
Nelson, David R.
Linnen, Catherine R.
Evolution of five environmentally responsive gene families in a pine‐feeding sawfly, Neodiprion lecontei (Hymenoptera: Diprionidae)
title Evolution of five environmentally responsive gene families in a pine‐feeding sawfly, Neodiprion lecontei (Hymenoptera: Diprionidae)
title_full Evolution of five environmentally responsive gene families in a pine‐feeding sawfly, Neodiprion lecontei (Hymenoptera: Diprionidae)
title_fullStr Evolution of five environmentally responsive gene families in a pine‐feeding sawfly, Neodiprion lecontei (Hymenoptera: Diprionidae)
title_full_unstemmed Evolution of five environmentally responsive gene families in a pine‐feeding sawfly, Neodiprion lecontei (Hymenoptera: Diprionidae)
title_short Evolution of five environmentally responsive gene families in a pine‐feeding sawfly, Neodiprion lecontei (Hymenoptera: Diprionidae)
title_sort evolution of five environmentally responsive gene families in a pine‐feeding sawfly, neodiprion lecontei (hymenoptera: diprionidae)
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10542623/
https://www.ncbi.nlm.nih.gov/pubmed/37791292
http://dx.doi.org/10.1002/ece3.10506
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