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The genomics and evolution of inter-sexual mimicry and female-limited polymorphisms in damselflies

Willink, Beatriz ; Tunström, Kalle LU ; Nilén, Sofie LU orcid ; Chikhi, Rayan ; Lemane, Téo ; Takahashi, Michihiko ; Takahashi, Yuma ; Svensson, Erik I. LU orcid and Wheat, Christopher West (2023) In Nature Ecology and Evolution
Abstract

Sex-limited morphs can provide profound insights into the evolution and genomic architecture of complex phenotypes. Inter-sexual mimicry is one particular type of sex-limited polymorphism in which a novel morph resembles the opposite sex. While inter-sexual mimics are known in both sexes and a diverse range of animals, their evolutionary origin is poorly understood. Here, we investigated the genomic basis of female-limited morphs and male mimicry in the common bluetail damselfly. Differential gene expression between morphs has been documented in damselflies, but no causal locus has been previously identified. We found that male mimicry originated in an ancestrally sexually dimorphic lineage in association with multiple structural... (More)

Sex-limited morphs can provide profound insights into the evolution and genomic architecture of complex phenotypes. Inter-sexual mimicry is one particular type of sex-limited polymorphism in which a novel morph resembles the opposite sex. While inter-sexual mimics are known in both sexes and a diverse range of animals, their evolutionary origin is poorly understood. Here, we investigated the genomic basis of female-limited morphs and male mimicry in the common bluetail damselfly. Differential gene expression between morphs has been documented in damselflies, but no causal locus has been previously identified. We found that male mimicry originated in an ancestrally sexually dimorphic lineage in association with multiple structural changes, probably driven by transposable element activity. These changes resulted in ~900 kb of novel genomic content that is partly shared by male mimics in a close relative, indicating that male mimicry is a trans-species polymorphism. More recently, a third morph originated following the translocation of part of the male-mimicry sequence into a genomic position ~3.5 mb apart. We provide evidence of balancing selection maintaining male mimicry, in line with previous field population studies. Our results underscore how structural variants affecting a handful of potentially regulatory genes and morph-specific genes can give rise to novel and complex phenotypic polymorphisms.

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Contribution to journal
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published
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in
Nature Ecology and Evolution
publisher
Nature Publishing Group
external identifiers
  • pmid:37932383
  • scopus:85175864988
ISSN
2397-334X
DOI
10.1038/s41559-023-02243-1
language
English
LU publication?
yes
id
143ed3d2-589b-4187-9b66-835e4e792cf5
date added to LUP
2023-12-05 16:04:07
date last changed
2024-04-18 11:49:47
@article{143ed3d2-589b-4187-9b66-835e4e792cf5,
  abstract     = {{<p>Sex-limited morphs can provide profound insights into the evolution and genomic architecture of complex phenotypes. Inter-sexual mimicry is one particular type of sex-limited polymorphism in which a novel morph resembles the opposite sex. While inter-sexual mimics are known in both sexes and a diverse range of animals, their evolutionary origin is poorly understood. Here, we investigated the genomic basis of female-limited morphs and male mimicry in the common bluetail damselfly. Differential gene expression between morphs has been documented in damselflies, but no causal locus has been previously identified. We found that male mimicry originated in an ancestrally sexually dimorphic lineage in association with multiple structural changes, probably driven by transposable element activity. These changes resulted in ~900 kb of novel genomic content that is partly shared by male mimics in a close relative, indicating that male mimicry is a trans-species polymorphism. More recently, a third morph originated following the translocation of part of the male-mimicry sequence into a genomic position ~3.5 mb apart. We provide evidence of balancing selection maintaining male mimicry, in line with previous field population studies. Our results underscore how structural variants affecting a handful of potentially regulatory genes and morph-specific genes can give rise to novel and complex phenotypic polymorphisms.</p>}},
  author       = {{Willink, Beatriz and Tunström, Kalle and Nilén, Sofie and Chikhi, Rayan and Lemane, Téo and Takahashi, Michihiko and Takahashi, Yuma and Svensson, Erik I. and Wheat, Christopher West}},
  issn         = {{2397-334X}},
  language     = {{eng}},
  month        = {{11}},
  publisher    = {{Nature Publishing Group}},
  series       = {{Nature Ecology and Evolution}},
  title        = {{The genomics and evolution of inter-sexual mimicry and female-limited polymorphisms in damselflies}},
  url          = {{http://dx.doi.org/10.1038/s41559-023-02243-1}},
  doi          = {{10.1038/s41559-023-02243-1}},
  year         = {{2023}},
}