A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida)

Abstract Inversions often underlie complex adaptive traits, but the genic targets inside them are largely unknown. Gene expression profiling provides a powerful way to link inversions with their phenotypic consequences. We examined the effects of the Cf‐Inv(1) inversion in the seaweed fly Coelopa fr...

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Main Authors: Emma L. Berdan, Claire Mérot, Henrik Pavia, Kerstin Johannesson, Maren Wellenreuther, Roger K. Butlin
Format: Article
Language:English
Published: Oxford University Press 2021-12-01
Series:Evolution Letters
Subjects:
Online Access:https://doi.org/10.1002/evl3.260
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author Emma L. Berdan
Claire Mérot
Henrik Pavia
Kerstin Johannesson
Maren Wellenreuther
Roger K. Butlin
author_facet Emma L. Berdan
Claire Mérot
Henrik Pavia
Kerstin Johannesson
Maren Wellenreuther
Roger K. Butlin
author_sort Emma L. Berdan
collection DOAJ
description Abstract Inversions often underlie complex adaptive traits, but the genic targets inside them are largely unknown. Gene expression profiling provides a powerful way to link inversions with their phenotypic consequences. We examined the effects of the Cf‐Inv(1) inversion in the seaweed fly Coelopa frigida on gene expression variation across sexes and life stages. Our analyses revealed that Cf‐Inv(1) shapes global expression patterns, most likely via linked variation, but the extent of this effect is variable, with much stronger effects in adults than larvae. Furthermore, within adults, both common as well as sex‐specific patterns were found. The vast majority of these differentially expressed genes mapped to Cf‐Inv(1). However, genes that were differentially expressed in a single context (i.e., in males, females, or larvae) were more likely to be located outside of Cf‐Inv(1). By combining our findings with genomic scans for environmentally associated SNPs, we were able to pinpoint candidate variants in the inversion that may underlie mechanistic pathways that determine phenotypes. Together the results of this study, combined with previous findings, support the notion that the polymorphic Cf‐Inv(1) inversion in this species is a major factor shaping both coding and regulatory variation resulting in highly complex adaptive effects.
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spelling doaj.art-ee3c7b6f8793465c97d3bc3251c26c6e2023-09-02T12:32:37ZengOxford University PressEvolution Letters2056-37442021-12-015660762410.1002/evl3.260A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida)Emma L. Berdan0Claire Mérot1Henrik Pavia2Kerstin Johannesson3Maren Wellenreuther4Roger K. Butlin5Department of Marine Sciences University of Gothenburg Gothenburg SE‐40530 SwedenDépartement de Biologie, Institut de Biologie Intégrative et des Systèmes (IBIS) Université Laval Québec QC G1V 0A6 CanadaDepartment of Marine Sciences University of Gothenburg Gothenburg SE‐40530 SwedenDepartment of Marine Sciences University of Gothenburg Gothenburg SE‐40530 SwedenThe New Zealand Institute for Plant and Food Research Ltd. Nelson 7010 New ZealandDepartment of Marine Sciences University of Gothenburg Gothenburg SE‐40530 SwedenAbstract Inversions often underlie complex adaptive traits, but the genic targets inside them are largely unknown. Gene expression profiling provides a powerful way to link inversions with their phenotypic consequences. We examined the effects of the Cf‐Inv(1) inversion in the seaweed fly Coelopa frigida on gene expression variation across sexes and life stages. Our analyses revealed that Cf‐Inv(1) shapes global expression patterns, most likely via linked variation, but the extent of this effect is variable, with much stronger effects in adults than larvae. Furthermore, within adults, both common as well as sex‐specific patterns were found. The vast majority of these differentially expressed genes mapped to Cf‐Inv(1). However, genes that were differentially expressed in a single context (i.e., in males, females, or larvae) were more likely to be located outside of Cf‐Inv(1). By combining our findings with genomic scans for environmentally associated SNPs, we were able to pinpoint candidate variants in the inversion that may underlie mechanistic pathways that determine phenotypes. Together the results of this study, combined with previous findings, support the notion that the polymorphic Cf‐Inv(1) inversion in this species is a major factor shaping both coding and regulatory variation resulting in highly complex adaptive effects.https://doi.org/10.1002/evl3.260Chromosomal evolutiongene expressiongenetic architecturepopulation genomics
spellingShingle Emma L. Berdan
Claire Mérot
Henrik Pavia
Kerstin Johannesson
Maren Wellenreuther
Roger K. Butlin
A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida)
Evolution Letters
Chromosomal evolution
gene expression
genetic architecture
population genomics
title A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida)
title_full A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida)
title_fullStr A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida)
title_full_unstemmed A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida)
title_short A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida)
title_sort large chromosomal inversion shapes gene expression in seaweed flies coelopa frigida
topic Chromosomal evolution
gene expression
genetic architecture
population genomics
url https://doi.org/10.1002/evl3.260
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