Comparative Evidence of an Exceptional Impact of Gene Duplication on the Developmental Evolution of Drosophila and the Higher Diptera

The importance of gene duplication in developmental body plan evolution is well-established, but for many megadiverse clades such as true flies (Diptera), a comprehensive understanding is still just emerging through comparative genomics. In a survey of 377 developmental gene families, we found that...

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Main Authors: Riyue Bao, Sammy E. Dia, Hussein A. Issa, Dalia Alhusein, Markus Friedrich
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-06-01
Series:Frontiers in Ecology and Evolution
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fevo.2018.00063/full
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author Riyue Bao
Sammy E. Dia
Hussein A. Issa
Dalia Alhusein
Markus Friedrich
Markus Friedrich
author_facet Riyue Bao
Sammy E. Dia
Hussein A. Issa
Dalia Alhusein
Markus Friedrich
Markus Friedrich
author_sort Riyue Bao
collection DOAJ
description The importance of gene duplication in developmental body plan evolution is well-established, but for many megadiverse clades such as true flies (Diptera), a comprehensive understanding is still just emerging through comparative genomics. In a survey of 377 developmental gene families, we found that in addition to the pea aphid, which has been previously shown to be genome-wide enriched with gene duplicates and was included as positive control, more than twice as many expanded developmental gene families were observed in Drosophila (49) compared to mosquito (21), flour beetle (20), and honeybee (14). Synonymous sequence divergence estimates and ortholog conservation analyses in additional dipteran genomes revealed that most Drosophila gene duplicates are ancient and accumulated during a time window that reaches back to the origin of brachyceran flies, ~180 million years ago. Further, available genetic data suggest that more than half of the Drosophila developmental gene duplicates remained partially or even fully redundant despite their ancient separation. We therefore speculate that the exceptional accumulation of developmental gene duplicates in Drosophila and the higher Diptera was proximally driven by the evolution of fast development, benefiting from increased genetic robustness. At the same time, the concomitant increase of opportunities for gene duplicate diversification appears to have been a source for developmental and phenotypic innovation during the unparalleled diversification of brachyceran Diptera.
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spelling doaj.art-a263e07b0a3849d99c313e4a05e02ca52022-12-21T18:51:58ZengFrontiers Media S.A.Frontiers in Ecology and Evolution2296-701X2018-06-01610.3389/fevo.2018.00063322427Comparative Evidence of an Exceptional Impact of Gene Duplication on the Developmental Evolution of Drosophila and the Higher DipteraRiyue Bao0Sammy E. Dia1Hussein A. Issa2Dalia Alhusein3Markus Friedrich4Markus Friedrich5Department of Biological Sciences, Wayne State University, Detroit, MI, United StatesDepartment of Biological Sciences, Wayne State University, Detroit, MI, United StatesDepartment of Biological Sciences, Wayne State University, Detroit, MI, United StatesDepartment of Biological Sciences, Wayne State University, Detroit, MI, United StatesDepartment of Biological Sciences, Wayne State University, Detroit, MI, United StatesDepartment of Anatomy and Cell Biology, School of Medicine, Wayne State University, Detroit, MI, United StatesThe importance of gene duplication in developmental body plan evolution is well-established, but for many megadiverse clades such as true flies (Diptera), a comprehensive understanding is still just emerging through comparative genomics. In a survey of 377 developmental gene families, we found that in addition to the pea aphid, which has been previously shown to be genome-wide enriched with gene duplicates and was included as positive control, more than twice as many expanded developmental gene families were observed in Drosophila (49) compared to mosquito (21), flour beetle (20), and honeybee (14). Synonymous sequence divergence estimates and ortholog conservation analyses in additional dipteran genomes revealed that most Drosophila gene duplicates are ancient and accumulated during a time window that reaches back to the origin of brachyceran flies, ~180 million years ago. Further, available genetic data suggest that more than half of the Drosophila developmental gene duplicates remained partially or even fully redundant despite their ancient separation. We therefore speculate that the exceptional accumulation of developmental gene duplicates in Drosophila and the higher Diptera was proximally driven by the evolution of fast development, benefiting from increased genetic robustness. At the same time, the concomitant increase of opportunities for gene duplicate diversification appears to have been a source for developmental and phenotypic innovation during the unparalleled diversification of brachyceran Diptera.https://www.frontiersin.org/article/10.3389/fevo.2018.00063/fullgene duplicationBrachyceraevolution of developmentgenetic redundancyphenotypic robustnessdisconnected
spellingShingle Riyue Bao
Sammy E. Dia
Hussein A. Issa
Dalia Alhusein
Markus Friedrich
Markus Friedrich
Comparative Evidence of an Exceptional Impact of Gene Duplication on the Developmental Evolution of Drosophila and the Higher Diptera
Frontiers in Ecology and Evolution
gene duplication
Brachycera
evolution of development
genetic redundancy
phenotypic robustness
disconnected
title Comparative Evidence of an Exceptional Impact of Gene Duplication on the Developmental Evolution of Drosophila and the Higher Diptera
title_full Comparative Evidence of an Exceptional Impact of Gene Duplication on the Developmental Evolution of Drosophila and the Higher Diptera
title_fullStr Comparative Evidence of an Exceptional Impact of Gene Duplication on the Developmental Evolution of Drosophila and the Higher Diptera
title_full_unstemmed Comparative Evidence of an Exceptional Impact of Gene Duplication on the Developmental Evolution of Drosophila and the Higher Diptera
title_short Comparative Evidence of an Exceptional Impact of Gene Duplication on the Developmental Evolution of Drosophila and the Higher Diptera
title_sort comparative evidence of an exceptional impact of gene duplication on the developmental evolution of drosophila and the higher diptera
topic gene duplication
Brachycera
evolution of development
genetic redundancy
phenotypic robustness
disconnected
url https://www.frontiersin.org/article/10.3389/fevo.2018.00063/full
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